Immature Excitatory Neurons in the Postnatal Ferret Paralaminar Nuclei and Their Relationship to the Amygdala Across Species

Abstract

The amygdala paralaminar nuclei (PL) contain immature excitatory neurons that develop on a delayed timeline from birth to adulthood and are more prominent in the amygdala of humans and other primates than in rodents. Whether this expansion is linked to brain complexity or is a feature of primates is unknown. We sought to identify the PL in the ferret (Mustela putorius furo), a small, gyrencephalic mammal that does not belong to the primate order. Here, we show that the amygdala of juvenile (P30–P67) and adult ferrets (>1 year) also contains a collection of immature excitatory neurons that express doublecortin (Dcx) and polysialylated neural cell adhesion molecule (Psa-Ncam). Similar to humans and mice, these immature neurons express Tbr1 and CoupTFII, but not FoxP2, which labels neighboring clusters of GABAergic cells in the intercalated nuclei. Ferret PL neurons extend into the ventral basolateral amygdala (BLA) and appear either in dense clusters surrounded by astroglia or as individual cells, and each subpopulation contains neurons with migratory morphology. This expansion of PL neurons into the amygdala is similar to what is seen in humans, but unlike in mice, where PL neurons are infrequent in the BLA. We compared these findings to the marmoset (Callithrix jacchus), a lissencephalic non-human primate, and the swine (Sus scrofa domesticus), a gyrencephalic mammal, and found immature neurons extending into the amygdala in both. Our study identifies the PL region of the ferret amygdala, which contains immature neurons with migratory features in juveniles and adults. Cross-species comparisons indicate that the expansion of PL neurons into the amygdala seen in primates with both high and low gyrencephalic indices has also occurred in species with gyrencephalic brains from different orders.