CORRELATION OF HABIT AND STRUCTURE IN THE FISH BRAIN

Transcription

1 AM. ZOOLOGIST, 4:21-32 (1964). CORRELATION OF HABIT AND STRUCTURE IN THE FISH BRAIN H. N. SCHNITZLEIN Department of Anatomy, University of Alabama Medical Center Birmingham, Alabama [This paper was presented in a symposium on recent advances in neuroanatomy, held at the XVIth International Congress of Zoology. Dr. Donald C. Goodman was asked to discuss the paper. His discussion, including a comment by Dr. Schnitzlein, is published as a separate article following Dr. Schnitzlein's paper. -Editor] INTRODUCTION It is the intent of this report to review some of the relations between the morphological structure and the functions of parts of the nervous system; their exaggeration and their abeyance in various fishes particularly as they are related to other vertebrates. It is beyond the scope of this presentation to include all of the relevant references. A comparison of the fish brain with that of other vertebrates presents some difficulties due to the great numbers and variations and also because the relations and homologies have been the subject of much controversy (Ariens Kappers, Huber, and Crosby, 1936). The differences stem from the fact that, thus far, a demonstrable lateral ventricle is lacking in most fish (Plate 2: Figs. 9, 10, and 11), and there is a very extensive and thin laterally-attached roof plate. More caudally, the cerebellum has an apparently unique valvula cerebelli and the terminations of the facial, the glossopharyngeal, and the vagus nerves in This investigation has been supported by Grants NB and NB from the United States Public Health Service. The author wishes to express his appreciation to Dr. E. C. Crosby for organizing and relating the data included in this review. The cooperation of Dr. E. G. Hamel, Jr., and Dr. H. H. Hoffman is gratefully acknowledged. The photographs of the gross specimens were made by Dr. H. R. Steeves, III. the brain stem may result in the development of secondary gustatory lobes in those fish which have exaggerated gustatory areas. These may completely distort the usual pattern for this portion of the vertebrate brain. (Kingsbury, 1897; Herrick, 1905). In attempting to establish homologous nuclear regions in the brain, three criteria have been used: (1) the location and general relations; (2) the intrinsic histology and cytology; (3) the connections, both afferent and efferent. With this method it has become evident that some portions of the fish brain are homologous with comparable areas of other vertebrates. It appears also that some regions are distinctive for fish. SPECIMENS AVAILABLE AND TECHNICS UTILIZED The fish used have included the ganoids, 1 i.e., the gar (Lepisosteus osseus), bowfin (Amia calva), paddlefish (Polydon spathula) and sturgeon, (Scaphirhynchus platorynchus), and a number of teleosts. The brains of these fish were serially sectioned either transversly or sagittally, and stained with thionin or impregnated according to the pyridine silver method with Protargol, or with the Golgi method. Representatives of amphibia were available from the collection of Dr. H. H. Hoffman, and of marsupials from the collection of Dr. E. G. Hamel. Preparations of other vertebrates were available in our own collections. SOME RELATIONS OF THE FISH BRAIN The olfactory nerves of fish extend from their cells of origin in the olfactory mucosa to the olfactory bulbs and are unmyelini The term "ganoid" would include those Actinopterygii of the orders Acipenseriformes, Semionotiformes, and Amiiformes. (21)

