Book - The Nervous System of Vertebrates (1907) 9
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Chapter IX. The Visceral Afferent Division
General Visceral Subdivision
The visceral afferent fibers bring impulses from the viscera to the central nervous system. They are distributed to the mucous surfaces in much the same way as the general cutaneous fibers to the skin. In the absence of special knowledge as to their appropriate stimuli it may be supposed that the fiber endings are stimulated by pressure as are the general cutaneous endings. Although it would be confusing to apply the term tactile to visceral impulses, it is probable that there is a close analogy between the two. The difference between cutaneous and visceral sensory apparatus is not in the form of the endings or the mode of stimulation, but in the connections of the two kinds of fibers in the central nervous system.
FIG. 77. A diagrammatic representation of the general visceral sensor)' com ponents in a trunk segment.
The visceral afferent fibers form a component of each of the dorsal nerves of the trunk and head with the exception, in most vertebrates, of the trigeminus and ophthalmicus profundus nerves. In the trunk (Fig. 77) the fibers have their ganglion cells in the spinal ganglia and go by way of the white rami communicantes through one of the ganglia of the sympathetic chain, and by way of sympathetic nerves to some of the organs of the viscera. In the spinal cord these fibers have their central endings in a part of the gray matter lying at the base of the dorsal horn, known as Clarke's column, and perhaps in connection with other cells which lie near the median plane dorsal to the central canal (Fig. 78). This column of cells and its central relations have long been known in man and mammals but it is only in recent years that its function as the center for sensory fibers of the sympathetic system has been proved. The neurites from the cells of Clarke's column go laterad to the surface of the cord and there turn cephalad to form a well denned tract known as the direct cerebellar tract, since it enters the cerebellum of the same side. As compared with the cutaneous sensory system the visceral afferent system in the trunk is very small.
FIG. 78. A transverse section through the region of Clarke's column of the thoracic cord of a new-born dog. FromCajal (Textura, etc.). A, Clarke's column; B, ending of collaterals in it; C, collaterals ending in the intermediate nucleus; D, reflex-motor collaterals; E, ventral commissure; F, middle commissure; G, dorsal commissure; H, cells of the dorsal commissure.
In the head, on the other hand, the visceral sensory surface is greatly increased on account of the gills and there are present special organs of the sense of taste whose fibers run in the same nerves as the general visceral afferent fibers. The relation of these organs and their fibers to the general visceral fibers is so close that they may be spoken of as special visceral sensory structures. Because of the extensive branchial surface and the great number of gustatory organs in the head, the combined visceral systems may be larger than the cutaneous. The visceral afferent fibers form usually the largest component of the X, IX and VII nerves. They are distributed to the gills and the lining of the pharynx and also to the mouth and the surface of the head and body wherever taste organs are found. In fishes the ganglion cells of this component in the vagus and glossopharyngeus are situated in the epibranchial ganglia and the peripheral fibers reach their destination by way of the branchial and pharyngeal rami and the ramus intestinalis vagi. In the VII nerve the visceral ganglion cells form a ganglion which in different classes of vertebrates may be more or less closely in contact with the ganglion of the VIII, the lateral line or the V nerve. The fibers enter the ramus palatihus and other rami of the facialis which reach the mucosa of the mouth and the gill of the spiracular cleft when that is present. In cyclostomes this component of the VII nerve is very small and its distribution has probably not been completely made out. The general arrangement of these components in the cranial nerves is shown in Figs. 51, 63, 79, 80.
In amphibia and all higher vertebrates owing to the disappearance of the gills this component is much smaller than in fishes. In mammals it runs in the following rami: chorda tympani, great superficial petrosal and main trunk of VII; pharyngeal and lingual rami of IX; and pharyngeal, superior laryngeal, pulmonary, oesophageal, gastric and sympathetic branches of the X nerve. Possibly other branches also, such as the vidian nerve, carry fibers of this component.
