Homology, neocortex, and the evolution of developmental mechanisms

Abstract

The six-layered neocortex of the mammalian pallium has no clear homolog in birds or non-avian reptiles. Recent research indicates that although these extant amniotes possess a variety of divergent and nonhomologous pallial structures, they share a conserved set of neuronal cell types and circuitries. These findings suggest a principle of brain evolution: that natural selection preferentially preserves the integrity of information-processing pathways, whereas other levels of biological organization, such as the three-dimensional architectures of neuronal assemblies, are less constrained. We review the similarities of pallial neuronal cell types in amniotes, delineate candidate gene regulatory networks for their cellular identities, and propose a model of developmental evolution for the divergence of amniote pallial structures.

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

“…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). 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).…”

Duplications and domain-generality.

“…They can also have strikingly different morphology: in the mammalian neocortex, excitatory cells tend to be pyramidal while they have stellate shape in the pallium in birds. Briscoe and Ragsdale (2018) A more concrete and well-understood case of how duplicated structures can be functionally integrated is the evolution of trichromacy in old-world and Howler monkeys (see e.g., Jacobs, 2009;Surridge et al, 2003, for reviews). As mentioned above, trichromacy evolved from dichromacy through duplication of an opsin.…”

Pseudo-repeats in doublecortin make distinct mechanistic contributions to microtubule regulation

“…13C-D). This suggests that the observed adjustments in the sequence of the DC domains may have a role in enabling forebrain development in higher vertebrates, potentially contributing to wider molecular synergies in this part of the brain and elaboration of the mammalian neocortex (Briscoe and Ragsdale, 2018).…”