Book - The Nervous System of Vertebrates (1907) 7
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Johnston JB. The Nervous System of Vertebrates. (1907) Blakiston's Son & Co., London.
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Chapter VII. Somatic Afferent Division. Special Cutaneous Subdivision
The typical sense organs of this system are the pit and canal organs which are found in rows on the head and along the lateral line of cyclostomes, fishes and aquatic amphibia. In Figure 61 are shown a large and a small organ of this type from a sucker embryo at about the time of hatching. The organ consists of high columnar supporting cells which form the whole thickness of the epidermis within the area of the organ, and of shorter thicker pear-shaped cells which do not reach the whole depth of the epidermis. The latter cells bear at their outer ends cuticular hairs or bristles which project beyond the surface. These are the sense cells. Beneath the organ a few nerve fibers come up from a deeper lying nerve, lose their medullary sheaths as they reach the organ and penetrate between the cells. Here the fibers divide in a very complicated manner (Bunker) and end by very fine branches on the surface of the cells. In the typical pit organs the surrounding epidermis is much thicker and rises up as a wall on all sides, the bottom of the pit being formed by the sense organ. Organs of this type are found in fishes in a line along the lateral surface of the body, and in a supraorbital, an infraorbital and a hyomandibular row (Fig. 62). The organs of these typical rows in fishes are usually enclosed in canals in the manner described in the chapter on embryology, but in cyclostomes and amphibia they remain in the form of pit organs. In many cases accessory lines of pit organs, or even canals, are present and in selachians the total number of organs is very large. The number of organs found in the typical rows of the head varies greatly, as is indicated by the following examples: Amia, 40; Menidia, 37; Gadus, 28; Chimaera, 93. It has recently been shown by experiment that the function of the pit and canal organs is to take account of vibrations in the water of a frequency too low for the production of sound (between 6 and 100 per second).
FIG. 61. A large and a small neuromast from a sucker (Catostomus) embryo at about the time of hatching.
FIG. 62. A diagram of the lateral line canals and nerves in the ganoid fish, Amia calva. After E. Phelps Allis.
In selachians there are found two other forms of sense organs which are histologically similar to the pit and canal organs and are also related to them in their nerve supply. These are the organs known as the ampullae of Lorenzini and the vesicles of Savi. The ampullae are found in groups including in some cases a large number of organs, imbedded in a soft gelatinous connective tissue in cavities about the skull or between other organs. The bodies which are imbedded in these groups, however, are only the enlarged ends of slender canals which after a longer or shorter course open on the surface. The development of the organs shows that the point at which the canal opens in the adult is the place from which the organ develops. Starting as pits at these points the tubes grow inward until they reach their final location. At the inner end of the tube there is developed a sense organ of the same type as the pit organ, but more complex in structure. The organs are supplied by branches of the nerves which supply the adjacent canals and are regarded as modified pit organs. The vesicles of Savi are small isolated sacs lying beneath the epidermis which contain pear-shaped hair cells and are also innervated by the same system of nerves as the canal organs. In ganoids also are similar organs called nerve sacs. Both are probably degenerated or at least modified organs of the same system with the canal and pit organs. All this system of organs has been commonly given the name of the lateral line system, because the lateral line canal is its most conspicuous part. Some years ago the term neuromasts was proposed by Wright for the organs whose sense cells are pear-shaped hair cells, as distinguished from the rodshaped cells found in the organs which are now known to be taste organs. This is a much more satisfactory name than the term lateral line organs.
It was shown in the chapter on embryology that the neuromast system develops in close connection with the ear. An examination of the ear in all its relations has led to the conclusion that it is fundamentally a part of the same system of organs as the neuromasts. The evidence of this in part will be given in detail in the present chapter but may be summarized here as follows, (i) The sense cells in the ear of all vertebrates are hair cells similar to those of the canal organs. (2) The sense cells are enclosed in canals which during development sink in from the surface as do the sensory canals and remain open to the surface for some time by way of the ductus endolymphaticus. (3) The hair cells of both neuromasts and ear respond to vibrations in the fluid which fills the canals. The cells of the ear of many fishes and of higher vertebrates respond to vibrations of a more rapid rate (more than 100 per second) than those to which the canal organs respond. (4) The sense cells of the ear are supplied by nerve fibers which in their development and their central endings correspond very closely to those of the canal organs. (5) The centers in which the nerves of the canal organs and ear end form one continuous structure whose histology and secondary connections in the different classes of vertebrates show that it has been derived from the general cutaneous centers.
