Book - Sex and internal secretions (1961) 19

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Young WC. Sex and internal secretions. (1961) 3rd Eda. Williams and Wilkins. Baltimore.
Section A Biologic Basis of Sex Cytologic and Genetic Basis of Sex | Role of Hormones in the Differentiation of Sex
Section B The Hypophysis and the Gonadotrophic Hormones in Relation to Reproduction Morphology of the Hypophysis Related to Its Function | Physiology of the Anterior Hypophysis in Relation to Reproduction
The Mammalian Testis | The Accessory Reproductive Glands of Mammals | The Mammalian Ovary | The Mammalian Female Reproductive Cycle and Its Controlling Mechanisms | Action of Estrogen and Progesterone on the Reproductive Tract of Lower Primates | The Mammary Gland and Lactation | Some Problems of the Metabolism and Mechanism of Action of Steroid Sex Hormones | Nutritional Effects on Endocrine Secretions
Section D Biology of Sperm and Ova, Fertilization, Implantation, the Placenta, and Pregnancy Biology of Spermatozoa | Biology of Eggs and Implantation | Histochemistry and Electron Microscopy of the Placenta | Gestation
Section E Physiology of Reproduction in Submammalian Vertebrates Endocrinology of Reproduction in Cold-blooded Vertebrates | Endocrinology of Reproduction in Birds
Section F Hormonal Regulation of Reproductive Behavior The Hormones and Mating Behavior | Gonadal Hormones and Social Behavior in Infrahuman Vertebrates | Gonadal Hormones and Parental Behavior in Birds and Infrahuman Mammals | Sex Hormones and Other Variables in Human Eroticism | The Ontogenesis of Sexual Behavior in Man | Cultural Determinants of Sexual Behavior
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Section F Hormonal Regulation of Reproductive Behavior


The Hormones and Mating Behavior

William C. Young, Ph.D.

Professor Of Anatomy, The University Of Kansas, Lawrence, Kansas


I. Introduction

comparative approach in the study of other

Reproductive behavior is composed of the activities, l^arts of the total behavior pattern which The difficulties encountered in initiating subserve reproduction more directly and studies are documented m the Hisimportantly than any other vital activity, ^^nj of the National Research Council CornMigration, whether it is the long distance ^"^^^^ for Research in Problems of Sex seasonal migration of many birds and fishes, ^Aberle and Corner, 1953). They are rethe shorter seasonal migration of certain fleeted m the circumstance that single chapmammals, or the vernal migration to the ^^rs were considered sufficient for the subwater of many amphibians, belongs in this J^^* m the first and second editions of Sex category. Aggressive behavior manifested «"f^ Internal Secretions (Stone, 1932b, during the establishment of territoriality 1939b). Since then, however, an accelerated and in the attainment of dominance within P^ce has been maintained, so much so that a group is an element in social behavior, an appraisal of progress can best be but it is also a step toward the achievement achieved by separate treatments of mating

behavior, parental behavior, aggressiveness,

^Many of the investigations to which there is j sexuality, and the problem of the

reference were made possible by grants from the -^ ' *

Committee for Research in Problems of Sex, neural mechanisms mediating such behav Xational Academy of Sciences-National Research ior. Mating behavior will be dealt with in

Council. Latterlv, as.sistance has been provided -l\ • pl-i^.^+pi.

bv Re.search Grants M-504 to M-504(C8) from the r^, | ' ■, . , • u u •

National Institute of Mental Health, of the Na- The dependence of mating behavior on

tional Institutes of Health, Public Health Service. the gonadal hormones has long been recognized. Their role in the expression of sexual behavior in man is equivocal (see chapter by Money; in addition, Cree\y and Rea, 1940; Tauber, 1940; Carmichael, Noonan and Kenyon, 1941 ; Filler and Drezner, 1944; Carter, Cohen and Shorr, 1947; Kinsey, Pomeroy and Martin, 1948; Kinsey, Pomeroy, Martin and Gebhard, 1953; Perloff, 1949; Waxenberg, Drellich and Sutherland, 1959; and many others), but for most vertebrates for which data exist the full display of mating behavior is given only when the gonadal hormones are present. The relationship may be more direct than any other between endocrine substances and behavior.^ When the gonads are removed mating behavior becomes greatly reduced in intensity or is no longer displayed; on replacement of the hormone it is again exhibited. If an inadequate amount is given, a partial response may be detected, or, as in a number of rodents and the cow, when an improper balance is administered an atypical pattern may be shown (Boling, Young and Dempsey, 1938; Melampy, Emmerson, Rakes, Hanka and Eness, 1957). However, when the threshold of the proper hormones is reached and, in species requiring estrogen and progesterone, the correct balance is given in the proper sequence, the pattern of behavior identical with that displayed before gonadectomy is restored. In what follows, the observations and experiments supporting this conclusion are reviewed, factors which influence, modify, and limit the action of gonadal hormones are enumerated, and sug - From the fact that deviations of behavior are well known in dysfunction of the parathyroid, the thyroid, the pituitary, and the adrenal cortex, and in hyperinsulinism (Hoskins, 1934; Shock, 11)44; Sherman, 1945; Medvei, 1949; Young, 1954), it might be concluded that general behavior is dependent on a normal functioning of these glands and therefore that a direct relationship exists. This may be true for cortisone and related steroids secreted by the adrenal cortex (Rome and Braceland, 1950, 1951, 1952; Derbes and Weiss, 1951). For the other endocrine organs, however, there still is no uneqivocal proof of a one-to-one relationship between the active principles produced by these glands and the changes in behavior associated with deficiencies or with excessive quantities. An indirect relationship traceable to derangements of metabolism or to physical deformity and handicap seems more likely.


gestions are made with respect to the character and scope of problems awaiting further study.

The discussion will begin with a description of mating behavior, for the end points investigators have used in obtaining their data have been derived from the elements or measures composing this behavior.^' * As the substance of our description becomes apparent, many will feel that a disproportional space has been given to the rat and guinea pig. This is explained by the circumstance that the rat and guinea pig have

^ Many articles in which mating behavior is described are cited in the older reviews (Stone, 1932b, 1939b; Young, 1941 ; Beach, 1942e, 1946, 1947, 1948, 1951, 1952; Bullough, 1945; Hartman, 1945; CoUias, 1950). A number of newer studies containing bibliographies or unusually complete descriptive accounts of mating behavior are noted here (Schlosberg, Duncan and Daitch, 1949; Baerends, Brouwer and Waterbolk, 1955; Morris, 1955b; Aronson, 1957; for fishes. Noble and Aronson, 1942; Aronson, 1944; Russell, 1955; for amphibians. Domm and Davis, 1948; Guhl, 1949; Richdale, 1951 ; Hinde, 1952, 1955a, b ; Hale, 1955 ; Morris, 1954; Wood-Gush, 1954; Moynihan and Hall 1955; for birds. Macirone and Walton, 1938; Stone and Ferguson, 1940; Snell, Fokete, Hummel and Law, 1940; Pearson, 1940; Beach and Holz, 1946; Reed, 1946; Reed and Reed, 1946; Beach and Pauker, 1949; Young and Grunt, 1951; Enders, 1952; Rowley and Mollison, 1955; Scott and Lloyd-Jacob, 1955; Larsson, 1956; Green, Clemente and de Groot, 1957; Rosenblatt and Aronson, 1958a, b; Beach and Rabedeau, 1959; for small mammals including the rabbit, cat and dog. Burger, 1952; for the domestic pig. Hafez, 1952; for the ewe. Carpenter, 1942a, b; Yerkes, 1943; Stellar, 1960; for infrahuman primates).

  • It is of historic interest that endocrinologists,

physiologists, biochemists, and anatomists who have contributed so importantly to our knowledge of the microscopic anatomy and physiology of reproduction, have given little attention to problems centering around the hormonal regulation of reproductive behavior. Much of the work in this field has been done by psychologists and much of the support that has encouraged effort in this direction can be attributed to their foresight, activity, and persistence. Endocrinologists, physiologists, and anatomists have done little with behavior, probably because of the former rather generally held belief, best expressed perhaps by Stockard and Papanicolaou (1919) and Moore and Gallagher (1930), that behavioral end points are so vague as to be of little value in experimental studies. This circumstance in the development of the subject is reflected by the absence of any discussion of the hormones and behavior in most textbooks of endocrinology.


been favored subjects for investigation, that much of the thread of thought which follows was developed during investigations of these species, and that for problems of concern to the endocrinologist this work still is the richest source of information. At the same time, we do not belittle the fact that much has been learned from observations and experiments on other lower mammals, submammalian vertebrates, infrahuman primates, and man. Important concepts not appreciated at the time were developed from early and relatively isolated studies of the ringdove (Craig, 1914, 1918) and chicken (Goodale, 1918). Latterly, careful observations by ethologists and zoologists have provided the substance for a comparative consideration of many problems. Some of the descriptions, notably that of the male guppy (Baerends, Brouwer and Waterbolk, 1955), are more refined than any given of a mammal and all are of value for the breadth they add to what otherwise would have been a laboratory study in the narrower sense.

II. Mating Behavior

A. THE MALE

The behavior varies from species to species, but in many species and particularly in mammals genital examination, if not copulation with ejaculation, is usually immediate when individuals of opposite sexes are placed together (Hamilton, 1914; Stone, 1922; Bingham, 1928; Yerkes and Elder, 1936; Young and Grunt, 1951; Larsson, 1956). In such a situation the interval between the beginning of a test and the first display of interest in the establishment of sexual relations may be taken as a measure of the strength of sexual behavior (Soulairac and Coppin-Monthillaud, 1951). The subsequent behavior is composed of several elements. The number distinguished depends somewhat on the investigator, but also on experience. In general when a species has been used extensively as have the rat and guinea pig the later articles should be consulted (Stone, Tomilin and Barker, 1935; Stone and Ferguson, 1940; Beach, 1944b; Beach and Holz, 1946; Soulairac and CoppinISIonthillaud, 1951 ; Young and Grunt, 1951 ; Larsson, 1956).

When a female rat is placed in a cage with a cage-adapted male the latter usually begins to copulate immediately. Often, however, he begins in a few seconds to examine her anogenital region. Another precopulatory act is a nibbling at the head or body. The copulatory act is described as coming with such a definiteness and orderly sequence of elements that it can easily be distinguished from precopulatory behavior (Stone, 1922) . The male mounts the female from the rear and clasps his forelegs about her laterolumbar region in what Beach (1944b) calls a clasp-without-palpation. While clasping the female, the male palpates her sides with rapid movements of his forelimbs and simultaneously his pelvic region is moved in rapid, piston-like thrusts (palpation-with-pelvic-thrusts). He then slips off the female's back rather weakly. In nearly every instance this termination of contact with the female indicates a failure to achieve intromission; behavior of this type is designated an incomplete copulation or attempt. With what Beach designates copulation or complete copulation, the palpation-with-pelvic-thrusts occurs, but a new element is added. After a final and unusually forceful thrust, the male lunges backward and often throws himself several inches from the female. This backward lunge nearly always is indicative of intromission. Stone and Ferguson (1940) estimated from a cinematographic study that the duration of these intromissions is Vs to 2/3 of a second and that during each intromission 2 and 9 pelvic thrusts occur. When intromission is terminated by ejaculation the backward lunge is omitted. Instead the male continues to press against the female, thus prolonging intromission, and then, releasing his clasp, slowly raises his forelegs as the ejaculate is emitted and the penis withdrawn. In most tests ejaculation is not seen during the first intromission, but it has been observed at this time in tests involving observations of sexual behavior over a period of hours (Beach, 1956). Usually, however, from 3 to 44 intromissions precede ejaculation. A spell of recovery, the refractory period, is then required, during which the male is uninfluenced by any sexual stimuli (Larsson, 1956). Satiation is not reached until there have been 3 to 10 ejacu


1176


HORMONAL REGULATION


lations and the activity culminating in these ejaculations may be spread over as much as 3 hours (Stone and Ferguson, 1940; Beach and Jordan, 1956). A quiescent or recovery period of 24 hours or more follows (Stone, Ferguson and Wright, 1940), although 5 or 6 days and even longer may be necessary (Beach and Jordan, 1956; Larsson, 1956). Beach and Jordan studied the changes in behavior preceding each successive ejaculation up to and including the sixth. The number of intromissions before ejaculation decreased from an average of 10.6 to 4.1. Ejaculation-latency (interval from the first mount to ejaculation) decreased from an average of 450 to 132 seconds. The refractory period (period of sexual inactivity following all but the terminal ejaculation) increased from an average of 324 to 818 seconds.

Unless otherwise noted, the description of the behavior shown by the male guinea pig is taken from that given by Young and Grunt (1951). When a female in heat is placed with a male he begins to follow her almost immediately, usually sniffing at the anogenital region. This behavior is nuzzling. Within a few seconds he may mount her, usually posteriorly but often elsewhere. If the forepaws are placed on the back of the female without other contact, the act is abortive mounting (Valenstein, Riss and Young, 1954) , but if the back of the female is covered it is mounting. ^Mounting may be accompanied by pelvic thrusts without intromission, but often it is followed by intromission with or without pelvic thrusts. The duration of intromission varies, depending partly on the male and partly on the responsiveness of the female. Frequently she withdraws from the male at the instant of intromission, in which case there is no opportunity for pelvic thrusts. More often there is a series of pelvic thrusts lasting 2 to 5 seconds or more. Following intromission of this type, males and females usually clean the genitalia even though there was no ejaculation. Ejaculation is known to have occurred only if the final thrust is conspicuously prolonged and accompanied by a drawing in of the flanks as in a spasm ; both animals then fall back on their haunches and clean the genitalia. If the male is watched, he can be seen to drag his butt along the floor of the cage somewhat as a dog infested with worms will do. During the test a sniffing or nibbling at the hair anywhere on the body of the female may be seen. The element is designated sniffing and nibbling.

In the guinea pig, in contrast to the rat, the single ejaculation usually marks the end of any strong interest in the female; in most tests it is accomplished within 10 minutes. If after ejaculation the first estrous female is replaced by a second, there may be a revival of interest (Grunt and Young, 1952c), but this feature of behavior has not entered into the determination of the strength of sexual behavior. Interest is also restimulated in the male monkey by the introduction of a second female (Carpenter, 1942a) and in the bull by a change of teasers (Cembrowicz, 1952; Almquist and Hale, 1956). The presence of a new estrous female does not have such an effect on a satiated male rat (Larsson, 1956) .

Ejaculation can be distinguished more easily in the guinea pig than in the rat; indeed it was not until 1934 that ejaculation was identified as a discrete element in the rat (Stone and Barker, 1934). As recently as 1946 Beach and Holz wrote, ejaculation referred solely to observable mating reactions," apparently without implication as to the discharge of seminal fluid.

These elements of the mating behavior pattern, along with the length of the interval between the beginning of the test and ejaculation in the guinea pig, are the end points that were used in the development of the scoring systems now prevalent in this country. The elements are given different values in an ascending order. In the rat the order is mounting and clasp-withoutpalpation, mounting and clasp-with-palpation and pelvic thrusts (referred to as attempts by Stone, Tomilin and Barker, 1935 and as incomplete copulation by Beach and Holz, 1946), copulation which consists of mounting, palpation and pelvic thrusts followed by the backward lunge signifying that intromission has occurred, and ejacidation. In the guinea pig the order is sniffing and nibbling, nuzzling, abortive mounting (scored as nuzzling), mounting, intromission, and ejaculation.

The ascending order is justified by the circumstance that in both species the elements tend to appear in this sequence during sexual maturation (Stone, 1924b ; Avery, 1925; Louttit, 1929; Webster and Young, 1951 j. Except for some cats given maximal sexual experience (Rosenblatt and Aronson, 1958a) , the order of disappearance following castration is the reverse of that during development in the rabbit (Stone, 1932a), hamster (Beach and Pauker, 1949), rat (Stone, 1939a; Beach, 1944b), and guinea pig (Grunt and Young, 1953). The sequence in which the elements reappear in the castrated male given androgen is the same as the order of appearance in the maturing animal (Stone, 1939a; Beach, 1944b; Grunt and Young, 1953).

In the laboratory at Kansas and elsewhere there has been concern that the same score can be achieved in more ways than one (Clark and Aronson, 1951 ; Valenstein, Riss and Young, 1954; Larsson, 1956). In studies of the guppy, the problem is complicated by the fact that excited males copulate with few or no preliminary acts; consequently, the most excited as well as the least excited individuals have low copulatory scores. During work with the male guinea pig it was found that subjects displaying little mounting and having only a few intromissions and possibly an ejaculation late in the test period often attain scores no higher than animals displaying much of only the lower measures of behavior. The possibility that this paradox might seriously lessen the validity of the scoring procedure has been checked. All the sexual behavior displayed during the tests was recorded (Riss, 1955) ; the average scores were then calculated and compared with the average quantity of each measure of behavior and the latency of ejaculation. Inspection of the table prepared by Riss reveals that both methods yielded rankorders that were essentially the same; consequently, the general accuracy of the older method is assumed. It is recommended, however, that in careful studies both methods should be used.

Soulairac (1952a), Soulairac and Coppin Monthillaud (1951), and Larsson (1956) in their work on the rat departed from the methods for estimating the strength of sexual behavior used by Stone, and by Beach during the first 10 to 15 years of his investigational activity. Sixty-minute rather than 10-minute tests were given and especial value was attached to the initial interval when the male displays no activity in the presence of the female, the number of intromissions preceding each ejaculation, the duration of each series of copulations, the intromissions per minute, the length of the refractory period following each ejaculation, and the number of ejaculations in 60 minutes.

Since the early 1950's, important changes in the procedure have been adopted by Beach and his associates (Beach and Jordan, 1956; Beach and Fowler, 1959). More recently similar procedures have been used in studies of the hamster (Beach and Rabedeau, 1959). Briefly, special observation cages and a recording system were devised. The latter consisted of three manually operated microswitches, each of which activates a marker which records on waxed paper pulled by a constant speed kymograph. Equally, if not more important, is the lengthening of the test until a criterion of sexual exhaustion has been met — in this case the lapse of 30 minutes without any mounting of the incentive female. Data contributing to six measures of sexual capacity are recorded: latency to the first intromission, frequency of ejaculation, intromissions per ejaculation, the frequency of mounts without intromission, the intercopulatory interval, and the postejaculatory interval.

Scoring procedures helpful in the selection of chickens and cattle for breeding have been devised by Wood-Gush and Osborne (1956) and Bane (1954), but will not be described here. They would be of value in endocrinological studies of behavior in these species.

Thus far in the discussion of patterns of behavior and scoring methods no reference has been made to the duality of "functions" or mechanisms" first noted by Craig (1918) and later given prominence by Nissen (1929), Beach (1942e, 1947, 1947-48, 1956, 1958), Soulairac (1952a-c), and Baerends, Brouwer and Waterbolk (1955). Not unrelated is the organic separation of activities associated with courtship and spawning which Clark, Aronson and Gordon (1954) felt may exist in the fishes they studied.

Nissen, obviously influenced by Moll (1897) and Gerhardt (1924), divided sexual "drive" into two behavior sequences, a contrectation drive which brings animals into the proximity of the sex object and, in rats, leads to nosing of the genitalia, gentle biting, and other sex play, and a detumescence drive which culminates in coitus.

Beach postulated that one of the two mechanisms is "erotic sensitivity" or the "susceptibility to sexual arousal." He thought of the arousal mechanism as being organized and functional in sexually inexperienced animals. It can be "conditioned" to a variety of nonsexual cues. "In male rats, cats, and dogs," he writes, "sexual arousal can be conditioned to new cues, but there is no evidence that females are similarly affected by experience." The sexual responsiveness of male primates is more labile and modifiable than that of male rodents and carnivores, and female primates differ from the females of lower species in that the arousal mechanism can be affected.

The other function is that of "potency" or the "capacity for sexual performance" ("mating responses" in Beach, 1947). It includes "the promptness with which mating is initiated, the frequency of copulation, and the rapidity with which ejaculation occurs." The function is mediated by what he calls the "executive" or "consummatory mechanism." It is thrown into action when sexual arousal reaches a threshold level. He continues: "The functional organization of the CM (consummatory mechanisms) is probably complete in inexperienced male and female rats, rabbits, dogs, and cats. The motor pattern of copulation is stereotyped and invariable, and is not materially altered by experience."

Development of the concept seems to have followed observations on the copulatory behavior of partially decorticate rats (Beach, 1940, 1944b, 1956). There was a proportional decrease in the percentage of tests in which copulatory behavior occurred, but the number of copulations during each positive test was not affected, even in the lesion group in which the percentage of postoperative copulators was lowest. As Beach interpreted the results, there had been a decrease in the ease of arousal to the point of the practical abolition of copulatory behavior, but without an effect on the actual copulatory pattern.

Experiments on the guinea pig (Valenstein, Riss and Young, 1955) have also provided evidence for dual functions, excitability, corresponding to susceptibility to sexual arousal, and the capacity for response corresponding to the capacity for sexual performance and depending on the existence of an organized neural pattern. The suggestion originated from the observation that an occasional male will achieve a complete copulation in only 1 or 2 of 10 tests with an estrous female, whereas in the other tests he will give the appearance of being generally indifferent. The capacity for the sexual response exists, but the level of excitability or arousal is so low that copulation usually does not occur. Under other conditions, excitability is shown, but no organized pattern is present and the male does not know how to copulate. Certain males brought up under conditions of isolation (see Table 19.3, groups II and IV) display excitability, but they lack an organized pattern and copulation is not achieved. In this respect the male guinea pig resembles the ringdove (Craig. 1914) and chimpanzee (Nissen, 1956) rather than the rat (Beach, 1958).

The place of the concept of duality of function in the present context is especially well indicated by Baerends, Brouwer and Waterbolk (1955) in their discussion of the structure of courting behavior of the male guppy, Lebistes reticulatus. The terms "appetitive behavior" and the "consummatory act" introduced by Craig (1918) are used. The former is variable in form and leads the animal toward the external situation necessary for evoking the consummatory act which is rigid and stereotyped. Craig reserved the term consummatory act for the final activity of definitive behavioral complexes and emphasized that after its performance appetitive behavior ceases and is succeeded by a state of relative rest. If the behavior of the male rat and guinea pig is placed within this frame of reference, the behavior leading up to ejaculation is appetitive; ejaculation, as the final act, is consummatory.

The concept of a duality of "function" has been described largely for purposes of clarification of terminology; it has not influenced the methods of scoring which are based on the display of the two functions as a sequence. The concept will be encountered again in the discussion of the role of the testis hormone in the display of sexual behavior (p. 1207), and in the presentation of the problem of the mechanism of hormone action (p. 1205).

The term "pseudofemale behavior" was coined by Morris (1954, 1955a) as a designation for feminine responses exhibited by males — presentation, squatting, lordosis, and others, depending on the species. Behavior of this sort is a part of the normal repertoire of many species and is displayed under a variety of conditions: by rhesus monkeys, rats, the lizard, Anolis carolinensis, and the ten-spined stickleback in the presence of aggressive males (Hamilton, 1914; Beach, 1939; Noble and Greenberg, 1941a; Carpenter, 1942b; Morris, 1952) ; by strongly excited male rats during mating tests (Stone, 1924a; Beach, 1945a) ; by sexually frustrated fish (Morris, 1952, 1955a) ; by sexually thwarted zebra finches (Morris, 1954); by fishes, pigeons, and hamsters in situations in which the stimulus was not apparent or at least not recorded (Riddle, 1924; Carpenter, 1933a; Beach, 1947; Schlosberg, Duncan and Daitch, 1949) ; and in newborn male guinea pigs (Boling, Blandau, Wilson and Young, 1939). At intervals of 2. 3, or 4 weeks, during a study of the stability of a conditioned breathing response to light, a formerly dominant male rabbit assumed the female role toward its two male partners (Brown, 1937). The display of feminine behavior has not entered into the scoring of males, but the frequency of its occurrence in the absence of any endocrine pathologic condition is of interest for the discussion of the determinants of patterns of sexual behavior given elsewhere (p. 1222).