FIG. 79. A reconstruction of the cranial nerve components in a tailed amphibian, Amblystoma. After Coghill.
Visceral Sensory Centers
The brain centers in which the visceral afferent fibers end in cyclostomes, ganoids, bony fishes, amphibia and mammals have been found to be directly continuous with the region of Clarke's column, namely, a column occupying the mesial portion of the base of the dorsal horn. In all cases these columns become greatly enlarged at about the junction of the spinal cord and medulla oblongata, rise dorsally mesial to the dorsal horns and join to form a median dorsal nucleus, the nucleus commissuralis, first described by Cajal in the mouse. The cells of the nucleus commissuralis lie imbedded among the fibers of a commissure which has been known in fishes as the commissura infima. Just cephalad of this nucleus and commissure the lateral walls of the brain spread apart and are connected dorsally only by the choroid plexus of the fourth ventricle. The visceral columns now appear as more or less prominent ridges continuing forward in the lateral walls of the fourth ventricle, which have been described as including the vagal and facial lobes.
FIG. 80. A simple diagram of the visceral nerves of the head in fishes.
As the visceral fibers in the X, IX and VII nerves enter these lobes many of them divide into terminal branches immediately, and in many fishes the visceral lobe is strongly thickened opposite each nerve root so that it appears somewhat like a string of beads (Figs. 2, 3, u). The bifurcation of the fibers and the formation of a longitudinal tract are not such prominent features in the visceral system as in the cutaneous. A part of the fibers, however, do turn caudad and in fishes form a diffuse bundle which extends to the nucleus commissuralis, where a part of the fibers cross to the opposite side in the commissura infima. In amphibia (Fig. 81) these fibers form a well defined bundle which on account of its relation to the three nerves, VII, IX and X has been given the name fasciculus communis. In terrestrial vertebrates the loss of the gills has led to a great reduction in size of this system, and the centers no longer form conspicuous ridges projecting into the ventricle. Instead, there is in mammals only a small, sharply defined longitudinal bundle of fibers comparable to the fasciculus communis, which is known as the fasciculus solitarius, and a small column of cells accompanying this bundle. In the mouse (Figs. 82, 83), as in fishes and amphibia, the descending fibers enter the nucleus commissuralis and help to form the commissure. In all classes a part of the fibers continue caudad beyond the commissura infima in the visceral column of the cord.
FIG. 81. Four transverse sections through the medulla oblongata of the frog to show the position and ending of the fasciculus communis and the nuclexis commissuralis. C. inf. H., commissura infima; nuc. of C., nucleus commissuralis; /. c. , fasciculus communis; d. h., dorsal horn.
FIG. 82. Transverse section through the medulla oblongata of the mouse at the level of the nucleus commissuralis. From Cajal (Beitrage u. s. w.)- A, nucleus commissuralis; B, nucleus of hypoglossus; C, decussation of lemniscus; D, fasciculus solitarius; b, c, endings of 'fibers of IX and X nerves.
In fishes, where these centers are best known, their structure is relatively simple. The terminal branches of the afferent fibers are short but very profusely subdivided and the dendrites of the cells often have the same characteristics, so that sections of this center prepared by the Golgi method show dense brushes of intricately interwoven fibers which have as a whole a very furry appearance (Fig. 84). Many of the cells are of type II whose neurites terminate within the lobe. In fishes whose gustatory apparatus is largely developed these intrinsic neurones are very numerous. Other cells send their neurites out of the sensory nucleus to end in the neighboring motor column, from which arise the viscero-motor nerves. These fibers constitute what may be called short viscero-motor connections. The remaining cells are cells of moderate size whose neurites go directly lateroventrad and near the surface of the medulla either bifurcate into cephalic and caudal branches or run forward or backward without dividing. The descending fibers form a diffuse bundle which, after giving part of its fibers to a nucleus adjacent to the nucleus commissuralis (bony fishes), grows smaller caudally and is lost to view in the cervical cord. The greater part of the fibers turn forward and form in the myelencephalon a diffuse bundle which runs parallel with and ventro- mesial to the spinal V tract. The bundle continues to receive fibers from all parts of the visceral column, runs on forward past the roots of the trigeminus and enters a large nucleus lying in the lateral wall of the metencephalon (Figs. 89, 92). This bundle has been called the secondary vagus tract in those fishes in which the vagal part of the visceral lobe is especially developed, but it is evidently a secondary visceral tract and the nucleus in which it ends, a secondary visceral nucleus. There is reason to believe that this tract and nucleus correspond to the direct cerebellar tract and its nucleus in man, but it is very desirable that the structures should be worked out in intermediate classes, especially reptiles and lower mammals.