The sense organs thus far spoken of lie in the semicircular canals and in the sacculus and utriculus and are the only sense organs of the ear in fishes. In addition to these there is developed in higher vertebrates the spiral-shaped cochlea with its complicated organ of Corti. The sense cells of this organ are also hair cells which respond to vibrations in fluid, of a still higher rate. Even this organ with its nerves and centers is so closely related to the rest of the ear that it must be regarded as a more highly specialized part of the same system of sense organs.
The function of the system as a whole seems to have been at first to aid an aquatic animal in directing its movements. Vibrations in the water caused by surface waves, by the movements of other animals, by its own movements, all these were capable of stimulating these organs, and reactions to such stimuli constituted the means by which the animal directed many of its movements. Some of these organs becoming deeply imbedded in canals were not directly influenced by large slow waves, but only by the shorter quicker waves which could enter the canals. Some of the canals becoming completely enclosed and being filled by a denser fluid which responded more readily to waves of less amplitude and higher rate, enabled the animal to be influenced by a wider range of vibrations, including those of high enough rate to produce sound. In this way the open pits, the canal organs, and the organs of the ear came to be differentiated and to serve for a wide range of stimuli. Finally a still higher and higher rate of stimuli were provided for by the development of the cochlea, and as vertebrates ceased to live an aquatic life the pit and canal organs which responded to slow waves in water ceased to be of use and were lost.
The phenomenon of equilibration is a constant phase in the control of movements. Indeed, keeping the equilibrium is a necessary condition for all directed movement. It is probable that many factors enter into this, including all forms of somatic afferent impulses and the brain centers concerned with them. In simple animals without special sense organs the maintenance of equilibrium depends upon tactile stimuli from without and upon impulses aroused by changes of pressure due to movements of parts of the body upon one another. These factors are apparently sufficient for the purpose in these animals and they undoubtedly play an important role in equilibration in all animals. As special sense organs are developed all those whose impulses may affect bodily movements take part in the maintenance of equilibrium. When the eyes are well developed and much used they are important for equilibrium, as our own experience of dizziness and a stumbling gait after being long blindfolded, and the feeling of equilibriumweariness after walking or riding a bicycle in extreme darkness, give evidence. In fishes the neuromasts must be of great importance directly or indirectly, because of their wide distribution over the body which enables them to receive stimuli from many directions, and because they are sensitive to vibratory stimuli to which the general cutaneous endings do not respond. Finally, the structure of the ear with its semicircular canals and contained sense organs is such as to make it the especial organ of equilibration. In case of the ear it is just the change of position of the animal's own body which arouses the vibrations that serve as the appropriate stimuli to the sense organs. Since the control of equilibrium in response to stimuli aroused from within is the most direct and effective, the ears have become the dominant factors in equilibration. It will appear below that the portion of the ear concerned with equilibration is measurably separate from that concerned with sound, and this separation extends to the brain centers.
FIG. 63. A reconstruction of the chief rami of the cranial nerves of a bony fish, Menidia, to show the arrangement of the several systems of components. After C. Judson Herrick.
