Succinic Dehydrogenase Histochemistry Reveals the Location of the Putative Primary Visual and Auditory Areas within the Dorsal Ventricular Ridge of <i>Sphenodon punctatus</i>

Abstract

In turtles, crocodilians, lizards and snakes, the dorsal ventricular ridge (DVR) is a nuclear cell mass that contains distinct visual and auditory thalamorecipient cell groups. In the tuatara (Sphenodon punctatus), the DVR is not organized into diverse cell groups but instead possesses a trilaminar cytoarchitecture resembling that characteristic of the telencephalic cortex in reptiles. To determine if visual and auditory fields might also be present in the DVR of Sphenodon punctatus, we used succinic dehydrogenase (SDH) histochemistry, which has been shown to delineate the visual and auditory fields of the DVR in turtles, crocodilians and lizards. We also used acetylcholinesterase (AChE) histochemistry to determine the boundary between the DVR and the basal ganglia in Sphenodon. We found an SDH-rich region in the neuropil ventral to the cell plate of the rostrolateral DVR and a slightly less intense SDH-rich zone in the neuropil deep to the cell plate of the ventromedial DVR. These SDH-rich zones appear to be located at the apical dendrites of the neurons of the adjacent cell plate. These SDH-rich zones were clearly located within the DVR and were distinct from the AChE-rich striatal part of the basal ganglia, which occupied the ventrolateral wall of the telencephalon. Based on findings in other reptiles, it seems likely that the SDH-rich zone in rostrolateral DVR represents the zone of termination of nucleus rotundus visual input to the DVR, whereas the zone in ventromedial DVR represents the zone of termination of nucleus reuniens auditory input. Because a trilaminar DVR such as that in Sphenodon might be the primitive DVR condition for reptiles, our results suggest that the cytoarchitecture of the DVR and the synaptic organization of its thalamic sensory input in the common ancestor of living reptiles might have been much like of the dorsal cortex.

Molecular anatomy of the alligator dorsal telencephalon

“…The hypothetical ancestral structure contained input, output, and IT neurons in an unknown configuration. It may, for example, have architecturally resembled the simple cortex found in the tuatara (Figure 1) (Reiner & Northcutt, 2000).…”

“…In other groups, like crocodilians, the DVR is densely packed with cells and can be divided into multiple territories with sharp boundaries (Crosby, 1917;Riss et al, 1969). In the remarkable brain of the tuatara, the DVR contains a thin cortex-like structure that appears to be continuous with the dorsal cortex at the lateral edge of the DT (Figure 1, cortex within the DVR) (Cairney, 1926;Durward, 1930;Reiner & Northcutt, 2000). The reptile DVR is often divided into an anterior ADVR and a posterior, or basal, BDVR (Ulinski, 1983).…”

Neuronal subtype specification in establishing mammalian neocortical circuits

“…Although this review highlights the significance of neocortical assembly in mammals, these insights also imply that neuronal specification and patterning may involve species-specific regulatory mechanisms in reptiles and birds. Of course, one cannot argue the presence of higher cognitive processing in birds and reptiles (Reiner and Northcutt, 2000) despite the lack of distinctive laminated cytoarchitecture. While an anatomically remote structure such as the DVR makes the direct comparison of neuronal subtypes between mammals and sauropsid brains devious, combinatorial approaches including molecular function and lineage analysis will eventually connect their ontogeny.…”

Variation in Reptilian Brains and Cognition

“…3 ). In Sphenodon, the DVR consists of a distinct cortical cellular band whose neurons possess ventrally directed dendrites that branch into an underlying neuropil where the ascending thalamic projections terminate [Reiner and Northcutt, 2000]. In turtles, gekkoid lizards, and lacertid lizards, there is a comparable cellular pattern (type I) in the DVR, whereas in snakes, scincomorph lizards, anguimorph lizards, and iguanoid lizards, the cellular pattern in the DVR is such that neuronal cell bodies migrate throughout the DVR, forming distinct nuclear divisions (type II).…”