FIG. 83. Transverse section through the medulla oblongata of a mouse four days old. From Cajal (Beitrage u. s. w.). A, hypoglossal nucleus; B, nucleus commissuralis; C, olive; D, spinal V tract; E, motor roots of IX and X; F, nucleus ambiguus; G, caudal portion of the nucleus of the descending root of the nervus vestibularis; H, fasciculus solitarius; a, pyramids; /, general cutaneous components in IX and X ( ?) ; h, collaterals of fasciculus solitarius ending in its accompanying nucleus.
FIG. 84. Transverse sections through the medulla oblongata of the sturgeon; A, at the level of the X nerve; B, at the level of the IX nerve. A is at a higher magnification than B.
Since the visceral centers are most highly developed in those forms in which the gustatory organs are most numerous, the further description of the secondary visceral nuclei will be given in the following section.
Special Visceral or Gustatory System
In fishes, as already stated (p. 22), the gustatory organs have a much wider distribution than in higher vertebrates. As far as is at present known the distribution of taste organs in the different classes of vertebrates is as follows. In cyclostome larval forms they have been found only in the pharynx, on the inner surface of the branchial arches. In adults they are also irregularly distributed over the surface of the head and branchial region of the body. Whether they occur in the trunk and tail region has not been ascertained. In ganoids they are present in the mouth and pharynx and in considerable numbers over the surface of the head. In embryos of bony fishes they are found in the pharynx, oesophagus and mouth. In adults they reach their greatest development both as to number and distribution, being found also on the surface of the head and in many forms on the fins and practically over the whole body. In amphibia they are found on the tongue and mucosa of the mouth, being especially numerous on the papillae of the tongue. The so-called multicellular glands in the roof of the pharynx of tadpoles are probably taste organs. In man they are found in small numbers on the general surface of the tongue, more numerous along the sides of the tongue, and most numerous on and around the circumvallate papillae and on a region at the back of the tongue corresponding to the papillae foliatae of some mammals. They are also numerous on the anterior surface of the soft palate and on the posterior surface of the epiglottis.
The following facts show that the taste organs have their origin in the entoderm. (1) They arise in the lining of the pharynx in Ammocoetes, and are not found in the skin during larval life. (2) In ganoids and bony fishes (Amia, Catostomus} they arise in the entodermal lining of the pharynx, oesophagus and mouth. After the time of hatching, the mucosa pushes out over the lips and taste organs appear in the spreading entoderm. (3) In amphibians (Amblystoma punclatum, Rana) the taste buds arise and remain throughout life in the entodermal area of the pharynx and mouth. Although the limits of ectoderm and entoderm have not been determined in reptiles, birds and mammals, the most reasonable inference from the position of the organs is that they lie in entodermal territory.
FIG. 85. Sense organs of bony fishes. A, a taste bud from the oesophagus of Catostomus at the time of hatching; B, a taste bud from the pharynx of the same embryo; C, two neuromasts from the skin of the same embryo.