The nerves which innervate the neuromasts are connected with the dorso-lateral surface of the medulla oblongata by three chief roots, one of which may be subdivided into two. As already stated (p. 20) the caudal root is distributed to the organs of the lateral line, the middle root supplies the organs of the ear, and the cephalic root, which may be double, innervates the three canals of the head. On their way to their areas of distribution the fibers usually run with fibers of other kinds and so form components of various nerve trunks. This will be clear from an examination of Figs. 62 and 63. In the former the canals of the head are shown with the nerves which innervate them but without the accompanying components of the other kinds. In Figure 63 the various components which constitute the cranial nerves of Menidia are shown as they are combined in nerve trunks. The neuromast components are shown in outline but the canals themselves are omitted on account of the complexity of the figure. The root and ganglion of the lateral line nerve is closely related to those of the vagus, as is nearly always the case. In many fishes also fibers from this root go into the IX nerve in which they run for some distance to reach their sense organs. In Menidia the fibers to the supraorbital canal, forming the ramus ophthalmicus superfacialis VII, run with the general cutaneous fibers which form the ramus ophthalmicus superfacialis V, the two constituting a supraorbital trunk. This is the most common arrangement in other fishes also. The fibers for the infraorbital canal in Menidia run with general cutaneous and general visceral fibers in the maxillary trunk. The fibers to the infraorbital row of sense organs are known as the ramus buccalis VII and in most fishes are independent of other components for the greater part of their course. The fibers destined to the hyomandibular canal form a component of the ramus hyomandibularis, which contains also general cutaneous, visceral sensory and visceral motor fibers. It will be seen immediately that all the neuromast fibers, no matter in what rami they run, have the same central connections as well as the same type of peripheral organs, and are therefore justly considered as a single system of nerve components. The distribution of these components in the cyclostomes (Fig. 51) and in amphibia (Fig. 79) should be compared with that in Menidia (Fig. 63).
Special Cutaneous Centers
In the brain of cyclostomes the neuromast fibers are intimately associated with the general cutaneous fibers and end in the same slightly specialized centers. (See previous chapter.) In the brain of a selachian or ganoid fish although the general and special cutaneous fibers are still almost as intimately associated, a higher development of the centers has taken place and the special cutaneous fibers end chiefly in the more highly developed portions. This can be illustrated best by describing the cutaneous centers with their roots and secondary connections in some detail. As stated above (p. 115) the general cutaneous fibers on entering the brain go in part by the spinal V tract to the nucleus of the dorsal funiculus and in part spread widely through the acusticum and cerebellum. The neuromast components also spread widely through the acusticum and cerebellum but only a small part of them go to the nucleus funiculi or to a small nucleus adjoining it. Thus the greater part of the nucleus funiculi, and, especially in higher vertebrates, cells accompanying the spinal V tract are related to general cutaneous components alone, while in the acusticum and cerebellum both general and special cutaneous fibers intermingle and presumably end in relation with the same cells. The intermingling of these components will be seen by reference to Figs. 64 and 65. In the acusticum and cerebellum there is to be noticed a great increase in size in true fishes as compared with cyclostomes and the presence of much more prominent granular and molecular layers. The outer portion of the cerebellum is composed of a dense layer of very fine fibers, interspersed with few cells, which continues caudally over the dorsal or lateral surface of the acusticum and forms what is known as the cerebellar crest. This corresponds to the molecular layer of the cerebellum of higher forms. The inner portion of both cerebellum and acusticum is composed of large and small cells and corresponds to the combined granular and Purkinje cell layer of higher forms.
FIG. 64. A transverse section of the brain of the sturgeon at the level of the VII and VIII nerves.
FIG. 65. A transverse section of the brain of the sturgeon at the level of the V nerve.
