Download Morphology of the hypothalamus in advanced teleost fishes

Zoofq~~cdJournalo/lheLinnean Sociply (198I ), 73: 343-350. With 4 hgures
Morpholog of the h pothalamus
in advance teleost fis es
B
B
DAVID G.SENN
Zoological Institute, R h e i m p n g 9,
CH-405 I Basel, Switzerland
AccepledJor publication January 1981
A remarkable structure in the hypothalamus of brachiopterygianand actinopterygian fishes consists
of the inferior lobes,nucleus rotundus and torus lateralis. Opticconnectionsare predominantamong
a variety of fibre paths.
KEY WORDS: -hypothalamus- diencephalon-optic system -Teleostei-comparativeanatomy.
CONTENTS
. .
Introduction
Material and methods
Results
. . . .
Discussion
. . .
Zusammenfassung .
References . . .
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
343
343
344
347
349
349
INTRODUCTION
Among vertebrates, teleost fishes are distinguished by a number of special
characters. Many of these concern the structure of the central nervous system. A
well known phenomenon is the arrangement (eversion) of cell masses in the
telencephalicarea (Kuhlenbeck, 1927 ;Nieuwenhuys, 1966).
Another speciality is found in the hypothalamus. Depending on the teleost
species, a distinct or even a pronounced lobe protrudes ventrolaterally on each
side(Fig. lA, B).The inferior lobes (Fritsch, 1878; Franz, 1912; Kuhlenbeck, 1977)
are not comparable to the corpora mammillaria of many land vertebrates but
represent a structure peculiar to teleosts. The area is best developed in the orders
Beryciformes (squirrel- and pinecone-fishes) and Perciformes (perch-like fishes).
MATERIAL AND METHODS
Dissected brains or the entire heads of various fishes were fixed in an AFEsolution (90 ml 80% alcohol, 5 m l 4 W fonnalin and 5 ml acetic acid). The tissues
were embedded in paraffin, Cut at 15 pm, impregnated with Bodian-silver and
counterstained with cresyl-violet.
343
0024-40am 11120343+O~SO~.OOIO
(8 198 I The Linnean Society of London
344
D. G . SENN
Photographs were taken on Kodak Panatomic-X film with an Asahi-Pentax
camera mounted on a Wild M- 1 1 microscope. Films were developed in MicrodolX.
Measurements for the quantitative part of this study were made with an
electronic planimeter (MOP AM 0 2 , Kontron).
RESULTS
The hypothalamus of teleosts is distinctly different from that of other
vertebrates. Externally, a pair of ventrolaterally extending hypothalamic lobes is a
major feature of the actinopterygian brain. Quantitative variation among teleosts
Figure I . The brain ofan advanced teleost, Chrornis chrornis (Perciformes)in A, ventral; B, lateral; and C,
dorsal view. The shape of the brain is markedly influenced by the highly developed optic tectum (tec)
and the inferior lobe (lob).Cer, Cerebellum; rhomb, rhombencephalon; tel, telencephalon. Bar scale,
1 mm.
HYPOTHALAMUS IN TELEOSTS
345
ranges from moderately elevated lobes up to hemisphere-like corpora reaching
almost the size of the optic tectum (Fig. 1A, B).
The lateral hypothalamic region of various teleost fishes has been described by
Fritsch (1878), Goldstein (19051, Franz (19121, Sheldon (1912), Holmgren (19201,
Kuhlenbeck ( 1927), and Demski, Evan & Saland (1975). It is composed of three
topographicallyand histologically different nuclear areas:
(1) The Torus luterulis (Figs 2A,B, 3) is found dorso-rostrally in the hypothalamus
at the lateral diencephalic surface. It consists of loosely arranged, mostly small
cells. The nucleus, which receives fibre endings of the optic tract, is well
developed in Polyptern and Calamoichthys (Brachiopterygii);it is smaller in
actinopterygianfishes (Fig. 2A).
(2) The Nucleus rotundus hypothulumi, mentioned by Fritsch ( 1878) and Franz ( 19 121,
is cytoarchitectonically the most conspicuous nucleus in the teleost
hypothalamus. In transverse sections (Fig. 2A, B, C), the nucleus is recognized
as a ring of densely packed, small and medium-sized cells surrounding a
neuropil mass. A three-dimensional reconstruction (Fig. 3) shows the nucleus
as a cup-like structure with a dorso-rostra1 opening. Optic fibres (from the
retina and the optic tectum) enter this opening to synapse with dentrites of
rotundus cells. Efferent fibres pass from the periphery of nucleus rotundus
hypothalami to reach the ipsilateralinferior lobe of the hypothalamus.
(3) The Lobus inferior hypothalami is quantitatively the most developed nucleus in
this area. Each of the paired lobes bulges laterally around a special wing of the
ventricular cavity (Charlton, 1928), the Recessus lateralis(Fig. 2D).