The taste organs differ from the pit and canal organs: (i) in being surface organs not sunken in pits but sometimes projecting above the surface as hillocks; and (2) in that the sense cells are long, slender and rod-shaped and extend the full depth of the epidermis. Each sense cell terminates at the surface by a rodlike or hair-like projection which is much shorter than the sense hairs of the neuromast organs. Since the taste organs are stimulated by chemical changes they do not need the long sense hairs which adapt the neuromasts to stimulation by vibrations in fluids. Beneath the organ nerve fibers penetrate the dermis, lose their sheaths and end by fine branches in contact with the sense cells. A more intimate union between the cells and terminal branches of the fibers has not been seen. To facilitate comparison between neuromasts and taste organs there are shown in Fig. 85 two taste organs and two neuromasts from the same embryo of a bony fish. The tall form of taste organ is taken from the lining of one of the gill arches and represents the prevailing form in the pharynx, where the organs are best developed. The lower organ is taken from the oesophagus near the opening of the duct of the swim bladder and is of the same form as those in the mouth. The sharp contrast between the sense cells in these and in the neuromasts requires no comment. In Fig. 86 is drawn a taste organ from the pharynx of the larva of a cyclostome and in Fig. 87 a taste organ from the skin of an adult of another species. The great difference in form of the two organs suggests a profound influence of the surrounding structures, but both organs have the same type of sense cells as are in the taste organs of all vertebrates.
FIG. 86. A taste organ from the pharynx of the ammoccetes of Petromyzon dorsatus.
The innervation of the taste organs is as follows. Those in the pharynx are innervated by the visceral branches of the vagus and glossopharyngeus nerves. Those in the mouth an- >upplied by the palatine and hyomandibular rami of the facialis, by the pharyngeal ramus of IX which extends into the roof of the mouth, and by the ramus lingualis of the IX nerve. Those on the surface of the head and body in ganoids and bony fishes are supplied by components of the ophthalmic and maxillary rami and by a great system of superficial nerves which have been known under the name of ramus later alls accessorius (or nerve of Weber). The name is unfortunate because it is likely to suggest some relation with the lateral line nerve, with which this nerve is to be sharply contrasted. The present nerve (Figs. 63, 88) arises from the visceral afferent root of VII and sometimes in smaller part from the corresponding root of X, passes up through the cranium to the dorsal surface of the head and is distributed to the back, the tail and the fins, wherever taste buds are found. It has been definitely shown that taste buds, wherever they are situated, arc always innervated by fibers derived from the visceral afferent roots of the VII, IX and X nerves and ending centrally in the visceral lobe. Where the taste buds are very numerous in the skin they are always innervated from the root of the facialis nerve and there is developed a special pars facialis of the visceral lobe. The innervation of the taste buds in man is still somewhat in doubt. It was long supposed that fibers were supplied to taste buds by three nerves, the ramus lingualis IX, the chorda tympani and the ramus lingualis V. In certain cases in which the Gasserian ganglion was removed and in which the clinical observations were continued for an unusually long time, it was clearly shown that taste was not at all impaired and that the trigeminus provided only for tactile sensation. This is in agreement with the conditions in lower vertebrates, but it is still possible thatj;aste fibers run in the trigeminus in exceptional cases. The homology of the chorda tympani has been in doubt because it was not certainly known whether the chorda of mammals is a pretrematic or posttrematic ramus. It seems clear now that it is a posttrematic nerve and that the ramus mandibularis VII as seen in the frog tadpole and in fishes is its homologue. The ramus lingualis IX is the homologue of the posttrematic ramus of - the IX nerve in fishes and amphibia, which is prolonged into the tongue.
FIG. 87. A taste organ from the skin of an adult Lampetra.
FIG. 88. A projection of the cutaneous branches of the communis root of the right facial nerve in a bony fish, Ameiurus. From C. Judson Herrick. All the branches drawn are gustatory in function. Those which supply taste buds within the mouth are not shown.
