Anatomy: The nucleus of BELLONCI and adjacent cell groups in
Selachians. 11. The nue/eus of BELLONCI. The nucleus commissurae
hippocampi (eminentia thalami). By J. L. AOOENS. (Communicated
by Prof. C. U. ARIËNS KAPPERS . )
(Communicated at the meeting of November 24, 1945.)
The nucleus of Bellonci.
In the unmyelinated part of the stria medullaris, as it reaches the front
end of the ganglion habenulae, cells begin to appear, which caudally
become more and more numerous, and continue into the commissura
habenularum. These cells form two nuclei , separated by a small gap. The
foremost of them, oblong in shape, extends caudally in the stria until it
turns medially to form the commissure (figs. I, 2, 7, 8). The hindmost
nucleus is an unpaired median cell mass, lying in the commissure and
filling it up al most entirely (figs. 3, 5-8).
The foremost nucleus, in accordanee with BERGQUIST (1932) , is interpreted by me as nucleus commissurae hippocampi or eminentia thalami
(BERGQUIST uses the latter term), the hindmost unpaired nucleus as the
fused nuclei of BELLONCI.
The latter, which we now shall deal with in detail. as Just said, almost
entirely fills .up the commissura habenularum, and consists of small eells
of the same size and type as the habenula cells. They are, however, far
more loosely arranged (figs. 3, 5, 6). These eells have not been described
before. They may be seen, however, in the figure BURcKHARoT (1907,
fig. 15) gives of a sagittal section through the origin of the epiphysis of
Spinax niger, andin that of KApPERS (1920, fig. 41) of a similar section
through the epithalamus of Scyllium canicula.
In Cyclostomes, where likewise it lies entirely embedded in the stria
meduIIaris , the nucleus of BELLONCI is paired. In Petromyzonts, on the
right side, it is situated as a separate cell group immediately ~eneath the
ganglion habenulae, while, on the left side, it has fused with th is ganglion
to the structure generally described as left habenula (AOOENS, 1943a).
Thus the nucleus of BELLONCI, paired in Cyclostomes, according to our
interpretation, in Selachians, has shifted dorsomedially in the stria, right
and left nucleus having fused to a single eell mass in the median plane.
It is natural to suppose that the nucleus of BELLONCI, whose cells all
of them are embedded in the compact unmyelinated stria medullaris,
mainly is supplied by this bundIe. This is opposed to JOHNSTON'S regarding
the unmyelinated stria as exclusively a hippocampus commissure, since
the nucleus of BELLONCI always chiefly is supplied by the stria medullaris,
the tractus olfacto-habenularis lateralis especiaIly. But above we have
already set forth as our opinion that also the commissura telencephali
95
superior of KApPERS, and moreover, unmyelinated fibres of the various
telencephalic habenular tracts may course in the unmyelinated stria.
In addition to the unmyelinated stria, the unpaired cell mass in the
commissura habenularum, interpreted by us as the fused nuclei of BELLONCI,
is supplied by myelinated fibres. When analysing the stria medullaris,
we reported myelinated fibres crossing in the pósterior part of the un~
myelinated commissura habenularum, Iying partly as sm all bundIes at its
periphery, and partly as widely scattered single fibres inside this bundIe
(figs. 3-8). The peripheral bundIes appeared to be the ' decussating part
of the tract interpreted by JOHNSTON as tractus septo~habenularis 1) , while
the internal fibres, which came forth media I to, and from the inner layers
of the optic tract, were held by us to belong to the tractus olfacto~habenu~
laris medialis. Since they pass between the most posterior cells of the
nucleus of BELLONCI, it is quite possible that they synapse with these.
In addition to the decussating fibres there are, however, also direct
myelinated fibres of the tractus olfacto~habenularis medialis to the nucleus
of BELLONCI, and very probably also an unmyelinated part of this tra ct
joins the stria medullaris in this region. The myelinated fibres would
then run scattered among these.
Something must be said here yet about the part of the tractus olfactohabenularis medialis, already mentioned in the first part of the paper,
which runs forward and joins the tractus strio~ and amygdalo~habenularis.
There is a separate medial bundIe of it, which traverses the crescentshaped bundIe depicted, but not labelled in figs. 1-3 which JOHNSTON
calls optic radiation in his figures 9 and 101) (Scyllium canicula), and
also in his figure 23 (Scyllium stellare). This bun dIe of the tractus
shaped bundIe depicted, but not labelled in figs. 1-3, whïch JOHNSTON
designates in his figure 44 (Acanthias vulgaris) as tractus septo~habenularis.