The inferior lobe is not a uniform cell mass; the area is subdivided into a
number of portions (Fig. 2D). In some cases, e.g. Cotydoru (Miller, 1944;
Kuhlenbeck, 197 7) a dorsal portion of the gray matter is differentiated as a nucleus
diffusus. Other species especially representatives of the Perciformes (perch-like
fishes) basically possess three nuclei, the medial, dorsal and lateral nucleus
(Fig. 2D). The medial and lateral nuclei, consisting of scattered small cells,
represent the major part of the inferior lobe. The dorsal nucleus (Fig. 2D) is
formed by a slightly bent layer of medium-sized to large cells.
The specialized hypothalamus of brachiopterygians and actinopterygians
shows a number of significantfibre connections:
The torus lateralis (remarkably developed in the brachiopterygians Polypterns
and Culumoichthys; moderately differentiated in teleosts) receives retinal optic
fibres. Terminal arborizations surround the rostral, ventral and lateral side of the
torus.
A distinct and compact optic bundle deviates from the main optic tract (Fig. 3)
and courses to the nucleus rotundus (cup-shaped, above) to enter it at its dorsorostral opening. In addition, two smaller tracts are found at this part of the
nucleus: a tecto-hypothalamictract (Fig. 3) curves around theedgeof the opening.
Rostrally, a rotundo-telencephalic tract (Fig. 3) can be followed passing by the
commissura horizontalis (Fritsch, 1878) to reach the contralateral basal part of the
telencephalic area. This region is differentiatedas a conspicuousround nucleus in
perch-like fishes; i.e. in those fishes which also have the best developed lateral
hypothalamus.
A bundle is formed at the surface of nucleus rotundus; it becomes compact
caudally to reach the inferior lobe of the hypothalamus (Fig. 3). Another bundle,
346
D. C. SENN
HYPOTHALAMUS IN TELEOSTS
34 7
' \
Optic fibres 10 Torus lateralis
Nucleus rotundus hypoihalomi
Lobus inferior hypoihalomi
Figure 3. Diagram of fibre tracts in the caudal hypothalamus in a teleost fish. Lateral view. 1, Tract
from nucleus rotundus to the inferior lobe; 2, cerebello-hypothalamictract; 3, tecto-hypothalamic
tract.
the cerebello-hypothalamic tract, connects the inferior lobe with the cerebellum.
Where these fibres originatecannot be discovered in my Bodian sections.
DISCUSSION
The hypothalamus of brachiopterygians and actinopterygians contrasts
morphologically and possibly functionally with that of other vertebrates. Its
rostra1 and middle parts are differentiated as in other vertebrates; they are mainly
formed as nucleus praeopticus and nucleus paraventricularis (Kuhlenbeck, 1931;
Bergquist, 1955; Senn, 1968a, 1970). Part of the caudal or infundibular
hypothalamus includes a teleostean speciality: the lobi inferiores (Figs 1, 2D)and
their associated structures. The lobi seem to be a derivative of the infundibular
part of nucleus paraventricularis. This part forms a laterally directed outpocketing
of the paraventricular nucleus, which then surrounds a laterally extended wing of
the infundibular ventricle: the recessus lateralis. This lateral ventricular extension
might correspond to the region of the sulcus lateralis infundibuli (AriensKappers,
Huber & Crosby, 1960;Senn, 1968b).
Among Osteichthyes, this speciality is basically observed in actinopterygians
and brachiopterygians, but not in sarcopterygians. In Calamoichthys calaban'cus
D. G. SENN
348
(brachiopterygian), the torus lateralis is quantitatively conspicuous (Senn, 19761,
whereas a separate nucleus rotundus is not observed; the inferior lobe is tiny. In
the teleosts studied, the inferior lobe is the main area.
A remarkable quantitative variation is observed within the teleosts (Fig. 4).From
measurements made so far, advanced teleosts (basically Beryciformes and
Perciformes) seem to have the most developed hypothalamic lobes. However,
more measurements are needed to cover a wider variety of teleosts.
At present, a discussion on function of this actinopterygian (and
brachiopterygian) hypothalamic speciality has to be preliminary. An experimental
2.(
,
I.!
Tectum
I
7Diencephalon
I
I
I
I
I
4
I.(
:.
:
I
I
I
I
~I I 4 II i!
A
-
I Hypothalamus
!
I
I
I
1
I
I
Lobus inferior
I
I
0.1
Nucleus rotundus
1
i
(
Co/omoichihys ESOX
Puniius
Ho/ocenirus Cicb/osomo Chromh
Torus lateralis
Coris
Figure 4. Quantitative comparison among different osteichthyans. The index of areas listed on the
right side is related to the total volume of the entire rhombencephalon (without cerebellum) = 1.0.
The dotted lines show the relative volume of the optic tectum; continuous lines refer to diencephalic
areas: torus lateralis, nucleus rotundus, lobus inferior, hypothalamus as a whole and the entire
diencephalon.
HYPOTHALAMUS IN TELEOSTS
349
study (Demski & Knigge, 197 1) reports that stimulation of the inferior lobe evokes
feeding and aggressive responses. The results were obtained from the sunfish
LepomiJ macrochirus, a generalized perciform fish.
