The Osteichthyes comprise at least three groups of bony fishes which are generally believed to share a common ancestor: the Crossopterygii, the Dipnoi, and the Actinopterygii. The intergroup relationships have long been disputed by paleontologists, and there is no consensus at the present time. It is usually argued either that the Crossopterygii and the Dipnoi are more closely related to one another than either is to the Actinopterygii (Romer, 1966; Gardiner, 1973) or that the three have been distinct groups since their earliest appearance (Schaeffer, 1969; Miles in Moy-Thomas, 1971). Jarvik (1968), however, has favored a closer affinity between the Crossopterygii and the Actinopterygii than between either of these groups and the Dipnoi.

New Observations on the Organization and Evolution of the Telencephalon of Actinopterygian Fishes

Forebrain evolution in bony fishes.

The telencephalon in ray-finned fish (actinopterygians) is everted, in contrast to the evaginated telencephalic hemispheres in all other vertebrates. In the more derived ray-finned fish, the teleosts, proliferation of neurons and their migration from the ependymal zone of the pallium renders comparisons between telencephalic cell groups of the teleosts and members of other vertebrate groups extremely difficult. The telencephalon of Polypterus (a primitive living ray-finned fish), although everted, is cytoarchitecturally much simpler than that of teleosts. We have thus applied immunohistochemical techniques to the study of the telencephalon of Polypterus to help clarify the evolution of the telencephalon in teleosts and facilitate comparisons between the telencephalon in ray-finned fish and other vertebrates. Antisera against the following neuroactive substances were used: 1) serotonin (5HT), 2) tyrosine hydroxylase (TH), 3) substance P (SP), 4) leucine-enkephalin (ENK), 5) neuropeptide Y (NPY), and 6) the neurotensin-related hexapeptide LANT6. Several features of the labeling patterns obtained suggested that the dorsal and ventral subdivisions of the area ventralis are homologous as a field to the basal ganglia and septum plus other basal telencephalic regions of land vertebrates, sharks and lungfish: 1) an abundance of SP +, NPY +, and ENK+ fibers; 2) an abundance of TH+ fibers, possibly of posterior tubercle/tegmental origin; 3) the presence of an SP + fiber bundle that appeared to descend from basal telencephalic levels and terminate in the posterior tubercle/tegmentum, which contain TH + (possibly dopaminergic) neurons; and 4) an abundance of 5HT+ fibers, presumably of posterior tubercle/tegmental origin. It was not possible, however, to recognize distinct pallidal and striatal subdivisions within the area ventralis of Polypterus. The olfactory pallium (Pl) was generally poor in most of the substances examined, except for the presence of LANT6+ fibers. The P3 pallid field was conspicuously rich in SP+ and ENK+ fibers throughout its extent, and the caudal and lateral parts of the P2 field were rich in SP+ fibers and ENK+ fibers. Since this is characteristic of the medial pallial and/or dorsomedial pallial walls of the telencephalon in lungfish, sharks, frogs, and reptiles, the P3 field and caudolateral part of the P2 field may be homologous to these portions of the telencephalon in other vertebrates. More rostromedial parts of P2 may correspond to those parts of the pallium in land vertebrates that are in receipt of specific sensory input from the thalamus, since low neuropeptide levels are characteristic of these regions. These results indicate that the dorsal part of the ventral area of the telencephalon in ray-finned fish may be homologous to the basal ganglia in other vertebrates. These results also suggest that the pallial portions of the telencephalon in Polypterus may include a region comparable to part of the isocortex or its homologues in amniotes. o 1992 Wiley-Liss, Inc.

An immunohistochemical study of the telencephalon of the senegal bichir (Polypterus senegalus)