In the domestic rat, but not in the wild Norway rat (Richter and Uhlenhuth, 1954), running is stimulated by testicular secretions, for after castration, decreases of 30 to 95 per cent occur (Hoskins, 1925a; Wang, Richter and Guttmacher, 1925; Heller, 1932; Richter, 1933). During the first 3 to 5 months of life, and possibly longer (Slonaker, 1912), the amount of activity rises; thereafter there is a gradual decline. Stone and Barker (1934) could find no significant relationship between the amount of running activity and the strength of sexual behavior as measured in direct tests or in an obstruction apparatus.

The differences between individuals of a species is a subject of universal comment. In the guinea pig and rat they are manifested by variations in the elements of the pattern and by variations in the scores. Some individuals ejaculate relatively soon after the beginning of a test and, in the guinea pig, without previous intromissions. In other animals ejaculation occurs later and is preceded by a number of intromissions. An occasional male will nuzzle and mount a female in heat, but in rej^eated 10-minute tests will not achieve ejaculation. Some animals of this type regularly require more time, others are not known ever to have copulated. The amount of running by apparently healthy males of the same age also varies greatly. It may be no more than a few hundred revolutions per day or it may be several thousand. In male cats conspicuous differences between individuals are seen in the pattern of decline in sexual behavior following castration (Rosenblatt and Aronson, 1958a).

The behavior characteristics of individuals tend to persist in rats and guinea pigs (Avery, 1925; Hitchcock, 1925; Stone, 1927; Stone, Tomilin and Barker, 1935; Stone, Ferguson and Wright, 1940; Stone and Ferguson, 1940; Shirley, 1928; Anderson, 1936; Beach, 1940, 1942g, 1944b; Soulairac, 1950; Young and Grunt, 1951 ; Grunt and Young, 1952b), chickens (Guhl, Collias and Allee, 1945; Wood-Gush and Osborne, 1956) , hamsters (Beach and Pauker, 1949), rabbits (Stone, 1932a), cats (Green, Clemente and


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de Groot, 1957), bulls (Hart, Mead and Regan, 1946), chimpanzees (Yerkes, 1939; Young and Orbison, 1944), and doubtless many other species. Usually they cannot be related to visible differences in the testes or to the quantity and quality of the semen (Lagerlof, 1954; Burrows and Titus, 1939; Beach, 1940; Young, 1949; Craig, Casida and Chapman, 1954; Wood-Gush and Osborne, 1956; Jakway and Young, 1958), although Rasmussen ( 1952) reported an inverse relationship between fertility and strength of sex drive in the rats he studied.

Differences in behavior are not necessarily related to the quantity of testicular hormone, provided a certain minimum is present. In an older study, examination of the accessory reproductive organs by techniques employed for hormone detection revealed that tlie relatively inactive rats in a group were actively secreting male hormone ( Heller, 1932). More recently it was found that the behavioral differences in male guinea pigs before castration continued to be displayed when the animals received equivalent amounts of testosterone propionate after castration (Grunt and Young, 1952b). This lack of correlation between patterns and the strength of mating behavior, and levels of gonadal hormones is suggestive with respect to the role of the hormones in the expression of mating behavior and is discussed elsewhere (p. 1199).

The extent to wdiich mating behavior in the male is dependent on testicular secretions cannot easily be deduced from the effects of castration. Their variation from species to species and from individual to individual of the same species is in fact so great that it has done much to nurture the doubt that gonadal hormones are the primary agents on which the sexual response depends (Kinsey, Pomeroy, Martin and Gebhard, 1953, p. 728 and elsewhere). The impact of the book (and the earlier volume on the male) on those not familiar with the experimental studies was such that a fairly detailed analysis of what has been found is given.

Courtship activity of the gobiid fish, Bathygobius soporator, was not reduced by castration, but the subjects became nondiscriminatory and courted males and gravid


and nongravid females in a like manner (Tavolga, 1955). A castrated salmon parr showed no interest in females (Jones and King, 1952). Male Hemichromis bimaculatus, on the other hand, exhibited typical movements of courtship and brooding for 202 days after castration (Noble and Kumpf , 1936) . During this time at least one male entered into as many as 13 successive spawnings with a normal female. Other males, castrated before the first spawning, took part in at least 11 successive spawnings in 146 days. At each spawning nuptial colors and genital tubes developed.

Male frogs castrated by Shapiro (1937a) displayed no signs of sexual activation when 70 per cent of the control animals were mating. Steinach (1894, 1910), on the other hand, reported that frogs displayed some degree of sexual behavior months after castration. The same articles contain reports of a diminished but nevertheless conscipuous sexual activity in male rats as much as a year after castration. The point may not be important, but it is recorded for what it is worth: the 1894 article, in which an interest was expressed in clinical observations on the sexual behavior of human castrates, emphasizes the retention of sexual behavior by castrates. The 1910 article, which seems to have been written out of a background of interest in the endocrine regulation of mating behavior, emphasizes the loss of lil)ido following castration.

The postcastrational behavior of several species of birds has been described. Complete castration of the pigeon did not prevent entirely the development of copulatory ability in all cases, but in others primary sexual activity was abolished (Carpenter, 1933a). The frequency of billing was reduced by castration, but it was eliminated in only 3 of 14 cases (Carpenter, 1933b). His results are taken to demonstrate "that the sexual hormones are of fundamental importance in predisposing sexual activity." Two of 16 gonadless pigeons "developed complete and emphatic masculine behavior" (Riddle, 1925) and he adds, "... it is clear, that the thing which is usually accomplished with the aid of the testis incretion may also be accomplished without it."

An incomplete and weak pattern of sex


HORMONES AND MATING BEHAVIOR


1181


ual behavior was displayed by two turkeys, castrated at 9 weeks of age (Scott and Payne, 1934). Sexual behavior is "wanting" in castrated ducks and roosters (Goodale, 1913, 1916b) , but elsewhere (Goodale, 1916a, 1918) it is evident that capons frecjuently crow and sometimes tread hens, although ordinarily these phases of the behavior of the cock are not manifested. Benoit (1929) stated that the capon normally shows no interest in hens, but one in which no testicular tissue could be found and which possessed a comb and wattles typical of the capon did tread hens. Domm (1927) referred to capons in his pens which crowed and trod hens, but when such individuals were examined small nodules of testicular tissue were found.

^^'llen articles dealing with mating behavior in castrated lower mammals are reviewed, the conclusions must be evaluated carefully. The significance of the statement that male guinea pigs castrated at 30 days of age have repeatedly been utilized as testers for estrous females (Moore, 1928; Moore and Gallagher, 1930) is lessened by the statement (Moore and Gallagher, 1930) that "such animals usually do not carry on copulation, but their pursuing instincts are still strong."

Display of the normal strength of copulation by the rat 4 months, 6 months, and 1 year after castration (Steinach, 1894) has not since been reported. To be sure, copulatory activity as long as 8 months after castration was recorded by Stone (1927), but "copulatory" denoted the overt elements of the copulatory response without indication as to insemination or intromission. In a later report (Stone, 1939a) the last ejaculation was seen 30 days after castration and the mean number of copulations at this time was 21.8 in 5 controls and 3.6 in 10 experimental animals.

The normally developed penis in the male guinea pig which retained its sexual ardor 6 months after castration (Guimarais. 1928) suggests there was androgenic stimulation. In a more recent study no such persistence of mating behavior was evident in any of 60 castrated males (Grunt and Young, 1953). Seward's (1940) statement that a prepuberally castrated guinea pig went through the


entire copulatory pattern ai)proximately a month after castration is not believed to constitute evidence for the postcastrational display of a strong sex drive. It is clear from the scale of sexual agressiveness he used and from what we now know about the sexual behavior of this species that intromission was not always distinguished and that ejaculation was not identified.

To the casual reader there is an ambiguity in the use of the word copulation which may have influenced our concepts of the effects of castration on lower mammals. Intromissions preceding ejaculation, and intromissions accompanied by ejaculation are a part of the complete masculine response, but in much of the work on the effects of castration, ejaculation was not the end point. In the articles on the rat before 1934, copulation was used without implication as to insemination (Stone, 1927) or even intromission in the case of castrated males. "Complete copulation" in the contemporary literature on the mating behavior of the rat does not include ejaculation. Mounting was an end point in a study of castration and replacement therapy in which the guinea pig was used (Sollenberger and Hamilton, 1939) , but reference was made to copulatory Ijehavior. For the careful reader, this use of copulation is not confusing, but for the hasty reader the effects of castration could easily be minimized, because the lower elements of the mating behavior pattern are influenced less by castration than are intromission and ejaculation (Stone, 1923, 1932a; Beach, 1944b; Beach and Pauker, 1949; Grunt and Young, 1953; Riss, Valenstein, Sinks and Young, 1955).

If allowance is made for the considerations discussed above, the investigations reported during the last 30 years are believed to lead to the conclusion that a gradual and conspicuous decrease in mating behavior follows the castration of such laboratory mammals as the rat, guinea pig, rabbit, hamster, and cat (Stone, 1923, 1927, 1932a, 1939a; Nissen, 1929; Beach, 1942d, 1944b; Beach and Holz, 1946; Beach and Pauker, 1949; Grunt and Young, 1952b, 1953; Green, Clemente and de Groot, 1957; Rosenblatt and Aronson, 1958a). The pattern of behavior still contains some of the mating reactions


1182


HORMONAL REGULATION


up to and including various degrees of mounting (Stone, 1927, 1932a; Beach, 1944b; Beacli and Holz, 1946; Grunt and Young, 1953 ) , but as the decrease in the score in one experiment indicates, the change is great, from an average of 7.8 in 290 tests before castration to an average of 2.0 in the tests of 29 animals 14 weeks after castration (Grunt and Young, 1952b).

Preliminary observations suggested that male dogs exhibit the full capacity for coitus and orgasm several months after castration (Beach, 1947-48). Subsequently (Beach, 1952), this extreme view was modified in a statement that the average sexual performance declines progressively after removal of the testes. Nevertheless, a real difference exists between the reaction of dogs and rodents to castration. Beach writes: "... nearly all animals retain some ability to penetrate the receptive bitch even two years after the operation. Furthermore, there are at least a few individuals in which there occurs no detectable loss of sexual responsiveness or ability to copulate. In point of fact some dogs are more vigorous and potent two years after castration than they were preoperatively."

The behavior of the boar is said to be "greatly altered" by castration (Wallace, 1949), but the descriptive account elsewhere in the article suggests that many elements of the mating behavior pattern are retained:

"One week after the operation there was a striking change in the animal's behaviour; from being excitable and one of the most ferocious of the boars, he was now sluggish, rather plaintive and exceedingly unwilling even to approach the dummy sow. After several attempts at the first trial he was forcibly driven and held right up to the dummy, when he mounted and mating reactions followed normally. In the next few weeks he fell again into the routine of collections, and though reluctant would always mount."

Parenthetically we would note that the interval necessary to drop the copulatory drive of the rabbit below the effective minimum for copulation varies directly with the strength of drive at the time of castration (Stone, 1932a) , and that castration depresses mating tendencies of the rat and hamster


least in tlie most vigorous copulators and most in the less active individuals (Beach, 1948; Beach and Pauker, 1949). Experience with the guinea pig has been different. The capacity for ejaculation is lost earlier by low score males, but when the average precastrational score was taken as 100 per cent and the subseciuent change as the percentage of variation from this level, the scores of the high, medium, and low score animals decreased at the same rate and to approximately the same base-line (Grunt and Young, 1953).

While discussing the effect of castration on the behavior of the rat and guinea pig, we would direct attention to data collected by Beach (1942d) and Grunt (1954). Beach described the intense excitement of prepubertally castrated and presumably sexually inexperienced male rats when confronted with a receptive female:

"They dashed wildly about the testing cage, often running in close circles around the female. Vigorous digging in the sawdust covering the cage floor was common. Some males lay on one side and moved all four legs in rapid running movements. Most of the males pursued the female, crowding her roughly against the cage walls, jumping over her and often landing directly upon her back. . . . The amount, intensity and duration of the sort of behavior described above appeared to be inversely related to the vigor and frec]uency of masculine copulatory responses."

Grunt has noted what may be a corresponding behavior during tests of castrated, sexually experienced male guinea pigs. The behavior, nondirected hyperexcitability , — not to be confused with the "state of agitation" described by Craig (1918) and Dell (1958) — is characterized liy a sudden straightening of the limbs, a jumping into the air, and frequently by a turning of the head. These actions occur suddenly and do not fit into any sequence of behavior usually seen. The excited movements seem to occur without reference to the female or to the other behavior exhibited during the test. The amount of the behavior increased as overt sexual behavior decreased. When such castrates were given 25 ju,g. or more testosterone propionate per 100 gm. body weight


HORMONES AND MATING BEHAVIOR


1183


daily the behavior decreased, whereas overt sexual behavior increased.

Relatively few castrated infrahmiuin i)rimates have been studied. Thorek (1924) castrated six male monkeys and reported that impotence set in gradually. About the end of 4 or 5 months all were sexually impotent and unable to react with an erection in the presence of females. A baboon, Papio hamadryas, was castrated by Zuckerman and Parkes (1939) in November, 1934. Until the middle of 1935, they wrote, he seemed aggressively masculine in his general and sexual behavior, but thereafter his attitude became more feminine. Beginning in November 1936, testosterone propionate was given weekly. From then on there was a considerable increase in the animal's vitality, aggressiveness, and sexual interest. The conclusion that "the development of sexual behavior in the prepuberally castrated chimpanzee is similar to that in the normal animal" (Clark, 1945) would be more convincing if data from systematic tests of the castrated male and control individuals had been presented. Even though no data are given, Zuckerman's comments in the discussion of a paper by Beach (1952) are relevant :

"I recall some experiments of my own — I am afraid the details escape me now — on a male drill, and on a few male rhesus monkeys, which suggested that after castration sexual activity declined rather consideral)ly. In the case of the drill I certainly remember that its sexuality became intensified after injection of androgen. The other thing I remember is that the intact adult male chimpanzee may occasionally manifest weak sexuality."

A conspicuous feature of many of the studies reviewed above is that the behavioral changes following castration are not as immediate as the changes in the accessories. Hypotheses have been advanced to account for this fact by Steinach (1894), Nissen (1929), and Beach (1942e, 1944a). The essential similarity of those proposed by Steinach and Beach is a reminder that there is probably no other phase of the problem of the hormones and mating behavior in which our progress in that time has been so negligible.


"Dementsprechend wiirde sich die Thatsache, dass das Begattungsvermogen beim Menschen und, wie wir sahen, auch bei cler Ratte monatelang nach der Castration unveriindert erhalten bleibt, durch den Umstand erklaren, dass die zur Zeit gesteigerte Erregbarkeit der betreffenden Centralorgane den Ausfall der von den Keimdriisen zufieissenden Impulse iiberdauert und erst nach liingerem Fortbestehen ganz allmiihlich abklingt" (Steinach, 1894, p. 338).

"Since testicular hormones are probably dissipated within a few days after castration, the more prolonged survival of sexual responsiveness is best explained on the basis of a relatively enduring change in the nervous system. It may be suggested that once the c.e.m. (central excitatory mechanism) has been sensitized by androgen, this neural mechanism remains in an excitable state for some time after the responsible hormones are withdrawn. In the absence of testicular androgens the essential central nervous elements gradually lose their responsiveness" (Beach, 1944a, p. 130).

Nissen 's hypothesis contains inconsistencies, •'* but is mentioned here because of the emphasis subsequent workers (Carter, Cohen and Shorr, 1947; Lehrman, 1956;-^ Rosenblatt and Aronson, 1958a ) have placed on the possibility that gonadal hormones exert their action through peripheral rather than central nervous structures. The gradual decrease in sexual behavior in the male, he postulates, is associated with tlie gradual loss in the capacity of the penis for tumescence, and thus in the capacity for initiating the sensory impulses resulting in sexual l)ehavior.

A hypothesis entirely different from those advanced by Steinach, Nissen, and Beach

-'The postcastrational changes in the uterine or \aginal cpitheHum which Nissen postulated may mediate sexual behavior in the female, must have been presumed to be rapid because he was aware that the changes in behavior following ovariectomy are immediate. However, he cited no histologic evidence, and the writer knows of no evidence, that what he calls "interpolated structures" atrophy more rapidly in the spayed female than in the castrated male.

Lehrman's \-iew expressed in 1956 has been modified. See his tiioughtfully prepared discussion in his chapter in this hook.


1184


HORMONAL REGULATION


followed the discovery that the adrenal cortex is a source of androgenic substances. The suggestion was made that such androgen compensates for the loss of testicular androgen following castration (Sollenberger and Hamilton, 1939; Spiegel, 1939; Hamilton, 1943a). Supporting evidence, however, has not been advanced. On the contrary, castrate men are found in which urinary titers are very low (Hamilton, 1943b). The level of sexual activity attained by prepuberally castrated male hamsters was not lower in animals that w^ere castrated and adrenalectomized (Warren and Aronson, 1957). In two experimental studies the postcastrational sexual behavior of the adult male dog and hamster was not altered further by adrenalectomy (Schwartz and Beach, 1954; Warren and Aronson, 1956). Neither desoxycorticosterone acetate nor cortisone substituted for testosterone in the restoration of mating behavior in the castrated male cat (Green, Clemente and de Groot, 1957). Also in the male cat, the persistence of sexual behavior after castration could not be attributed to any androgens secreted by the adrenal cortex ( Gooper and Aronson, 1958).

As in other fields of endocrinologic study, investigators interested in the hormonal control of mating behavior turned from experiments involving ablation of the organs thought to be involved to replacement therapy. Gonad transplantation, the administration of crude extracts, and treatment with chemically purified and synthetic hormones were attempted. The results following gonad transplantation and the use of crude extracts are largely of historical interest and are summarized in the older reviews. The discussion which follows is limited to the results obtained after administration of the synthetic androgens, for the most part, testosterone propionate.

In general, claims of the effectiveness of testosterone propionate have been advanced with fewer reservations than those with respect to the effects of castration. Infrequent injections into male salmon parr were only partly effective in restoring the pattern of behavior in castrates (Jones and King, 1954). On the other hand, the full pattern


of Ijehavior was induced in young male guppies by treatment with pregneninolone or testosterone (Eversole, 1941). Daily injections of testosterone propionate or acetate were effective in castrated cockerels (Roussel, 1936; Davis and Domm, 1943), rats (Shapiro, 1937b; Moore and Price, 1938; Stone, 1939a; Beach, 1944b; Beach and Holzi-Tucker, 1949), rabbits (De Fremery and Tausk, 1937), and guinea pigs (Moore and Price, 1938; Grunt and Young, 1952b). AVhen castration was performed several weeks or months before the beginning of replacement therapy, 4.5 to 8.9 mg. restored copulatory ability in the rat, and 150 mg. did so in the rabbit. When rats were castrated and injected daily beginning 48 hours later, 50 to 75 /^g. of testosterone l)roiiionate were sufficient for the maintenance of most of the measures of sexual behavior at the precastrational level. After the attainment of this level by injected, castrated guinea pigs at the end of the 8 weeks, 25 /xg. per 100 gm. body weight per day was more than a maintenance dose.

Results obtained by Grunt and Young (1952b, 1953) suggested new concepts of the role of testicular hormone in the maintenance of male sexual behavior. As we have noted (p. 1179), every colony of animals contains males showing different degrees of sexual performance. The point was made the ol)ject of an experiment in which males were divided into high, medium, and low score groups on the basis of their performance in 10 preliminary tests. They were then castrated and, after the regressive changes had reached a base-line, injected daily with 25 fjug. hormone per 100 gm. body weight. It was found that individuals characteristically high, medium, or low score before gonadectomy returned to the corresponding level during the period of replacement therapy. Hormone injections of 50, 75, and 100 ;u.g. per 100 gm. body weight daily were no more stimulating to sexual behavior than the smaller quantity. Subsequently, 8 low" score males were injected daily for 30 days with 500 /xg. testosterone propionate per 100 gm. body weight, but not even this large amount raised the level of the animals' performance above that dur


HORMONES AND MATING BEHAVIOR


1185


ing the pretreatmcnt jicriod (Kiss and Young, 1954) .« 

These data from the niah' guiiK'a i)ig, especially when they are considered against the background of information collected from the female (p. 1190), from the experiments on the action of heterosexual hormones in other species (p. 1198), and from studies of the effects of certain drugs on behavior patterns of the rat (Soulairac and Coppin-]\Ionthillaud, 1951 ) , supjiort the hyl)othesis that a somatic or constitutional factor limits the action of the hormone, and accounts for the differences displayed during the precastrational period. As Grunt anrl Young (1952b) visualized the situation, animals in their reactivity to testosterone propionate could be likened to an exposed but undeveloped photographic film or plate, the hormone to the developer. The pattern of behavior or picture" that would be brought out by the hormone would depend on wdiat had been taken; with this the character of

"Elsewhere (Young, 1954), attention is directed to the striking parallel between the reaction of male guinea pigs to testosterone propionate and the recorded reactions of patients receiving corticotrophin or cortisone. The susceptibility of persons to these substances is subject to much variation and does not seem to bear a direct relation to dosage or the length of time during which the drugs are administered, apart from the fact that there seems to be an ill defined threshold which must be exceeded before mental symptoms can be expected (Trethowan and Cobb, 1952). It is emphasized also that the major psychic alterations which develop under the influence of corticotrophin and cortisone represent, in most instances, intensification of pre-existing disorders of personality (Rome and Braceland, 1950, 1951, 1952), or were determined, at least, by jjrevious personality patterns (Fox and Gifford, 1953; Gifford, 1953). Observations by Cleghorn (1952) and by Goolkes and Schein (1953), on the other hand, suggest that the parallel is coincidental. Until the problem has been resohed, the possibility that basically similar relationships exist in the response to gonadal hormones and cortisone should not be overlooked. Of intere.st in connection with the reaction to adrenal cortical steroids, is tlie observation (Moog, 1953) that the experimental niaxiiiiuiii of alkaline phosphatase in the duodenal wall of the mouse did not rise after an 18day maximum was reached, even when the dosage of cortisone was increased 3-fold. The fact is taken to indicate that the rate at which the enzymesynthesizing mechanism operates and the extent to which it proceeds are controlled by the reacting tissue.


the soma was held to be analogous. The amount of hormone or "developer," provided a certain minimum or threshold (defined in this case as the smallest amount of hormone that will restore sexual behavior to the precastrational level) was present, would be of no consequence.

The hy])othesis that the action of testosterone propionate on the tissues mediating sexual behavior" is limited by the responsiveness of the tissues and that excessive quantities are without effect has implications for the frequently expressed view that a direct relationship exists between the amoimt of circulating androgen and the strength of sexual behavior. The former hypothesis was suggested by what was seen following the injection of an androgen into the guinea pig. The latter opinion is sujiported by reports that supplementary androgen administered to intact rats and ral)bits tends to increase the amount of sexual behavior (Stone, 1938; Beach, 1940, 1942e, 1942h, 1947; Cheng and Casida, 1949; Cheng, Ulberg, Christian and Casida, 1950; Kagan and Beach, 1953; Craig, Casida and Chapman, 1954), and that a quantity of testosterone propionate greater than that required to restore the normal level of mating activity in castrates increased the strength of behavior beyond this level (Beach and Holz-Tucker, 1949).

Within the last year there has been some modification of this view. The results from an investigation in which there was a comparison of the ])re- and postcastrational sexual activity of male rats receiving the same amount of androgen per animal postoperatively were taken to indicate that some of the individual differences shown by castrated males were due in part to differences in the hormone dosages, but that the rela ■ Ovn- use of the term "tissues mediating mating beha\ior" is frankly ambiguous and requires exphmation. VVlen (he role of the gonadal hormones is "acti\'ational" as it is in the adult, we think of them as acting on the nervous tissues and possibly on the muscular tissues participating in the display of mating behavior. If the role is "organizational," as it may be during the embryonic and fetal ])eriods (p. 1222), the action is presumed to be on the neural centers that later become invohed in the display of mating behavior.