The fibre connections (Fig. 3) demonstrate this special hypothalamic region to
be optic, at least for a good part. Part of the optic tract (retinal fibres) enters the
nucleus rotundus (p. 345) which gives rise to fibres coursing into the inferior lobe.
Also the torus lateralis receives a few fibres of the optic tract. A fibre tract is found
coursing between the optic tectum and nucleus rotundus (its direction is not
known yet).
In addition, fibre connectionsto other parts of the brain are recognized (without
knowing their direction at present): the inferior lobe is connected with the
cerebellum (Fig. 3) and a rotundo-telencephalic tract courses between nucleus
rotundus and the basal part of the telencephalon. Future experimental investigationsshould provide more information on the variety of fibre connections.
It is remarkable that the special differentiation of the caudal hypothalamus in
most teleosts does not imply major changes in the ‘regular’ optic system. As in
other vertebrates, optic fields are well differentiated in the tectum, the prectectum
and the ventral thalamus. Why should teleosts possess an additional (partly)optic
area, which is placed in the hypothalamus?
ZUSAMM ENFASSUNG
Actinopterygier (und Brachiopterygier) besitzen im Hypothalamus eine
spezielle, oft beachtlich ausgeprtigte Region; diese besteht aus den Lobi inferiores,
dem Nucleus rotundus hypothalami und dem Torus lateralis. Unter den
reichhaltigen Faserverbindungen haben die meisten optischen Charakter.
REFERENCES
ARlENS UPPERS, C. U., HUBER, G. C. & CROSBY, E. C., 1960.The Comparafiue AnafomyofthcNrmour Sysfmof
Vertebrates Including Man. New York: Hafner.
BERGQUIST, H.,1953.On the development of the diencephalic nuclei and certain mesencephalic relations in
kpidochelys olivacea and other reptiles. Acfaroologica,34: 155-190.
CHARLTON, H. H., 1928.A gland-tike cpendymal structure in the brain. Proceedings offhr Academy ofScimes of
Awulrrdam. 31: 823-836.
DEMSKI, L. S.&KNIGCE, K. M.. 191 1.Thetelencephalonand hypothalamusoftheBluegill(LcpomirmMochinu):
evoked feeding, aggressive and reproductive behavior with representative trontal sections. Journal o/
Cmnparatiue Neurology, 143: 1-16.
DEMSKI, L. S., EVAN, A. P. & SALAND, L. C., 1915. The structure of the inferior lobe of the teleost
hypothalamus.JoudofComparatiue Neurology, 161 :483-498.
FRANZ, V., 1912. Beitrage zur Kenntnis des Mittelhirns und Zwixhenhirns der Knochenfixhe. M a
neurobiologica, 6: 402-450.
FRITSCH, G.. 1018. L‘nfcrsuchungm Pber dmfcincren Bau der Fischgehim. Berlin: Cutman.
GOLDSTEIN, K., 1905.Untersuchungen ilber das Vorderhirn und Zwischenhirn einiger Knochenfische. Archiu
jiirmikroshopirche Anafmnir, 66: 135-219.
HOLMGREN, N., 1920.Zur Anatomie und Histologie des Vorder- und Zwischenhirns der Knochenfixhe. Acfa
zoologica, I : 1Sl-315.
KUHLENBECK, H., 1921. VorksungmubrrdaJ Zmlrolnnvmrysfmdcr Wirbeliierc.Jena: Fischer.
KUHLENBECK, H., 193 I. Ueber die Crundbatandteile des Zwixhenhirnbauplans bei Reptilien.
Morphologisches Jahrbuch, 66: 244-3 11.
e sI., Basel&NewYork: Karger.
KUHLENBECK, H., 1971.Thr C r n l r ~ N r m o u r S y s f m o f V r r f e ~ a fI,
MILLER, R. N., 1944. The diencephalic cell masses in the teleost Cotydora p&us. Journal ofMorphology, 74:
331445.
NIEUWENHUYS, F., 1966.The interpretation of cell masses in the teleostean forebrain. In R. Hassler & H.
Steptian (Eds), Evolufion o j fhe Forebrain: 52-39. Stuttgart: Thieme.
350
D. G. SENN
SENN, D. G., 1968a. Bau und Ontogenese von Zwischen- und Mittelhirn bei Lacertu siculu (Rafinesque). Acta
anatomzca, 5 5 , Supplement I : 1-150.
SENN, D. C., 1968b. Ueber den Bau von Zwischen- und Mittelhirn von Anniellapulchra Gray. Acla anatomtca, 69:
239-261.
SENN, D. G., 1970.The stratificationin thereptiliancentralnervoussystem. Actaanutomica, 75:521-552.
SENN, D. G., 1976. Notes on the forebrain and midbrain of Culamoichthys culaban’cus Smith 1865 (Polypteridae,
Brachiopterygii). Acta zoologica, 57: 129-135.
SHELDON, R. E., 1912. Theolfactory tracts and centers in teleosts.joumalofComparatiueNeuroloKy,
22: 177-253.