Rapid Interhemispheric Switching during Vocal Production in a Songbird

Abstract

To generate complex bilateral motor patterns such as those underlying birdsong, neural activity must be highly coordinated across the two cerebral hemispheres. However, it remains largely elusive how this coordination is achieved given that interhemispheric communication between song-control areas in the avian cerebrum is restricted to projections received from bilaterally connecting areas in the mid- and hindbrain. By electrically stimulating cerebral premotor areas in zebra finches, we find that behavioral effectiveness of stimulation rapidly switches between hemispheres. In time intervals in which stimulation in one hemisphere tends to distort songs, stimulation in the other hemisphere is mostly ineffective, revealing an idiosyncratic form of motor dominance that bounces back and forth between hemispheres like a virtual ping-pong ball. The intervals of lateralized effectiveness are broadly distributed and are unrelated to simple spectral and temporal song features. Such interhemispheric switching could be an important dynamical aspect of neural coordination that may have evolved from simpler pattern generator circuits. As for all vertebrates, the songbird cerebrum has two halves (or hemispheres), each of which controls mainly the muscles in one half of the body. Many motor behaviors such as singing rely on high coordination of activity in both hemispheres, yet little is known about the neural mechanisms of this coordination. By using electrical stimuli to briefly perturb the activity of neurons in the motor pathway during song production, we study their involvement in generating the different elements of a song in zebra finches. We find mostly disjoint time intervals in which stimulation of either the right or left hemisphere is effective in distorting a song. This interhemispheric switching of stimulation effectiveness is evidence of a novel form of ping-pong–like motor coordination. Because left–right alternation is the basis of many motor patterns such as swimming and walking, we speculate that interhemispheric switching in songbirds has its evolutionary roots in older circuit principles invented for locomotion.