At first we have interpreted the crossed and direct myelinated fibres
of the tractus olfacto-habenularis media lis going to the nucleus of BELLONCI
in a different way. We regarded them as the homologues of collaterals
of the so~called fibrae tectales nervi optici of KRAUSE (1898) in Teleosts.
JANSEN (1929), confirmed by CHARLTON (1933) and MEADER (1934),
demonstrated these fibrae tectales to be a component of the supraoptic~
commissure.
1) The interpretation of this tract is by no means sure. The fibre bundIe JOHNSTON
depicts in his f~gure H (Acanthias vulgaI1l.s) as arising from the medial forebrain bundl!!',
probably is a part of the tractus olfact~habenularis medialis mentioned below. The
fine fibre bundIes described by BÄCKSTRÖM as given oH by the medial forebrain bundIe
te:- the stria medulJaris (see Part I), more probably belong to the combined tractus strioand amygdalo-habenularis and olfact~habe:lUlaris medialis. In Acanthias vulgaris the
decussation of the so-called tractus septo-habenularis is much stronger developed than in .
Scyllium canicula , in that here also fibres of the tractus olfact~habenularis medialis
partake i:l the formation of ·the decussation.
2) In this figure the designations tractus septcthabenularis and op tic radiation are
interchanged.
96
Now JEENER (1930) deseribed in Idus idus horizontal myelinated fibres.
already observed by B. HALL ER (1898) and SHELDON (1912). eonneeting
the eell group he interprets as eminentia thalami with the fibrae teetales.
He suggests these horizontal fibres to be eollaterals of the latter. As I at
first supposed that the eminentia thalami of JEENER might be in reality the
nucleus of BELLONCI, I was led to homologize the fibres eoming forth
medial to, and from the inner layers of the optie traet. in ScyIlium. with the
eollaterals of JEENER. MEADER (1934) calls the fibrae teetales eommissura
.
interteetalis ventralis. Henee the abbreviation e.i.v. in our figures.
JANSEN (1929) has eome to about the same view we originally held.
sinee he homologizes the rostral part of the dorsal thalamus of Teleosts
with the nucleus of BELLONCI of Amphibians. In this he bases himself
principally on the statement of HOLMGREN (1920) that eollaterals of the
medial optie traet end in the eminentia thalami 1) of Teleosts. Probably
these eollaterals are the same as the horizontal fibres of B. HALLER.
SHELDON and J EENER. On their possible signifieanee we shall return in
the seetion on the nucleus eommissurae hippoeampi.
The myelinated fibres of the tractus olfacto-habenularis medialis to the nucleus of BELLONCI
have not been specimcally described. They are depicted, however, in the figure KAPPERS
(1920, fig . 40) gives of a sagittal section through the epithalamus of Scyllium canieula. The
tractus olfacto-habenularis medialis as a whoie, probably combined with the tractus strioand amygdalo-thalamieus, has been several times observed by the older authors. It is the
accessory optic root from the ganglia habenulae described by VIAULT (1876) in Trygon.
as is apparent from his fig . 21. Further it is the tractus descendens ganglii habenulae of
EOlNGER (1892) and KApPERS (1906). of which HALLER (1898) maintains that part of
its fibres go into the optie nerve. It must be mentio::led here ·t hat DUMERIL (1865) generally
is misquoted as having stated that, in Selachians, the optic root, partly or even entirely,
arose from the ganglia habenulae. He regarded these ganglia themselves as uncrossed optic
roots (his " racine postérieure ou supérieure et principale du nerf optique" ) , arising, like
the crossed roots (racine antérieure) , from the op tic tectum and joining the latter.
It may be poi.'lted out that the optic fibres Erom the habenula of VIAULTand HALLER
have nothi:lg to do with the small bundIe of the tractus olfacto-habenularis lateralis, closely
resembling an optie bundie, we described in the first part of the paper. This lies farther
forward.
The supply of the nucleus of BELLONCI. in Selaehians, exclusively by
habenulo~petal traets. is at varianee with the eurrent view that the nucleus
in question reeeives an additional supply by optie fibres. I will not give
now a survey of the supply of the nucleus throUghout Vertebrates, but
will only point out that also in Mammals (1938) and Cyclostomes (1943,
'43a) 1 eould find no optie fibres going to the nucleus. In Reptiles (1938)
and Birds (1940) I must leave this point undeeided.