2 22 H. N. SCHNITZLEIN ated as in other vertebrates. The length of these nerves varies greatly in different fish. In the gar (Fig. 1), in which the olfactory bulbs are sessile and the olfactory mucosa is situated at the rostral end of the snout, the olfactory nerves may be nearly one-fourth the length of the fish. Thus, in a gar measuring two feet, the olfactory nerves are approximately six inches long. In the chain pickerel (Esox niger), which also has sessile bulbs (Fig. 2) the olfactory nerves are intermediate in length. In the goldfish (Carassius auratus) and catfish (Ictalurus punctatus), however, pedunculated olfactory bulbs (Figs. 3 and 4) result in olfactory nerves perhaps less than 1 mm long. In the young goldfish, the olfactory bulbs are adjacent to the telencephalic hemispheres. As a fish grows, elongation of the skull may result in an increase in length of the olfactory fila, as occurs in the growing gar, or in an increase in the olfactory stalk, as occurs in the goldfish. The length of the olfactory nerve then is evidently determined by two factors: (1) the distance of the nasal mucosa from the base of the telencephalon, and/or (2) the length of the olfactory stalks that connect the bulb with the brain. The considerable differences in the shape and the size of the olfactory bulbs in fishes may be related in part to the shape of the front end of the head and to the relative development of the olfactory system. The typical lamination of the vertebrate olfactory bulb, as exemplified in the opossum (Obenchain, 1925; Loo, 1931; Hamel, 1963), has a varying but recognizable representation in fishes, being in general more typical in ganoids such as the bowfin (Fig. 6) and less typical in the teleosts (Figs. 7, 8). In those teleosts which lack an olfactory ventricle and in which the bulbs are sessile, as in the darter (Etheostoma caeruleum), instead of a concentric fiber and cellular arrangement there is a single pattern of lamination (Fig. 8A), medial to lateral or lateral to medial, depending on the place of entrance of the olfactory fila. The most typical cells of the vertebrate olfactory bulb are the mitral cells (Fig. 12). The typical dendrites of these cells spread toward the periphery of the bulb to come into synaptic relation with the entering olfactory fila. The axons of the mitral cells contribute to the olfactory tracts which project to more caudal brain centers. A comparison of the mitral cells of the goldfish with those observed in Golgi preparations of the frog bulb (from the collection of Dr. H. H. Hoffman) indicates lihitniiiiiiiliiil! I Lepisosteus I osseus ;^^HH^^E FIG. 1. Photograph of the dorsal aspect of the brain of the gar, in situ. FIG. 2. Photograph of the dorsal view of the brain of the chain pickerel, in situ. FIG. 3. Photograph of the dorsal view of the goldfish brain, in situ. FIG. 4. Photograph of the dorsal aspect of the catfish brain, in situ. Abbreviations: b. olf., olfactory bulb; cer., cerebellum; lob. gust., gustatory lobe; n., nares; N.olf., olfactory nerve; tect. op., optic tectum; tel, telencephalon; tr. olf., olfactory tract (stalk).