1186


HORMONAL REGULATION


tively small differences in androgen level did not account for all the variance between castrates (Beach and Fowler, 1959).

To the extent that they exist, the differences between the rat and guinea pig could be one of species. A point is made of this in a recent study in which a long experience with the response of individual muscles and other tissues and organs of male guinea pigs to testosterone propionate is summarized (Kochakian and Cockrell, 1958). The stronger than normal responses displayed by the rat, mouse, and hamster are not encountered in the guinea pig. The latter species apparently possesses some mechanism or mechanisms to protect it from large amounts of androgen. A corresponding difference in the effect of testosterone propionate on the sexual maturation of the two species has also been noted (derail, 1958) .

The efforts to restore noi'mal running activity in castrated male rats have yielded results unlike those obtained during efforts to restore mating behavior. In 15 experiments with castrated rats and in 3 with senile rats, testis grafts and the injection of macerated testicular tissue did not bring about any significant improvement in activity (Hoskins, 1925b). Bull testis extract given during a 15-day period was without consistent effect in 9 intact and 4 castrated animals (Heller, 1932). Richter and Wislocki (1928), on the other hand, transplanted testes into the recti muscles and wall of the scrotum and found that, when the grafts became vascularized and "took," an increase in activity occurred, but the increase was much less than that seen by Wang, Richter and Guttmacher (1925) following the transplantation of ovaries into castrated males. The latter result appears to be anomalous, but more recently quantities of testosterone propionate up to 25 mg. did not increase the bodily activity of 9 senile males (Hoskins, Levene and Bevin, 1939), whereas estriol glucuronide and two other estrogens fed to senile male rats 3 to 7 times a week for 3 to 5 weeks were generally effective in augmenting activity (Hoskins and Bevin, 1940). The suggestion which comes from these studies is that running activity in the male is induced by estro


gens as it is in the female (Richter and Hartman, 1934; Young and Fish, 1945).

B. THE FEMALE

As in the male, an understanding of the relationship between the hormones and mating behavior depends on a knowledge of the behavior. In fishes, and apparently in aml)hit)ians (Noble and Aronson, 1942), mating behavior in the female is largely in the nature of a passive response. Indicators of receptivity are noted (Schlosberg, Duncan and Daitch, 1949; Clark and Aronson, 1951 ; Baerends, Brouwer and Waterbolk, 1955; Morris, 1955b), but sharp end points have not been described. Birds and mammals are different. In the latter especially mating or estrous behavior is well defined. It includes some form of presentation or lordosis, frecjuently a male-like mounting of other animals with or without copulatory thrusts, and, especially in the rat, a great increase in running activity. Although the point has not been checked by comparable observations of the two sexes, records of the display of masculine sexual behavior by female mammals give the impression that it is displayed more commonly than is feminine behavior by males (Beach, 1947). This is certainly true in the guinea pig and a similar difference between the sexes has been noted in fishes (Morris, 1955a).

Not every species displays the three types of estrous behavior. The rat and domestic pig (Altmann, 1941 ) do so, but cyclic running activity as such has not been identified in the guinea pig. It is probable, if our knowledge of other species were more complete, that an increase in general activity, if not in running activity, would be found to be associated with the mating period. The restless, irritable, and explorative behavior conspicuous in the estrous rhesus monkey (Gari)enter, 1942a j is an example.

In studies of the guinea pig and rat quantitative estimates of the duration of heat have been made by recording the length of time lordosis can be elicited in response to fingering (Young, Dempsey, Hagquist and Boling, 1937, 1939; Blandau, Boling and Young, 1941). The average duration of the single lordosis and the interval from the first lordosis to the longest lordosis are re


HORMONES AND MATING BEHAVIOR


1187


cent additions to the information collected at the time of estrus (Goy and Young, 1957b). When the rat has been used there has been a numerical evaluation of the responses such as lordosis, quivering of the ears, darting, and crouching when the female is approached by the male or fingered (Ball, 1937b), or the calculation of a quotient, the copulatory quotient, which is the number of lordosis responses divided by the number of times the female was mounted by the male multiplied by 100 (Beach, 1944c). In a study of the female rabbit the nvmiber of successful matings was divided by the attempts made by the male. A proportion was obtained which could be plotted for each day (Klein, 1952). Receptivity of the female cat can be assessed by daily 10minute mating tests with especially trained males. The end point chosen for quantitative assessment of the behavioral change was the first occurrence of full mating accompanied by the presence of sperm in the vaginal smear (Michael and Scott, 1957) .

Mounting, or pseudomale behavior, as Morris (1955a) calls it, is measured in the guinea pig by watching animals known to be about to come into heat and counting the number of times individuals mount other animals (Young and Rundlett, 1939; Goy and Young, 1957b) , and in the rat by dividing the sum of points obtained in a test by the duration of the test (Koster, 1943).

Running activity, the first of the elements of female sexual behavior to be studied (Slonaker, 1912), has long been measured by means of activity wheels. That developed by Farris (1941) is probably the most elaborate. The number of revolutions of a turntable is registered by a magnetic counter which is photographed at selected intervals by a time-lapse mechanism. Total activity including restlessness is better measured by stabilimeter cages in which any movement of the animal rocks the cage in a motion which is recorded (Richter, 1927; Wilbur, 1936; Hunt and Schlosberg, 1939; Smith, 1940; Bousfield and Mote, 1943; Eayrs, 1954). Eayrs pointed out that, although both types of apparatus are believed to measure the same thing, the two techniques measure components of activity having different motivational siiinificanco.


The temporal relationships between lordosis, male-like mounting, and running activity are generally close because in lower mammals all are displayed near the time of ovulation. The quantitative relationships are not close. Some rats are relatively inactive at the time of estrus (Hitchcock, 1925; Stone and Barker, 1934). Male-like mounting in guinea pigs is variable (Avery, 1925), but the amount is not related to the duration of estrus (Young, Dempsey and Myers, 1935; Young, Dempsey, Hagquist and Boling, 1939). The variability within each type of behavior has the effect of creating differences between individual females that are fully as striking as those between males (Hitchcock, 1925, Young and Fish, 1945, for running activity in the female rat; Young, Dempsey and Myers, 1935, Young, Dempsey, Hagquist and Boling, 1939, for the length of heat and the amount of mounting activity in the guinea pig; Blandau, Boling and Young, 1941, for the length of heat in the rat; Young and Orbison, 1944, for the character of sexual responses in the chimpanzee; de Alba and Asdell, 1946, for the strength of heat in the cow; JMichael, 1958, for the behavior patterns in the female cat).

The length of heat in the guinea pig is not related to the number of developing follicles (Young, Myers and Dempsey, 1933) or to the ovarian condition, at least, within the limits of the ovarian pathology encountered by Young, Dempsey, Myers and Hagquist (1938). Nor is the estrone content of the follicular fluid necessarily related to the degree of sexual desire in the mare (Andrews and McKenzie, 1941). In what appears to be the single study in which such data were collected, male-like mounting was generally proportional to the number of developing follicles (Young, Dempsey, Myers and Hagquist, 1938), although numerous exceptions were found. Cystic follicles frequently occur in nvmphomanic cattle (Pearl and Surface, 1915; Calder, 1927; Hammond, 1927; Fernandez, 1940; Walton, Edwards and Hammond, 1940), although not all cows with cystic ovaries are nymphomanic (Casida, ]\IcShan and Meyer, 1944).

The absence of estrous behavior follow


1188


HORMONAL REGULATION


ing ovariectomy provides convincing evidence for the importance of this organ in lower mammals and in the infrahuman primates which have been studied (Ball, 1936; Robson, 1938; Young and Orbison, 1944). The experiments of Allen and Doisy (1923) demonstrated that substances within the Graafian follicle are directly responsible, but a more complete understanding of the nature of the relationship was obtained after purified preparations became available. It was then shown that the display of the copulatory response and male-like mounting by ovariectomized guinea pigs depends on the subcutaneous^ injection of a relatively small quantity of an estrogen followed after an interval by the injection of a small amount of progesterone (Dempsey, Hertz and Young, 1936; Young and Rundlett, 1939 ». An atypical response sometimes follows injection of the estrogen, but restoration of the behavior characteristic of the individual before ovariectomy depends on supplementary treatment with progesterone (Boling, Young and Dempsey, 1938). Although in different proportions, the same combination of hormones was later found necessary for the stimulation of estrus in the rat (Boling and Blandau, 1939; Beach, 1942a), mouse (Ring, 1944), hamster (Frank and Fraps, 1945; Kent and Liberman, 1947), and cow (Melampy, Emmerson, Rakes, Hanka and Eness, 1957). Even in the rabbit, a species in which the preovulatory swelling and ovulation depend on the stimulation of coj)ulation, there is a brief period when an injection of progesterone will heighten the degree of estrus in an already moderately

  • For the estrogens, and possibly for progesterone, the manner of injection is important. Intraperitoneal injections of an estrogen into female guinea pigs in amounts that are sufficient

when given subcutaneously are generally ineffective. When a divided dose of an estrogen given subcutaneously was followed by an intravenous injection of water-soluble estrone and subcutaneously administered progesterone, the length of heat was 15.7 hours compared with 9.3 hours in the estrogen-conditioned animals injected only with progesterone (Collins, Boling, Dempsey and Young, 1938). Differences in the manner of injection which are not always clear from the published articles make comparison difficult. This circumstance must be kept in mind in the remarks which follow.


estrous animal (Sawyer and Everett, 1959). In the four small mammals the amount of estradiol benzoate necessary to condition the animals for heat varies from 5 to 33 R.U., the amount of progesterone that will bring such animals into heat is from 0.05 to 0.4 mg. (Table 19.1). In contrast to the male which requires numerous daily injections for the restoration of normal mating behavior, the female is brought into heat by single injections of each hormone given 24 to 38 hours apart.

When the response of the female guinea l)ig to estrqgen and progesterone was being studied it was clearly apparent that the amounts of these substances sufficient to induce a vigorous lordosis and mounting behavior were not stimulating normal estrous vaginal changes and that the females would not accept the males. It was later found that stimulation of the vaginal changes characteristic of heat in intact females required treatment with larger quantities of estrogen given over a period of 72 hours followed by progesterone (Ford and Young, 1951). De])ending on the animal, some adjustment of the amounts of hormone and intervals may be necessary, but when such a procedure is employed spayed animals will accept the male. Of especial interest for experimental studies, is the demonstration by Larsson (1957) that the sexual activity of the male rat is not influenced by the way estrus is induced in the female, i.e., whether it is by

TABLE 19.1

Amounts of estrogen and progesterone required for the induction of sexual receptivity



a;




Species


li


si


References



rn« 


R




p^




R.U.


mg



Guinea pig. .


5


0.1


Dempsey, Hertz and Young (193()); Hertz, Meyer and Spiel man (1937); Collins, Boling, Dempsey and Young (1938)


Rat


10


0.4


Boling and Blandau (1939)


Mouse


10


0.05


Ring (1944)


Hamster. . .


33 0.05


Frank and Fraps (1945)


HORMONES AND MATING BEHAVIOR


1189


hormones received endogenously or exogenously.

In connection with the above described findings in the guinea pig, i.e., the apparent relatively higher threshold of vaginal epithelium to estrogenic stimulation, and the dependence of cornification on a small amount of progesterone, three observations on other species should be noted here. In the ewe the hormonal recjuirements for the vaginal changes characteristic of estrus and the behavior changes are about the same (Robinson, Moore and Binet, 1956). In the cat vaginal cornification does not seem to be dependent on progesterone (Ford, 1954). In the cat, in experiments with amounts of two estrogens below 12 /tg. per day, at which dosage the latent period to mating exceeded 7 days, the appearance of a fully cornified vaginal smear invariably preceded the mating response (Michael and Scott, 1957; Harris, Michael and Scott, 1958) . At high dose levels the occurrence of mating preceded the vaginal smear change by about 24 hours. A comparison of the vaginal and central nervous system thresholds to estrogenic stimulation must await the results from measurements of the mean rate of release at these sites which these investigators appear to have undertaken.

Estrogen and progesterone participate in the induction of heat in the ewe, but the sequence is different from that in rodents. It is clear from studies of ewes at the beginning of the breeding season (Schinckel, 1954a, b), from studies of anestrous ewes given pregnant mare serum (PMS) and progesterone (Dutt, 1953; Robinson, 1954b) , and from experiments on spayed ewes given estrogen and jirogesterone (Robinson, 1954a, 1955; Robinson, Moore and Binet, 1956) that normal heat behavior is not displayed unless treatment with an estrogen of endogenous or exogenous origin is preceded by progesterone. Progesterone, 12.5 mg., twice daily for 3 days followed 2 days later by 1000 I.U. of PMS was an optimal treatment when anestrous ewes were used (Robinson, 1954b). When the effectiveness of progesterone and estradiol was tested on spayed ewes, 75 mg. of progesterone given in 6 injections over 3 days followed 2 days later by 38 jug. of estradiol induced heat in


90% of the injected animals (Robinson, 1955 ».

Except that estrogen and progesterone act together in the induction of heat in laboratory rodents, the cow, and the ewe, the processes whereby this end is achieved are not known. The subject is discussed in the section on the mechanism of hormone action (p. 1204) where the important studies of Sawyer and Markee (1959), Sawyer and p]verett (1959), and Kawakami and Sawyer ( 1959a, b) are related to the problem. What might be thought of as a complication is that progesterone terminates estrus in the ral)bit (Makepeace, Weinstein and Friedman, 1937; Sawyer and Everett, 1959), ferret (Marshall and Hammond Jr., 1945), sheep and goat (Phillips, Fraps and Frank, 1946), reduces the estrogen-induced sexual activity of the rhesus monkey (Ball, 1941a) , antagonizes the effect of estradiol on spayed gilts (Day, Anderson, Hazel and Melampy, 1959), and, in large doses, antagonizes the action of estrogen in ovariectomized cows (Melampy, Emmerson, Rakes, Hanka and Eness, 1957). We cannot reconcile such actions with its role as a priming substance in the ewe beginning with the ovulation preceding heat. Sawyer and Everett (1959), citing the study by Dutt (1953), refer to such an estrus as one "that appears on the 'rebound' from progesterone treatment."

The termination of estrus by progesterone is not inconsistent with its action in helping to stimulate heat. In the guinea pig, rat, mouse, hamster, and cow the small amount of progesterone produced in the developing follicle about the beginning of the preovulatory swelling touches off the estrus-mechanism, but the larger amounts produced about the time of ovulation may be inhibitory. Experimental evidence supporting this view has recently been ]irovided by Sawyer and Everett (1959) and by Kawakami and Sawyer ( 1959a ) in their investigations which are reviewed in more detail elsewhere (p. 1206).

A purified estrogen alone or an estrogenic substance is said to be sufficient for the stimulation of mating reactions in ovariectomized cats (Bard, 1939; Maes, 1939; Michael and Scott. 1957; Harris, Michael and Scott, 1958), dogs (Kunde, D'Amour, Carlson and


1190


HORMONAL REGULATION


Gustavson, 1930; Robson and Henderson, 1936; Robson, 1938; Leathern, 1938), ferrets (Marshall and Hammond, Jr., 1945), goats (Phillips, Fraps and Frank, 1946) , and monkeys (Ball, 1936; Hartman, 1938). This could be taken to indicate that progesterone is not involved in the induction of sexual receptivity in these species.

Theoretically, there is no reason why estrogens alone should not be sufficient, but for several of these species an important point has yet to be checked. Until the character of the behavior induced by the estrogen has been shown to be identical or nearly identical with that displayed before ovariectomy, the possibility of action by a small amount of progesterone should not be excluded. Of the investigators mentioned above. Bard appears to be the only one who compared the behavior following treatment with that before ovariectomy. He states that 2000 Allen-Doisy R.U. of estradiol benzoate were sufficient to throw many cats into full heat and that the estrus induced in this way was in every respect the same as that which occurs spontaneously. He never encountered a cat in which full estrus could not be provoked by giving estradiol benzoate or some other form of estrin.

When the hormonal induction of mating behavior in the male was being described, it was pointed out that individuals which were characteristically high, medium, or low score before castration returned to the corresponding level during the period of replacement therapy, whether the amount of injected testosterone propionate was 25 or 500 yug. per 100 gm. body weight per day. During studies in which the hormonal induction of estrous behavior in ovariectomized females was being investigated, some attention was given to the character of the behavior following repeated injections, although the experiments were not as systematic as those on the male. Nevertheless, the tendency for a particular type of response to recur was revealed when the length of estrus and the character of the lordosis were being recorded (Boling, Young and Dempsey, 1938; Goy and Young, 1957b) , when mounting behavior was being studied (Young and Rundlett, 1939), and during an investigation of


the hormonal control of running activity (Young and Fish, 1945).

Despite an earlier report to the contrary (Collins, Boling, Dempsey and Young,, 1938), and the fact that the length of heat in the female guinea pig is not related to the number of developing follicles (Young, Myers and Dempsey, 1933; Young, Dempsey, Myers and Hagcjuist, 1938) , Goy and Young (1957b) found that the length of heat in sjiayed injected animals is related to the conditioning quantity of estrogen. However, this lengthening was made by the addition of weak responses without any alteration in the intensity curves; consecjuently, the increase in the duration of estrus may not represent a prolongation of the period of receptivity to the male. Other data obtained during the same experiment are consistent with this suggestion. Tentatively, therefore, the guinea pig seems to be a species in which large quantities of male and female hormones are not more stimulating to sexual l)eiiavior than threshold amounts.

The hormonal basis for male-like mounting is in need of clarification. This behavior coincides closely with estrus in many species and is generally thought to be stimulated by the ovarian hormones present at this time (Hamilton, 1914, Carpenter, 1942b, for the rhesus monkey; Corner, 1921, McKenzie, 1926, Altmann, 1941, for the pig; Williams, 1921, Hammond, 1927, for the cow; Long and Evans, 1922, Hemmingsen, 1933, Beach, 1938, 1942f, Ball, 1940, for the rat; Hammond, 1925, for the rabbit; Loeb, 1914, Avery, 1925, Louttit, 1927; Young, Dempsey and Myers, 1935, for the guinea pig; Yerkes, 1939, for the chimpanzee; Markley and Bassett, 1942, for the marten; Pearson, 1944, for the shrew; Shadle, 1946, for the porcupine; Beach, 1947, for the dog and cat. It is exhibited by some apparently normal chickens (Domm, 1947; Guhl, 1949) and turkeys (Hale, 1955).

Uncertainty with respect to the hormonal basis of mounting behavior is introduced by the fact that such behavior is seen under a variety of conditions. In the guinea pig it is easily induced by injections of estrogen and progesterone (Young and Rundlett, 1939) except in a strain in which it is not displayed spontaneously (Goy and Young, 1957b).


HORMONES AND MATING BEHAVIOR


1191


Tablets of stilbestrol dipropionate or estradiol were effective incitants in intact cows and heifers unless a functioning corpus luteum was present (Hammond, Jr., and Day, 1944). Male-like behavior is displayed at other times than at estrus by cows with ovaries containing cystic follicles or that are otherwise diseased (Pearl and Surface, 1915; Calder, 1927; Fernandez, 1940; Casida, McShan and Meyer, 1944; Garm, 1949; Wayman and Asdell, 1952), by apparently healthy cows which are not in heat when they are mounted by estrous cows (Weber, 1911; Hammond, 1927; de Alba and Asdell, 1946; Roark and Herman, 1950), and by an anestrous ewe which had not been brought into heat following treatment with pregnant mare serum and testosterone (Cole, Hart and ]\liller, 1945). On two occasions an anestrous lioness (female B) performed the gross coital movements of the male after an estrous animal (female A) had forced herself under B's body (Cooper, 1942). Gassner (1952), in contrast to Garm (1949), doubts that nymphomania in cows is a consequence of hyperestrogenism; he suggests that it is caused by certain metabolites of an androgenic nature secreted by the ovary or, more likely, by the adrenal cortex.

The problem is further complicated by results which led Beach and Rasquin (1942) to express doubt that mounting behavior by the female rat is stimulated by ovarian hormones. They presented evidence (1) that masculine copulatory reactions are exhibited by intact females with equal frequency at all stages of the estrous cycle, (2) that ovariectomy prepuberally or during adulthood eliminated receptive behavior, but had no obvious effect on the execution of the male pattern, and (3) that injection of estrogen and progesterone into spayed females revived receptivity without altering masculine behavior. In the same year Beach (1942b) reported that testosterone propionate increased the masculine reactions of females 95 per cent; consequently, as far as this hormone is concerned, an influence on the display of masculine behavior l)y the female is not questioned.

As matters stand, the necessity for androgens need not be invoked to account for the male-like mounting disi)layed so commonly


by the female guinea pig. The rat is responsive to exogenous androgen but does not require hormones of ovarian origin. The cow requires some hormone of ovarian or adrenal origin, but, in the opinion of Gassner, probably a metabolite of androgenic nature having its origin in the adrenal cortex. Hammond, Jr., and Day (1944) found, however, that estrogenic substances were effective stimulants of masculine behavior by cows. Reconciliation of the diverse observations may not be easy, but it should not be impossible.

Investigations of running activity have been limited to the rat; consequently, what is said with respect to its hormonal control applies with certainty only to this species. In contrast to the experience when the hormonal requirements of the mating response were being studied (Boling and Blandau, 1939; Beach, 1942a), single injections of estradiol benzoate with or without progesterone were ineffective (Young and Fish, 1945) . On the other hand, the addition of human pregnancy urine to the drinking water, daily injections of estrone, or the implantation of pellets of estrone restored activity to a level only slightly below that displayed before ovariectomy (Richter and Hartman, 1934; Young and Fish, 1945). For some reason, when pellets of estrone were implanted the activity tended to be cyclic, even though the amount absorbed from day to day must have been nearly uniform. In a recent personal communication. Dr. Ernst Barany of the Department of Pharmacology, Uppsala, has written that running activity was increased in some spayed female rats when 0.5 fxg. of estradiol benzoate was given in a single injection; 5 or 10 fxg. seem to have been more effective. Latency was always about 48 hours. Estrone was not more active weight for weight than estradiol. Explanation should be sought for what appear to be contradictory results.

A consideration of the data bearing on the hormonal regulation of mating behavior in the female suggests the following generalization. Displa^^ of the three types of estrous behavior, the copulatory response, male-like mounting, and running activity, is induced by the gonadal hormones, and possibly, in the case of running activity in the wild Norway rat (Richter and Uhlenhuth, 1954) and mounting behavior in the cow (Gassner, 1952), by substances of adrenal cortical origin. The lack of a direct quantitative relationship between the components of the total pattern is believed to be accounted for by the existence of different mechanisms, each of which has its own threshold or level of responsiveness to the hormone or combination of hormones for which it is a target organ. Often within individuals this reactivity is remarkably constant, for following ovariectomy and replacement therapy with the appropriate hormones, each type of behavior tends to be displayed in the amount shown before the operation.

The relationship between estrus and the time of follicular growth and ovulation is summarized in the writer's earlier review (Young, 1941). It is sufficient to note here that in spontaneously ovulating mammals below the primates mating behavior usually is restricted to the hours or days preceding or immediately after ovulation. The occasional cow may be an exception. Folley (1952) states: "Provided a cow will stand quietly in stocks, the bull will mount at any time during the oestrous cycle and the cow will allow that." According to Burger (1952), sows not in heat will "ride" proestrous penmates. When ovulation is dependent on the stimulus of copulation as in the rabbit, cat, and ferret, indications are that heat does not occur unless large follicles ready for the preovulatory swelling are present (Robinson, 1918; Pincus and Enzmann, 1937; Dawson and Friedgood, 1940). In infrahuman primates which have been studied females become sexually receptive considerably earlier in the follicular phase than do lower mammals and willingness to accept the male is apparent during more of the cycle. Carpenter (1942b) states that free-ranging rhesus monkeys have a period of receptivity occupying about one-third of the reproductive cycle. The chimpanzee is not greatly different; in adult females the first marked willingness to accept the male coincides with the attainment of genital swelling early in the follicular phase (Yerkes and Elder, 1936; Y^oung and Orbison, 1944) . Termination of the period of receptivity is within 1 or 2 days after ovulation and detumescence on approxi


mately day 18 to 20 of the 35- to 37-day cycle (Yerkes and Elder, 1936; Young and Yerkes, 1943) . During the luteal phase there is a general absence of sexual interest (Young and Orbison, 1944) . A diagrammatic representation of the relationships in lower mammals and primates including man is reproduced in Figure 19.1.