The taste fibers enter the same centers with the general visceral fibers and no means has yet been discovered of distinguishing between the two. However it is probable that of the two sorts of secondary fibers mentioned in the last section, one serves general visceral and the other chiefly gustatory functions. Those which make direct connections with the motor nuclei of the cranial nerves carry only impulses from the visceral surfaces analogous to tactile impulses from the skin and give rise to reflex contractions of the branchial muscles controlling the respiratory movement >. It is inherently probable that a part of the fibers of the long tract to the metencephalic nucleus have general visceral functions, especially as such a tract is present in mammals coming forward from the trunk, where taste organs are out of the question. We must at present suppose that when taste buds were first developed in vertebrates they came to be innervated by the general visceral fibers which already supplied the area in which the taste buds appeared. As the gustatory system came to be more important the long secondary tracts came especially into its service for the reason that these long tracts make possible more complex reflexes adapted to the capturing of food.
It is in the bony fishes, where the gustatory apparatus has reached an enormous development, that the secondary and tertiary connections of the taste center have been most fully worked out (Figs. 89, 90). Here the secondary visceral tract has the same general arrangement as has been described above. As the gustatory elements greatly preponderate in it, we may call it the secondary gustatory tract. Caudally a part of this tract extends into the spinal cord and a part ends in an interior secondary gustatory nulceus adjoining the nucleus commissuralis. Complex relations between this and the adjacent nucleus funiculi (cutaneous center) perhaps enable the animal to correlate tactile with gustatory impulses in the control of movements for the capture of food. Cephalad the tract ends in the metencephalic nucleus, which Herrick calls the superior secondary gustatory nucleus. Part of the fibers end in the nucleus of the same side and part cross to the opposite side in a commissure which may be called the inferior cerebellar commissure. This commissure contains also fibers arising from the cells of the secondary nucleus. The nucleus is an enlargement of the gray matter bounding the fourth ventricle laterally and is very rich in cells and in terminal ramifications of fibers. From this nucleus, in addition to the commissural fibers, arises a tract which runs to the inferior lobes of the diencephalon. Other fibers from the secondary gustatory nucleus seem to go into the cerebellum and the tectum mesencephali. These may serve the more fully to bring about correlations with the somatic muscles in addition to the connections in the funicular region. From the inferior lobes two tracts already well known in lower vertebrates may forward the gustatory impulses. One of these is the tractus lobo-bulbaris which runs back through the myelencephalon and makes connections with the motor nuclei of the cranial nerves. The second tract is the tractus lobo-epistriaticus which carries impulses to that large coordinating center of the forebrain (epistriatum) which is primarily a part of the olfactory apparatus and in amphibia, reptiles and mammals develops into the hippocampal lobe and adjacent parts of the true olfactory cortex. (See Chapter XVIII.) It is possible that this tract is retained in higher vertebrates and serves as the path of gustatory sensations in the true sense. The chief central gustatory connections are shown in Figs. 89 and 90.
The arrangement of the secondary gustatory tracts and nuclei in selachians throws light on certain important structures peculiar to the brain of ganoids and teleosts. In both these classes the superior secondary gustatory nucleus is large, lies hi the lateral wall of the metencephalon and sends its commissure through a part of the cerebellum which projects into and largely fills up the ventricle of the mesencephalon, the valvula cerebelli. In selachians no valvula is present. The cerebellum corresponds to that part of the cerebellum of bony fishes which is folded upward and outward. This will be clear from a comparison of Fig. 91, which represents a sagittal section of the cerebellum of a newly hatched bony fish, with Fig. n, representing a sagittal section of a selachian brain. The superior secondary gustatory nuclei in selachians are situated higher in the dorso-lateral wall of the metencephalon than in bony fishes and their commissure crosses in the roof of the brain at the junction of the tectum opticum and cerebellum. This commissure has been described in selachians and amphibia as the decussation of the velum medullare anterius. It is obvious that it is homologous with the inferior cerebellar commissure which passes through the valvula of bony fishes. Hence it must be supposed that the valvula has been formed by a growth and folding inward of the velum of selachians. The cause for the growth of this large structure is to be found in the great increase in the gustatory system in ganoids and bony fishes.