3 RELATIONS OF FISH BRAIN 3 btolf. " -i METRIC 1

4 24 H. N. SCHNITZLEIN that these mitral cells are apparently less well developed in amphibians than in some fish or in some mammals. Some controversy has resulted from attempts to establish homologies between the fish telencephalon and comparable regions in other vertebrates (Droogleever Fortuyn, 1961; Niewenhuys, 1962). The differences stem largely from the lack, thus far, of a demonstrable lateral ventricle, the lack of prominent ventricular sulci, and the presence of an extensive and thin laterallyattached roof plate. As a basis for comparison of the areas rostral to the anterior commissure, representative vertebrates have been utilized. The brain of a mammal, the opossum (from the collection of Dr. E. G. Hamel), which lacks a corpus callosum and in which the relations are still somewhat more primitive in character than in most mammals; the brain of a frog, Rana pipiens (Hoffman, 1963), in which the relatively simple relations characteristic of tailless amphibians are evident; and the brains of two fishes, a ganoid, (Fig. 9), and a teleost (Fig. 10), are illustrated. According to the interpretation of Droogleever Fortuyn (1961), with which our findings agree, the dorso-medial segment is termed the primordial hippocampus and the lateral part is the primordial piriform area and amygdala (Figs. 9, 10, and 11). The dorsal area between the primordial hippocampus and the primordial piriform area is usually termed primordial general pallium (in the tailed amphibian, Herrick, 1933; and the tailless amphibian, Hoffman, 1963). Such interpretations have been made on the basis of nuclear configurations, specific cell types, and fiber connections. The typical hippocampal cells in many vertebrates, the so-called double pyramids, are demonstrated in Golgi preparations of a teleost, the goldfish (Fig. 14). They may be compared with the published illustrations of comparable hippocampal cells in the frog (Hoffman, 1963), where they are less well developed; in the rabbit (Caial, 1895); and in the alligator (Crosby, 1917). The anterior commissure, present in almost all vertebrates, although not recognizable in cyclostomes, is a major interhemispheric connection of the amygdaloid complex and the piriform lobe area throughout the remainder of the vertebrate series. Comparisons of this area through the anterior commissure in the opossum (from a preparation by Dr. Hamel), in the frog (Hoffman, 1963), in the bowfin (Fig. 11), and in the goldfish (Schnitzlein, 1962), indicate the similarities which are, to us convincing of the homology of the lateral forebrain areas with the amygdala and the piriform lobe. The hippocampal commissure in teleosts has a typical relation dorsally to the anterior commissure and apparently also interconnects the region regarded as the primordial hippocampi. Both the primordial amygdaloid area and the primordial hippocampi are connected caudally with the habenula in a fashion characteristic of vertebrates (Schnitzlein, 1962; Hoffman, 1963). Centrally located in the hemispheres are the striatal areas (Figs. 5, 9, 10, 11, and 16). The base of the hemisphere, rostral to the anterior commissure, is occupied by a region comparable to the tuberculum olfactorium. This is variously developed, being larger in the bowfin (Fig. 9) and the paddlefish and small and relatively poorly developed in the goldfish (Fig. 10). Caudally this is replaced by the lateral preoptic area (Fig. 11 A). Medially and ventromedially is the septal area (Figs. 9, 10, and 11) which probably increases or decreases with the relative development of the olfactory and the gustatory systems. Phylogenetically, the development of the dorsal thalamus is correlated with that of the non-olfactory cortical regions and with the striatal areas or their primordia. There is also, undoubtedly, a relation between the manner of life of the animal and the development of the dorsal thalamus, the striatal areas, and the non-olfactory cortical areas or their primordia. Terrestrial animals need to respond to a wide environmental range of experience. This is reflected in the gradual appearance (from amphibians to mammals) of specialized

5 RELATIONS OF FISH BRAIN 25 cutaneous and proprioceptive receptors and, of course, in the disappearance of the lateral line system. With the gradual appearance of such terminations, new nuclei and long conduction pathways, such as the spino-thalamic and the medial lemniscus, with endings in the dorsal thalamus, make their appearance. As is to be expected, the piscian dorsal thalamus (Schnitzlein, 1962) is possibly the least outstanding portion of the diencephalon, even in the highly specialized fishes. Comparisons with a comparable level through the nucleus rotundus of the alligator (Huber and Crosby, 1926) makes this evident. The ventral thalamus is relatively larger than the dorsal thalamus in the fishes studied. It may well be noted that the optic connections from the retina in fishes are projected to the ventral nucleus of the lateral geniculate (Fig. 5), which is ventral thalamus, as well as to the optic tectum, and to the pretectal gray. The hypothalamus (Fig. 5) is the largest part of the diencephalon in fish and proportionately larger in fish than in other forms. Here certain nuclei and tracts are not common to the main phylogenetic line, but are peculiar to fish or, in some instances, relatively much better developed in fish than in other forms (Crosby, 1963). As in other vertebrates, the fish hypothalamus receives olfactory impulses through the medial forebrain bundle (Fig. 5) as well as the fascicles from the hippocampus and the amygdala. It seems probable that the amount of olfactory fibers will be regulated in part by the peripheral olfactory development. Gustatory impulses are relayed to the hypothalamus of the fish by special paths, the sizes of which depend on the development of the sense of taste in the fish under consideration. Among those that have many taste buds supplied by the facial, the glossopharyngeal, and the vagus nerves are the carp and the catfish. Where the entering gustatory fibers are numerous, their regions of termination are enlarged to form gustatory lobes (Fig. 3) which may completely distort the usual configuration of the vertebrate brain stem (Herrick, 1905). The specialized character of such gustatory lobes is indicated not only by their size but also by the microscopically observed lamination which frequently indicates a high sensory specialization and correlation. From such gustatory lobes, in forms such as the goldfish, a large ascending uncrossed secondary gustatory tract (Fig. 5) goes forward, either to relay in the secondary gustatory nucleus at midbrain levels for discharge to the hypoloteral forebrain bundle optic tectum secondary trigminal tract corpus cerebelli secondary gustatory telencephalon clfactory bulb tract gustatory lobe striatum descendng olfactory tract (m. f. b.) and ascending visceral tract (m. f b.) optic tract lateral geniculate lobo-cerebellar tract descending tegmento-spinal tracts hypothalamus FIG. 5. Schematic diagram of a lateral view of the brain of an idealized fish. This diagram illustrates some of the major connections particularly of the optic tectum and the hypothalamus.