At this point the statement of a concept which has emerged from experimental studies of the guinea pig is appropriate. It applies to the male as well as to the female and is mentioned because it is a part of a thread of thought which has developed Irom the work as a whole rather than from any single facet. The concept is based on the distinction between "responsiveness" and "vigor." It had its genesis in the observations suggesting that differences in the character of the response to gonadal hormones are related to the character of the soma (Young, Dempsey, Myers and Hagquist, 1938), but clarification was achieved only after the behavior of female guinea pigs from different genetical strains had been studied (Goy and Young, 1957b).

Responsiveness in the female is a measure of the effectiveness of a hormone in inducing the estrus characteristics of the individual, but regardless of the character of the estrus relative to that displayed by other animals. Vigor refers to the character of the estrus, i.e., the length of time strong lordoses can be elicited, the duration of the maximal lordosis, and the amount of male-like mounting. Responsiveness in the male is the effectiveness of a hormone in maintaining or restoring the pattern of behavior characteristic of the individual, but regardless of the pattern relative to that seen in other animals. Vigor refers to the character of the behavior including such measures as length of the interval between the beginning of a test and ejaculation, the number of intromissions preceding ejaculation, and the length of the recovery period following ejaculation.

It is clear from work with the female ( 1 ) that responsiveness and vigor are influenced by the genetical background (p. 1215), and (2) that they are separable in the sense that a responsive animal may be high or low in vigor and vice versa. Examination of Table VI in the review by Y'oung (1957) reveals that the highly inljred strain 13 females are highest in vigor despite the fact that they are lowest in responsiveness. Strain 2 females are highest in responsiveness but intermediate in vigor. The genetically heterogeneous females are lowest in vigor but intermediate in responsiveness. A comparable analysis of males has not been made.





Fig. 19.1. Association of .sexual receptivity with phases of the lepiochictive cycle in female laboratory rodents, the chimpanzee, and man. (From W. C. Young, Pregnancy Wastage. Charles C Thomas, 1953. With permission of the publisher.)



III. Problems Common to the Male and Female

Thus far in our consideration of the hormones and mating behavior, reference has been made to a number of problems common to both sexes, but for the most part the discussion has dealt with those related rather specifically to one sex or the other. Turning now to problems common to both sexes we find a number that are of importance.

A. Specificity of the Relationship Between the Hormones and Response

AYhat probably is an oversimplified concept has been presented. It is that androgens stimulate masculine behavior in males and that estrogens, or estrogens and progesterone, stimulate feminine behavior in females. There is evidence, however, for many deviations from this relationship in intact untreated animals, as well as in animals under experimental conditions. The occurrence of these deviations is the basis for much of the doubt that has been expressed with respect to the specificity of sex hormone action.

An early opinion was that ovarian hormones stimulate only female morphologic and behavioral characters and that testicular hormones stimulate onlv male sex char


1194


HORMONAL REGULATION


acters (Lipschiitz, 1924, 1927; Steinach and Kun, 1928). Moore (1941, 1947) and Beach (1947), calling attention to the many observations and experiments bearing on the subject, were among the first to question this concept. More recently, opinions have been expressed which are even more critical. Eayrs (1952) states "... there is no truly specific relationship between any one hormone and the pattern of behavior which it facilitates." Kinsey, Pomeroy, Martin and Gebhard (1953, pp. 729, 748) concluded that, even for lower mammals, the designation "sex hormone" is unfortunate; they are simply "among the physiologic agents which step up the general level of metabolic activity in an animal's body, including the level of its nervous function and therefore of its sexual activity."

The approach we have chosen in discussing the problem is through an analysis of the many deviations from the relatively straightforward relationships described thus far. The nature of these deviations is indicated in Table 19.2, which contains a list of 8 possible relationships between behavioral response and gonadal hormone action. Relationships 1, 5, and 7 are commonly encountered and have been discussed; the less common relationships 2, 3, 4, 6, and 8 will now be reviewed.

Relnfionship 2. A number of instances of the display of masculine behavior by males in response to estrogen action can be cited. Some fishes (Aronson, 1957), castrated male rats (Ball, 1937a, 1939; Beach, 1942d), castrated cats (Green, Clemente and de

TABLE 19.2

Eight possible relationships between behavioral

response and gonadal hormone action


Relationship


Sex


Hormonal Stimulus


Induced Behavior


1*


Male


Androgenic


Masculine


2


Male


Estrogenic


Masculine


3


Male


Androgenic


Feminine


4


Male


Estrogenic


Feminine


5*


Female


Estrogenic


Feminine


6


Female


Androgenic


Feminine


7t


Female


Estrogenic


Masculine


8


Female


Androgenic


Masculine


  • The typical relationship.

t A common relationship.


Groot, 1957 », and capons (Goodale, 1918; Finlay, 1925; Davis and Domm, 1943; Guhl, 1949) receiving implanted ovaries or estrogens displayed varying degrees of masculine behavior. As these reports are read, one generalization seems justified. It is that in several instances the estrogenic substances were not strongly effective in stimulating masculine behavior (Ball, 1937a, 1939; Beach, 1942d). In another study (Miihlbock, 1940), 2 castrated male rats injected daily for a long time with 1 mg. estradiol did not retain the copulatory ability present at the beginning of the injection period. Ball (1937a) stated that estradiol restored the ejaculatory pattern in some castrated male rats, but Beach (1956) in a number of attempts was not able to induce ejaculatory responses in estrogcnized, castrated male rats. Because a broad experience with fishes is summarized, Aronson's comment is quoted: "Thus while certain androgens seem to duplicate the endocrine function of the testes the effectiveness of the estrogens is less clear."

Guinea pigs have been used (Antliff and Young, 1956). The reproductive performance of 30 intact male guinea pigs was determined. The animals were then castrated and, beginning either immediately or 10 weeks later, 28 were injected daily with estradiol, estrone, or testosterone propionate. Regardless of when the injections were begun, the results were approximately the same. When they were started immediately after castration and continued for 16 weeks, the average scores in the last five tests were 24.8 per cent below the precastrational level in the males receiving testosterone propionate, 46.1 per cent in the males receiving estrone, and 74.5 per cent in those receiving estradiol. When treatment was started 10 weeks after castration and continued for 16 weeks the average scores based on the last 5 tests were 14.0 per cent below the precastrational level in the males receiving testosterone propionate, 23.9 per cent lower in the males receiving estrone, and 78.1 per cent lower in the males receiving estradiol. The latter level was close to that to which the behavior of the untreated castrates had regressed. No male receiving an estrogen ejaculated and only


HORMONES AND MATING BEHAVIOR


1195


when estrone was given was intromission achieved by some animals. Clearly estrone was a better substitute for testosterone propionate than estradiol, but not even this substance substituted completely.

Male cats appear to be different. The response to 6000 R.U. of estradiol or to 1 to 5 mg. stilbestrol was normal, provided castration had been performed recently. Otherwise, not even testosterone propionate was effective (Green, Clemente and de Groot, 1957).

Relationship 3. The display of feminine responses by intact untreated male monkeys, rats, lizards, fishes, pigeons, hamsters, and rabbits has been noted (p. 1179). In a rat displaying this behavior spontaneously, histologic examination of the testes and seminal vesicles indicated that spermatogenic and androgenic activity were normal (Beach, 1945a). Castration was followed by an immediate loss of the female response, but after an interval and following the injection of testosterone propionate, the frefiuency of lordosis and hopping compared favorably with that seen preoperatively. Presumably, therefore, the feminine behavior was shown in response to androgenic stimulation of testicular origin. As Beach stated, cases of this kind are not common. In our opinion they correspond to the much more frequently occurring relationship 7 in which estrogenic substances are responsible for the masculine behavior displayed by females.

Elsewhere it is reported that 7 of 8 intact male rats displayed elements of the female pattern of behavior following injections of 10 to 23 mg. testosterone i)ropionate (Beach, 1941 L The responses were observed fre(luently enough to assure Beach of their presence, but they were described as being difficult to elicit, sluggishly performed, and quickly terminated. Two of 4 male mice showed lordosis during injections of 2 mg. of testosterone proportionate over a 7-day period (Engel, 1942). Male lizards receiving testosterone propionate displayed elements of the female pattern of behavior, l)rovided they were subordinate during fights within the group (Noble and Greenberg, 1941a). In neither of the last two studies were quantitative data given.


Relationship 4- Injections of estrogens into male laughing gulls stimulate them to respond to the sex call of the males and to "food beg" with lowered head, a posture necessary for copulation of the female with the male (Noble and Wurm, 1940b). The male herring gull appears to react less definitely. Injections of stilbestrol into the eggs fairly early in incubation and into the birds for 22 months after hatching had little effect on the behavior of three males. Three weeks after the injections were discontinued their activity approached that of many testosterone-injected male birds (Boss, 1943). Some castrated male rats and guinea pigs receiving implants of ovaries (Steinach, 1912), and some intact and castrated male rats and mice treated wdth estrogens displayed feminine behavior (Kun, 1934; Ball, 1939; Engel, 1942). In Ball's experiments pellets of estrone were without effect, but 8600 R.U. estradiol benzoate administered within 2 weeks were followed by lordosis in response to vigorous mounting by males. The behavior is described as being "at a very low level" and Dr. Ball pointed out that much more estrogen was required than would have been necessary to produce corresponding reactions in spayed females. An estimation of "how much more" can be made from the work of Boling and Blandau (1939) when they showed that estrous behavior was displayed by 18 of 20 female rats receiving single injections of 100 R.U. estradiol benzoate; 10 R.U. were sufficient when supplementary progesterone was given. The subcutaneous implantation of from 1 to 160 diethylstilbestrol tablets weighing between 50 and 1000 mg. each was without apparent effect on the sexual behavior of the adult boar (Wallace, 1949).

Nothing that is reported by Kawakami and Sawyer (1959a), following the injection of male rabbits with estrogen and progesterone, is inconsistent with what has been found when other male mammals have been given female hormones. The only observable effect on two intact males was an inhibition of sexual aggressiveness. One of the 2 was castrated and 4 months later injected with estrogen and progesterone. At this time he lost interest in mounting females and the electroencephalogram ( EEG) arousal thresh


1196


HORMONAL REGULATION


old had dropped, as it does in females similarly treated, but it is not stated that estrus was induced.

Relationship 6. The display of feminine behavior by females treated with androgens has been reported. The action of small amounts of androgen in the production of breeding behavior in the black-crowned night heron (Noble and Wurm, 1940a) is believed to be normal. Three intact and 3 spayed lizards containing pellets of testosterone propionate displayed estrous behavior and accepted other treated females or males in copulation (Noble and Greenberg, 1941b). In an experiment involving injections of testosterone propionate into a female mammal, 4 of 10 spayed rats exhibited lordosis, 7 showed the hopping response, and 1 displayed quivering of the ears (Beach, 1942b). It was said of the reactions that they did not appear frequently. Treatment with testosterone propionate in various combinations and amounts after PMS was followed by the appearance of estrous responses in anestrous ewes (Cole, Hart and Miller, 1945), but ovulation also occurred in some animals; consequently, the the hormone responsible for estrus cannot be stated with certainty.

Striking effects are described by Klein (1952) in his review of experiments performed by Gaston Mayer and himself. Following the implantation of pellets of testosterone propionate or acetate into the ears of intact female rabbits, estrous behavior was displayed that was comparable with and even stronger than that w^iich followed treatment with estrogens. As in the work on the ewe, identification of the hormonal stimulus is made difficult by the occurrence of ovulation with generations and generations" of corpora lutea. Intact female cats, on the other hand, were brought into heat with testosterone propionate, and ovulation did not occur. Largely because of the striking display of feminine behavior by rabbits containing pellets of androgen (Klein, 1952), Kawakami and Sawyer (1959a) studied the effects of androgen on the behavior of estrogen-primed ovariectomized female rabbits and on the associated EEG arousal thresholds. With a high dose especially, estrus was maintained, but it


should be noted that in this experiment the testosterone appears to have substituted for progesterone in maintaining estrus rather than to have acted by inducing estrus.

The strongest opinion that androgen stimulates feminine behavior in females is perhaps that held by clinicians. Their many reports that androgens increase sexual desire in the human female (Shorr, Papanicolaou and Stimmel, 1938; Loeser, 1940; Salmon, 1942; Salmon and Geist, 1943; Greenblatt, 1943; Abel, 1945; Carter, Cohen and Shorr, 1947; Foss, 1951 ; Waxenburg, Drellich and Sutherland, 1959), apparently more effectively than endogenous estrogens, certainly strengthens the likelihood suggested by much of the work with lower mammals that androgen substitutes for estrogen. However, before the possibility of such an action is given complete acceptance, we should be able to exclude the remote possibility that the effective substance is the androgen rather than a metabolite with estrogenic action (Dorfman and Ungar, 1953; Dorfman and Shipley, 1956; West, Damast, Sarro and Pearson, 1956; Davis and Plotz, 1957).

Relationship 8. The frequency with which masculine behavior is displayed by intact females suggests that the neural mechanisms mediating tiiis behavior are well developed. If so, it could follow that the display of masculine behavior by the female in response to androgenic stimulation is more easily achieved than the display of feminine behavior by males in response to estrogenic stimulation (relationship 4). From what follows and from the numerous cases cited by Dorfman and Shipley, (1956, pp. 194-197), this seems to be true, but it will be clear, that even here, there is much evidence for the refractoriness encountered in the other relationships involving the action of heterosexual hormones.

No details are given, but pregneninolone and testosterone induced male mating behavior in immature and mature female guppies after 20 days of treatment (Eversole, 1941), and methyl-dihydrotestosterone injected into intact female mekadas was effective as early as the 3rd day (Okada and Yamashita, 1944). Elements of male sexual behavior appeared in a definite se


HORMONES AND MATING BEHAVIOR


1197


quence following the implantation of pellets of testosterone propionate into female Xiphophorus hellen (Noble and Borne, 1941), a species which has long been known to undergo spontaneous sex reversal from female to male (Essenberg, 1925). The change is less pronounced in adult female platyfish given methyl testosterone; they exhibited the first phase of courtship behavior, but precopulatory and copulatory behavior w^ere not seen (Laskowski, 1953). Female lizards given pellets of testosterone propionate displayed courtship behavior and went through the complete male copulatory pattern (Noble and Greenberg, 1941b). Injections of large amounts of testosterone propionate induced male behavior in adult and immature female blackcrowned night herons. Smaller ciuantities induced female behavior and estrogens appear to have been without effect except on the genital tract (Noble and Wurm, 1940a). Female canaries sang following injections of testosterone propionate (Leonard, 1939) and also exhibited posturing and pairing characteristics of males, but they did not tread receptive females (Shoemaker, 1939). Free-living valley quail containing pellets of testosterone propionate assumed the male role without copulating. Their reactions were described as being slower and weaker than those of males given the hormone (Emlen and Lorenz, 1942). The same hormone did not induce male behavior in female herring gulls (Boss, 1943). The administration of androgen to intact hens (Hamilton and Golden, 1939), ovariectomized poulards (Davis and Domm, 1941), and to ovariectomized pullets (Davis and Domm, 1943) was followed by crowing and some "waltzing," but no copulatory behavior. The latter was observed in 3 of 24 brown leghorn pullets some of which were observed 4 years (Domm and Blivaiss, 1947), and in 1 of 2 white Leghorn hens several months after the implantation of pellets of testosterone propionate (Zitrin, 1942). A regimen of 500 mg. testosterone l)roi)ionate per day into female chicks stimulated comb and wattle growth, but no crowing, wing-flapping, or other cock-like attitudes occurred during the 55 days they were observed (Hamilton, 1938) . In another


expriment crowing, described as a short, feeble, high-pitched squeak which lasted about a second, was observed in 10 of 75 female chicks containing pellets of testosterone or given oil solutions (Hamilton and Golden, 1939). The crowing behavior disappeared frequently after the 1st week and almost completely by the 4th week, although the comb showed a continued response to androgen.

An intersexed mouse whose usual behavior was that of a female displayed the copulatory pattern of the male when injected with large doses of testosterone propionate (Raynaud, 1938). Except for this somewhat ambiguous case, masculinization of a female mammal by the use of purified androgenic substances seems first to have been achieved by Hu and Frazier (1939). Adult female rabbits injected 6 days a week with 1 mg. testosterone propionate for 21 to 32 days displayed vigorous masculine behavior which persisted after the injections until the external genitalia had returned to the female type. The female rabbits into which Klein (1952) implanted pellets of testosterone propionate or acetate displayed "quite a typical" male behavior, provided they were with other females. As we have noted (p. 1196), feminine responses were exhibited when they were in the presence of males. When 100 mg. testosterone propionate were administered to anestrous female sheep 3 days before PMS was given they mounted other females (Cole, Hart and Miller, 1945) , but the authors note that such animals were also subject to their own estrogen and progesterone as well as to exogenous androgen. Mounting behavior and aggressiveness were displayed by 3 intact and 3 ovariectomized dairy heifers receiving 25 mg. testosterone propionate daily (Gassner, 1952). In this work the behavior displayed by the ovariectomized animals could not be ascribed to the presence of functioning follicles.

An increase in the amount and strength of masculine behavior followed the injection of testosterone propionate into intact (Ball. 1940) and spayed female rats (Beach, 1942b). Ball injected 2 mg. twice a week following a 3-week period when half this amount had been given. She regarded the reactions as definitive but also as somewhat


1198


HORMONAL REGULATION


rudimentary. In Beach's experiments each female received 24 mg. over a period of 2 weeks. This amount of androgen was followed by a shift from a peak at the level of "sexual clasp" (the measure of lowest degree) to a peak at "palpation and thrust," the next higher measure. The complete pattern, i.e., palpation with pelvic thrusts and a backward lunge (copulation), composed 8 per cent of the total responses compared with 1 per cent after ovariectomy, and 60 to 65 per cent in normal males. It is evident from a later publication (Beach and Holz-Tucker, 1949) that 50 to 75 ^gtestosterone propionate daily (0.7 to 1.0 mg. over a 2-week period) is sufficient to maintain this level of behavior in the male. We assume that the display of the copulatory response in 8 per cent of the tests when females were injected required about three times the amount of hormone that was necessary for induction of the corresponding response in 60 to 65 per cent of the tests when males were injected.

Some female guinea pigs are responsive to testosterone propionate. Frequent injections or pellet implantation is followed by a random display of mounting. In addition, that displayed by spayed animals containing pellets and injected with estrogen and progesterone exceeds by far that exhibited in response to the same treatment before pellet implantation or after the pellet has been absorbed (Goy and Young, 1958). On the other hand, the androgen given these animals was not effective in strain 2 females which do not show mounting behavior spontaneously.

When explanation is sought for what might seem to be anomalous effects it is clear that more than one problem exists. The estrogenic stimulation of masculine behavior in the male (relationship 2) and the androgenic stimulation of feminine reactions in the female (relationship 6) may well be comparable with the many actions of heterosexual hormones on the genital tracts and accessories described by Burrows (1949) in his review. A mimicking action by heterosexual hormones is common and in studies involving the tissues mediating behavior, as in studies of tissues of the genital tract (Hisaw, 1943), the ef


fective quantity of the heterosexual hormones tends to be large. This fact alone attests to a considerable degree of specificity.

The stimulation of feminine behavior in the male (relationships 3 and 4) and of masculine behavior in the female (relationships 7 and 8) is another problem. It was long ago suggested that each sex contains the mechanism capable of mediating the behavior of the opposite sex (Goodale, 1918; Sand, 1919; Pezard, 1922; Finlay, 1925; Zawadowsky, 1926; Beach, 1938, 1941, 1945a), and that under suitable stimulation the behavior of the opposite sex is disi^layed. We reaffirm the general truth of this hypothesis, but will point out that often in many lower vertebrates and mammals the hormone of the opposite sex is not a "suitable" stimulus to induce the full behavior of that sex. The point is illustrated by what is seen in the relationships 3, 4, 7, and 8. The tissues mediating masculine behavior in females are very responsive to estrogens (relationship 7). They will respond to androgens (relationship 8), but not infrequently the behavior is obtained only with difficulty and at a low level. Rarely, as in the case described by Beach (1945aj, the tissues mediating feminine behavior in males are very responsive to androgens (relationship 3) ; more often, however, they are refractory. They are also refractory to estrogens (relationship 4) and this fact is reflected by the difficulty in stimulating feminine responses in males when estrogens are administered. We feel that the responses members of the different sexes give to hormonal stimulation are predetermined; in this sense a specific rather than a nonspecific relationship exists. This view was well expressed by Boss (1943) when he wrote: ". . . genetical factors are strongly involved, not only in determining the specific behavior pattern of the taxonomic unit, but also of the sex. It is a widely if not a generally valid rule that the same amounts of a hormone do not produce identical reactions in the two sexes of a given species." The view is also consistent with the conclusions reached by Burns (1942, 1949) during his studies of the role of fetal gonadal hormones in sexual differentiation.


HORMONES AND MATING BEHAVIOR


1199


Before leaving the subject of the specificity of the relationship between hormone and response, we would recall the results from the numerous attempts to substitute adrenal steroids and other compounds for progesterone (Hertz, Meyer and Spielman, 1937; van Heuverswyn, Collins, Williams and Gardner, 1939; Soderwall, 1940; Torstveit and Mellish, 1941; Isaacson, 1949; Melampy, Emmcrson, Rakes, Hanka and Eness, 1957 ) . Heat behavior was induced in ostrogen-conditioned females by a number of these substances, but their relative effectiveness was much less than that of progesterone. In a study in which the female guinea pig was used the relative effectiveness of a number of adrenal steroids and similar compounds was from !4 (desoxycorticosterone acetate) to 1/40 (11-ketoprogesterone, 11 -hydroxy progesterone, and corticosterone). Hydrocortisone, cortisone, 17-hydroxy-desoxycorticosterone, 17-hydroxy progesterone, 21 -desoxy hydrocortisone, adrenosterone, 4-androstene-3,17dione, and the amorphous fraction were ineffective or had only slight activity (Byrnes and Shipley, 1955 ) .

B. THE MANNER OF HORMONE ACTION, I.E., ORGANIZATION OR ACTIVATION

An important problem pertaining to the hormonal regulation of mating behavior has to do with the manner of hormone action. It has long been recognized that these substances might organize patterns of behavior (Stcinach, 1912, 1913, 1916; Sand, 1919; Lipschiitz, 1924; Nissen, 1929); in the opinion of the writer, this would be in the sense of producing changes in the resjionscs to hormones different from those normally associated with an individual, giving due regard to age, sex, strain, and species. Or, the hormones might simply activate an individual to respond in accordance with the ciiaracter of a substrate already established (Goodale, 1918; Ball, 1937a, 1939; Young, Dem])sey, Myers and Hagcjuist, 1938; Beach, 1941, 1945a). The po.s-<il)ility that they might do both has received less emphasis; conceivably the action could be organizational before birth or hatching, or before sexual maturation, and activational in the adult.


The behavior of the congenitally anomalous freemartin (Folley and Malpress, 1944; de Alba and Asdell, 1946) and sexintergrade pigs (Baker, 1925) provides some support for the hypothesis that gonadal hormones organize patterns of behavior. More direct evidence comes from a number of experimental studies.