Closing the diseussion of the nucleus of BELLONCI and its eonneetions.
it must be remarked that no efferent traets eould be found in the pre~
parations at our disposal.
1) It must he remarked that HOLMQ'REN uses the term eminentia thalami in a much
wider sen se than usual (cf. KUHLENBOCK, 1929; JEEN.ER, 1930) .
97
Nucleus commissurae hippocampi (eminentia thalami) .
The foremost of the two nuclei embedded in the stria medullaris, the
nucleus commissurae hippocampi, begins, as aforesaid , approximately -at
the same level as the ganglion habenulae and extends caudally in the
stria until it turns medially to form the commissure (figs. I , 2, 7, 8). In
cross-sections through its hindmost part, close to its medial side, the
nucleus of BELLONCI begins to appear, always, however , separated from it
by a sm all gap.
Like those of the nucleus of BELLONCI the cells of the nucleus commissurae hippocampi are of the same si ze and type as the habenula ' cells.
They lie very scattered, however, still more so than those of the nucleus
of BELLONCI. Thus the nucleus is less weIl circumscribed than the latter,
it especially being diffieult to say where it begins exactly. Moreover, part
of its cells lie outside the stria, ventral to it, and these are not easily
diffeJ;entiated from their surroundings. In the reconstructions it is not
tried to indieate this , the nucleus , for the sake of clearness, being represented as lying entirely inside the stria.
As with the nucleus of BELLONCI we may safely assume that the nucleus
commissurae hippocampi, embedded for a large part in the unmyelinated
stria, chiefly is supplied by this bundIe. This, however , is no proof of
}OHNSTON'S contention that the unmyelinated stria is exclusively a hippocampus _commissure. According to HERRlcK (1933), in Urodeles, the
nucleus commissurae hippocampi, besides from the commissura hippocampi,
which here has freed itself from the commissura habenularum, also receives
impulses from the stria medullaris s. stro
There is still another connection of the nucleus commissurae hippocampi. When describing the tractus olfacto-habenularis lateralis in the
first part of the paper, we mentioned in a note that, in addition to the
principal tract , there is present a separate posteri9r part of th is tract.
The principal tract ascends to the striB medulla ris just in front of the
panglia habenulae. The posterior part lies at the level of the foremost end
of these ganglia . lts fibres come forth from the outer layers of the optie
tract and, bending horizontally, pass beneath the unmyelinated stria.
Here they cross the ascending fibres of the tractus olfacto-habenularis
medialis. How they end could not be made out with certainty, but possibly
they do so medial to the stria medulla ris, in the region of the nucleus
commissurae hippocampi. These fibres may be seen, but are not labelled
in fig . 1. They closely resembIe the horizontal fibres connecting, in Teleosts,
the eminentia thalami with the so-called fibrae tectales nervi optici, and
may be their homologues. As the horizontal fibres of Teleosts, according
to B. HALLER and SHELDON , are efferent, it is more probable that the fibres
considered by us as a posterior part of the tractus olfacto-habenularis
lateralis are ,not such , but an efferent tract of the nucleus commissurae
hippocampi (eminentia thalami).
7
98
In Petromyzonts the nucleus commissurae hippocampi was described
by us (1943, '43a) as a cell plate, Iying at the boundary between tel- and
diencephalon and separated from the ventricIe by the primordium hippocampi and nucleus of BELLONCI (see especially our figure of a horizontal
section: 1943a, fig. 1). According to HERRICK and OBENCHAIN (1913), and
BERGQUIST (1932), who also described this nucleus in Petromyzonts, it is,
however, adjacent to the ventricIe. being intercalated between the primordium hippocampi in front and the nucleus of BELLONCI behind. In .
M yxinoids, where the nucleus also is present as a well-defined structure,
it lies medial to the ventral thalamus, between th is and the median plane
(1943a: fig . 4).
Comparing the reconstructions of ScyIlium (figs. 7, 8) with those of
Cyclostomes and Necturus (1943: figs. 6-8; '43a: fig. 2), it appears that
the nucleus commissurae hippocampi, as also the nucleus of BELLONCI,
occupy the same level in Petromyzonts, Selachians and Urodeles, the
former Iying always close in front of the latter. In Myxinoids, on the
rontrary, the nucleus commissurae hippocampi lies at the level of the
nucleus of BELLONCI of the other groups and the latter on that of the
nudeus commissurae hippocampi of these, the relationship of the two nuclei
being reversed. No doubt this· is a secondary condition, but how it has been
brought about , I am not prepared to say.
.
