Organizational Conservation and Flexibility in the Evolution of Birdsong and Avian Motor Control

Birds and mammals have independently evolved complex behavioral and cognitive capabilities yet have markedly different brain structures. An open question is to what extent, despite these differences in anatomy, birds and mammals have evolved similar neural solutions to complex motor control and at what level of organization these similarities might lie. Courtship song in songbirds, a learned motor skill that is similar to the fine motor skills of many mammals including human speech, provides a powerful system in which to study the links connecting the development and evolution of cells, circuits, and behavior. Until recently, obtaining cellular-resolution views of the specialized neural circuitry that subserves birdsong was impossible due to a lack of molecular tools for songbirds. However, the ongoing revolution in cellular profiling and genomics offers unprecedented opportunities for molecular analysis in organisms that lack a traditional genetic infrastructure but have tractable, well-defined behaviors. Here, I describe recent efforts to understand the evolutionary relationships between birdsong control circuitry and mammalian neocortical circuitry using new approaches to measure gene expression in single cells. These results, combined with foundational work relating avian and mammalian brains at a range of biological levels, present an emerging view that amniote pallium evolution is a story of diverse neural circuit architectures employing conserved neuronal elements within a conserved topological framework. This view suggests that one locus of pallial neural circuit evolution lies at the intersection between the gene regulatory programs that regulate regional patterning and those that specify functional identity. Modifications to this intersection may underlie the evolution of pallial motor control in birds in general and to the evolutionary and developmental relationships of these circuits to the avian pallial amygdala.