From the dawn of comparative neuroanatomy the central nervous system of the lamprey has attracted the attention of a great number of workers. Owing t o its alleged primitiveness and simplicity’ it was expected that analysis of the brain and spinal cord of these forms would yield the “prototype”2 i.e., the natural starting point for the study of the development and differentation of the vertebrate neuraxis. Hence, many so-called evolutionary trends, like for example the progressive migration, differentiation, segregation, and specialization of neurons and neuron groups, were considered as having their point of departure in the brain of the lamprey or in lamprey-like brains. Unfortunately, many of these trends have been described in a straightforwardly phylogenetic setting without any clear justification for doing so. In fact, all of these trends are naturally based on the study of a single or a few related features and should be considered on that account as typologic rather than phylogenetic. Lampreys have a long, independent phylogenetic history behind them and n o recent group of vertebrates, let alone the entire vertebrate kingdom, can be said t o have arisen from them. However, it cannot be denied that the lampreys retain more features of the presumed ancestral craniates than d o any other members of the group,3 and therefore deserve especial attention. The first part of the present paper will survey the structural organization of the brain and spinal cord of the lamprey. This survey is based on a study of the literature and o n our own Nisslstained and silver-impregnated material of Lampetra fluviatilis. In the second part of this paper the central nervous system of the lamprey will be placed in a comparative perspective. Some of the “trends” referred to above will be review ed. It should be noted that our present-day knowledge of the central nervous system of the lamprey is based on the study of many different species. It stands t o reason that these species differ sufficiently t o be distinguished by the taxonomist. However, neuroanatomically there are no appreciable differences among them; hence, I feel justified in using in the present treatise the term “lamprey” without any further specification.*

The brain of the lamprey in a comparative perspective.

The class of bony fishes or Osteichthyes is usually subdivided into two subclasses, the Actinopterygii or ray-finned fishes and the Sarcopterygii or lobe-finned fishes. The subclass last mentioned, the telencephalon of which will be treated in the next chapter, can further be subdivided into the Dipnoi or lungfishes and the Crossopterygii or tassel-finned fishes. The Actinopterygii constitute by far the most abundant group of recent vertebrates. They are usually subdivided into three superorders, the Chondrostei, Holostei, and Teleostei. Interestingly, these three superorders may be considered as representing three subsequent stages or gradations of actinopterygian evolution. The Chondrostei are considered as descendants of the Palaeoniscoidei, a primitive group of paleozoic fishes. During the early and middle Mesozoic times, the Chondrostei were supplanted by the Holostei, which in turn were largely replaced in the last phase of the Mesozoic era and the Cenozoic era by the expanding and now-abundant Teleostei.

The Telencephalon of Actinopterygian Fishes

Resume

Les resultats de l'analyse du developpement embryonnaire du telencephale de Polypterus senegalus, ainsi que d'une courte description du telencephale de l'adulte ont ete compares aux donnees presentes dans la litterature scientifique, concernant le developpement et la structure du telencephale des Chondrosteens (Ch), des Holosteens (H) et des Teleosteens (T). Par l'organogenese et la morphologie de son telencephale, Polypterus presente de nombreux points de ressemblance avec les trois groupes ci-dessus cites. Dans la liste des resultats qui vont etre donnes, nous avons adopte le principe suivant: si le processus de developpement ou la structure dont il est fait mention concerne non seulement Polypterus, mais aussi les autres groupes de Poissons osseux, les initiales de ces groupes (Ch, H, T) seront ajoutees entre parentheses.



1
Comme chez tous les Gnathostomes, la morphogenese du telencephale du Polyptere commence par une inversion legere de ses parois laterales.

2
Par la suite, cette inversion, disparait. Les parois de l'ebauche telencephalique commencent a faire saillie dans la cavite ventriculaire et, correlativement, les taeniae (c'est-a-dire les deux lignes le long desquelles se rattache le toit telencephalique originellement etroit) se deplacent lateralement (H, T).

3
Ulterieurement, les taeniae se deplacent en direction ventrale, et l'apparition de sillons externes bilateraux (sulcus externus) indique les debuts du processus d'eversion (Ch, H, T).

4
Chez les Chondrosteens, les Holosteens et les Teleosteens, c'est l'epaississement des parois telencephalique qui domine pendant reversion; chez Polypterus au contraire, ces parois croissent bien plus suivant leur dimension dorsoventrale qu'en epaisseur.

5
Les bulbes olfactifs apparaissent au debut sous forme d'epaississements des parois telencephaliques. Plus tard, ils prennent la forme d'evaginations separees, possedant en propre leur cavites ventriculaires (Ch, H).

6
Outre reversion et l'evagination reelle bulbaire, une pseudoevagination (Kallen) se produit dans le telencephale de Polypterus. Ce processus conduit a la formation d'un septum ependymaire etendu (Ch, H).

