Molecular anatomy of the alligator dorsal telencephalon

Abstract

The evolutionary relationships of the mammalian neocortex and avian dorsal telencephalon (DT) nuclei have been debated for more than a century. Despite their central importance to this debate, non-avian reptiles remain underexplored with modern molecular techniques. Reptile studies harbor great potential for understanding the changes in DT organization that occurred in the early evolution of amniotes. They may also help clarify the specializations in the avian DT, which comprises a massive, cell-dense dorsal ventricular ridge (DVR) and a nuclear dorsal-most structure, the Wulst. Crocodilians are phylogenetically and anatomically attractive for DT comparative studies: they are the closest living relatives of birds and have a strikingly bird-like DVR, but they also possess a highly differentiated reptile cerebral cortex. We studied the DT of the American alligator, Alligator mississippiensis, at late embryonic stages with a panel of molecular marker genes. Gene expression and cytoarchitectonic analyses identified clear homologs of all major avian DVR subdivisions including a mesopallium, an extensive nidopallium with primary sensory input territories, and an arcopallium. The alligator medial cortex is divided into three components that resemble the mammalian dentate gyrus, CA fields, and subiculum in gene expression and topography. The alligator dorsal cortex contains putative homologs of neocortical input, output, and intratelencephalic projection neurons and, most notably, these are organized into sublayers similar to mammalian neocortical layers. Our findings on the molecular anatomy of the crocodilian DT are summarized in an atlas of the alligator telencephalon.

Morphological evolution of the vertebrate forebrain: From mechanical to cellular processes

“…The hypothesis of cellular homology also prescribes that the same cell types were anatomically "rearranged" into distinct laminae in the mammalian neocortex and into distinct components of the sauropsid DVR, by coopting different developmental mechanisms (Briscoe & Ragsdale, 2018a. We strongly agree with this assertion in terms of the mechanisms: In the neocortex, a single neural progenitor from the dorsal pallium sequentially generates the components of the microcircuit (Telley et al, 2019).…”

“…A renewed version of the DVR-neocortex homology hypothesis has been supported by recent findings revealing that neurons in distinct laminae of the mammalian neocortex display similar microcircuitry and molecular markers as those observed in different components of the DVR and in the dorsal cortex/Wulst of sauropsids (Ahumada-Galleguillos, Fernández, Marin, Letelier, & Mpodozis, 2015;Briscoe & Ragsdale, 2018aDugas-Ford, Rowell, & Ragsdale, 2012;Faunes, Botelho, Ahumada Galleguillos, & Mpodozis, 2015;Fredes, Tapia, Letelier, Marín, & Mpodozis, 2010). This interpretation asserts that there are homologous neuronal populations in both structures so that the same canonical input-output processing microcircuit was present in the amniote last-common ancestor and was allocated to the mammalian neocortex and to the sauropsid DVR and dorsal cortex/Wulst (Briscoe & Ragsdale, 2018b).…”

Homology, neocortex, and the evolution of developmental mechanisms

“…Six transcription factors characterize the avian mesopallium (17), which, as defined by Jarvis et al (11), includes a dorsal division associated with the Wulst and a ventral division in the DVR. Gene expression experiments in alligators revealed a similar bipartite organization, with mesopalliumlike cells in the dorsal cortex and a mesopallium in the DVR (17,18). Cell populations in turtle and lizard cortices also express several of the mesopallium transcription factors, indicating that mesopallium-like cell types are shared across sauropsids (16).…”

“…For example, the paralogous genes RORA and RORB, both of which regulate the differentiation of neocortical input neurons (23,24), are expressed by pallial input cells of birds and reptiles (10,11,16,18). These two transcription factors, together with SATB1 (16,18), may participate in a conserved gene regulatory network for the identity of pallial input cells, including their connections and physiological properties (Fig. 2, ancestral input cell).…”

Field Homology: Still a Meaningless Concept

“…Birds and nonavian reptiles do not possess a neocortex, but their telencephala do contain several classes of excitatory neuronal cell types that are remarkably similar to mammalian neocortical neurons in terms of their connectivity patterns [Briscoe et al, 2018;Briscoe and Ragsdale, 2018b]. Rather than being stacked into a 6-layered cortical structure, these avian and reptilian neuronal cell types are generally organized into clustered nuclei within a structure called the dorsal ventricular ridge.…”