Although it lies outside the scope of this paper, something may be said
here about the two sulci designated in the figures as sulcus telo-diencephalicus internus and sulcus praeopticus (figs. 5-8).
Our sulcus telo-diencephalicus internus is the sulcus intra-encephalicus
nnterior of VON KUPFFER (1906). This is a vertical groove extending from
the preoptic recess dorsally into the region of the velum transversurn. It
is present in all Vertebrate classes, in the embryonic state at least (VON
!~L1PFFER, 1906; V . HALLER, 1922, '29, '34 ; KUHLENBECK, )929; BERGQUIST, 1932; HERRICK , 1933).
I have , been led to name this groove sulcus telo-diencephalicus intern us
in the following way. In my figures of adult Petromyzon f1uviatilis
(1943, '43a) 1 designated as sulcus telo-diencephalicus internus the groove
between the primordium hippocampi and nucleus of BELLONCI, considering
it as the internal boundary between telencephalon and diencephalon. lt
is the sulcus Iimitans hippocampi of }OHNSTON (1912), the first thalamic
sulcus of H ERRICK and OBENCHAIN (1913) and the sulcus thalami anterior
of BERGQUIST (1932). There can be no doubt that th is groove between
the primordium hippocampi and nucleus of BELLONCI in the adult Petromyzon is the dorsal part of the groove which in the Ammocoetes is called
by VON KUPFFER (1906) and V . HALLER (1922) sulcus intra-encephalicus
<1nterior.
The sulcus praeopticus is a vertical sulcus of the telencephalon
medium, lying at its beginning, considerably in front of the sulcus telo-
99
ciiencephalicus internus (figs. 5-8). It has not been reported before in
Selachians and is homologized by us with the similar sulcus described
under this name by KUHLENBECK (1929) in Amphibians.
Summary.
A description and discussion are given of the ganglia habenulae, the
nucleus of BELLONCI and the nucleus commissurae hippocampi (eminentia
thalami) of ScyIlium canicula, which, in essence, apply to Selachians
generally, of all of whose three groups, Sharks, Rays and Holocephali,
representatives we re examined.
Contrary to the prevailing notion, the right ganglion habenulae is iarger
than the left, though only to a small extent, and gives rise to a stronger
and more myelinated fasciculus retr9flexus.
Right as weil as left ganglion habenulae are divided into a medial and
a lateral nucleus, of whieh the latter is subdivided into a pars dorsalis
and a pars ventralis. The pars dorsalis of the right lateral nucleus consists
of large, loosely arranged cells, embedded in a dense myelinated network.
The pars dorsalis of the left lateral nucleus is only differentiated from
the rest of · the ganglion by the possession of scarce myelinated fibres.
The myelinated part of both right and left fasciculus retroflexus ex~
clusively arises from the pars dorsalis of the lateral habenular nucleus.
An analysis is given of the stria medullaris and commissura habenularum.
The existence pf a tractus tecto-habenularis is confirmed and, as a new
finding for Vertebrates generally, a tractus tegmento-habenularis is
reported.
The nucleus of BELLONCI was demonstrated. Right and left nucleus
have fused to a median cell mass, lying in the commissura habenularum.
No optie connections of the nucleus could be found.
The nucleus commissurae hippocampi (eminentia thalami) lies on either
side, in front of the nucleus of BELLONCI, partly embedded in the stria
medullaris and partly ventral to it. A fibre tract, probably efferent, connected with the nucleus commissurae hippocampi is described, whieh
comes forth from the outer layers of the optie tract and is homologized
with the horizontal fibres connecting, in Teleosts, the nucleus commissurae
hippocampi (eminentia thalami) with the so-called fibrae tectales nervi
optici of KRAUSE (commissura intertectalis ventralis MEAOER).
The sulcus intra-encephalicus anterior of VON KUPFFER is named sulcus
telo-diencephalicus internus, as it is homologized with the groove so
designated by us in Petromyzonts.
A sulcus praeoptieus is reported for Selachians.
LITERATURE CITED 1 ).
AOOENS,
J. L.
(1938) . The presence o} a nucleus of BELLONCI in Reptiles and Mamma is.
Proe. Ko:J.. Ned. Akad . v . Wetensch., Amsterdam, 41. 11, 1134-1145.
1) Titles of papers cited which are not found in this list of literature, may be looked
up in the Iists of my prev ious 'contributions to the subject (1938, '40, '43a) .
100
(1940) , The nucleus of BELLONCI in Birds. Proc. Ned. Akad. v . Wetenseh. ,
Amsterdam, 43, Il, 1093-1106.