FIG. 89. A parasagittal section through the brain of the spotted sucker, Minytrema melanops, to show the gustatory centers and tracts. From C. Judson Herrick.
The sketch is designed to illustrate the course of the ascending secondary gustatory tract and the connections of its terminal nucleus. The plane of the section is slightly oblique so that the caudal end and the ventral side are nearer the median line than are the cephalic and dorsal borders. The figure is a composite, made by outlining one section with the camera lucida and filling in the details from this section and the three sections of the same series on each side immediately adjacent, omitting irrelevant detail. The features introduced are schematized as little as possible. The whole course of the ascending secondary gustatory tract from the facial lobe is shown. The origin of the tract from the vagal lobe lies farther lateral.
b., tract between secondary gustatory nucleus and n. lateralis valvulae; com.h., commissura horizontals, FRITSCH; com. r. VII, communis (gustatory) root of the facialis; desc.sec.X, descending secondary gustatory tract from the vagal lobe; /./.w., fasciculus longitudinalis medialis; in/.lob.lat., lateral lobule of inferior lobe (hypoaria, C. L. HERRICK); inf.lob.m., median lobule of inferior lobe (mammillare, C. L. HERRICK); n.corL, nucleus corticalis, FRITSCH; n.IX, motor nucleus of the glossopharyngeus; n.lat., nucleus lateralis valvulae; n.rot., nucleus rotundus, FRITSCH; n.st., nucleus subthalamicus, C. L. HERRICK; n.V, motor nucleus of the trigeminus; n.VII, motor nucleus of the facialis ',r.X.s., sensory root fibers of the vagus; sec.gust.t., ascending secondary gustatory tract from the facial and vagal lobes; tr.l.b., tractus lobo-bulbaris; tr.t-c., tractus tecto-cerebellaris; tr.t-lob., tractus tecto-lobaris, JOHNSTON (commissura ventralis, C. L. HERRICK). The area marked n.juniculi contains also the inferior secondary gustatory nucleus.
FIG. 90. A diagram of the gustatory paths in the brain of the carp as seen from the left side. From C. Judson Herrick.
n. VII. s., n.IX.s., and n.X.s., represent the sensory root fibers of the facialis, glossopharyngeus and vagus respectively, or gustatory neurones of the first order (7). The secondary tracts, both ascending and descending, are marked II. The tertiary path to the inferior lobe is marked 777; the path to the cerebellum and valvula, Hi. The return path from the inferior lobe to the motor nuclei of the oblongata (tractus lobo-bulbaris) is marked IV. The commissures of the inferior and superior secondary nuclei are indicated by shaded areas (the latter marked c). n.op., the optic nerve. The area marked n.fun. includes the funicular nucleus and the inferior secondary gustatory nucleus.
In selachians a part of the secondary fibers from the visceral lobe cross to the opposite side as do the internal arcuate fibers from the cutaneous nuclei. The tertiary tract from the superior secondary gustatory nucleus goes as in bony fishes to the inferior lobes. Apparently in the more primitive brains the inferior lobes as a whole were related to both gustatory and olfactory systems ( cf. Chap. XVII). The relations in selachians are taken as the basis for the general diagram of visceral sensory structures, Figure 92. Figures 112-117 in Chapter XV may also be consulted.