6 26 H. N. SCHNITZLEIN thalamus, or to pass to the hypothalamus directly. The marked interconnections which exist in many fishes between the optic tectum and the hypothalamus suggest the modification of the correlated visceral, visual, and cutaneous impulses in both areas by this interplay. Consequently, there is no direct relation between the size and the differentiation of the hypothalamus as a whole and the relative development of any one of the modalities discussed, since the hypothalamus represents the correlative activity of many modalities. The amout of optic tract projection to the tectum in fishes varies from essentially none in the blind fish (Charlton, 1933) to a sufficient number to form a macroscopic system as in the pickerel. It is of interest that although the superficial layer of the optic tectum, where optic fibers enter, is greatly reduced in blind fish (Fig. 17), the deeper portions of the tectum are still well represented. This representation is correlated with the projections to the tectum (Fig. 5) of the somatic impulses from the brain stem, such as the secondary trigeminal tract (Pearson, 1936), and with the visceral impulses from the hypothalamus (Crosby, 1963). Therefore, the optic tectum is essentially a somatic-visceral-optic correlation center in fishes in which the optic projection usually plays a leading role. Both the hypothalamus and the optic tectum discharge to the lower centers through relays in the tegmentum, or reticular formation, and to the cerebellum by the REFERENCES Ariens Rappers, C. U., G. C. Huber, and E. C. Crosby The comparative anatomy of the nervous system of vertebrates, including man. The Macmillan Co., N. Y. Cajal, S. Ram6n y Les nouvelles idees sur la structure du systeme nerveux chez l'homme et chez les vert bres. Trans, by L. Azouiay. C. Reinwald et Cie, Paris. Charlton, H. H The optic tectum and its related fiber tracts in blind fishes. A. Troglichthys rosae and Typhlichthys eigenmanni. J. Comp. Neur. 57: Crosby, E. C The forebrain of Alligator mississippiensis. J. Comp. Neur. 27: lobocerebellar or tectocerebellar paths (Pearson, 1936). Swiftly moving fishes have a large spinocerebellar system and usually, at least, a large corpus cerebelli (Fig. 5). The auricular lobes of the cerebellum, where present, are definitely related to the vestibular system. Impulses relayed over lateral line nerves also reach a peculiar rostral extension known as the valvula cerebelli. Large or small, the cerebellum of fishes has no part homologous to the cerebellar hemispheres of mammals other than the auricular lobes that are forerunners of the flocculus. It does contain regions comparable to portions of the mammalian vermis. In fishes, grossly and to some extent microscopically, the cerebellum (Figs. 1-4), as well as other brain regions, shows variations which reflect to a great extent variations in the size of the diverse pathways which project upon it. In view of the very different habits, forms, and developmental patterns evident in fish, it is to be expected that there will be great variation in their brains. Homologies, more evident in some areas of the fish brain than in other portions, can be established for many regions. While exaggeration and specialization of some areas of the brain, such as the gustatory lobes or olfactory bulbs, indicate development of single modalities, other areas, such as the optic tectum or the hypothalamus, being correlative centers, vary with the amount of any one or with a combination of several peripheral and/or central systems. Crosby, E. C, and M. J. C. Showers Comparative anatomy of the preoptic area and the hypothalamus. Chapter 2. In W. Haymaker and W. Nauta (eds.), Hypothalamus anatomical, functional, and clinical aspects. Droogleever Fortuyn, J Topographical relations in the telencephalon of the sunfish. Eupomotis gibbosus. J. Comp. Neur. 116: Hamel, E. G., Jr Unpublished observations. Herrick, C. J The central gustatory paths in the brains of bony fishes. J. Comp. Neur. 15: The amphibian forebrain. VIII. Cerebral hemispheres and pallial primordia. J. Comp. Neur. 58:

7 RELATIONS OF FISH BRAIN 27 Hoffman, H. H The olfactory bulb, accessory olfactory bulb, and hemisphere of some anurans. J. Comp. Neur. 120: Huber, G. C, and E. C. Crosby On thalamic and tectal nuclei and fiber paths in the brain of the American alligator. J. Comp. Neur. 40: Kingsbury, B. F The structure and morphology of the oblongata in fishes. J. Comp. Neur. 7:1-36. Loo, Y. T The forebrain of the opossum, Didelphis virginiana. Part II. Histology. J. Comp. Neurol. 52: Nieuwenhuys, R The morphogenesis and the general structure of the actinopterygian forebrain. Acta Morph. Neerlando-Scand. 5: Obenchain, J. B The brains of the South American marsupials, Caenolestes and Orolestes. Field mus. nat. Hist. pub. 224, Zool. Series 14: Pearson, A. A The acustico-lateral centers and the cerebellum, with fiber connections, of fishes. J. Comp. Neur., G. C. Huber Memorial Vol. p Schnitzlein, H. N The habenula and the dorsal thalamus of some teleosts. J. Comp. Neur. 118:

8 28 H. N. SCHNITZLEIN EXPLANATION OF PLATES PLATE 1 FIG. 6A. Drawing of a cross section stained with thionin through the olfactory bulb of the bowfin. FIG. 6B. Drawing of a cross section through the olfactory bulb impregnated with pyridine silver of the bowfin. FIG. 6C. Drawing of a section stained with thionin through the junction of the sessile olfactory bulb and the telencephalon of the bowfin. FIG. 6D. Drawing of a comparable level to Figure 6C, impregnated with pyridine silver. FIG. 7A. Drawing of a section stained with thionin through the olfactory bulb of the goldfish. FIG. 7B. Drawing of a comparable level to Figure 7A, impregnated with pyridine silver. FIG. 8A. Drawing of a section stained with thionin through the junction of the sessile olfactory bulb and the telencephalon of the darter. FIG. 8B. Drawing of a section of a comparable level to Figure 8A impregnated with pyridine silver. amyg.: amygdala b. olf. ace: accessory olfactory bulb cell mit.: mitral cells fila. olf.: olfactory fila fiss. circ: circular fissure 1. epend.: ependymal layer 1. glom.: glomerular layer 1. glom. et 1. mit.: layer of glomeruli and mitral cells 1. gran.: granular layer 1. plex. int.: internal plexiform layer nuc. olf. ant.: anterior olfactory nucleus pars, striat.: striatal region prim, hipp.: primordial hippocampus prim. hipp. "a": primordial hippocampus, dorsal portion ABBREVIATIONS prim. hipp. "b": primordial hippocampus, ventral portion prim, pir., p. dors.: dorsal portion of the primordial piriform lobe prim, pir., p. vent.: ventral portion of the primordial piriform lobe tel.: telencephalon tr. olf. interm.: intermediate olfactory tract tr. olf. lat.: lateral olfactory tract tr. olf. lat., ped. dors.: dorsal peduncle of the lateral olfactory tract tr. olf. med.: medial olfactory tract vent, olf.: olfactory ventricle PLATE 2 FIG. 9. Drawing of a cross section stained with thionin through the rostral telencephalon just caudal to the olfactory bulb of the bowfin. FIG. 10. Drawing of a cross section stained with thionin through the rostral hemisphere of the goldfish. FIG.11A. Drawing of a cross section stained with thionin through the brain of the bowfin at the level of the anterior commissure. FIG. 11B. Drawing of a cross section through the brain of the bowfin at the level of the anterior commissure. Pyridine silver impregnation. comm. ant.: anterior commissure comm. hipp.: hippocampal commissure 1. f. b.: lateral forebrain bundle m. f. b.: medial forebrain bundle nuc. diag. bd.: nucleus of the diagonal band nuc. olf. ant., pars, lat.: lateral part of the anterior olfactory nucleus nuc. olf. ant., pars, vent.: ventral part of the anterior olfactory nucleus nuc. preop.: preoptic nucleus nuc. sept, hipp.: septo-hippocampal nucleus nuc. sept, lat.: lateral septal nucleus ABBREVIATIONS nuc. sept, med.: medial septal nucleus op. chiasm: optic chiasm pars, striat: striatal portion of the telencephalon prim, amyg., corticomed.: corticomedial portion of the primordial amygdala prim. gen. cortex (pars dor.): primordial general cortex (pars dorsalis) prim. hipp. "a": dorsal part of the primordial hippocampus prim. hipp. "b": ventral part of the primordial hippocampus