The small cells are vastly more numerous in the cerebellum than in the acusticum and the small bodies of the cells closely packed together suggest the names granule cells and granular layer. The great majority of these cells are very small, have from one to three short dendrites with small claw-like branches and give rise to extremely fine neurites. These are the granule cells in a strict sense. Their neurites turn toward the outer surface of the cerebellum or acusticum, as the case may be, and run parallel with the surface, forming the molecular layer. In most forms these fibers bifurcate on entering the molecular layer, one branch running forward and one backward. A considerable part of the neurites of granule cells in the cerebellum pass to the opposite side through the roof, forming the superior commissure of the cerebellum. The larger part of the molecular layer fibers end within the cerebellum; the smaller part, consisting of both crossed and uncrossed fibers, pass caudally in the cerebellar crest which grows gradually smaller and dwindles away toward the caudal end of the acusticum. The smaller number of small cells in the cerebellum and acusticum are of the form known as cells of type II, whose neurites divide into terminal branches in the near vicinity of the cell. A single granule cell is shown in Fig. 39, and in Figs. 64 and 65 are shown the relations of the granular and molecular layers in the brain of the sturgeon. In cyclostomes the molecular layer extends along the lateral surface of the acusticum. In selachians there is a folding of the acusticum in such a way that the molecular layer forms the floor of a longitudinal groove on the lateral surface (Fig. 66) and in the sturgeon this folding has gone so far that the groove has been closed up by the fusion of the opposed surfaces of the molecular layer. That part of the acusticum which lies above the fold is the lobus lineae lateralis (Fig. 3) and in the sturgeon it is almost separated from the rest of the acusticum by the cerebellar crest. The large cells in the acusticum and cerebellum may be described as of two main types with intermediate forms. The first type consists of cells with large bodies and rather coarse dendrites whose many branches spread widely through the granular layer. These cells show no special arrangement and no great peculiarities; they are most like the large cells in the dorsal horn of the cord or in the nucleus funiculi. Their neurites go as internal arcuate fibers to join the tractus bulbo-tectalis of the opposite side of the brain. These cells will be referred to as acusticum cells. Such cells are shown in Fig. 58 A, from the acusticum of a cyclostome and in Fig. 67 from the sturgeon.
FIG. 66. A transverse section of the medulla oblongata of Scyllium to show the folding of the cerebellar crest and tuberculum acusticum. ac, tuberculum acusticum; c.c., cerebellar crest; L.I.I., lobus lineae lateralis; L.v., lobus vagi.
FIG. 67. Transverse section of the acusticum of the sturgeon to show acusticum cells and a Purkinje cell, ex., cerebellar crest; L.v., lobus vagi.
The cells of the second type are also large but they differ from the first in having both a special arrangement and a special form differentiation. The cell-bodies stand in the granular layer next to the molecular layer and are somewhat elongated vertically to the surface. The dendrites arise from the end of the cell next to the molecular layer and spread in that layer. The dendrites are noticeably straight, have a stiff appearance, and all their branches in the molecular layer are provided with great numbers of little spine-like projections. The possession of such dendrites brings these cells into the same category with the Purkinje cells of the human cerebellum. Since the dendrites are imbedded in the myriads of fine fibers of the molecular layer it is probable that the small spines serve for contact or perhaps a closer connection with the fine fibers. A single Purkinje cell is shown in Fig. 39 and one is drawn in the upper part of Fig. 67. From the inner end of the cell-body, which is frequently slender and pointed, arises the neurite which may take one of three courses. Some of them go ventro-mesially close beneath the floor of the fourth ventricle and either make connections with the motor nuclei of the cranial nerves of the same region or enter the longitudinal fiber tracts closely related to those nuclei and go to nuclei of more distant nerves. The fibers from the cerebellum which have this destination form two or more bundles which curve down over the inner face of the acusticum and reach the motor column in the region of the trochlearis and abducens nuclei. All these fibers may be referred to as the short motor connections of the acusticum and cerebellum. Other fibers from the Purkinje cells, especially in the acusticum, go as internal arcuate fibers to join the tractus bulbo-tectalis. Still other fibers from Purkinje cells in the acusticum go as arcuate fibers on the outer surface of the brain to destinations which are as yet little understood. Some may go to a nucleus comparable with the lower olive of human anatomy, others go to the cerebellum. The latter would correspond to the external arcuate fibers of man. The destination of the larger part of the neurites of Perkinje cells in the cerebellum of lower forms is not known. In mammals (p. 245) the neurites of Purkinje cells are very widely distributed to distant parts of the brain and spinal cord and it is an interesting problem to know how low in the scale of vertebrates this condition makes its appearance. The cells in the acusticum intermediate between these two types are equally large but have not such definite form and arrangement as the Purkinje cells (Fig. 68). The difference lies chiefly in the form and position of the dendrites. A part of the dendrites ramify in the granular layer and a part in the molecular layer. Those which lie in the granular layer are like those of the first class of cells, but any dendrites which enter the molecular layer take on the characters of Purkinje cell dendrites. In these intermediate forms every gradation is found between the acusticum and Purkinje cells. The number of the acusticum and intermediate cells is much greater in the acusticum, that of the Purkinje cells much greater in the cerebellum.
