Convergent gene expression highlights shared vocal motor microcircuitry in songbirds and humans

Abstract

Vocal learning is a skilled motor behavior observed in several mammalian and avian species and is critical for human speech. While convergent gene expression patterns have highlighted similar primary motor and striatal pathways for vocal imitation in songbirds and humans, the extent of molecular and circuit convergence remains unresolved. Here we profiled the four principal song nuclei of the zebra finch (HVC, LMAN, RA, Area X) and their surrounding brain regions using RNA-Seq and compared them with specialized markers we identified for human speech brain regions. Expanding previous work, both songbird RA and HVC exhibited convergent specialized gene expression of [~]350 genes with human laryngeal sensorimotor cortex. The songbird HVCRA intratelencephalic (IT) neurons were the predominant cell type that was convergent with human, specifically layer 2/3 IT neurons, while the songbird RA extratelencephalic (ET) projection neurons exhibited convergent expression with human layer 5 ET projection neurons. The molecular specializations of both songbird LMAN and human Brocas area were more unique to each species. These findings demonstrate the extent of convergent molecular specializations in distantly related species for vocal imitation and emphasize important evolutionary constraints for this complex trait. One-Sentence SummaryOur data provide hundreds of candidate genes to study the molecular basis and evolution of song and speech across species.