Dantchakoff (1938a, b, 1947) stated that female guinea pigs born to mothers given intrauterine injections of testosterone propionate contained a normal female genital tract with ovaries and a more or less well developed epididymis, ductuli efferentes, prostate, Cowper's gland, and penis. In their behavior, when they were given male hormone, they performed completely as males. Alales receiving testosterone propionate prenatally and after birth possessed only the male genital tract and its accessories, but the development of most parts was precocious as was the display of masculine behavior (Dantchakoff', 1938c). If such transformations can be produced, the fact would suggest strongly that male hormone has an organizing action on the tissues mediating mating behavior, at least when the hormone is present in the early stages of embryonic or fetal development. Unfortunately, many details of Dantchakoff's procedure are not clear from her articles, and no controls were established in the form of animals receiving androgen postnatally only. Partly because of this circumstance, new experiments were undertaken (Phoenix, Goy, Gerall and Young, 1959; Tedford and Young, 1960). From what follows it will be clear that an androgen when given prenatally does have an organizing action on the tissues mediating mating behavior.

Pregnant females were injected intramuscularly with 5 mg. of testosterone propionate on day 10 of the pregnancy and with 1 mg. daily from day 11 to day 68 of tiie gestation period. At birth the external genitalia of the female offspring were indistinguishable macroscopically from those of the sibling males and examination of the genital tracts by laparotomy was necessary for identification of the sex. Internally there were hypertrophied Wolffian ducts (detectable microscopically), failure of Miillerian duct-urogenital sinus fusion, and, by the


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HORMONAL REGULATION


time of sexual maturation, abundant evidence of ovarian dysfunction. Tests given after these female hermaphrodites had been gonadectomized and injected with estrogen and progesterone, or with an androgen, revealed that striking modifications of the behavior pattern had been produced.

Much less of the feminine measures of behavior was displayed; there was a decrease in the percentage of tests positive for estrus, in the duration of estrus, and in the duration of maximal lordosis. An effect on the tissues mediating the masculine component of the pattern was revealed l)y the greater amount of male-like mounting. The hermaphroditic females had become more responsive to the androgen than ovariectomized but otherwise normal females. The effects on the females receiving the androgen prenatally were permanent. During pregnancy there were no detectable effects on the "mothers" into which the hormone was being injected (Diamond, 1960), and there were no lasting effects. Any effects on normal young females treated with testosterone propionate postnatally from day 1 to day 80 were transitory (Phoenix, Goy, Gerall and Young, 1959).

The ovarian dysgenesis, clearly apparent only after sexual maturity, was manifested by disparities in the process of folliculogenesis. They varied from retardation of follicular development, but with eventual ovulation and formation of normal-appearing corpora lutea, to anovulatory follicular development. The dysgenesis is believed to reflect damage, possibly in the nature of a masculinization, to the hypothalamicopituitary gonadal axis and to provide evidence for a central as opposed to an exclusively peripheral action of the androgen (Tedford and Young, 1960) .

Some precocity of behavior may have been shown by the male siblings; the possibility is being tested by Dr. A. A. Gerall. However, after sexual maturity the behavior of the male siblings was not significantly different from that of the untreated controls (Phoenix, Goy, Gerall and Young, 1959).

The portion of the embryonic and fetal periods during which the androgen must be administered in order to masculinize the female is being determined. At the time of


the present writing it is clear that 40 mg. testosterone propionate given between days 15 and 20 of gestation were without any detectable effect on the behavior displayed after the attainment of adulthood. However, the period 30 to 65 days of gestation is critical in the sense that injections of androgen need not be started iDefore this time in order to suppress lordosis and intensify masculinity (Goy, Bridson and Young, 1961). The results from experiments in progress may reveal that the critical period is even shorter.

The injection of estrogens into most pregnant female mammals that have been studied soon terminates the pregnancy by resorption or abortion, but some work has been done with the chicken. Domm and Davis (1948) observed the behavior of intersexual brown Leghorn fowls resulting from a single injection of each of several estrogens on or before the 4th day of incubation. vSome individuals were similar to normal males in their general appearance, but others were nearly indistinguishable from females. The sexual reactions of the intersexual males are described as varying from essentially masculine in the case of those transformed the least to neutral in the case of those whose general appearance was altered the most. Confusion and the ability to perform only certain preliminary phases of masculine behavior are noted, but there was no squatting when they were placed with normal males.

The action of the exogenous hormone in this experiment can be thought of as depending on the interpretation of what happened. If the changes are regarded as having been in the direction of feminization, it could be considered that the estrogen left its imprint on the tissues mediating mating behavior and that a modification of organization occurred. But Domm and Davis seem to have regarded the change as a "displacement reaction," displayed when the normal male pattern was impossible, rather than as feminization. The abnormal behavior was attributed to the low level of hormone concentration.

Use of the Sweltzer technique (Pincus and Hopkins, 1958), which involves dipping the eggs into solutions of steroids (or other


HORMONES AND MATING BEHAVIOR


1201


substances) before they are incubated, may be advantageous in future studies of the effect of prenatally administered hormones on the behavior disphiyed as adults. In their frankly preliminary communication Pincus and Hopkins noted that raasculinization of the female was not accomplished as easily as feminization of the male. This relationship is the reverse of that encountered in mammals and is not unexpected. If it is seen generally in birds, extensive experiments will be of more than ordinary interest.

Results from a series of experiments on intact albino rats during the prepubertal period are not suggestive of an organizational action; on the contrary, damaging effects are indicated, but in view of what has been found during the work on the guinea pig, the rat should be restudied. Females injected with androgens or estrogens during the first 10 days after birth experienced a permanent impairment of cyclic rei)roductive function. They are described as displaying no sexual behavior (Wilson, Young and Hamilton, 1940; Wilson, Hamilton and Young, 1941; Wilson, 1943). The effect could not be attributed solely to gonadal failure because in neither group could estrus be induced with estrogen and progesterone, even with 10 or more times the quantity of estrogen required to condition normal animals. Treatment of males with androgen induced serious alterations of structure and function accompanied by impotence, especially when 0.75 to 36.0 mg. of testosterone propionate were given between the day of birth and day 28 (Wilson and Wilson, 1943). Ejaculation was less frequent in the injected animals and the mean number of mountings per test was low.

In other experiments on immature rats no such damaging action followed the administration of testosterone propionate into males or of estradiol benzoate into females; instead, the precocious activation of previously organized neuromuscular mechanisms was reported (Stone, 1940; Beach, 1942c). In comparing these results with those obtained by Wilson, Young and Hamilton (1940). Wilson, Hamilton and Young (19411. Wilson (1943), and Wilson and Wilson (1943) the circumstance should be


considered that administration of the hormones was not begun by Stone and Beach until day 22 to 26 and day 14, respectively. That the age of the animal at the time of treatment could be crucial has been brought out by Barraclough (1955) and by Doeg and Leathern (1958) and traced to an imbalance induced at the hypophyseal level. In mice injected with estradiol or testosterone at 5 days of age there was a premature opening of the vagina followed by conspicuous irregularities in the cycles. Abnormalities of the latter type were much less marked when treatment with the steroids was delayed until the 20th day.

Results different from those reported by Wilson and Wilson (1943) were also obtained when young male guinea pigs, castrated the day of birth, were injected daily with testosterone propionate for 120 days (Riss, Valenstein, Sinks and Young, 1955; Gerall, 1958). The animals appeared normal and the development of behavior was not different from that in intact controls. The difference in this case may be attributable to the greater maturity of the guinea pig at birth.

The suggestion from the work on sexually immature animals that androgens and estrogens do not have an organizing action on l)atterns of behavior is reinforced by the demonstration that the develoj^ment of sensitivity to gonadal hormones can occur when the gonads are absent. Female guinea pigs and rats spayed immediately after birth and first injected with estrogen and progesterone 10 months (rat) and 2 years (guinea pig) later were as reactive as animals ovariectomized during adulthood (Wilson and Young, 1941). A female rat in which there was congenital absence of the ovaries, tubes, and uterus displayed typical feminine behavior following injections of estrogen and progesterone (Beach, 1945b). The male is not different, for the capacity to respond to androgen develops in the absence of the testes (Beach and Holz, 1946; Riss, Valenstein, Sinks and Young, 1955).

The problem of the manner of hormone action in adults was brought into sharp focus by Ball (1937a), although Goodale had noted as early as 1918 that the behavior of the capon receiving an implanted ovary


1202


HORMONAL REGULATION


was either wholly unmodified or, if modified, it was not in the direction of feminization. Ball demonstrated that female hormones, instead of feminizing the castrated male rat as Kun (1934) had claimed, increased their male activity.

New evidence that hormones activate adults in accordance with previously organized neural mechanisms rather than organizing new patterns has recently been provided (Goy and Young, 1958). Female guinea pigs from a genetically heterogeneous stock (T stock) displaying male-like mounting spontaneously and from a strain (strain 2) in which this behavior is not shown (Goy and Young, 1957b) were spayed and brought into heat with estrogen and progesterone. On completion of the control tests, 15-mg. pellets of testosterone propionate were implanted into each animal. Estrus was again induced 24 days later by repeating the previous treatment, and 4 months later, without additional androgen, a final test was made. The average number of mounts per test in the T stock animals was 2.3, 41.8, and 3.8, respectively. In the strain 2 animals the averages were 0.0, 0.0, and 1.3. Two points are clear: (1) the androgen activated the T stock females to display mounting at the time of the second test, but there was no lasting, organizational effect; (2) the androgen was not effective in stimulating mounting in a strain which does not display this behavior spontaneously, consequently in these animals there was no evidence either for an activating or an organizing action.

C. AGE OF THE ANIMAL AND THE HORMONAL REGULATION OF MATING BEHAVIOR

Most of the attention devoted to the hormonal regulation of mating behavior has been centered on the adult during the period of reproductive activity. No investigator has tested a group of animals from youth to old age in an effort to relate any changes in the strength and pattern of behavior to changes in quantity of hormone or in reactivity of the tissues mediating such behavior. Considerable information exists but it is fragmentary and interpretation is difficult.

Injections of a pituitary gonadotrophic


substance (hebin) into 3-day old male chicks were followed 6 days later by crowing and after 10 days by initial treading reactions (Domm and Van Dyke, 1932a). Injections of androgen were followed by crowing on the 4th day of age and by treading on the 15th day (Hamilton, 1938; Breneman, 1939; Noble and Zitrin, 1942). A comparison of the effective quantities in young birds and in somewhat older cockerels (Davis and Domm, 1943) can only be made by inference; 0.5 to 1.0 mg. daily seems to have been sufficient for the younger birds, whereas 2.50 to 3.75 mg. were required for two older birds. Apparently the sensitivity of 30-day chicks was not greater than that of 2-day chicks.

Of the investigations in which manunals were used, that by Steinach and Kun (1928) was one of the first. Control male rats in their colony were not attaining maturity until 60 to 70 days of age, but experimental animals given 9 to 18 injections of a watersoluble extract of anterior pituitary beginning at 4 to 5 weeks of age displayed mature sexual behavior as early as 38 to 45 days of age. More recently, data have been obtained bearing on the response of prepubertal rats and guinea pigs to testosterone propionate. The report by Stone (1940) that the median age of the first copulation (mounting, palpation and pelvic thrusts with intromission ) in the intact rat was set ahead about 20 days was confirmed by Beach (1942c). In Stone's experiment 0.62 mg. testosterone propionate was injected daily; in Beach's experiment 1.0 mg. was given. As in the case of the chicken, comparison with the adult is hazardous, but the report (Beach and Holz-Tucker, 1949) that 50 to 75 /.g. testosterone daily is necessary for the maintenance of the preoperative level of copulation in adults suggests that the sensitivity of the young rats used by Stone and Beach to testosterone propionate was less than in the adults used by Bcacli and HolzTucker.

Results from two studies of young guinea pigs are presented for comparison with those obtained from the chicken and rat. The development of mating behavior was followed by weekly tests from within a week after birth to. 120 days of age (Riss,


HORMONES AND MATING BEHAVIOR


1203


Valonstcin, Sinks and Young, 1955; Gerall, 1958). Experimental males were castrated within 2 days after birth and injected daily witii up to 500 ixg. testosterone propionate per 100 gm. body weight. In neither experiment, and contrary to what was found in the rat, was the time of the first ejaculation or the ultimate level of sexual behavior affected; mounting may have been precocious.

Examination of data ol)tained from young female chickens and jjrepubertal female rats and guinea i)igs injected with gonadotrophic hormone, with estradiol benzoate alone, or with estradiol benzoate in combination with l)rogesterone reveals results that are not clear. Masculine head furnishings and an "astonishing hypertrophy" of the oviducts were seen in brown Leghorn females receiving daily injections of pituitary gonadotroiihin for 14 to 36 days beginning at 21 to 47 days of age, but behavior was "apl)arently unaffected" (Domm and Van Dyke, 1932b). Female white Leghorn chicks injected with 0.17 mg. estradiol benzoate daily beginning the 15tli day of age squatted for treading males after 18 to 26 treatments, but chicks in which injections were started the 2nd day and continued for 34 days were never seen to scjuat for a treading male (Noble and Zitrin, 19421.

Estrous reactions were induced in 4 of 18 spayed female rats given estradiol benzoate and progesterone beginning the 20th day, and in 6 of 20 ovariectomized guinea pigs injected beginning the 15th day. By the 30th day all of 6 injected rats and 14 injected guinea pigs responded, from which it was concluded (1) that mating behavior can be induced precociously, and (2) that the sensitivity to estrogen which is characteristic of the adult does not develop until after the 20th day (Wilson and Young, 1941). The possibility of inducing precocious estrous behavior in the female rat was demonstrated shortly thereafter by Beach 1 1942c I.

The information yielded by these experiments on young male and female animals is not sufficient to justify more than the cautious generalization that early in the l)repubertal period the tissues mediating mating behavior acquire the responsiveness


to androgenic or estrogenic stimulation which characterizes them as adults. In neither the rat nor the guinea pig does the presence of the gonads seem necessary for the acquisition of this responsiveness.

Scattered data contribute information with respect to changes in sexual behavior associated with advancing adulthood and old age but the lacunae are large. In old rats running activity in the male (Hitchcock, 1925) and female (Slonaker, 1924) is less than in young rats. A number of observations on the male rabbit (Stone, 1932a I, rat (Stone, 1939a; Beach and Holz, 1946), and guinea pig (Grunt and Y^oung, 1952a) indicate that copulation frequency is lower in old animals. Some of the most careful observations have been reported by Larsson (1956, 1958a). Ejaculations per hour by male rats increase up to 1 year of age and decrease after 20 months. Intromissions per hour are greatest at puberty and decline slowly but steadily thereafter. The duration of each series of copulations is prolonged as animals age,- likewise the length of the refractory periods. Light had a greater inhibitory effect on the number of ejaculations per hour in the older animals than in the younger ones (Larsson, 1958c). The difference was attributed to an enhancement of the inhibitory influence of unconditioned and conditioned stimuli with increasing age.

The relationship between age and the character of copulatory behavior in female laboratory mammals does not seem to have been investigated. The only information we have found was obtained during a relatively short period when the hormonal regulation of estrous behavior in the female guinea pig was first being studied (Y'oung, Dempsey, Hagquist and Boling, 1939). Table 2 in that article contains a record of the length of consecutive heat periods in 30 females during the academic years 1935-36 and 1936-37. The mean length of the first 4 heat periods in 1935-36 was 7.3 hours; the mean length of 4 heat periods 6 to 9 months later was 8.1 hours. It is clear that the detection of any changes as the female guinea pig ages will depend on observations of animals older than 12 to 18 months.

If the figures presented by Hitchcock


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(1925), Slonaker (1924), Stone (1932a, 1939a), Grunt and Young (1952a), and Larsson (1956, 1958a) are indicative of changes in the running activity of male and female rats and in the mating behavior of male rats and guinea pigs, these changes could be attributed to a reduction in the quantity of endogenous hormones, or to a decrease in the sensitivity of the tissues to such hormones. Indirect evidence supports the former rather than the latter hypothesis, although until the point has been checked experimentally the possibility that both changes occur may not be excluded.

Hooker (1937) concluded from assays of bull testis extract that after 5 years of age the hormone content gradually decreases. Determination of the male hormone in urine from men of different ages led Kochakian (1937) to conclude that the amount excreted by men 50 to 76 years of age is only about 1/6 that excreted by men 22 to 29 years of age. According to I3ingemanse, Borchardt and Laqueur (1937), old men excrete less capon comb-growth-promoting substance than middle-aged men. Schou (1951), after making serial determinations over 10 years, stated that there is a steady decrease in the excretion of androgenic substance between the 39th and 62nd years, with advancing age the production of 11desoxy-17 ketosteroid precursors is markedly reduced. Some of the decline is attributed to a decrease in androgen precursor from the testes (Pincus, 1956). In women a secretory decline in ovarian estrogen is gradual, with a sharp drop in the 7th to 9tli decades.

The results from two experiments invoh'ing the injection of gonadal hormones into old rats are consistent with the suggestion that the decrease in the intensity of reproductive behavior in old animals is attril)utable to a decreased production of hormones, but, unfortunately, they do not eliminate the possibility that the amount of injected hormone simply compensated for a decrease in responsiveness. Hoskins and Bevin (19401 showed that the running activity of old male rats was increased by injections of estriol glucuronide. (It will be recalled that under experimental conditions estrogens seem to be more effective than androgens in


the stimulation of running activity in the male rat.) Minnick, Warden and Arieti (1946) injected 8 28-month-old male rats with 1.25 mg. of testosterone propionate for 15 days and 9 with a preparation from pregnant mare serum. In both groups the average copulatory scores increased approximately 10-fold after only 8 days of treatment.

It is obvious from this miscellaneous information that alterations in sexual behavior as animals mature and age may be assumed. How much should be attributed to changes in the quantity of gonadal hormones and how much to changes in the reactivity of the tissues mediating such behavior can only be conjectured.

D. PROBLEM OF THE MECHANISM AND SITE OF ACTION OF GONADAL HORMONES

Little to nothing is known about the mechanism whereby gonadal hormones stimulate mating behavior. At the molecular level the likelihood that such information will be revealed in the near future is not great. Beyond the statement that gonadal hormones bring about their many effects by regulating the activity of tissue enzymes, this basic endocrinologic problem has not been answered (Dempsey, 1948; Pincus, 1952; Zuckerman, 1952; Szego and Roberts, 1953; Kochakian, 1959; chapter by Villee), even by those who have examined the tissues which, by virtue of their accessibility and structure, are best adapted to histochemical and cytochemical procedures. Furthermore, the neural tissues mediating mating behavior have not been identified in the sense that attention can be directed to cells in which change or changes in response to hormonal stimulation could be correlated with the expression of sexual behavior. We suggest, however, that when the mechanism of hormone action has been worked out for the more accessible tissues, such as the uterine epithelium (Rosa and Velardo, 1959) or myometrium (Csapo, 1955, 1959a, b), much of the knowledge will be applicable to the tissues mediating mating behavior. The response is to the same hormones, many of the same problems of reactivity exist, and a number of the same rules apply. With respect to the latter, the


HORMONES AND MATING BEHAVIOR


1205


synergism between the estrogens and progesterone is encountered in both types of tissue, and there is a consistency of species differences in certain behavioral and tissue responses to androgens (Gerall, 1958). To the writer, one of the most impressive examples of this parallelism is the responses of vaginal epithelium and the neural tissues mediating mating behavior. In the guinea |)ig, normal-appearing vaginal cornification (Ford and Young, 1951 ) and normal mating behavior are induced only when the administration of an estrogen is followed by progesterone. In the ewe, on the other hand, there is a reversal of this relationshij). Normal vaginal responses are induced only when an estrogen is preceded by progesterone, and normal behavioral responses delU'nd on the same sequence of hormonal action (Robinson, Moore and Binet, 1956; jNloore and Robinson, 1957).

At the molar level we may be somewhat l)etter off, because the search for the neural correlates of sexual behavior has been a subject of research in many laboratories (see reviews by Beach, 1942e,"j, 1943, 1947, 1948, 1951, 1958; and the recent articles by Harris, Michael and Scott, 1958; Kawakami and Sawyer, 1959a; Sawyer and Kawakami, 1959). In considering what has been accomplished and the problems, it is well to start with the suggestion contained in a number of the articles cited above that in the male and female two different mechanisms are involved. The significance of this fact, if it may be so regarded, is that the emergence of a single explanation, applicable to the two sexes, for the mechanism of action of the gonadal hormones in bringing sexual behavior to expression is unlikely.

The evidence for the suggestion that two mechanisms are involved comes from many sources. It has long been held that the neural mediators of sexual behavior in male mammals are different from those in females (Beach, 1942e, 1943, 1951, 1958). The neocortex is more heavily involved in mating performance in the male than in the female. As we noted earlier, the disappearance or reduction of mating behavior after hormonal withdrawal is gradual rather than abrupt in the male, whereas it is abrupt in the female. When replacement therapy is given.


the restoi'ation of mating behavior is slow in the male rather than inmiediate, as it is in the female. In males a single chemical substance, an androgen, is effective in maintaining sexual behavior, but in females of many species two substances, an estrogen and progesterone are involved. In the female ral)bit, EEG arousal thresholds have been correlated with mating behavior, but in males sex drive could not be correlated with arousal thresholds (Kawakami and Sawyer, 1959). Whether the female or male is being investigated, some knowledge of the time required for the hormones to exert their effects, coupled with information bearing on the temporal and qualitative aspects of gonadal hormone metabolism would be important in any analysis of the mechanisms of hormonal action. When females were being studied it became clear that up to 24 hours elapse after the injection of an estrogen before the animals are conditioned to respond to progesterone. The latter substance, on the other hand, w^as effective in an average of about 5 hours (Collins, Boling, Dempsey and Young, 1938; Boling and Blandau, 1939; Frank and Fraps, 1945). Inasmuch as both hormones were contained in the same oily vehicle and injection was subcutaneous, more than a matter of transport from the site of injection must be involved. This consideration is emphasized by the results obtained when estrogens were placed directly on the reactive tissue in the case of the vagina, or on what is believed to be the reactive tissue in the case of the brain. After intravaginal administration of estrone, the mitotic activity of the epithelial cells did not begin until after a latent period of 12 hours (Biggers and Claringbold, 1955). Whether the administration of estrogen to female cats was subcutaneous or direct in the posterior hypothalamus, the latent period to mating was at least 3 days (Harris, Michael and Scott, 1958). The slower and more gradual action of androgens might handicap a worker seeking to learn something about the temporal relationships between hormone and response in the male. Nevertheless, in the male as in the female the interval before overt responses can be elicited may well exceed (1) the time required for the transport of effective quantities of tlie hormones to the tissues


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HORMONAL REGULATION


on which they act, and (2) the period during which the chemical integrity of the injected hormones is maintained (Fee, Marrian and Parkes, 1929; Kochakian, 1939; Davis and Plotz, 1957). Inquiries into the mechanism of hormonal action should be directed toward the events taking place during this interval.

References to relationships specific for the female have been made by Young (1941) and de Alba and Asdell (1946). The former noted that estrogens stimulate responses approximating those of the true heat, but the responses fall short of those displayed when progesterone is given. At the time, the nature of this "facilitating action" was not known ; it was only known that the chain of events initiated by the estrogen reciuires progesterone for its completion and that the latter hormone acts to terminate heat as well, at least in the rabbit, ferret, sheep, and goat (Makepeace, Weinstein and Friedman, 1937; Marshall and Hammond, Jr., 1945; Phillips, Fraps and Frank, 1946; and more recently, Sawyer and Everett, 1959). De Alba and Asdell postulated the development of a refractory condition and central nervous block after the threshold to estrogen has been reached in the cow, but if such a state develops, the means are not known. Such a block was not observed by Melampy and Rakes (1958).