7
Tot au cours du developpement, deux regions, qui sont respectivement l'area dorsalis telencephali ou pallium et l'area ventralis telencephali ou subpallium, peuvent etre distinguees d'apres des differences cytologiques (Ch, H, T).

8
La zone periventriculaire de l'area ventralis telencephali se differencie en un nucleus subpallialis dorsalis et un nucleus subpallialis ventralis (Ch, H, T). D'autres cellules de l'area ventralis migrent vers une position submeningee et forment un noyau subpallialis lateralis (H, T).

9
Une colonne de cellules migrantes dirigee rostroventralement, et provenant de la portion la plus dorsocaudale du manteau subpallie, aboutit a la formation du complexe des noyau entopedonculaires (Ch, H, T).

10
Dans l'area dorsalis telencephali du Polyptere, la couche du manteau embryonnaire persiste chez l'adulte sous forme d'une zone etroite de substance grise periventriculaire. Cette zone ne montre ni aux stades larvaires, ni chez l'adulte, de signe de differenciation en territoires distincts.

11
L'area dorsalis telencephali ou pallium du Polyptere montre un stade d'organisation bien plus simple que celui des Chondrosteens, des Holosteens et des Teleosteens.

12
Une couche cellulaire externe etendue se forme dans la partie rostrale evaginee du telencephale du Polyptere. Comme chez Acipenser, cette couche est en continuite avec la zone glomerulaire et appartient integralement a la formation bulbaire.





Abstract

In this paper an analysis of the development of the forebrain of Polypterus senegalus, and a short description of the adult telencephalon of that species has been presented. The results of this study have been compared with data obtained from the literature on the development and structure of the forebrain of the Chondrostei (Ch), Holostei (H), and Teleostei (T). It appeared that, with regard to the embryology and morphology of its forebrain, Polypterus shows many points of resemblance to the three groups mentioned. In the subsequent survey of results these similarities have been indicated as follows: if the process or feature mentioned occurs not only in Polypterus, but also in the other bony fish groups, the initials of these groups (Ch, H, T) are added in brackets.



1
As in all Gnathostomes the morphogenesis of the forebrain of Polypterus commences with a slight inversion of its lateral walls.

2
During further development this inversion disappears. The walls of the telencephalic anlage begin to protrude into the ventricular cavity, and concomitantly the taeniae (i.e. the lines of attachment of the initially narrow telencephalic roof plate) move laterally (H, T).

3
Later the taeniae are displaced ventrally, and the appearance of bilateral external grooves (sulci externi) marks the beginning of an eversion (Ch, H, T).

4
In the Chondrostei, Holostei and Teleostei the thickening of the telencephalic walls continues during the eversion, but in Polypterus these walls increase much more in dorsoventral length than in thickness.

5
The bulbi olfactorii develop initially as thickenings of the telencephalic walls. In later stages they assume the configuration of separate evaginations, with ventricular cavities of their own (Ch, H).

6
Apart from eversion and true evagination, an extensive pseudoevagination (Kallen) occurs in the forebrain of Polypterus. This process leads to the formation of an extensive ependymal septum (Ch, H).

7
Early in development two regions, i.e., the area dorsalis telencephali or pallium and the area ventralis telencephali or subpallium can be delimited on account of cytological differences (Ch, H, T).

8
The periventricular zone of the area ventralis telencephali differentiates into a nucleus subpallialis dorsalis and a nucleus subpallialis ventralis (Ch, H, T). Other cells within the area ventralis migrate to a submeningeal position and form a nucleus subpallialis lateralis (H, T).

9
A rostroventrally directed migration of cells, originating from the most dorsocaudal part of the subpallial mantle layer, leads to the formation of a complex of entopeduncular nuclei (Ch, H, T).

10
In the area dorsalis telencephali of Polypterus the embryonic mantle layer persists as a narrow zone of periventricular gray. Neither in the larvae nor in the adult does this zone show signs of a differentiation into separate fields.

11
The area dorsalis telencephali or pallium of Polypterus is much more simply organized than that of the Chondrostei, Holostei and Teleostei.

12
In the rostral, evaginated part of the forebrain of Polypterus an extensive external cell layer is formed. As in Acipenser this layer is coextensive with the glomerular zone and belongs entirely to the bulbar formation.

J. Arnoult

Papers

Le développement du télencéphale d'un poisson osseux primitif, Polypterus senegalus Cuvier