FIG. 68. A section through the same region as in Fig. 67, to show cell forms intermediate between acusticum and Purkinje cells.
These facts lead to the conclusion that all these cells have been derived by modification from the simple large cells of the general cutaneous nuclei. The modification is due directly to the influence of the fine fibers of the molecular layer and in the cerebellum, where the granule cells are collected in greatest numbers and the fine fibers are most numerous, the large cells are nearly all specialized into Purkinje cells. The presence of great numbers of granule cells, of cells of type II and of highly developed Purkinje cells marks the cerebellum as the most highly specialized part of the special cutaneous nuclei. The specialization of both cerebellum and acusticum is to be attributed to the influence of the special cutaneous system of Nsense organs. In higher vertebrates these centers no longer receive many general cutaneous fibers, but undergo a still higher specialization, in part as the centers for the ear and in part as an apparatus for controlling bodily movements.
It is necessary now to follow the tractus bulbo-tectalis which receives the greater part of the secondary fibers from the special cutaneous nuclei, and see its relations in the mesencephalon. The roof of the mesencephalon in the fishes begins to show a differentiation into two parts, a median somewhat dome-shaped, bi-lobed tectum opticum and a lateral thicker mass forming a semicircular border about the tectum on either side. These lateral masses are known as the colliculi or the lateral mesencephalic nuclei. The origin and significance of these parts are more fully treated in Chapter XVI. A process of differentiation is seen in this region analogous to that which has been described in the cutaneous centers of the medulla oblongata. In the simplest condition in vertebrates the fibers which pass from the cutaneous center in the hindbrain to the midbrain (tractus bulbo-tectalis) end indiscriminately in all parts of the roof of the midbrain. When the colliculi are well developed it is noticed that the greater part of the tract ends in them, not in the tectum opticum. From these nuclei in bony fishes tertiary tracts go to the tectum opticum, as well as to the inferior lobes and the motor centers of the medulla oblongata. From the tectum opticum in fishes an important tract goes to the cerebellum. The presence of this tract is one of the first evidences of the development of coordinating functions on the part of the cerebellum, which was originally a simple general cutaneous center.
The distribution of the root fibers of the acustico-lateral system of nerves to the special cutaneous nuclei in the medulla oblongata and cerebellum of fishes is shown in Fig. 69. This figure should be compared with that for the general cutaneous centers (Fig. 59). The central tracts from the special cutaneous centers in fishes are identical with those from the general cutaneous centers.
FIG. 69. A diagram to show the central endings of the special cutaneous components in fishes.
In aquatic amphibia and in the tadpoles of land forms the acustico-lateral system has essentially the same relations as in fishes. In terrestrial forms, however, the pit organs disappear because they are serviceable only in the water. Only the enclosed canals of the ear with their sense organs persist. In reptiles, birds and mammals also, the inner ear is the only representative of this system of sense organs which holds so prominent a place in fishes. In mammals the VIII nerve is divided into two parts, the N. vestibularis and the N. cochlearis, and for these nerves two sets of nerve centers have been developed from the acusticum of fishes. The vestibular nerve supplies the sense organs in the vestibule and semicircular canals which represent nearly the whole of the ear of lower vertebrates, and its centers retain in general the form and position of the acusticum in fishes. For the detailed description of these nuclei the student must be referred to the larger text-books on the human brain, but the following general summary is in place here. The fibers upon entering the brain bifurcate into small ascending and larger descending branches. The bundles of the large descending root are surrounded by and interspersed with cells which constitute its end-nucleus. Mesially this is continuous with a broad nucleus beneath the ventricle, called the mesial nucleus of the vestibular nerve. The two together correspond to the acusticum of fishes caudal to the VIII root. The anterior portion of the mesial nucleus is especially important and lateral to it is the lateral nucleus usually known as Deiter's nucleus, which is closely related to the bifurcation of the vestibular fibers and to the first portion of the descending branches. The ascending branches pass upward in a tortuous course toward the cerebellum. Many of them end in the superior nucleus of the vestibular nerve, dorsal to the lateral nucleus, and the rest enter the region of the nucleus tecti of the cerebellum. These ascending branches with their nuclei are the equivalent of the ascending VIII fibers and the continuous gray matter of the acusticum and cerebellum in fishes.