9 prim, pir., p. dors.: dorsal portion of the primordial piriform lobe prim, pir., p. vent.: ventral part of the primordial piriform lobe prim. pall, dors.: primordial general pallium (pars dorsalis) rec. preop.: preoptic recess stria term.: stria terminalis RELATIONS OF FISH BRAIN 29 PLATE 3 tr. amyg. hab.: amygdalo-habenular tract tr. hipp.-sept.: hippocampo-septal tract tr. hipp.-hab.: hippocampo-habenular tract tr. olf. lat.: lateral olfactory tract tr. sept.-hipp.: septo-hippocampal tract tub. olf.: olfactory tubercle vent, impar.: median ventricle FIG. 12. Photomicrograph of a Golgi preparation of the olfactory bulb of the goldfish showing a mitral cell with its dendrite extending toward the periphery. X 250. FIG. 13. Outline drawing of a section through the olfactory bulb showing the location of the mitral cell illustrated in Figure 12. FIG. 14. Photomicrograph of a Golgi preparation of the rostral hemisphere of the goldfish. Two double pyramidal neurons are indicated by arrows. X 250. FIG. 15. Outline drawing of a section through the rostral hemisphere showing the location of the neurons photographed in Figure 14. FIG. 16. Photomicrograph of a striatal cell from the hemisphere of a goldfish impregnated by the Golgi method. X 250. FIG. 17. Cross section through the mesencephalon of the blind cave fish, Troglichthys rosae, (Charlton, 1933). Impregnated with pyridine silver. The optic tectum is evident. X 65.

10 30 H. N. SCHNITZLEIN 6 vent.olf.- vent olf. olf. lot., ped dors b. olf- ace. tr. olf. lot mm. cell. mit. / ^-tr. olf. med. filo olf. B 0.5mm. PLATE 1

11 pars striat RELATIONS OF FISH BRAIN rim. pall dors hipp "a" prim gen cortex /(pars dor) rim, hipp "o" ' Vr : "*"r ':= prim amyg IUC sept med nuc. olf. ant. pars lot. tub olf nuc 5ept med. nuc olf ant., Amid CalVQ pars vent. Carassius auratus tub olf 0 5mm. prim pall dors ii prim pir, p dors. stria term Amia calva A tr olf. lot. et tr amyg. habdiag bd. I mm. PLATE 2

12 H. N. $CHNITZLEltf PLATE 3