Stalking the Everted Telencephalon: Comparisons of Forebrain Organization in Basal Ray-Finned Fishes and Teleosts

Abstract

Compared to land vertebrates and the other fishes, the basal ray-finned fishes and teleosts have morphologically unusual forebrains. The telencephalic pallium is everted, and its diencephalic inputs arise largely – not from what is clearly the dorsal thalamus but rather – from an enigmatic group of migrated nuclei of the basal diencephalon. The subpallia exhibit much less variation than the pallia. The polypteriforms have a long, thin pallial sheet that can be divided into four zones which recent data suggest could correspond to the ventral, lateral, dorsal, and medial pallia of tetrapods, with some caveats. In sturgeons and gars, the pallium is thicker and divisible into three or four zones. The data available for sturgeons and gars are not sufficient for the formulation of more than a barely working hypothesis, although a review of the existing literature has illuminated some basic unresolved issues in these taxa. The voluminous literature on the pallium of teleosts is briefly summarized. The thickened pallium is divided into four zones which are compared with those of the polypteriforms and those of the tetrapods. The topographical position of the primary olfactory target in the pallium is lateral, which is unexpected in an everted pallium. Several recent hypotheses have sought to explain this organization: partial eversion, caudolateral eversion and displacement, simple eversion with changed olfactory connections, and not quite so simple an eversion with preserved topology. These hypotheses are evaluated and some persisting problems are enumerated.

Subdivisions of the adult zebrafish pallium based on molecular marker analysis

“…In embryonic and adult zebrafish, tbr1 is expressed throughout the pallium 7, 53, 54 . In adult ray-finned fishes, Dm has been proposed to be homologous to the ventral pallium (pallial amygdala) based on topological, connectional and functional data 29– 31, 64– 66 . In contrast, Nieuwenhuys (2009) proposed that Dm is homologous to the lateral pallium based on topology and Yamamoto et al (2007) suggest that Dm together with Dd and Dld is homologous to the dorsal pallium.…”

“…Being homologous to the lateral pallium, it should be located next to Dm in the embryo, the presumptive ventral pallium. The discrepancy between the position of Dp in the adult and an expected location next to Dm has led to different models to explain the different position of Dp in the adult pallium: “the partial pallial eversion model” by Wullimann and Mueller 31, 32, 52, 74 , the “eversion-rearrangement theory” by Northcutt and Braford 33, 64, 75 , and the “new eversion model” by Yamamoto and colleagues 37 . In the “partial pallial eversion model” 31, 32, 52, 74 , based on connectional and gene expression data, it has been proposed that the homolog of the lateral pallium does not participate in the eversion.…”

“…Our gene expression analysis does not support this part of their modified partial eversion model. Based on differential gene expression we can identify Dp, which is not located submeningeally, but has its own ventricular zone even in the adult 4, 64, 76 . New neurons are still generated in the zebrafish pallium in the adult 77, 78 .…”

“…In addition, it has been noted that Dc shows no significant immunoreactivity to Calretinin, Neuropeptide Y or Thyrosine hydroxylase separating it from the surrounding areas of the pallium 79 . Other models based mainly on topology suggest that Dm, Dd and Dld are homologous to the dorsal pallium 37 , whereas others have homologized Dd with the dorsal pallium 4, 29, 30, 33, 64 and have suggested that Dc is not a separate unit, but represents the deeper zone of the periventricular areas of Dm, Dd and Dl. Our gene expression data is consistent with the second part of the “modified pallial eversion model” of Mueller and colleagues.…”

The Vertebrate mesolimbic reward system and social behavior network: A comparative synthesis

“…Describing homologies between the teleost telencephalon and other vertebrates is especially difficult due to the eversion, rather than invagination, of the neural tube during development (Wullimann and Mueller, 2004;Yamamoto et al, 2007;Braford, 2009;Nieuwenhuys, 2011). However, we are now gaining insight into potential teleost homologies to tetrapod brains from recent neurochemical, hodology, and developmental evidence instead of relying on topography alone (Wullimann and Mueller, 2004).…”