An Adaptive Threshold in Mammalian Neocortical Evolution

TL;DR

This study investigates the evolutionary mechanisms behind neocortex expansion in mammals, revealing a neuronal threshold that distinguishes phenotypic groups and emphasizing the role of neurogenic period length in cortical development.

Contribution

It introduces a neuronal threshold concept for neocortex expansion and models proliferative progenitor divisions as key to crossing this threshold in mammalian evolution.

Findings

Gyrencephaly is an ancestral trait in mammals.

A neuronal threshold of 10^9 neurons distinguishes phenotypic groups.

Length of neurogenic period predicts cortical neuron number within groups.

Abstract

Expansion of the neocortex is a hallmark of human evolution. However, it remains an open question what adaptive mechanisms facilitated its expansion. Here we show, using gyrencephaly index (GI) and other physiological and life-history data for 102 mammalian species, that gyrencephaly is an ancestral mammalian trait. We provide evidence that the evolution of a highly folded neocortex, as observed in humans, requires the traversal of a threshold of 10^9 neurons, and that species above and below the threshold exhibit a bimodal distribution of physiological and life-history traits, establishing two phenotypic groups. We identify, using discrete mathematical models, proliferative divisions of progenitors in the basal compartment of the developing neocortex as evolutionarily necessary and sufficient for generating a fourteen-fold increase in daily prenatal neuron production and thus traversal of the neuronal threshold. We demonstrate that length of neurogenic period, rather than any novel progenitor-type, is sufficient to distinguish cortical neuron number between species within the same phenotypic group.