A M . 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-01804 and NB-04295 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)
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).
RELATIONS OF FISH BRAIN
bTolf.
"
- i METRIC 1
£3
24
H . N. SCHNITZLEIN
that these mitral cells are apparently less almost all vertebrates, although not recogwell developed in amphibians than in some nizable in cyclostomes, is a major interhemispheric connection of the amygdaloid
fish or in some mammals.
Some controversy has resulted from at- complex and the piriform lobe area
tempts to establish homologies between the throughout the remainder of the vertebrate
fish telencephalon and comparable regions series. Comparisons of this area through
in other vertebrates (Droogleever Fortuyn, the anterior commissure in the opossum
1961; Niewenhuys, 1962). The differences (from a preparation by Dr. Hamel), in the
stem largely from the lack, thus far, of a frog (Hoffman, 1963), in the bowfin (Fig.
demonstrable lateral ventricle, the lack of 11), and in the goldfish (Schnitzlein, 1962),
prominent ventricular sulci, and the pres- indicate the similarities which are, to us
ence of an extensive and thin laterally- convincing of the homology of the lateral
attached roof plate. As a basis for com- forebrain areas with the amygdala and the
parison of the areas rostral to the anterior piriform lobe. The hippocampal commiscommissure, representative vertebrates have sure in teleosts has a typical relation dorbeen utilized. The brain of a mammal, sally to the anterior commissure and apthe opossum (from the collection of Dr. parently also interconnects the region reE. G. Hamel), which lacks a corpus cal- garded as the primordial hippocampi. Both
losum and in which the relations are still the primordial amygdaloid area and the
somewhat more primitive in character than primordial hippocampi are connected
in most mammals; the brain of a frog, caudally with the habenula in a fashion
Rana pipiens (Hoffman, 1963), in which characteristic of vertebrates (Schnitzlein,
the relatively simple relations character- 1962; Hoffman, 1963).
istic of tailless amphibians are evident;
Centrally located in the hemispheres are
and the brains of two fishes, a ganoid, (Fig. the striatal areas (Figs. 5, 9, 10, 11, and
9), and a teleost (Fig. 10), are illustrated. 16). The base of the hemisphere, rostral
According to the interpretation of Droog- to the anterior commissure, is occupied by
leever Fortuyn (1961), with which our a region comparable to the tuberculum
findings agree, the dorso-medial segment olfactorium. This is variously developed,
is termed the primordial hippocampus and being larger in the bowfin (Fig. 9) and
the lateral part is the primordial piriform the paddlefish and small and relatively
area and amygdala (Figs. 9, 10, and 11). poorly developed in the goldfish (Fig. 10).
The dorsal area between the primordial Caudally this is replaced by the lateral prehippocampus and the primordial piriform optic area (Fig. 11 A). Medially and venarea is usually termed primordial general tromedially is the septal area (Figs. 9, 10,
pallium (in the tailed amphibian, Herrick, and 11) which probably increases or de1933; and the tailless amphibian, Hoffman, creases with the relative development of
1963). Such interpretations have been the olfactory and the gustatory systems.
made on the basis of nuclear configuraPhylogenetically, the development of the
tions, specific cell types, and fiber connec- dorsal thalamus is correlated with that of
tions. The typical hippocampal cells in the non-olfactory cortical regions and with
many vertebrates, the so-called double the striatal areas or their primordia. There
pyramids, are demonstrated in Golgi prep- is also, undoubtedly, a relation between
arations of a teleost, the goldfish (Fig. 14). the manner of life of the animal and the
They may be compared with the published development of the dorsal thalamus, the
illustrations of comparable hippocampal striatal areas, and the non-olfactory corticells in the frog (Hoffman, 1963), where cal areas or their primordia. Terrestrial
they are less well developed; in the rabbit animals need to respond to a wide environ(Caial, 1895); and in the alligator (Crosby, mental range of experience. This is re1917).
flected in the gradual appearance (from
The anterior commissure, present in amphibians to mammals) of specialized
25
RELATIONS OF FISH BRAIN
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 hypo-
loteral forebrain bundle
optic tectum
secondary
trigminal
tract
corpus
cerebelli
secondary gustatory
tract
gustatory lobe
telencephalon
clfactory bulb
striatum
descendng olfactory
tract (m. f. b.)
and
ascending visceral
tract (m. f b.)
lobo-cerebellar
tract
descending
tegmento-spinal
tracts
optic
tract
lateral
geniculate
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.
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
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.
REFERENCES
Ariens Rappers, C. U., G. C. Huber, and E. C.
Crosby. 1936. The comparative anatomy of the
nervous system of vertebrates, including man.
The Macmillan Co., N. Y.
Cajal, S. Ram6n y. 1895. 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. 1933. The optic tectum and its
related fiber tracts in blind fishes. A. Troglichthys
rosae and Typhlichthys eigenmanni. J. Comp.
Neur. 57:285-325.
Crosby, E. C. 1917. The forebrain of Alligator
mississippiensis. J. Comp. Neur. 27:325-402.