More precise information with respect to the neural responses of estrogen-primed rabbits to progesterone is contained in the study of Kawakami and Sawyer (1959a). Sawyer and Everett (1959) had previously shown that progesterone at first facilitates and subsequently inhibits the release of pituitary ovulating hormone and that these effects are paralleled by a heightened degree of estrus and later by a depression of heat to the anestrous state. In the investigation by Kawakami and Sawyer, alterations in two types of neural thresholds accompanying these changes were followed: (1 ) the EEG arousal threshold for direct stimulation of the midbrain reticular formation, and (2) the EEG after-reaction threshold for low frequency stimulation of hypothalamic or rhinencephalic nuclei. Presumptive evidence is presented for believing that the former is more closely linked to sexual behavior and the


latter to pituitary activation. Briefly, a lowering of the arousal threshold soon after the administration of progesterone and its elevation later correlated with the behavioral changes and were taken as evidence for the action of progesterone on central nervous system tissues. Presumably because of the authors' o]Hnion that it was not possible to do so, neither the significance of the lowered threshold for the change in behavior was indicated, nor was any clue given w'ith respect to the nature of the initial preparatory or ]iriming action of the estrogen.

Identification of the neural tissues involved in the disjilay of sexual behavior is a part of the problem of tlie mechanism of action of the hormones in bringing such behavior to expression. In the case of female lower mammals, this behavior, whether it be appetitive or consummatory, is thought to be associated with subcortical tracts and nuclei rather than with the cortex (Beach, 1958b). This belief is consistent with the opinion that a sexual center or centers might be found and much effort has been directed toward this objective. In their brief review of the early investigations, Harris, Michael and Scott (1958) stated that, largely from negative evidence from ablation experiments the neural area on which the integrity of the mechanism for the full expression of sexual behavior depends lies somewhere in the upper mesencephalon, hypothalamus, or preoptic region. Confirmation of this hypothesis was thought to be given by Kent and Liberman (1949) wlio placed progesterone directly into the third ventricle of the hamster brain and observed typical mating behavior wuthin an hour. The results obtained following refinements of this procedure on female cats have not only added support to this view, but would seem to have excluded the involvement of the cerebellum, preoptic region, frontal white matter, caudate nucleus, thalamus, and amygdaloid complex, although in 4 of 11 members of tlie latter group (preoptic region to amygdaloid complex) some components of the sexual response were seen (Harris, Michael and Scott, 1958).

The direction of attention to these effects of steroid hormones when they are placed in contact with the hypothalamus must not


HORMONES AND MATING BEHAVIOR


1207


diA'crt effort from investigations of other parts of tlie brain. In this connection, the concluding statements by Kawakami and Sawyer (1959a) are relevant and cautionary. In their words, the areas in the brain which are affected by steroids are so extensive as to suggest that the whole nervous system is influenced primarily and localized systems of integrated behavior secondarily. Sex steroids affect simultaneously . . . the midbrain reticular system, which probably includes a mamillary body mating-behavior 'center' and the rhinencephalic-hypothalamic system, which includes the basal tuberal gonadotropic 'center'."

When the male is considered, very different facets of the problem of the mechanism of hormone action are encountered (Nissen, 1929; Beach, 1942e. 1958; Soulairac, 1952a-e; Soulairac and Coppin-Monthillaud, 1951; Larsson, 1956; Lehrman, 1956; Rosenblatt and Aronson, 1958a, b).

The concept that male sexual behavior has appetitive and consummatory portions has been discussed (p. 1178). Not unrelated in the minds of investigators interested in the mechanism of hormonal action, is the circumstance that these parts of the pattern are thought to be mediated by different parts of the nervous system. Walton (1950) stated, the motor activities in the pattern, associated by the writer with the appetitive portion, are innervated by the voluntary central nervous system and all have a high degree of cortical representation. Erection and ejaculation, regarded as consummatory, are innervated through the sacral autonomic ner\-es and may be stimulated to function independently of the motor part of the pattern.

Beach who has considered this dichotomy more persistently than any other investigator states in his review published in 1958 that the mechanisms cannot yet be described in ])recise neurologic terms, but it is possible to indicate something with respect to their composition. According to him, the consummatory mechanism (CM) of male (and female) primates embrances centers and systems extending into the neocortex. The cortex and various subcortical tracts and nuclei are thought to be involved in the CM of male carnivores, but not in female carni


vores, and not in the male or female rat. In the animals composing these last groups, the highest essential centers of the CM lie in the diencephalon. It is because of this, apparently, that the coital act can be performed without practice. The latter, however, is certainly not true in the guinea pig, another rodent (Valenstein, Riss and Young, 1955; Valenstein and Young, 1955; Goy and Young, 1957a); consequently cortical involvement would be assumed in males and females of this species. The arousal mechanism (AM) is said not to depend on the cortex in female rodents or carnivores. In these groups the AM is diencephalic, but the AM of male rodents and carnivores and of male and female primates includes cortical elements. Influenced by the observation that castrated carnivores and primates can copulate, provided the requisite degree of arousal is attained, Beach concluded that in the males of many species the CM does not dei^end on androgen. To the reviewer, this conclusion may require modification. For one thing, agreement is not general that castration of carnivores and primates is without effect (p. 1183) and that any apparent effects can be counteracted by a sufhciently high degree of arousal. For another, ejaculation, a consummatory response in the male, is the first element to disappear following castration.

The dependence of the AAI on gonadal hormone stimulation is not questioned. A hypothesis that has long had general acceptance was advanced by Beach (1942e, 1944b, and elsewhere). Androgens are assumed to raise the excitability of the central excitatory mechanism (c.e.m.), thus increasing the male's susceptibility to arousal, and to lower the thresholds in the neural circuits mediating the male copulatory pattern. Elevation of the c.e.m. is also related to the excitatory value of the stimulus object; consequently, hormonal and psychologic factors are mutually compensatory in elevating excitability. Like androgen, estrogen when present in the male is said to raise the excitability of the c.e.m. and thus to increase his susceptibility to arousal. In the female it is believed to function by lowering the threshold in the neural circuits mediating the copulatory pattern.


[208


HORMONAL REGULATION


That more is involved may be indicated by scattered observations on the rat and guinea pig. Male rats with inadequate penile development are hyperactive in their display of the lower measures of sexual behavior when they are in the presence of estrous females (Beach and Holz, 1946). Male guinea pigs also display hyperactivity, but in the experiments in which this hyperactivity was recorded the most accurately, it seems to have been an expression of the lack of organization of the motor centers traceable to insufficient contact with other animals (Valenstein, Riss and Young, 1955) rather than to any underdevelopment of genital structures. The writer assumes that hyperactivity of this sort is explained by the inability of the animal to achieve the outlet that is had when ejaculation occurs. A different type of hyperactivity is displayed by castrated male rats and guinea pigs (Beach, 1942d; Grunt, 1954). This nondirected hyperexcitability, as Grunt called it, seems to be a reflection of a frustration and is regarded as an indicator of cortical activity in the absence of androgenic stimulation. AVhile discussing the problem with Dr. John Money, the suggestion was made that the effect of the gonadal hormones on central nervous tissue could be in the nature of a coordinating or integrating action rather than a matter of excitation. Such a hypothesis is consistent with the display of the nondirected hyperexcitability described by Grunt. However, it may not be applicable to the female, the effect of ovarian hormones on the tissues mediating lordosis may be of another order.

Nissen (1929), Lehrman (1956), and Rosenblatt and Aronson (1958a) have contributed to the raw material to be examined in considering the subject. All stress the role of peripheral structures, but see the chapter by Lehrman for a full discussion of the problem. Nissen, in an article containing a point of view which still finds expression, postulated that some organ other than the gonads, but in functional dependence on them, effects a tumescence or tension in itself or in another tissue or organ. This tension initiates afferent impulses which stimulate sex activity. In the male the penis or prostate was thought of as the hormone-dependent


organ or "interpolated structure"; in the female, sensory impulses initiating sexual behavior were believed to be initiated in their turn by tension in the uterine or vaginal tissues.

Lehrman in his more recent discussion of the subject emphasizes that any conclusion that behavior patterns are organized and originate in neural centers is based on a priori statements and has yet to be demonstrated. Writing out of a background of observations on maternal behavior, he added that patterns of this behavior reflect relationships between the center and the periphery which have not been sufficiently considered. The criticism is directed to the view that hormones act on central nervous mechanisms specific for the behavior pattern concerned (Lashley, 1938; Tinbergen, 1951) to the exclusion of peripheral receptors. Or, it may have been stimulated by the emphasis Beach (1942e) placed on the action of gonadal hormones in increasing the excitability of the c.e.m. and in lowering the threshold of motor circuits without mentioning their possible action on receptors as he has done elsewhere (Beach and Levinson, 1950). As matters stand, judgement with respect to Lehrman 's criticism must be withheld. His suggestion is consistent with the clinical opinion that the effect of androgens in inci'easing libido in women may be ascribed to local changes in the external genitalia (Carter, Cohen and Shorr, 1947). Support would also seem to come from an experimental study containing evidence (1) that there is an increased olfactory sensitivity in women after puberty or following the administration of estrogens, and (2) that in male rats olfactory sensitivity is decreased by castration (Le Magnen, 1952a, b, 1953). Temporarily at least, the case is weakened by the failure of Carr and Pender (personal communication) to find that gonadal secretions have a measurable effect on the absolute olfactory threshold of male rats for urine from estrous females.

Soulairac (1952a-e) has advanced a hypothesis which must also be considered in any discussion of the mechanism of hormonal action. According to him, the number of ejaculations decreased following treatment of the rat with testosterone propionate,


HORMONES AND MATING BEHAVIOR


1209


thyroxine, or .stilbestrol, whereas intromissions and the length of the refractory period were unaffected. Inhibition of the pituitary was assumed to account for this alteration in the pattern and Soulairac concluded tliat the primary factor for the regulation of ejaculation resides in this gland. The frecjuency of intromissions and the duration of copulatory activity, on the other hand, were increased by the neuro-excitatory drugs, caffeine and strychnine; these elements therefore were concluded to be dependent on the central nervous system and sensory stinuilation. Prostigmine and aneurine prolonged the refractory period without influencing the duration of copulatory activity; the refractory period therefore is concluded to depend on the state of metabolism of the nervous tissue, in particular the enzymatic processes controlling synaptic transmission and other neuronal activity.

The validity of this hypothesis has yet to be established. In a sense it is an extension of the view that patterns of male behavior are composed of appetitive and consummatory portions (Craig, 1918; Nissen, 1929; Beach, 1942e, 1947, 1956, 1958b; Baerends, Brouwer and Waterbolk, 1955). The more recently expressed doubt that the inter-relationship between neural activity and behavior in the male cat is a unitary variable (Rosenblatt and Aronson, 1958a) is a part of the trend. If the different components of sexual behavior are relatively independent, as they have long appeared to be in the female (Young and Rundlett, 1939; Beach, 1943 », analysis of the mechanism of hormonal action will be greatly complicated. Aliller (1957) stated that help may come from studies involving electrical stimulation of different parts of the brain, and it has (Kawakarai and Sawyer, 1959a, b; Sawyer and Kawakami, 1959), but even this optimistic note is tempered by the enumeration of complications in the articles published simultaneously by Green, Clemente and de Groot (1957) and by Herbert and Zuckerman (1957). We have enumerated other considerations which we believe must be taken into account before a synthesis, corresponding to those attempted by Beach (1958) and Dell (1958), of all that is invoh-cd in the hormonal stimulation of mat


ing behavior may be claimed. It would be surprising if there are not many additional considerations which are not now apparent.

E. NONCiONADAL HORMONES AND MATING BEHAVIOR

Information bearing on the relationship of nongonadal hormones to mating behavior has been obtained from many studies in which attention was directed particularly to the pituitary, adrenal cortex, and thyroid. Because of the chemical similarity between adrenal cortical and gonadal hormones, the likelihood of direct action would seem greatest in the case of the adrenal cortex, but except for one report based on a study of the rat (Richter and Uhlenhuth, 1954), and another based on a clinical study ( Waxenberg, Drellich and Sutherland, 1959) , little evidence in support of such a possibility can be found.

The results obtained by Soulairac, Teysseyre and Soulairac (1955) following the injection of cortisone into male rats are admittedly difficult to interpret; at the best an indirect rather than a direct action is indicated. Desoxycorticosterone acetate administered to castrated male hamsters did not increase their sexual activity (Warren and Aronson, 1956), nor did adrenalectomy of the mature male appreciably effect reproductive behavior or the ability to impregnate females when the animals were maintained on desoxycorticosterone acetate. As we have noted (p. 1199), desoxycorticosterone acetate (van Heuverswyn, Collins, Williams and Gardner, 1939; Marvin, 1958; Melampy, Emmerson, Rakes, Hanka and Eness, 1957), an aciueous adrenal cortical extract (Torstveit and Mellish, 1941), and a number of other steroids isolated from the adrenal cortex or having adrenal hormonelike activity (Byrnes and Shipley, 1955) substituted for progesterone in the induction of estrus in spayed guinea pigs and ovariectomized cows, but all lacked the potency of progesterone.

Ring (1945) postulated that estrogen injected into the spayed female rat indirectly stimulates the adrenal cortex to release substances having progesterone activity and that estrus might result from the synergistic action of the two liormones. The writer does


1210


HORMONAL REGULATION


not feel that the percentage of spayed adrenalectomized female rats brought into heat by estradiol benzoate alone was sufficiently low to give strong support to this hypothesis. Simpson and Williams (1949) also rejected the suggestion as being unlikely. Noting that the dose of estradiol required to induce mating in spayed-adrenalectomized and in spayed rats was the same, they expressed doubt that the adrenal cortex participates in the induction of heat responses in females. Shortly thereafter a single report of such activity appeared (Christy, Dickie and Woolley, 1950) ; spayed female mice with adrenal cortical hyperplasia or neoplasma are said to have exhibited irregular cycles and to have mated in normal fashion. However, until cases involving a comparable action by normal adrenal glands are found, the weight of the evidence is against the direct participation of cortical hormones in the stimulation of mating behavior.

A recent suggestion that the adrenal has the sort of action on behavior generally attributed to the gonadal hormones followed the observation that gonadectomy does not greatly reduce the running activity of male or female wild Norway rats (Richter and Uhlenhuth, 1954). The authors postulated that steroids from the adrenals contribute to the production of running activity. In support of the hypothesis they pointed out (1) the adrenals of wild rats are larger than those of domesticated rats, (2) they contain more Sudan IV stained lipids, and (3) the sharp drop in activity after gonadectomy of domestic rats can be entirely or partially prevented by therapy with cortisone or desoxycorticosterone acetate.

Waxenberg, Drellich and Sutherland (1959) have summarized their clinical notes on 14 patients with metastatic breast cancer for whom there was objective evidence of improvement following adrenalectomy and who reported sex functioning before the operation. In 12 there was a postoperative decrease in all the variables not previously at zero levels. After presenting evidence that oophorectomy has little effect on sexual behavior, it was concluded that any discussion of the hormonal basis of human sexuality must concern itself as much with the adrenals as with the ovaries.


The possibility of a direct action by the pituitary is thought to be excluded by the numerous reports of mating behavior by hypophysectoraized male and female rats ( Nelson and Gallagher, 1936; Muhlbock, 1940; Astwood and Dempsey, 1941; Ball, 1941b), female rabbits (Robson and Schonberg, 1937), female dogs (Robson and Henderson, 1936), and female cats (Maes, 1940). Indirect effects are of course assumed. The reduction in the running activity of the rat to a level one-third to one-half that before hypophysectomy (Levinson, Welsh and Abramowitz;, 1941 ) may be such an effect. Dempsey's (1939) failure to induce estrus in completely hypophysectomized guinea pigs may also have been a conseciuence of effects on metabolism rather than anything more direct.

The thyroid has received much attention, but (luantitative and well controlled data are not numerous. Too often it is simjily stated that mating did or did not occur following treatment with thyroid substances, antithyroid drugs, or after thyroidectomy. Numerous reports of this type are cited in some recent reviews (Maqsood, 1952; Young, Rayner, Peterson and Brown, 1952; Peterson, Webster, Rayner and Young, 1952). In the same articles efforts are made to account for the many contradictory statements and to indicate something of what must be done if the problem is to be clarified.

^Maqsood directs attention to the precocious sexual behavior of young male rabbits and lambs, to the improved libido of adult male rabbits and goats ( quoted from Turner, Mixner and Reineke, 1943), and to the prevention of the seasonal decline in lil)ido in rams resulting from the administration of thyroxine or other thyroid substances in "optimal doses." He states that thyroxine when injected in large doses adversely affected development of the gonads and accessory sex organs in the growing male rabbit, and emphasizes the importance of considering the normal rate of thyroxine secretion when thyroid materials are being administered. The inference seems clear that the reduction or loss in sexual interest by guinea pigs (Doderlein, 1928) , white Leghorn hens (Belawenetz, 1928; Collias, 1946), and cows (Van Landingham, Hyatt, Weakley, and


HORMONES AND MATING BEHAVIOR


1211


Henderson, 1947) should be regarded as an adverse effect of the thyroid substance given these animals. Blaxter's (1952) comment, however, on the claim that cows are more difficult to get to calf following the feeding of iodinated casein should be noted.

"The interpretation of such data is extremely difficult and cannot warrant the conclusion they drew. In other experiments with Jersey cows given iodinated casein throughout the larger part of their lactation the cows reproduced quite normally. Holstein cows, under the same conditions, however, failed or were slow to conceive. Some of these cows were closely related and the small numbers (total 20) again make conclusion difficult. In Crichton's experiments lasting for 4 years, neither the interval between calvings nor the number of services necessary for conception revealed any effect of either iodinated protein or ^-thyroxine administration on reproductive performance.

"There is thus no reliable evidence of any gross abnormality in the reproductive performance of the hyperthyroid dairy cow. At the same time there is insufficient evidence available to judge whether a small impairment does not in fact take place."

Numerous reports state that the strength of sexual behavior was reduced if not abolished in hypothyroid males and females (Rickey, 1925, in thyroidectomized male rats; Petersen, Spielman, Pomeroy and Boyd, 1941, in the thyroidectomized bull; Brody and Frankenbach, 1942, Spielman, Petersen, Fitch and Pomeroy, 1945, in thyroidectomized cows; Blivaiss, 1947a, b, in thyroidectomized brown Leghorn hens and roosters; Maqsood, 1952, in thyroidectomized and thiouracil-fed male rabbits; Peterson, Webster, Rayner and Young, 1952, in thyroidectomized, but not in propylthiouracil-fed, female guinea pigs). A restoration of sexual behavior followed the feeding of thyroid substance to the bull and cows. After a rest of 90 days the administration of a single 5-gm. dose of dinitrophenol to the bull restored normal activity and sexual behavior in 12 hours. The elevation in metabolism seems to have been regarded as the common denominator.

Rickey (1925) noted that thyroidectomized female rats mated, and Lee (1925)


reported that thyroidectomized female rats showed the same heat reactions when placed with males that were displayed by normal females. Folley (1938) stated that 3 weeks after weaning no difficulty was encountered in mating 8 of 10 rats thyroidectomized during lactation. Treatment with antithyroid drugs did not prevent female (Krohn and White, 1950; Leathem, 1951) or male (Jones, Delfs and Foote, 1946) rats from mating. Chu (1945) states that 14 thyroidectomized female rabbits became pregnant 17 to 108 days after the operation and Krohn (1951) writes that, although thyroidectomized rabbits were occasionally reluctant to mate, in general they did so and brought their litters to term. There was said to be no evidence of infertility when thyroidectomized hens and roosters were mated (Greenwood and Blyth, 1929). As we have noted, thyroidectomy of the female guinea pig was followed by a reduction in the percentage found in heat, but it did not prevent all from coming into heat and mating (Petersen, Webster, Rayner and Young, 1952). Daily injections of thyroxine for several weeks increased general excitability as reflected in heightened startle reflexes, but did not raise sexual excitability in the male rat (cited as unpublished, Beach, 1942e).

From these results it is apparent that reproductive processes, including the display of mating behavior in the male and female, often require a functioning thyroid gland, that a level of thyroid activity exists which is optimal for reproduction, and that deviations in either direction may be followed by changes in if not the elimination of mating behavior. But a considerable deviation can occur without preventing reproduction and therefore mating. Something of the range within whicli mating can occur is indicated by data presented in three studies. Following thyroidectomy of 32 female rabbits the basal metabolic rate fell 25 to 30 per cent below normal, but in tests of their reproductive performance the animals were mated 63 times (Sax and Leibson, 1937). In a later experiment involving thyroidectomy and treatment with a thyroid preparation the range of basal metabolic rate within which mating occurred was 1.56 to 3.32 cal. per kg. per hour (Sachs, 1939). Not all the female


1212


HORMONAL REGULATION


rabbits thyroidectomized by Krichesky (1939) mated, but the oxygen consumption of those that did varied from 14 to 38 per cent l)elow average.

Results from the only experiments in which the measurement of sexual behavior was attempted are consistent with the hypothesis that marked deviations from the normal level of thyroid activity are not incompatible with the capacity for mating. In a study in which the male guinea pig was used (Young, Rayner, Peterson and Brown, 1952; Young and Peterson, 1952) it was found that, within the limits of an extreme hyperthyroidism and an extreme hypothyroidism, as estimated from measurements of oxygen consumption, heart rate, and the concentration of serum protein-bound iodine, the change in sexual behavior was not greater than in the controls. It was also shown that thyroid activity in groups of untreated high score and low score males was not different, thus eliminating the possibility that a deficiency of thyroid function could have accounted for the differences. In thyroid-parathyroidectomized male rats mating performance within 30 days after the operation was not significantly different from that in the preoperative tests (Heidenreich, Alexander and Beach, 1953). Transitory decreases in sexual behavior followed the administration of thyroxine and benzylthiouracil to male rats (Soulairac, Desclaux and Coppin, 1950), but by the 6th day the activity of the animals receiving thyroxine was again normal and by the 14th day normal or nearly normal activity was being displayed by those receiving the goitrogen. The circumstance that the changes following the establishment of opposite states were so nearly parallel made interpretation difficult.

A study of the female guinea pig in which measurements of sexual behavior were made revealed that the percentage of surgically thyroidectomized animals showing heat responses w^as 57.8 compared with 84.6 in the controls, 89.7 in females fed propylthiouracil in the drinking water, and 94.7 in animals injected with thyroxine (Peterson, Webster, Rayner and Young, 1952). The sensitivity of propylthiouracil-fed ovariectomized individuals to estrogen and progesterone was not different from that of the controls, but later tests of females thyroid


ectomized and given P'^^, ovariectomized, and injected with estradiol and progesterone revealed that fewer animals came into heat and that heat was shorter than in the controls (Hoar, Goy and Young, 1957). The reduced number of corpora lutea was suggestive of a hypo-ovarian condition; probably therefore the effect was general rather than confined to the neural tissues mediating mating behavior, but a lowered responsiveness of the experimental females to estradiol was also shown.

These data from the male and female guinea pig and from the male rat do not necessarily contradict the claims based on studies of other species such as the bull (Peterson, Spielman, Pomeroy and Boyd, 1941) that sexual behavior is inhibited in hypothyroid individuals. It is thought rather that the relationship between the tliyroid and reproduction varies from species to species and from individual to individual (Young and Peterson, 1952) :

"There may be species or individuals in whicli the range of thyroid activity coml)atiljle with reproduction extends from a relatively high degree of hyperthyroidism to a relatively low degree of hypothyroidism. The male guinea pig would seem to fall in this category. There may be other species in which the limits compatible with reproduction are narrower and they may lie in the middle of what we refer to as the spectrum of the thyroid activity, or they may lie toward either end. Reproduction in a species or individual dependent on a high level of thyroid activity might be adversely affected by a change toward hypothyroidism, whereas the converse might be true for a species or individual normally functioning at a relatively low level."