The taste buds are evidently unable to persist on the surface of the body in terrestrial animals, and in amphibia, reptiles, birds and mammals they are confined to the mouth cavity. Besides the great modification in structure of the gustatory system which this change entailed, a great change in function has been brought about. In primitive fishes the taste organs in mouth and pharynx detected indications of food brought by the respiratory water current. In fishes where the taste buds are situated on the surface of the body they serve to detect the presence of food, and frequently special organs such as the barblets about the mouth, or the fins, are richly provided with taste buds and are dragged about on the bottom or otherwise used in the active search for food. In short, the function of the taste organs of fish-like vertebrates is to detect food and to discover its location. In terrestrial animals, on the other hand, the taste organs in the mouth can rarely be used in the search for food. Their only service is to test the food after it is taken into the mouth to discover if it is desirable to eat. Terrestrial vertebrates depend chiefly on the senses of smell and sight for finding food. This explains the relatively slight importance of the sense of taste and the small size of its apparatus in higher vertebrates. At the same time, in higher vertebrates the general visceral system has been reduced in the head by the loss of the gills and more highly developed in the trunk in connection with the sympathetic system.
FIG. 91. Part of a sagittal section of the brain of a newly hatched bony fish, Catostomus, to show the relations of the secondary gustatory tract and the valvula cerebelli.
FIG. 92. A diagram representing the centers and tracts related to the visceral sensory components in fishes.
A comparison of the diagram for the visceral and gustatory apparatus with those for the general and special cutaneous apparatus will show how widely these divisions of the nervous system differ from one another. The student should now turn to the tabular definition of the two divisions (on p. 101) and review this in connection with the figures in this and previous chapters.
Demonstration or Laboratory Work
- Review the dissections called for in Chapter V, Nos. i and 2 with reference to the visceral nerves and the visceral lobe in the brain.
- Study the taste buds in sections of young fry of bony fishes, in frog tadpoles, and in the mammalian tongue.
- In haematoxylin or Weigert sections of the brain of a bony fish, selachian or frog, study the sensory roots of the X, IX and VII nerves and the formation and course of the fasciculus communis.
- Study the endings of visceral sensory fibers and the types of cells in the vagal and facial lobes in sections of the fish brain prepared by the method of Golgi.
- The secondary and tertiary gustatory tracts and the secondary nuclei are best studied in Golgi and Weigert sections in the brains of teleosts, ganoids or selachians.
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Gushing: The Taste Buds and their Independence of the N. trigeminus. Johns Hopkins Hospital Bulletin, Vol. 14. 1903.
Dohrn, Anton: Studien zur Urgeschichte des Wirbelthierkorpers. No. XIII. Mitth. Zool. Sta. zu Neapel. 1888.
Gaskell, W. H.: On the Structure, Distribution and Functions of the Nerves which innervate the Viscera and Vascular Systems. Jour, of Physiol., Vol. 7. 1886.
Herrick, C. Judson: The Cranial Nerves and Cutaneous Sense Organs of North American Siluroid Fishes. Jour. Comp. Neur., Vol. n. 1901.
Herrick, C. Judson: The Organ and Sense of Taste in Fishes. Bull. U. S. F. C. 1902.
Herrick, C. Judson: On the Phylogeny and Morphological Position of the Terminal Buds of Fishes. Jour. Comp. Neur., Vol. 13. 1903.
Herrick, C. Judson: The Central Gustatory Paths in the Brains of Bony Fishes. Jour. Comp. Neur. and Psych., Vol. 15. 1905.
Johnston, J B.: The Brain of Petromyzon. Jour. Comp. Neur., Vol. 12. 1902.
Johnston, J. B.: The Cranial Nerve Components of Petromyzon. Morph. Jahrb., Bd. 34. 1905.
Johnston, J. B.: The Radix mesencephalica trigemini. Ganglion isthmi. Anat. Anz., Bd. 26. 1905.
Onuf and Collins: Experimental Researches on the Central Localization of the Sympathetic with a Critical Review of its Anatomy and Physiology. Arch. Neur. and Psychopath., Vol. 3. 1900.
Schaffer, Jos.: Ueber das Epithel des Kiemendarms von Ammocoetes nebst Bemerkungen iiber intraepitheliale Driisen. Arch. f. mik. Anat. Bd. 45. 1895.
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