Crosby, E. C, and M. J. C. Showers. 1964. 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. 1961. Topographical relations in the telencephalon of the sunfish. Eupomotis gibbosus. J. Comp. Neur. 116:249-263.
Hamel, E. G., Jr. 1963. Unpublished observations.
Herrick, C. J. 1905. The central gustatory paths
in the brains of bony fishes. J. Comp. Neur. 15:
375-456.
•
. 1933. The amphibian forebrain. VIII.
Cerebral hemispheres and pallial primordia. J.
Comp. Neur. 58:737-759.
RELATIONS OF FISH BRAIN
Hoffman, H. H. 1963. The olfactory bulb, accessory
olfactory bulb, and hemisphere of some anurans.
J. Comp. Neur. 120:317-368.
Huber, G. C, and E. C. Crosby. 1926. On thalamic
and tectal nuclei and fiber paths in the brain of
the American alligator. J. Comp. Neur. 40:97-228.
Kingsbury, B. F. 1897. The structure and morphology of the oblongata in fishes. J. Comp. Neur.
7:1-36.
Loo, Y. T. 1931. The forebrain of the opossum,
Didelphis virginiana. Part II. Histology. J.
Comp. Neurol. 52:1-147.
Nieuwenhuys, R. 1962. The morphogenesis and
27
the general structure of the actinopterygian forebrain. Acta Morph. Neerlando-Scand. 5:65-78.
Obenchain, J. B. 1925. The brains of the South
American marsupials, Caenolestes and Orolestes.
Field mus. nat. Hist. pub. 224, Zool. Series 14:
175-232.
Pearson, A. A. 1936. The acustico-lateral centers
and the cerebellum, with fiber connections, of
fishes. J. Comp. Neur., G. C. Huber Memorial
Vol. p. 201-294.
Schnitzlein, H. N. 1962. The habenula and the
dorsal thalamus of some teleosts. J. Comp. Neur.
118:225-268.
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.
ABBREVIATIONS
prim. hipp. "b": primordial hippocampus,
amyg.: amygdala
ventral portion
b. olf. ace: accessory olfactory bulb
prim, pir., p. dors.: dorsal portion of the
cell mit.: mitral cells
primordial piriform lobe
fila. olf.: olfactory fila
prim, pir., p. vent.: ventral portion of the
fiss. circ: circular fissure
primordial piriform lobe
1. epend.: ependymal layer
tel.: telencephalon
1. glom.: glomerular layer
tr. olf. interm.: intermediate olfactory tract
1. glom. et 1. mit.: layer of glomeruli and
tr. olf. lat.: lateral olfactory tract
mitral cells
tr. olf. lat., ped. dors.: dorsal peduncle of the
1. gran.: granular layer
lateral olfactory tract
1. plex. int.: internal plexiform layer
tr. olf. med.: medial olfactory tract
nuc. olf. ant.: anterior olfactory nucleus
vent, olf.: olfactory ventricle
pars, striat.: striatal region
prim, hipp.: primordial hippocampus
prim. hipp. "a": primordial hippocampus,
dorsal portion
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.
ABBREVIATIONS
nuc. sept, med.: medial septal nucleus
comm. ant.: anterior commissure
op. chiasm: optic chiasm
comm. hipp.: hippocampal commissure
pars, striat: striatal portion of the
1. f. b.: lateral forebrain bundle
telencephalon
m. f. b.: medial forebrain bundle
prim, amyg., corticomed.: corticomedial
nuc. diag. bd.: nucleus of the diagonal band
portion of the primordial amygdala
nuc. olf. ant., pars, lat.: lateral part of the
prim. gen. cortex (pars dor.): primordial
anterior olfactory nucleus
general cortex (pars dorsalis)
nuc. olf. ant., pars, vent.: ventral part of the
prim. hipp. "a": dorsal part of the primordial
anterior olfactory nucleus
hippocampus
nuc. preop.: preoptic nucleus
prim. hipp. "b": ventral part of the primordial
nuc. sept, hipp.: septo-hippocampal nucleus
hippocampus
nuc. sept, lat.: lateral septal nucleus
RELATIONS OF FISH BRAIN
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
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
PLATE 3
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.
29
30
H . N. SCHNITZLEIN
6
vent olf.
vent.olf.-
olf. lot., ped dors
b. olf- ace.
tr. olf. lot.
7
cell. mit.
/
filo olf.
0.5mm.
0.5mm.
PLATE 1
^-tr. olf. med.
B
RELATIONS OF FISH BRAIN
31
9
10
pars striat
rim. pall dors.
hipp "a"
prim gen cortex
/(pars dor)
rim, hipp "o"
'•Vr : "*"r •':=•©
prim
nuc. olf. ant.
pars lot.
amyg
IUC
sept med
tub olf
tub olf
nuc 5ept med.
Amid
CalVQ
nuc olf ant.,
pars vent.
Carassius
auratus
•0 5mm .
ii
prim pall dors
prim pir,
p dors.
stria term
tr olf. lot.
et tr amyg. hab-
Amia calva
A
I mm.
PLATE 2
diag bd.
H . N. $CHNITZLEltf
PLATE 3