From these several nuclei the following chief tracts arise (Fig. 70) : (i) fibers from the nucleus of the descending root to the cerebellum; (2) fibers from the same nucleus which go as internal arcuate fibers to the opposite side and then either ascend in the medial lemniscus (p. 258) or descend into the spinal cord; (3) fibers from Deiter's nucleus, some of which go to the cerebellum, but most of which go to the opposite side to run forward or backward in two or more bundles. The larger part of the fibers which cross to the opposite side run in the fasciculus longitudinalis medialis and may correspond to the "short motor connections" of the acusticum in fishes. Although there is greater complexity, the central apparatus of the vestibular nerve in mammals corresponds in a striking manner to that of the acustico-lateral system in fishes.
It is usually stated that the cochlear nerve includes a branch to the macula acustica of the sacculus in addition to the fibers to the organ of Corti. Recent studies on the human embryo show, however, that the branch in question belongs to the vestibular nerve and is quite independent of the cochlear nerve (Streeter). The fibers of the cochlear nerve bifurcate on entering the medulla oblongata and end for the most part in two nuclei, the ventral and dorsal cochlear nuclei, which lie lateral and dorsal to the vestibular nuclei. Two important things are to be noticed in regard to the centers for the cochlea. The first is that these nuclei are superficial with respect to the vestibular nuclei. In this they offer a clear illustration of the general law that the more highly specialized structures in the brain, and hence those which have appeared later in the phylogeny, are placed toward the outer surface with respect to older structures to which they are related. It is probable that these nuclei have been developed from the acusticum of lower vertebrates and have taken up the superficial position as they developed. The second point is that no cochlear fibers go to the cerebellum. Apparently the development of the cochlea has come so late as compared with the evolution of the brain that the cerebellum had already assumed functions of correlation inconsistent with its serving primary sensory nerves. On the other hand, some fibers of the cochlear nerve go beyond its primary nuclei, by way of the corpus trapezoideum and the secondary tracts, to higher centers. The fibers arising in the two cochlear nuclei go by a direct or indirect course chiefly to the lateral lemniscus of the same or opposite side (p. 258). The main facts with regard to the central connections of the cochlear and vestibular nerves are shown in the most diagrammatic form in Fig. 70, in order to facilitate comparison with the arrangements in lower vertebrates (Fig. 69). The further consideration of the central relations will be more appropriate in the chapter on the correlating centers.
FIG. 70. A diagram to show the central endings of the vestibular and cochlear nerves and of the optic tract in man and the chief secondary tracts related to them. Compare Fig. 60.
Demonstration of Laboratory Work
- Dissect the lateral line system and ear and their nerves in the dogfish or skate.
- Study sections of lateral line organs from a selachian or from teleost embryos, stained with iron haematoxylin or prepared by a special nerve method.
- Review the dissection of the selachian and teleost brain (Chapter II, No. 2 and Chapter V, No. 2) with reference to the great development of the acusticum and cerebellum in selachians, and the correlation with the large number of acustico-lateral organs.
- Study the roots of the acustico-lateral system of nerves in the brain of a selachian or ganoid fish in Weigert or Golgi sections.
- In Golgi sections of a fish brain study cells of acusticum and cerebellum to follow the evolution of the Purkinje cells. Notice the granules and cells of type II.
- In Weigert or Golgi sections of a fish brain note the internal arcuate fibers to the lemniscus system.
Literature
Allis, E. P., jr.: Lateral Line System in Amia. Jour. Morp., Vol. 2. 1889.