The nature of any stimulating or supporting action of the thyroid on mating behavior is unknown. When the male guinea pig was being studied the rate of oxygen consumption was increased from 52.4 to 80.1 cc. per 100 gm. body weight per hour by the injection of thyroxine without increasing the average strength of sexual behavior (Young, Rajmer, Peterson and Brown, 1952), and depressed to 37.3 cc. by thyroidectomy and injections of I^^^ without decreasing the average score significantly (Young and Peterson, 1952). In another experiment


HORMONES AND MATING BEHAVIOR


1213


(Peterson and Young, 1955j the mean rate of oxygen consumption of male guinea pigs exposed to cold was 77.3 cc. per 100 gm. body weight per hour whereas that of males kept at room temperature was 52.0, but the difference in mating behavior scores was not significant. Clearly in these experiments a considerable change in oxygen consumption was not accompanied by changes in sexual behavior.

Under other conditions, a relationship was found between the rate of oxygen consumption and the amount of sexual behavior. When males were given daily tests of sexual vigor the oxygen consumption of animals in 3 of 4 strains correlated significantly with sexual behavior (Riss, 1955). On the other hand, when the oxygen consumption of the fourth strain was elevated to a point approximating that of the strain having the highest rate, sexual behavior did not increase proportionately. In a subsequent experiment the rate of energy output was elevated by a change from isolation to unisexual group-living and the intensity of the sexual response increased correspondingly (Riss and Goy, 1957) . As before, the extent of the effect was limited by the nature of the animal. No assumptions were made concerning the physiologic meaning of the relationship between the rate of oxygen consumption and the strength of sexual behavior. The increased energy output may have permitted the change in activity, but there is no evidence that it was i:)rimary to the change.

F. THE SOMATIC FACTOR AND MATING BEHAVIOR

When the data bearing on the hormonal regulation of mating behavior in the male and female were being reviewed attention was directed to evidence for the conclusion that the character of the behavior induced by gonadal hormones is determined in a large part by the nature of the soma or substrate® on which the hormones act. Ad "In this review and in other discussions of the subject by the author and his associates soma or substrate is used in the sense of all the tissues mediating sexual behavior. The capacity for response to hormonal stimulation is assumed to be a function of the character of those tissues, however it is determined.


ditional evidence is provided by the many studies revealing the difficulty of inducing the behavior of the opposite sex by the administration of heterosexual hormones (p. 1198).

The principle seems first to have been stated by Goodale (1918), who was impressed by the failure of ovaries implanted into capons to feminize their behavior and he wrote, "the character of the sexual reactions seems to depend upon the substratum, while the gonad merely determines that it shall be given expression." Statement of the principle was also made or at least implied following the discovery that there is no constant relationship between the concentration of gonadal hormone and the amount of running activity in male rats (Heller, 1932), after investigations of the effects of heterosexual hormones on behavior (Ball, 1937a; Beach, 1941, 1942d), following efforts to correlate the ovarian condition and follicular development with mating behavior (Young, Dempsey, Myers and Hagquist, 1938), following the demonstration that individual differences in behavior before gonadectomy persisted throughout an experimental period when all the animals received the same hormonal treatment (Boling, Young and Dempsey, 1938; Boling, Blandau, Rundlett and Young, 1941; Young and Fish, 1945; Beach and Holz-Tucker, 1949; Grunt and Young, 1952b ) , and after observations that varied behavioral patterns were displayed by male rats in which there was no evidence of differences in the secretion of testicular androgens (Soulairac, 1950). Extension of the l^rinciple to tissues other than those mediating behavior is indicated by the substance of many articles reviewed by Hamilton (1948).

We dwell on tlie relationship between the character of the substrate and the pattern of behavior because the former as a determinant of the latter has much to do with the consistency with which the differences between individuals are displayed and with the circumstance that the same hormone given to different animals in the same amounts brings out such different patterns of behavior. It follows that identification of factors modifying the substrate or soma


1214


HORMONAL REGULATION


would help us in our analysis of the basis for the differences between individuals.

The possibility that differences in reactivity of the soma are associated with age, inherent rhythms in the tissues, seasonal changes, and the nutritional level is discussed by Young (1941) . More recently, new information bearing on the influence of age (Hooker, 1942; Price and Ortiz, 1944; Price, 1947; Thung, Boot and Mlihlbock, 1956), season (Bates and Riddle, 1941; Quin and Van Der Wath, 1943; Bradbury, 1944; McCormack and Elden, 1945; Phillips, Fraps and Frank, 1946; Lyman and Dempsey, 1951; Denniston, 1957; Michael and Scott, 1957; Harris, Michael and Scott, 1958; Kawakami and Sawyer, 1959a), and inherent rhythms (Emmens, 1939; del Castillo and di Paola, 1942; Jones and Astwood, 1942; Clark, 1947; Gillman and Gilbert, 1948) has been presented, but as we noted in 1941, when animals are homogeneous with respect to these factors, all can be eliminated.

An effect of abnormal thyroid activity in the male guinea pig can be discounted by the demonstration that the strength of sexual behavior can be so different in individuals in which the level of thyroid activity is so nearly the same. Some limiting action was demonstrated by Riss (1955) and by Riss and Goy (1957), but not even in the rigorous tests they gave was evidence found that oxygen consumption fixes the strength of sexual behavior. In the female, on the other hand, the level of thyroid activity seems to be important for the maintenance of normal responsiveness (Innes, Young and Webster, 1947; Peterson, Webster, Rayner and Young, 1947 ; Peterson and Young, 1955; Hoar, Goy and Young, 1957), but as with age, seasonal changes, and the nutritional level, deviations from the mean can easily be detected and controlled. This leaves us with little to fall back on except the genetical factor and experience, possibilities that must be considered separately.

The assumption that genetical factors are influential in determining the character of the soma is based on many observations. An impaired sexual behavior was encountered in inbred rats in which demonstrable defects in folliculogenesis and germ cells did not exist (Evans, 1928; Craig, Casida


and Chapman, 1954). Evidence that differences in the running activity of rats are inherited is presented by Rundquist (1933) and Brody (1942). Rasmussen (1952) estimated the strength of sex drive of male and female rats tested in a modified Columbia obstruction apparatus and conducted selective breeding for five generations. In the first generation of selection the differences in the number of crossings were not great, but in the F5 generation male and female offspring of parents with high sex drive crossed about six times as frequently as the offspring of parents with low sex drive. Symptoms of heat vary in breeds of cattle (Lagerlof, 1951). The Simmenthaler cows in Switzerland, the Telemark cows in Norway, and the Swedish Highland breed have as a rule intense and pronounced heat symptoms. In the Swedish red cattle the heat is often so weak that in winter it is detected with difficulty. Three triplet Shorthorn bulls raised in the same environment were alike in their lack of interest in serving (Olson and Petersen, 1951 ) . The mating behavior of six pairs of twin bulls was followed from IY2 to 7 years. During this time the individual pairs were extraordinarily alike, but the differences between the pairs were very great (Bane, 19541. Differences in libido in the brown Leghorn cock are under genetical control (Wood-Gush and Osborne, 1956). In a breeding experiment it was revealed that the females had made a significant contribution to the genetical variance (WoodGush, 1958a).

The highly inbred guinea pigs (strains 2 and 13) in the colony at Kansas exhibit significant differences in their patterns of behavior. Males in strain 2 nibble and nuzzle more actively, whereas the frequency of mounting, intromission, and ejaculation is greater in strain 13 (Valenstein, Riss and Young, 1954) . Their rates of sexual maturation are slower than that of males from the genetically heterogeneous stock. The differences were not overcome by injecting animals castrated soon after birth with large amounts of androgen (Riss, Valenstein, Sinks and Young, 1955). The possibility that quantitative or qualitative nutritional factors in the mother's milk or some feature of the care might account for the differences


HORMONES AND MATING BEHAVIOR


1215


was excluded in an experiment in which inbred and genetically heterogeneous young were interchanged the day of birth. As before, the sexual behavior of the inbreds was significantly lower than that of the heterogeneous males ( Valenstein and Young, 1953).

Genetical factors are important determinants of the character of the soma in the female. Ovariectomized guinea pigs from the inbred strains and genetically heterogeneous stock at Kansas have been studied following their injection with controlled cjuantities of estradiol benzoate and progesterone (Goy and Young, 1957b). As in the male, differences were seen in every measure of behavior studied: responsiveness to treatment as determined by the percentage of females brought into heat, duration of the induced heat, length of the interval between injection of progesterone and the beginning of heat, duration of maximal lordosis, interval between the beginning of heat and maximal lordosis, and amount of male-like mounting. The rank order of these measures varies greatly and, with respect to the behavior of males from the same strains, unpredictably (Young, 1957).

Attempts have been made to study the mode of inheritance of the elements composing the patterns of behavior in males and females. The display of courtship and copulatory behavior in crosses of the two fishes, Xiphophorus {Platypoecilus) maculatus and X. helleri, was recorded in an inherently difficult study (Clark, Aronson and Gordon, 1954). Some influence of heredity was revealed, but the genetical data were not such that a precise analysis in Mendelian terms could be made. No special correlations were possible between known genes and behavioral elements of the parental species, between diagnostic morphologic features and behavior, or between courtship and copulatory behavior. Intraspecies crosses have been studied in the guinea pig and their behavior reported briefly (Jakway, 1959; Goy and Jackway, 1959). This species, and doubtless otlier mammals, presents some advantages not possessed by fishes, notably the numerous well defined measures displayed by the female. On the other hand, as in the work on fishes, analysis


has been of average rather than of individual performance. In their inheritance, elements of the patterns behave independently. Within the male, dominance of the lathargic strain 13 type of behavior is limited to the lower measures (circling, nuzzling, mounting). A dominance of the strain 2 type of behavior is suggested for the higher measures (rate of intromission and number of ejaculations). Within the female three independent genetical factors appear to determine the character of estrus. Latency and duration of heat, and percentage of response show phenotypic dominance of the strain 2 type. Duration of the maximal lordosis is determined by a single genetical factor without dominance. Inheritance of male-like mounting is also of an intermediate type, but more than one genetical factor is indicated and the possibility of modifiers exists. Beyond observations of this type, little progress has been made, but the possibility of further analysis is clearly evident.

The suggestion that the character of the soma is influenced by experience or perhaps better, until the type of experience can he defined, by contact with other animals, is based on studies of cattle, chickens, ringdoves, turkeys, cats, rats, dogs, guinea pigs, and chimpanzees. The problem is discussed by Beach (1942e, 19421, 1947, 194748, 1958a), Ford and Beach (1951), Kagan and Beach (1953), Valenstein, Riss and Young (1955), Valenstein and Young (1955), Valenstein and Goy (1957), Goy and Young (1957a), Young (1957), Rosenblatt and Aronson (1958a, b), Zimbardo (1958), Wortis and Rosenblatt (1959), Wood-Gush (1958b), Schein and Hale (1959). What seems to be the first demonstration of the importance of contact with other animals for the organization of the mature pattern of behavior was given by Craig (1914) following his study of ringdoves reared in isolation. For many years little was done with the factors to which he directed attention, but since 1940 the importance of psychologic factors for the organization and modification of patterns of mating behavior has been the subject of many articles and discussions.

Conditioned reflexes leading to copulation


1216


HORMONAL REGULATION


and ejaculation in bulls are inhibited l)y strange surroundings, by delays in admitting the bull to the cow in estrus, by pain at the time of service, and by too frequent services under the same conditions (Milovanov and Smirnov-Ugrjumov, 1944). White Leghorn cocks tend to be consistent in the frequency of matings when they are not inhibited by the presence of other males. When, however, 4 cocks raised together without contact with hens for about 3 months were placed in a pen containing 7 hens, a suppression developed which tended to persist after the dominant cock was removed (Guhl, Collias and Allee, 1945). No clearcut difference was found between brown Leghorn males reared in isolation until the age of 61/9 months and males wliicli had been reared with other birds (WoodGush, 1958b). In an experiment with turkeys, birds raised in groups displayed less apparent sexual behavior than the isolated birds (Schein and Hale, 1959). This result will be recalled when that obtained by Beach (19421) on rats is described (second paragraph below).

From what was observed during a study of the male dog (Beach, 1947-48), satisfactory sexual relations were placed high on the list of experiences augmenting sexual interest in later tests. Attack or aggression by a female, however, is an experience which can have a depressing effect. Rosenblatt and Aronson (1958a) reported that castration of the male cat was followed by the eventual loss of sexual behavior with copulatory responses dropping out first, followed some time later by the loss of mounting behavior. On the other hand, sexual experience before castration retarded the loss of sexual behavior for periods up to 2l/i years.

Following a study of the rat, Beach (1942i) reported (1) that the proportion of copulators was highest among males raised in isolation, and (2) that during tests in which no copulation occurred, males raised in isolation tended to be more responsive to the female than males raised with females. The high incidence of copulations among the isolated animals was attributed to two factors : greater excitability resulting from the novelty of contact with a second animal, and greater weight. The relative sexual inactivity of males raised in segrega


tion was attributed partially to an increase in homosexual tendencies.

In a later study (Kagan and Beach, 1953) male rats were placed in individual cages from the 36th day of age until the end of the experiment. From day 37 to day 100 the animals were given different kinds of experience. Males in group A were exposed once a week to a receptive female, group B males were exposed at weekly intervals to a male, group C males were placed once a week in an empty cage, and group D males received no conditioning. Beginning day 99 the rats were tested with a receptive female. No group differed significantly with respect to the number of males displaying some copulatory behavior, but the complete pattern including ejaculation was displayed more than twice as frequently by the males lacking previous contact with other rats than it was by the animals which had been exposed to either males or females. The data are taken to indicate that patterns of social behavior formed before complete mating is physically possible tend to persist and partially to inhibit the normal sexual responses.

The results from a recent study of rats reared in isolation (Zimbardo, 1958) are at variance with those reported by Beach and Kagan. Except for the frequency of mounts, according to Zimbardo, the differences in sexual performance between males reared in isolation and those reared in part-time cohabitation are large and, in general, statistically reliable. The latter mounted faster than those reared in isolation, copulated sooner and with greater frequency, and had a larger percentage of the total group ejaculating. Zimbardo concluded that the sexual performance of male rats reared in isolation is inferior to that of rats reared in cohabitation and that in this respect the rat is similar to, rather than different from, the guinea pig The development of sexual behavior in chimpanzees was studied by Nissen (1954). Males and females, after having been raised in a nursery for 2 to 3 years, were transferred to large cages where they lived in sex-mixed groups. Before puberty the sexes were separated and placed in adjacent cages so that they could still have visual and auditory contact with each other. Starting well after


HORMONES AND MATING BEHAVIOR


121'


puberty the animals were paired under observation in male-female combinations, and in such a way that the younger inexperienced animal was with an older experienced animal of the opposite sex. In many hundreds of sessions the complete pattern did not occur, although almost all the component or unit acts composing the pattern did appear. In Nissen's words, except for minor modifications, the component acts are either innate or learned in early life without the act of learning being observed. The complete sequential pattern of mating behavior, on the other hand, is not innately determined, or at best, the innate factor is only a readiness or predisposition to learn.

The establishment of the biologically effective pattern of mating behavior, in which there is a precise temporal organization of the components and in which the response of each animal is adjusted to that of the other, seems to be a matter of trial-and-error learning, which can be viewed in terms of the statistical probability that certain concatenations of behavior on the part of the two animals will occur. Several factors can be identified as increasing or decreasing such a probability. First and foremost is the activity level, the more and the more varied the activity, the more likely is the occurrence of the critical pattern. Closely related with this first factor is that of age. As the chimpanzee matures, he slows up in the amount of activity in which he engages. As he slows up, the probabilities of there being the concatenation mentioned above are reduced.

The guinea pig probably has been studied more completely than any other species. Preliminary experiments yielded data bearing on the performance of segregated versus isolated males, the influence of frequent copulatory experience, the strength of sexual behavior of dominant and submissive males, and the effect of confinement of adult males with females.

When relatively young and sexually inexperienced males were tested (Young, Grunt and Valenstein, 1951), experience gained during 10 tests did not reveal any difference between the performance of 37 males raised with other males and that of 32 isolated males which could not be accounted for by adaptation to the presence of another animal at the time of the tests.


In an exi)eriment in which freciucnt sexual experience was given (Riss, unpublished data ) , 4 males having average scores of 11.2, 8.4, 6.6, and 5.5 in 10 perliminary tests were tested daily for 51 days. Improvement was shown by the male whose score was 6.6. He became the most active copulator in the group with an average score of 9.2 for the last 20 of the 51 daily tests, but he was the only male whose behavior clianged.

A comparison of these results obtained on the guinea pig with those obtained by Larsson (1959) on the rat would be of interest, but different data were recorded so a coml)arison cannot be made. Larsson found, however, that learning intervened only in determining the lengths of the postejaculatory latencies; the other changes appearing in the pattern of behavior with increasing age were consequences of maturing processes.

In a study of dominance and submissiveness (Riss, unpublished data) the behavior of 16 male guinea pigs that had received 10 lireliminary tests deviated markedly in a competitive situation, according to the dominance or submissiveness of the animal, but when they were replaced in isolation the behavior returned to a level not greatly different from that shown during the preliminary tests. Clearly this experience had little or no lasting influence on the pattern of behavior characterizing the individuals.

Sexual performance was affected significantly in these experiments only after a number of low score males had been confined with adult females for 60 days (Riss and Young, 1953). Before their confinement with the females the average score achieved by 7 males in 10 tests was 3.8 whereas after confinement and return to isolation the average score in 10 tests was 4.9. The difference is significant at the 5 per cent level. A group of 7 males never removed from isolation had average scores of 4.5 and 4.7.

If any impression came out of these preliminary experiments, it was one of fixation or stability of the individual pattern of sexual behavior. Not until experiments were performed in which very young animals were used, was there any clear indication of the extent to which contact with other animals affects ]iatterns of behavior in the male guinea pig (Valenstein, Riss and Youne,


1218


HORMONAL REGULATION


TABLE 19.3

Comparison of sexual behavior of male guinea pigs raised in isolation with that of males raised unth females

Data obtained from 7 tests, day 77 to 120, after all males were isolated.

(From E. S. Valenstein, W. Riss and W. C. Young, J. Comp. & Physiol. Psychol., 48, 397, 1955.)


Animals (Group)


Heterogeneous males (I)

Isolated day 25

Social situation

Strain 2 males (II)

Isolated day 25

Social situation

Strain 13 males (III)

Isolated day 25

Social situation

Heterogeneous males (IV)

Isolated day 10

Social situation


No.


Lower Measures


Mountings


Intromissions


Ejaculations


Average animal


Per cent

displaying


Average

per animal


Per cent

displaymg


Average

per animal


Per cent

displaying


Average

per animal


Per cent

displaying


7


70.2


100


17.4


71


12.6


71


4.4


71


7


36.4


100


19.6


100


20.6


100


6.7


100


17


149.0


100


.1.2


35


0.5


6


0.06


6


19


97.3


100


18.0


100


18.0


90


3.7


84


7


129.4


100


2.0


71


0.0



0.0



7


96.4


100


6.4


80


7.6


57


0.6


57


10


120.8


100


10.6


30


6.5


30


1.5


30


10


52.9


100


14.3


100


19.6


100


5.3


100


Average Score


7.5 9.9


3.6 3.0


4.9 8.1


1955). The subjects were from the genetically heterogeneous stock and the inbred strains 2 and 13. Experimental males (the isolated males) were placed alone with their mothers from the day of birth until day 25 and isolated thereafter. Control males (the socially reared males) were raised with animals of the same age from the day of birth until day 73 when they were isolated; the mothers were removed on day 25. Both groups of males were given the first of 7 weekly tests on day 77.

The data (Table 19.3, group I) revealed that the performance of the genetically heterogeneous males raised in the social situation was somewhat better than that of the males brought up in isolation, although the difference is not statistically significant. The clearest picture came from the results obtained from strain 2 males in which the development of the measures of behavior above mounting seemed almost completely dependent on the contact they had had with other young animals (Table 19.3, group II). The strain 13 males showed some development of the complete sexual pattern following their experience in the social situation (Table 19.3, group III), but the level reached, although significantly higher than that attained by the isolated males, was considerably below that of the strain 2 and heterogeneous males.

As the work progressed, male cage-mates


were found to provide sufficient experience for the organization of sexual behavior in other males. Males raised with spayed females, on the other hand, performed more poorly than males of the same strain raised with intact females or males (Valenstein and Goy, 1957) . Apropos of this, it has been observed repeatedly in the Kansas laboratory that even a sluggish male mounted by an estrous female is stimulated to mount in return. Untreated spayed females, however, liave never been observed to initiate mounting. It is possible, therefore, that the poorer performance of the males raised with spayed females is explained by a lack of provocation to attempt mounting and thereby to gain experience.

A number of conclusions became apparent. (1) The importance of contact with other animals for the development of normal patterns of sexual behavior in the male guinea pig has been demonstrated. (2) The influence exerted by contact with other animals operates within the limits of a certain genetical background. (3) The influence of contact with other animals can be exerted very early in the life of an individual.

Just how early in the life of a male contact with other animals can be effective was shown by Valenstein in an experiment designed to test the hypothesis that the very slight diffei'ences in the heterogeneous animals weaned on day 25 and brought up in


HORMONES AND MATING BEHAVIOR


1219


the two social situations might be explained by the earlier maturation of animals in this stock. He suggested that if males were weaned and isolated at 10 days of age instead of on day 25, a greater difference might be shown between the isolated animals and those brought up in the social situation. In the first test a completely convincing confirmation of the hypothesis was given (Table 19.3, group IV). The failure to obtain a greater difference in the earlier experiment with the heterogeneous males (group I) was obviously attributable to the circumstance that the contact these animals had with other animals during the first 25 days was sufficient to insure the development of essentially normal patterns of sexual behavior.

The possibility that an adult male without previous opportunity for organization of the higher measures of sexual behavior could improve his sexual performance by contact with other animals at an older age has been investigated (Valenstein and Goy, 1957) . Each of several genetically heterogeneous males which had not exhibited any of the more mature behavior in tests given during the period of isolation was placed with 2 females for 23 days when they were 320 to 430 days of age. In subsequent tests all these males demonstrated the ability to mount, to have intromissions, and to ejaculate. Strain 2 males at older ages did not acquire the copulatory pattern so readily; 2 of 5 achieved intromission and ejaculation after being placed with females, Ibut none of the remaining 3 displayed any of the higher measures of sexual behavior. The result is consistent with the earlier finding (Valenstein, Riss and Young, 1955) that young males from this strain require a longer time to organize this pattern of behavior. The data as a whole indicate that the emergence of sexual behavior patterns in the male guinea pig is not restricted to an early critical period comparable with that described in the literature dealing with imprinting (Lorenz, 1937). On the other hand, an analysis of the data i)resented by Valenstein and Goy (1957) reveals that contact with other animals is not as effective in organizing tissues for mating in older males as it is in young males.

What was regarded as a crucial test of the effect of the experiential factor on the


character of the soma w^as a comparison of the response of isolated and socially reared strain 2 males to androgenic stimulation (Valenstein and Young, 1955). Following 7 tests which revealed the difference in their performance, the males brought up under the two social conditions were castrated, allowed to go without treatment until the regression in sexual behavior had reached the base-line of change, and then injected daily with testosterone propionate until the precastrational level of behavior was reached. The return of each group to the level characterizing it before castration is evidence for the conclusion that the responsiveness of the tissues mediating mating behavior to androgenic stimulation had been altered by a psychologic factor.

The results from the studies on the male guinea pig are felt to have provided a sound basis for a hypothesis that would account for the establishment of patterns of sexual behavior in this species. They suggest that the nervous organization on which response to sexual stimulation depends is influenced at a very early age by contact with other animals. On the other hand, genetical as well as experiential factors are important and the pattern displayed in response to androgenic stimulation is a resultant of the co-action of the two factors. But indirectly the testicular hormone may also be involved in the establishment of these patterns of behavior. To be sure, their organization, as estimated by mounting proficiency, can occur in the absence of the testes (Beach and Holz, 1946; Riss, Valenstein, Sinks and Young, 1955). On the other hand, if the organization of these patterns depends on experience gained through mounting, the testis hormone, by increasing this activity, may exert an indirect influence on the neural tissues in which the organization of patterns occurs.

