Multispecies characterization of immature neurons in the mammalian amygdala reveals their expansion in primates

Structural changes involving new neurons can occur through stem cell-driven neurogenesis, and through incorporation of late-maturing "immature" neurons into networks, namely undifferentiated neuronal precursors frozen in a state of arrested maturation. The latter have been found in the cerebral cortex and are particularly abundant in large-brained mammals, covarying with the size of the brain and cortex. Similar cells have been described in the amygdala of some species, although their features and interspecies variation remain poorly understood. Here, their occurrence, number, morphology, molecular expression, age-related changes, and anatomical distribution in amygdala subdivisions were systematically analyzed in eight diverse mammalian species (including mouse, naked mole rat, rabbit, marmoset, cat, sheep, horse, and chimpanzee) widely differing in neuroanatomy, brain size, life span, and socioecology. We identify converging evidence that these amygdala cells are immature neurons and show marked phylogenetic variation, with a significantly greater prevalence in primates. The immature cells are largely located within the amygdala's basolateral complex, a region that has expanded in primate brain evolution in conjunction with cortical projections. In addition, amygdala immature neurons also appear to stabilize in number through adulthood and old age, unlike other forms of plasticity that undergo marked age-related reduction. These results support the emerging view that large brains performing complex socio-cognitive functions rely on wide reservoirs of immature neurons.