(1943), De kern van BELLONCI en aangrenzende celgroepen bij de Cyclostomen .
I. Petromyzonten. Ve,rs1agen Ned. Akad. v . Wetenseh. , Amsterdam, Afd .
Natuurkunde 52, 260-269.
(1943a), Id. II. Petromyzonten (Vervolg). Myxinoïden . Ibid. , 506-515.
BÄcKSl1RÖM', K. (1924), Contributions to the forebrain morphology in Selachians. Act.
Zool. 5, 123-240.
BeCCAR1, N . (1943), Neurologia comparata anatomo-funzionale dei Vertebrati, compreso
l"uomo. Firenze, SANSONI Edizoni Scientifiche.
BURCKHft;RDT" R. (1907) , Das Zentral-nervensystem der Selachier als Grundlage für eine
Phylogenie des Vertebratenhirns. I. Teil. Einleitung und Scymnus lichia. Abh.
Kais. Leop.-Car. Akad. Naturforsch. 73, 241-450.
CHAiRL-rol'!, H. H . (1933), The optie tectum and its related fibre tracts in blind Fishes.
A. Trogliehthys rosae and Typhlichthys eigenmanni. J. Comp. Neur. 57,
285-325.
DUMÉRIL, A. (1865), Histoire :1aturelle des Poissons ou Ichthyologie générale. I. Paris,
Libr. EncycI. RORET.
EDINGER, L. (1892) , Untersuchungen über die vergleichende Anatomie des Gehirns.
2. Das Zwischenhirn. Erster Theil: Das Zwischenhirn der Selachier und der
Amphibien . Abh. Senckenb. Naturforsch. Ges. 18. 3-55.
HALt.;ER, B. (1898), Vom Bau des Wirbelthiergehirns. I. Theil. Salmo .und Scyllium.
Morph. Jb. 26, 345-64 L
HALLER, V . (1922), Die epithelialen Gebilde am Gehirn der Wirbeltiere. I. Z . Anat. u.
Entw.-Gesch. 63, 118-202.
(1929), Die Gliederung des Zwischen- und Mittelhirns der Wirbeltiere. Morph.
Jb. 63, 359-407.
(1934) , Äuszere Gliec!erung des Zentrabervensystems. Hb. Vergl. Anat. d.
Wirbelt. Il , 1. Berlin u. Wien, URBAN & SCHWARZFJNBERG .
JEEiN ER, R. (1930), Évolution des een tres diencéphaliques périventrieulaires des T éléostomes. Proe. Kon. Akad. v. Wetensch. , Amsterdam, 33, 11, 755-770.
JOHNSlt>N, J. B. (1911). The telencephalon of Selachians. J. Comp. Neur. 21,1-113.
KAPPERS, C. U. ARIIËNS (1906), The structure of the Teleostean and Selachian brain.
Ibid. 16, 1-109. Also thesis Amsterdam 1904.
(1920), Die vergleiehende Anatomie des Ne.rvensystems der Wirbeltiere u:1d
des Menschen. I. Haarlem, De Erven F . BOHN.
KRAUSE, K. (1898), Experimentelle Untersuchungen über die Sehbahnen des Goldkarpfens
(Cyprinus auratus) . Arch. Mikr. Anat. u. Entw.--Gesch. 5l, 820-838.
KUPl'FER, K. v. (1906) , Die Morphogenie des Centralnervensystems. HERTWIGS Hb. d.
Entw.-Lehre d. Wirbeltiere, Bd. 2, Tl. 3.
MEADER, R. G. (1934) , The optie system of the Teleost, Holocentrus. 1.' The primary
optie pathways and the corpus genieulaturn complex. J. Comp. Neur. 60,
361-407.
SHELDON , R. E. (1912), The olfactor.Y tracts and centers in Teleosts. Ibid. 22, 177-399.
S11ERZI, G . (1909), Il sisterna nervoso centrale dei Vertebrati. Vol. 11: Pesci, Libro I:
Selad, Parte I: Anatomia. Padova, A. DRAGHI.
THOMSON, J. STUART (1919), The morphology of the prosencephalon of Spinax as a
type o~ Elasmobranch forebrain . Transact. R. Soc. Edinburgh 52 (1921),
487-50'0.
.
VIAULT, F . (1876) , Recherches histo1ogiques sur la structure des centres nerveux des
Plagiostomes. Arch. Zool. Exp. et Gén. 5, HI-528.