Ayers, H. : Vertebrate Cephalogenesis II. A Contribution to the Morphology of the Vertebrate Ear, with a Reconsideration of its Functions. Jour. Morph., Vol. 6. 1892.
Barker, L. F.: The Nervous System and its Constituent Neurones. 1899.
Beard, J. : On the Segmental Sense Organs of the Lateral Line and the Morphology of the Vertebrate Auditory Organ. Zool. Anz.. Jahrg. 7. 1884.
Brauer, A.: Beitrage zur Kenntniss der Entwickelung und Anatomic der Gymnophionen. Zool. Jahrb., Suppl. 7. 1904.
Bunker, F. S. : On the Structure of the Sense Organs of the Lateral Line of Ameiurus nebulosus Le. S., Anat. Anz., Bd. 13. 1897.
Coggi, A.: Sviluppo degli organ! di senso laterale, della ampolle di Lorenzini e loro nervi rispettivi in Torpedo. Archivio Zool., Vol. i. 1902.
Coggi, A.: Su lo sviluppo e la morphologia della ampolle di Lorenzini e loro nervi. Archivio Zool., Vol. 2. 1905.
Cole, F. J.: Cranial Nerves of Chimaera monstrosa. Proc. Roy. Soc. Edinb., Vol. 38. 1896.
Cole, F. J.: Cranial Nerves of Gadus. Trans. Linn. Soc. London. Ser. 2, Zool. 7. 1898.
Ewart, J. C.: The Sensory Canals of Laemargus. Trans. Roy. Soc. Edinb., Vol. 37. 1893.
Ewart, J. C. and Mitchell, J. C.: The Sensory Canals of the Common Skate (Raia batis). Trans. Roy. Soc. Edinb., Vol. 37. 1893.
Herrick, C. Judson: The Cranial Nerves of Menidia. Jour. Comp. Neur. Vol. 9. 1899.
Herrick, C. Judson: Cranial Nerves of Siluroid Fishes, Jour. Comp. 'Neur., Vol. n. 1901.
Johnston, J. B.: The Brain of Acipenser. Zool. Jahrb., Abth. f. Anat. u, Ontog., Bd. 15. 1901.
Johnston, J. B.: The Brain of Petromyzon. Jour. Comp. Neur., Vol. 12 1902.
Koltzoff, N. K.: Entwickelungsgeschichte des Kopfes von Petromyzon planeri. Bull. Soc. Imper. Natural de Moscou, Annee 1901, No. 3-4. 1902.
Leydig, Franz: Ueber die Schleimcanale der Knochenfische. Arch. f. Anat., Physiol. u. wiss. Med. 1850.
Leydig, F.: Ueber Organe eines sechsten Sinnes. Dresden. 1868.
Mayser, P.: Vergleichend-anatomische Studien iiber das Gehirn der Knochenfische mit besonderer Beruchtigung der Cyprinoiden. Zeit. f. wiss. Zool., Bd. 36. 1881.
Merkel, Fr.: Ueber die Endigungen der sensiblen Nerven in der Haut der Wirbelthiere. Rostock. 1880.
Mitrophonow, Paul: Etude embryogenique sur les Selaciens. Arch, de Zool. Exper., Tome i. 1893.
Parker, G. H.: Hearing and allied Senses in Fishes. Contr. Biol. Lab. U. S. F. C., Woods Hole, Mass. 1903.
Parker, G. H.: The Functions of the Lateral Line Organs in Fishes. Bull. Bureau of Fisheries. Vol. 24. 1904.
Streeter, G. L.: Concerning the Development of the Acoustic Ganglion in the Human Embryo. Verh. anat. Ges. 19. Vers. 1905.
Wilson, H. V.: The Embryology of the Sea Bass. Bull. U. S. Fish Com., Vol. 9. 1891.
Wright, R. Ramsay: On the Skin and Cutaneous Sense Organs of Ameiurus. Proc. Canadian Inst. Toronto, N. S. Vol. 2. 1884.
Johnston JB. The Nervous System of Vertebrates. (1907) Blakiston's Son & Co., London.
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