Neural population dynamics during sleep in a songbird vocal circuit resemble sharp wave ripple activity

During vocal learning, juvenile songbirds use auditory feedback and trial-and-error motor learning to transition from acoustically simple, highly variable songs to complex and stereotypical adult songs. Similar to motor skill learning in mammals, vocal learning in songbirds requires a set of interconnected brain areas that make up an analogous basal ganglia-thalamocortical circuit known as the anterior forebrain pathway (AFP). Although neural activity in the AFP has been extensively investigated during awake singing, very little is known about its neural activity patterns during offline sleep periods.

In this work, we used chronically implanted Neuropixels probes to investigate neural activity in the AFP during offline periods of natural sleep. We found that neurons in the pallial region LMAN (lateral magnocellular nucleus of the nidopallium) transitioned from sparse synchronous firing to asynchronous firing during sleep, which corresponded to slow wave sleep (SWS) and rapid eye movement (REM) sleep, respectively. SWS periods were associated with increased spiking variability for LMAN neurons, but not for neurons in the striatal region Area X (proper name). Coinciding with the increased spiking variability, we observed that populations of LMAN neurons were co-activated at specific time points during sleep in bursting events that were characterized by a negative deflection in the local field potential (LFP) and a transient increase in gamma power. Overall, the LMAN population bursting events were highly reminiscent of sharp-wave ripple (SWR) activity observed in rodent hippocampus.

Contrary to our expectations, we did not observe strong cross-area field coherence between LMAN and Area X, although individual LMAN-Area X LFP pairs did show coherence > 0.5. These results provide the first description of cross-area dynamics within the AFP during sleep. Furthermore, the observation of SWR-like events during sleep in LMAN suggests that large-scale population events have diverse functions across vertebrates.