Evolution of pallium, hippocampus, and cortical cell types revealed by single-cell transcriptomics in reptiles

Abstract

Computations in the mammalian cortex are carried out by glutamatergic and γ-aminobutyric acid-releasing (GABAergic) neurons forming specialized circuits and areas. Here we asked how these neurons and areas evolved in amniotes. We built a gene expression atlas of the pallium of two reptilian species using large-scale single-cell messenger RNA sequencing. The transcriptomic signature of glutamatergic neurons in reptilian cortex suggests that mammalian neocortical layers are made of new cell types generated by diversification of ancestral gene-regulatory programs. By contrast, the diversity of reptilian cortical GABAergic neurons indicates that the interneuron classes known in mammals already existed in the common ancestor of all amniotes.

Concentric ring topology of mammalian cortical sectors and relevance for patterning studies

“…Adjacent to the avian dorsal pallium domain, in a parolfactory position, there is a so‐called “mesopallium” domain that recently has been postulated to be homologous with the mammalian claustro‐insular region on the basis of its topology, neurogenetic chronology, specific genoarchitectonic properties, and pattern of tangentially migrating derivatives (Puelles, ; Puelles et al, , ; Puelles, Ayad, et al, ). The reptilian neopallial primordium and claustroinsular mesopallium correlates have been recently pinpointed at a far rostral location and are of relatively small size (Puelles et al, ; Desfilis, Abellán, Sentandreu, & Medina, ; see also Tosches et al, ).…”

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

“…Yet, similar molecular markers are also found in the mammalian amygdalar complex, including endopiriform nucleus and claustrum (ventral and lateral pallium), which suggests that these are widespread pallial phenotypes in amniotes and supports similarity between the DVR and the mammalian amygdalar complex (Belgard et al, 2013;Medina, Abellán & Desfilis, 2013;Montiel & Aboitiz, 2018;Puelles, 2001). Another possibility is that microcircuit similarities between the neocortex and DVR are due to evolutionary convergence, with co-option of similar genes in different brain regions (Belgard & Montiel, 2013;Belgard et al, 2013;Montiel & Aboitiz, 2018;Montiel et al, 2016;Pfenning et al, 2014;Tosches et al, 2018). Another possibility is that microcircuit similarities between the neocortex and DVR are due to evolutionary convergence, with co-option of similar genes in different brain regions (Belgard & Montiel, 2013;Belgard et al, 2013;Montiel & Aboitiz, 2018;Montiel et al, 2016;Pfenning et al, 2014;Tosches et al, 2018).…”

Reptilian Cognition: A More Complex Picture via Integration of Neurological Mechanisms, Behavioral Constraints, and Evolutionary Context

“…Nevertheless, in general terms, the medial cortex (MC) of reptiles is the putative homologue to parts of the mammalian hippocampus, the part of the brain responsible for spatial cognition . The MC exhibits projections similar to that of hippocampal mossy fibers and mammalian hippocampal cell types appear to be conserved or derived from a common ancestor . While not all mammalian hippocampal subfields are represented in the MC of reptiles, recent studies using gene expression data suggest there may be mammalian‐like hippocampal subfields in parts of the reptilian cortices .…”

“…While not all mammalian hippocampal subfields are represented in the MC of reptiles, recent studies using gene expression data suggest there may be mammalian‐like hippocampal subfields in parts of the reptilian cortices . Interestingly, the reptilian dorsal cortex (DC) has been ascribed similarities in structure and neuronal types with parts of the hippocampus, structural similarities with other areas of the mammalian brain important for memory use (e.g., the entorhinal cortex and subiculum) …”