Abstract
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 other behavioral states. Here, we used chronically implanted Neuropixels probes to investigate spontaneous neural activity in the AFP during natural sleep and awake periods in male zebra finches. We found that during sleep, neuron populations in the pallial region LMAN (lateral magnocellular nucleus of the nidopallium) spontaneously exhibited synchronized bursts that were characterized by a negative sharp deflection in the local field potential (LFP) and a transient increase in gamma power. LMAN population bursts occurred primarily during non-rapid eye movement (NREM) sleep and were highly reminiscent of sharp-wave ripple (SWR) activity observed in rodent hippocampus. We also examined the functional connectivity within the AFP by calculating the pairwise LFP coherence. As expected, delta and theta band coherence within LMAN and Area X was higher during sleep compared to awake periods. Contrary to our expectations, we did not observe strong coherence between LMAN and Area X during sleep, suggesting that the input from LMAN into Area X is spatially restricted. Overall, these results provide the first description of spontaneous neural dynamics within the AFP across behavioral states.
Significance statement Although cortical and basal ganglia circuits are known to be required for learning in both mammals and birds, little is known about the ongoing spontaneous activity patterns within these circuits, or how they are modulated by behavioral state. Here we prove the first description of cortical-basal ganglia network activity during sleep and awake periods in birds. Within the pallial area LMAN, we observed population-wide bursting events that were highly reminiscent of hippocampal sharp-wave ripple (SWR) activity, suggesting that large-scale population events have diverse functions across vertebrates.
Footnotes
The authors declare no competing financial interests.
This research was supported by the Agence Nationale de la Recherche (SleepinBrainDyn) and the CNRS (International Emerging Action, project BirdSleep) to AD; the EUR NEURO (EUR/7410-5) and Bordeaux Neurocampus - GPR BRAIN 2030 (GP/7200R-12) to EGZC; the Deutsche Forschungsgemeinschaft (ON 151/1-1) and the Daimler und Benz Stiftung (PN 32-09/18) to JMO; the BayFrance program (FK23 2019) to CL, HY, NG, and JMO. The authors would further like to thank and acknowledge Melanie Dumont for excellent animal caretaking and Manon Rolland for help with experiments.
↵*Authors contributed equally
