Uncoordinated sleep replay across hemispheres in the zebra finch

Abstract

Bilaterally organized brain regions are often simultaneously active in both humans1,2,3 and animal models,4,5,6,7,8,9 but the extent to which the temporal progression of internally generated dynamics is coordinated across hemispheres and how this coordination changes with brain state remain poorly understood. To address these issues, we investigated the zebra finch courtship song (duration: 0.5-1.0 s), a highly stereotyped complex behavior10,11 produced by a set of bilaterally organized nuclei.12,13,14 Unilateral lesions to these structures can eliminate or degrade singing,13,15,16,17 indicating that both hemispheres are required for song production.18 Additionally, previous work demonstrated broadly coherent and symmetric bilateral premotor signals during song.9 To precisely track the temporal evolution of activity in each hemisphere, we recorded bilaterally in the song production pathway. We targeted the robust nucleus of the arcopallium (RA) in the zebra finch, where population activity reflects the moment-to-moment progression of the courtship song during awake vocalizations19,20,21,22,23,24 and sleep, where song-related network dynamics reemerge in "replay" events.24,25 We found that activity in the left and right RA is synchronized within a fraction of a millisecond throughout song. In stark contrast, the two hemispheres displayed largely independent replay activity during sleep, despite shared interhemispheric arousal levels. These findings demonstrate that the degree of bilateral coordination in the zebra finch song system is dynamically modulated by behavioral state.