Before leaving the male, we would call attention to the hypothesis that in the rat and guinea pig the copulatory response is innate rather than acquired (Stone, 1922; Louttit, 1929; Beach, 1942g, 19421, 1951; Kagan and Beach, 1953) . The data reviewed for the guinea pig j^rompted us to question the validity of the hypothesis for this species. The report that palpation with pelvic thrusts occurs in the rat as early as day


1220


HORMONAL REGULATION


21 (Beach, 1942c » suggested that such contact with siblings might be sufficient to organize the adult pattern of sexual behavior in this species (Valenstein, Riss, and Young, 1955). Beach (1958a) believes, however, from the results of a more recent experiment, that this possibility can be excluded.

Males were isolated at 14 days just when the eyes are opening and before they could possibly have had experience mounting their cage-mates. At age 90 to 100 days 13 experimental animals and 12 siblings which had been reared together were tested. In the first 10-minute test, 4 of the experimental and 5 of the control males mated. The copulatory performance of the experimental animals was perfect. Without exception the first mount resulted in intromission. The latencies (seconds from the time the female is placed in the cage to the first intromission) were 195, 180, 60, and 8 seconds. In the controls the latencies were 110, 105, 75, 40, and 25 seconds. The average number of intromissions before ejaculation was 8.2 for the experimental males and 7.0 for the controls. Zimbardo (1958» was frankly critical of this latter experiment and, as we have noted, states that his results are in agreement with those obtained from the guinea pig. If he is correct, the rat is not a species in which development of the copulatory response l)y the male is innate; on the contrary, it should l)e placed with the guinea pig, cat, and chimpanzee in which some influence of contact with other animals contributes to the patterning of sexual behavior.

Regardless of the status of the rat/" foi'

^"The reader who has reached this point will be keenly aware of the extent to which data from the rat and guinea pig have contributed to the thinking of investigators interested in the hormones and mating behavior. He will also recall that there are many references to similarities and differences between these species. For his convenience, they are listed here.

Differences between the species would appear to be more numerous than similarities. The hormones which elicit male and female behavior are the same (Dempsey, Hertz and Young, 1936; Boling and Blandau, 1939; Beach, 1942a; Stone, 1939a; Beach and Holz-Tucker, 1949) and in both species it is clear that differences between individuals have a somatic rather than a hormonal basis (Young,


no investigator has denied that there is some influence of contact with other animals, the conclusion is clear that in all species studied the character of sexual behavior is influenced l)y an experiential factor. Of importance for one who would generalize, is the fact that most studies were of male ; only in Nissen's work on the chimpanzee were data obtained from the female. As a means of narrowing this gap, a study of the female guinea pig was undertaken (Goy and Young, 1957a). The results, although leaving much to be explained, are striking. In the strains which display mounting behavior the amount disl)layed by females reared in isolation was consistently less than that displayed by females raised with other animals. In all strains the duration of heat was shorter in the isolated females, as was the duration of lordosis. The effect on mounting behavior was not imexpected, especially if this measure of estrous behavior is a homologue of the behavior displayed by the male (Beach, 1943 ». At the moment, however, we cannot account for the shorter duration of heat and maximal lordosis in the isolated females. These measures are generally thought to be reflex in nature and therefore independent of any influence from other animals.

A final suggestion with respect to ex Dempsey, Myers and Hagquist, 1938; Beach and Holz-Tucker, 1949 ; Grunt and Young, 1952b ; Valenstein and Young, 1955; Goy and Young, 1957b). The basic pattern of behavior in females of the two species is similar (Ball, 1937b; Young, Dempsey and Myers, 1935; Blandau, Boling and Young, 1941), but the patterns of beha\ior characteristic of the males are different (Stone, 1922, 1924b; Stone, Tomilin and Barker, 1935; Stone and Ferguson, 1940; Beach, 1944b; Beach and Holz, 1946; Young and Grunt, 1951). In the male rat the strength of sexual behavior is considered proportional to the amount of exogenous testicular hormone (Beach and Holz-Tucker, 1949; Beach, 1956); data from the male and female guinea pig do not support such a conclusion (Grunt and Yoimg, 1952b; Riss and Young, 1954; Goy and Young, 1957b). Malelike mounting by the female rat does not coincide closely with estrus and appears to be displayed independently of the ovarian hormones (Beach and Rasquin, 1942) ; in the female guinea pig mounting is displayed only during the proestrum and estrus, or in spayed animals only following treatment with estrogen and progesterone (Young. Dempsey, Hagquist and Boling, 1939; Young and Rundlett, 1939; Goy and Young, 1957a, b).


HORMONES AND MATING BEHAVIOR


1221


perience and the deterniinution of the nature of the response to gonadal hormones has a genesis that is entirely different from anything presented in the earlier part of our discussion. Green, Clemente and de Groot (1957) reported that prepubertal male cats displayed masculine behavior when testosterone was administered, and feminine behavior when stilbestrol tablets were given intramuscularly. They characterized the effect as "reversible." When adult males were treated, masculine behavior was displayed, not only in response to testosterone propionate, but also in response to the female hormones, estradiol and stilbestrol; this effect was "irreversible."

The authors' explanation for the different action of the steroids before and after puberty was frankly speculative. It seemed "unlikely that education in any ordinary sense is involved after the first coitus," and they suggest that "the type of first sexual experience may determine the subsequent behavioral reaction to hormones that have the same effect on the secondary sex characteristics and reproductive tract both before and after puberty."

Elsewhere they continue, "Perhaps the simplest explanation is that before sexual experience, the steroids set the stage for later education and determine the animal's receptivity to another kind of experience; that is, they determine the mood of the prepuberal animal. Without full experience then, the mood is reversible; but once experience has been acquired, the pattern of behavior is set and is not changed by the administration of the steroids of the opposite sex. The steroids in the adult would thus be assumed to increase drive in a nonspecific way." Clearly, in this latter investigation, there are difficulties, especially if an extension of the hypothesis to the female is to be inferred. At this stage, a considered evaluation of what is proposed cannot be given.

For all who are investigating the patterning of mating behavior through contact with other animals, the circumstance that some of the results have varied when the development of such behavior in different species was being studied need not concern us, except as it stimulates further and


better designed exjieriments and reveals any evolutionary trend. A common denominator is that at many levels the experiential factor has been demonstrated to be related to the character of the behavior brought to expression by the gonadal hormones. Against this background, a number of problems are of obvious interest: identification of the effective element or elements in the contact with other animals, the locus of action — whether it is on the arousal mechanism or the consummatory mechanism, or both, any relationship between the age of the animal and the influence of these experiential factors on the character of behavior, any effect of the presence of gonadal hormones on the learning process, and, no doubt, others. Fortunately, most of these problems are already receiving attention.

IV. Concluding Remarks

The frequency with which reference is made to the many articles that have appeared since sexual behavior was discussed in the second edition of Sex and Internal Secretions attests to the activity during that interval. The years were characterized by a gratifying accumulation of data, by important advances in methodology, and by a challenging speculation with respect to factors regulating the display of sexual behavior during adulthood and influencing its development in young animals. These have been seen to be genetical, psychologic or experiential, and hormonal. The part played by each can be visualized by recalling two generalizations which emerged from the numerous data reviewed in the preceding sections. The first is that the pattern of mating behavior is mediated by tissues in which a certain organization has developed or, perhaps better, by tissues on w^hich a certain character has been conferred. The second is that mating behavior is always displayed with a certain strength or vigor, regardless of the pattern. We will risk a temporary confusion by adding that, whereas the strength or vigor of behavior can be thought of and dealt with as a separate concept, in the animal it is also a part of the pattern of behavior (Young, 1957). No species is an exception to these general


1222


HORMONAL REGULATION


izations and they are applicable to both sexes.

In the adult, and possibly in the neonatal and sexually immature animal as well, there is no evidence that the hormones have any effect on the organization of the tissues mediating mating behavior. Genetical factors are of obvious importance and account for the differences between species, for the differences between sexes, and, in subhuman species if not in man as well, for many of the differences between individuals. Psychologic or experiential factors are also important, and, as with genetical factors, the extent depends on the species and the sex. But, in contrast to the genetical factors, the influence of psychologic factors is greater in the higher than in the lower mammals. These factors probably have achieved a dominant role in man in whom there is a clear dependence on his culture (Ford and Beach, 1951; ]\Iead, chapter 24), his experience (Heller and Maddock, 1947; Kinsey, Pomeroy, ]\Iartin and Gebhard, 1953; and many others ) , and his sex of assignment and rearing (Finesinger, jVIeigs and Sulkowitch, 1942; Ellis, 1945; Money, 1955; Money, Hampson and Hampson, 1955, 1957; Hampson, Hampson and Money, 1955; Hampson, ]\loney and Hampson, 1956 L In two lower mannnals, the guinea pig and cat, psychologic factors are clearly operative (Valenstein, Riss and Young, 1955; Rosenblatt and Aronson, 1958a, b); more in the male, we believe, than in the female (Young, 1957 1 . The conclusion that, in even the neonatal and young animal, the development of the pattern of behavior may be independent of gonadal hormone action is based on results from a number of experiments. When the gonads have been removed within a day or two after birth or have been congenitally absent, normal patterns of behavior were later displayed, provided of course the appropriate hormones were administered, and in the male, provided there had been contact with other animals (Wilson and Young, 1941 ; Beach, 1945b; Beach and Holz, 1946; Riss, Valenstein, Sinks and Young, 1955 L

During the prenatal period the situation is quite different. The operation of genetical factors is assumed, but more dramatic is


the demonstrated action of hormonal factors, especially on the female (Phoenix, Goy, Gerall and Young, 1959) . During this period they seem to be organizational, very much as they are organizational in the differentiation of the genital tracts (Burns, 1942, 1949, and his chapter in this book; .lost, 1947, 1953, 1957; Wells, Cavanaugh and Maxwell, 1954; Price, 1957). Preliminary evidence indicates that when a male hormone is present, the capacity for the eventual display of masculine behavior develops and the capacity for the display of feminine behavior is suppressed in males and in females. Without more information, the comparison may not be extended to the role of a fetal female gonadal hormone. Development of the capacity for displaying the copulatory response (lordosis) may reciuire the presence of such a hormone or it may be genetically determined, but experiments comparable with those performed especially by Jost and by Wells, Cavanaugh and Maxwell have yet to be performed by investigators interested in the development of the capacity for displaying mating behavior.

Returning now to the concept that mating behavior is always displayed with a certain strength or vigor, we find ourselves limited to the postpubertal period when the complete pattern is displayed. As we have noted, the potential strength or vigor with which mating behavior is displayed is a part of the pattern and as such is genetically and, in man, possibly psychologically determined. But in all subhuman mammals and almost certainly in the human male (see chapter by Money), the strength or vigor of male behavior is related to the gonadal hormones. The evidence is not clear for the human female. The retention of sexual responsiveness after the natural or a surgical menopause (Filler and Drezner, 1944) suggests an emancipation from hormonal control. On the other hand, the enhanced sexual desire following the administration of testosterone propionate (Shorr, Papanicolaou and Stimmel, 1938; Salmon, 1942; Greenblatt, 1943; Carter, Cohen and Shorr, 1947) suggests that, as in the male, emancipation is not complete.

Tlie vievv- we have attempted to express


HORMONES AND MATING BEHAVIOR


1223


with respect to the role of gonadal hormones in the development and expression of mating behavior was long ago stated by Zuckerman and Parkes (1939) in another context: "Androgen stimulation induces the two main types of change. The first leads to assumption of permanent characters, the second to the assumption of characters which disappear when androgen stimulation ceases."

Their thought was of secondary sexual characters, of genital tract structure, and, we would guess, only incidentally of behavior. Twenty years later we may go further than the data available to them permitted and extend the hypothesis to the tissues mediating mating behavior. We would direct attention to the possibility that in these tissues the same rules apply, but, in addition to hormonal (and genetical) factors, psychologic factors have appeared, and, as animals have evolved, a picture has been created in which there is a mingling and in some way an interaction of all these factors. Elucidation of the manner in which this occurs and its extent will depend on the continued effort of investigators from many disciplines.

A final remark has to do with an aspect of the subject that has not had treatment in the present review. The discussion up to this point has dealt principally with mating behavior, that restricted part of the total behavior which subserves reproduction more directly than it does any other vital activity. However, as investigations have proceeded, it has become apparent that the action of the gonadal hormones is much broader than we realized years ago when attention was first being focused on the relationship of these substances to mating behavior. The fact will be apparent from what has been written about the role of these substances in parental behavior (chapter by Lehrman) and in social behavior (chapter by Guhl). Recent work suggests that this concept may be extended even further. Not all the behavior associated with the male or the female is reproductive. Many differences between the behavior of males and females have been described, and many more are a part of the cultural lore. The .subject is too vast for review here, but two exami)les will be mentioned. The male chim


l^anzee is said to be a fighter and a bluffer, the female is treacherous and more difficult than the male to bluff consistently (Yerkes, 1943; Hebb, 1946). Differences between the sexes are seen in the play configuration of preadolescent children (Erikson, 1951). In their chapter in this book, Hampson and Hampson have discussed this "psychologic sex" and suggested that it "does not have an innate, preformed instinctive basis as some have maintained," but rather is "undifferentiated at birth ... a sexual neutrality in the place of the Freudian bisexuality . . . and that the individual becomes differentiated as masculine or feminine, psychologically, in the course of the many experiences of growing up."

As evidence has accumulated (Burns, 1942, 1949, and his chapter in this book; Jost, 1947, 1953, 1957; Wells, Cavanaugh and Maxwell, 1954) that the fetal gonad (probably the testis rather than the ovary) is the source of a hormone with androgenic properties, investigators have asked if the action of this substance may not extend beyond the genital tract and tissues mediating mating behavior, to the "behavior beyond that which is purely sexual" (Phoenix, Goy, Gerall and Young, 1959). Undoubtedly this hypothesis will soon be tested. If it is found to be true, an unsuspected action of the gonadal hormones will have been revealed, an action, we predict, that will be a bond between the work of the experimental embryologists who have concerned themselves so completely with all that is involved in the development and differentiation of the genital tracts, and the work of the psychologists and psychiatrists for whom the development and differentiation of neural tissues presents problems of equal interest and importance. In addition, a big circle will have been completed. Analysis of sexual differentiation during the embryonic and fetal periods began with the work of the experimental embryologists, much of which is reviewed in Editions 1 and 2 of Sex and Internal Secretions. A segment of the work reviewed in this chapter was started in that atmosphere, and attention is directed to the fact that, once the basis was established, much of the conceptualization outlined here developed from the investigations and thought of that group of older colleagues.


V. References

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Morris, D. 1955a. The causation of pseudofemale and pseudomale behaviour; a further comment. Behaviour, 8, 46-56.

Morris. D. 1955b. The reproductive behaviour of the river bullhead (Cottus gobio L.). witli special reference to the fanning activity. Behaviour, 7, 1-33.

MoYNiH.AN, M., and Hall, M. F. 1955. Hostile, sexual, and other social behaviour patterns of the spice finch (Lonchvra punctulata) in captUit;- Behaviour. 7, 33-76.


MiJHLBGCK, 0. 1940. Keine antagonistische Wirkung des Oestradiolbenzoates auf die Kopulationsfiihigkeit mannlicher mit Testosl(>ronpropionat behandelter Ratten. Acta, brev. neerl. Physiol., 10, 69-74.

Nelson, W. O., and Gallagher, T. F. 1936. Some effects of androgenic substances in the rat. Science, 84, 230-232.

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NissEN, H. W. 1954. Personal communication."

Noble, G.K.,.\ND KuMPF, K. F. 1936. The sexual behavior and secondary sex characters of gonadectomized fish. Abstract, Proc. Am. Soc. Zool., Anat. Rec, 67, Suppl. 1, 113.

Noble, G. K., and Wurm, M. 1940a. The effect of testosterone propionate on the blackcrowned night heion. Endocrinology, 26, 837850.

Noble, G. Iv., and Wurm, M. 1940b. The effect of hormones on the breeding of the laughing gull. Abstract, Proc. Am. Soc. Zool., Anat. Rec, 78 (Suppl. 1), 50.

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Noble. G. K., and Greenberg, B. 1941b. Effects of seasons, castration and crystalline sex hormones upon the urogenital system and sexual behavior of the lizard (A)iolis carolinensis) . I. The adult female. J. Exper. Zool., 88, 451479.

Noble, G. K., and Aronson, L. R. 1942. The sexual behavior of Anura. I. The normal mating pattern of Rana pipiens. Bull. Am. Museum Nat. Hist., 80, 127-142.

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Okada, Y. K., and Yamashita, H. 1944. Experimental imcslijiatidii of tlie manifestation of .sec<)ii(l;ir\- scNuid cliaracfrrs in fish, using the Mekada, Oryzni.s loli/>is ( Temminck & Schlegel) as material. J. Fac Sc Imp. Univ. Tokvo., Sect.IV, 6, 383-437.

" The material cited in this chapter was selected from the substance of a talk given by Dr. Nissen and entitled, "Development of Sexual Behavior in Chimpanzees." The complete paper is containefl in an unpublished symposium, "Genetic, Psychological, and Hormonal Factors in the Establishment and Maintenance of Patterns of Se.xual Behavior in Mammals." A copy of the symposium is on file in the Uni\-ersity of Kansas Library, F 591.16 Sv68 1954


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PiNcus, G. 1956. Aging and urinary steroid excretion. In Hormoiien and the Aging Process, E. T. Engle, and G. Pincus, Eds., pp. 1-20, New York: Academic Press, Inc.

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Price, D., and Ortiz, E. 1944. The relation of


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Reed, C. A., and Reed, R. 1946. The copulatory behavior of the golden hamster. J. Comp. Psychol., 39, 7-12.

RicHDALE, L. E. 1951. Sexual Behavior in Penguins. Lawrence : University' of Kansas Press.

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Richter, C. P., and Hartman, C. G. 1934. The effect of injection of amniotin on the spontaneous activity of gonadectomized rats. Am. J. Physiol., 108, 136-143.

Richter, C. P., .and Uhlenhuth, E. H. 1954. Comparison of the effects of gonadectomy on spontaneous activity of wild and domesticated Norwa}' rats. Endocrinology, 54, 311-322.

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Riddle, O. 1924. A case of complete sex-reversal in the adult pigeon. Am. Nat., 58, 167-181.

Riddle, O. 1925. Birds without gonads: their origin, behaviour, and bearing on the theory of the internal secretion of the testis. Brit. J. Exper. Biol., 2, 211-246.

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Ring, J. R. 1945. The hormonal induction of mating responses in the spayed-adrenalectomized female rat. Endocrinology, 37, 237-244.

Riss, W. 1955. Sex drive, oxygen consumption and heart rate in genetically different strains of male guinea pigs. Am. J. Physiol., 180, 530534.

Riss, W., and Young, W. C. 1953. Somatic. p.sychological, and androgenic determinants in the development of sexual beha\ior in the


HORMONES AND MATING BEHAVIOR


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Riss, W., V.alenstein, E. S., Sinks, J., and Young, W. C. 1955. Development of sexual behavior in male guinea pigs from genetically different .stocks under contioUed conditions of androgen treatment and caging. Endocrinology, 57, 139-146.

Riss, W., and Goy, R. W. 1957. Modification of sex drive and O2 consumption by isolating and grouping male guinea pigs. J. Comp. & Physiol. Psychol., 50, 150-154.

Roark, D. B., and Herman, H. A. 1950. Physiological and histological phenomena of the bovine estrual cycle with special reference to vaginal-cervical secretions. Univ. Missouri Coll. Agric. Res. Bull., No. 455.

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Robinson, T. J. 1954a. The necessity for progesterone with estrogen for the induction of recurrent estrus in the ovariectomized ewe. Endocrinology, 55, 403-408.

Robinson, T. J. 1954b. The production of coincident oestrus and ovulation in the anoestrus ewe with progesterone and pregnant mare serum. J. Endocrinol., 10, 117-124.

Robinson, T. J. 1955. Quantitative studies on the hormonal induction of oestrus in spayed ewes. J. Endocrinol., 12, 163-173.

Robinson, T. J., Moore, N. W., asd Binet, F. E. 1956. The effect of the duration of progesterone pretreatment on the response of the spayed ewe to oestrogen. J. Endocrinol., 14, 1-7.

RoBSON, J. M. 1938. Induction of oestrous changes in the monkey and bitch by triphenyl ethylene. Proc. Soc. Exper. Biol. & Med., 38, 153-157.

Robson, J. M., and Henderson, W. R. 1936. The action of oestrin on the bitch. Proc. Roy. Soc, London, ser. B. 120, 1-14.

RoBSON, J. M., AND ScHONBERG, A. 1937. Oestrous reactions, including mating, produced by triphenyl ethylene. Nature, London, 140, 196.

Home, H. P., .-vnd Braceland, F. J. 1950. Use of cortisone and ACTH in certain diseases: psychiatric aspects. Proc. Staff Meet. Mayo Clin., 25, 495-498.

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Rowley, I., and Mollison, B. C. 1955. Copulation in the wild rabbit, Oryctolagus cuniculus. Behaviour, 8, 81-84.

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ScHiNKEL, P. G. 1954b. The effect of the ram on


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SCHLOSBERG, H., DuNCAN, M. C, AND DaITCH,

B. H. 1949. Mating behavior of two livebearing fish, Xiphophorus hetleri and Platypoecilus maculatus. Phvsiol. Zool., 22, 148161.

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VAN HeUVERSWYN, J., COLLINS, V. J., WiLLIAMS,

W. L., and G.\rdner, W. U. 1939. The progesterone-like activity of desoxycorticosterone. Proc. Soc. Exper. Biol. & Med., 41, 552-554.

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HORMONES AND MATING BEHAVIOR


1239


A study of differences in the sex drive of cockerels. Brit. J. Anim. Beliav., 4, 102-110.

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Pages where the terms "Historic" (textbooks, papers, people, recommendations) appear on this site, and sections within pages where this disclaimer appears, indicate that the content and scientific understanding are specific to the time of publication. This means that while some scientific descriptions are still accurate, the terminology and interpretation of the developmental mechanisms reflect the understanding at the time of original publication and those of the preceding periods, these terms, interpretations and recommendations may not reflect our current scientific understanding.     (More? Embryology History | Historic Embryology Papers)
Young WC. Sex and internal secretions. (1961) 3rd Eda. Williams and Wilkins. Baltimore.
Section A Biologic Basis of Sex Cytologic and Genetic Basis of Sex | Role of Hormones in the Differentiation of Sex
Section B The Hypophysis and the Gonadotrophic Hormones in Relation to Reproduction Morphology of the Hypophysis Related to Its Function | Physiology of the Anterior Hypophysis in Relation to Reproduction
The Mammalian Testis | The Accessory Reproductive Glands of Mammals | The Mammalian Ovary | The Mammalian Female Reproductive Cycle and Its Controlling Mechanisms | Action of Estrogen and Progesterone on the Reproductive Tract of Lower Primates | The Mammary Gland and Lactation | Some Problems of the Metabolism and Mechanism of Action of Steroid Sex Hormones | Nutritional Effects on Endocrine Secretions
Section D Biology of Sperm and Ova, Fertilization, Implantation, the Placenta, and Pregnancy Biology of Spermatozoa | Biology of Eggs and Implantation | Histochemistry and Electron Microscopy of the Placenta | Gestation
Section E Physiology of Reproduction in Submammalian Vertebrates Endocrinology of Reproduction in Cold-blooded Vertebrates | Endocrinology of Reproduction in Birds
Section F Hormonal Regulation of Reproductive Behavior The Hormones and Mating Behavior | Gonadal Hormones and Social Behavior in Infrahuman Vertebrates | Gonadal Hormones and Parental Behavior in Birds and Infrahuman Mammals | Sex Hormones and Other Variables in Human Eroticism | The Ontogenesis of Sexual Behavior in Man | Cultural Determinants of Sexual Behavior


Reference: Young WC. Sex and internal secretions. (1961) 3rd Eda. Williams and Wilkins. Baltimore.


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