Multi-channel EEG recordings during sleep in juvenile zebra finches highlight developmental changes in sleep structure and functional connectivity similar to mammals

Abstract

Despite their phylogenetic differences and distinct pallial structures, mammals and birds show similar electroencephalography (EEG) traces during sleep, consisting of distinct rapid eye movement (REM) sleep and slow wave sleep (SWS) stages. Studies in human and a limited number of other mammalian species shows that this organization of sleep into interleaving stages undergoes radical changes during lifetime. Do these age-dependent variations in sleep patterns also occur in the avian brain? Does vocal learning have an effect on sleep patterns in birds? To answer this question, we recorded multi-channel sleep EEG from juveniles and adult zebra finches for several nights. Whereas adults spent more time in SWS and REM sleep, juveniles spent more time in intermediate sleep (IS). The amount of IS sleep was significantly larger in male juveniles engaged in vocal learning compared to female juveniles, which suggest that IS sleep could be important for learning. In addition, we observed that the functional connectivity increased rapidly during maturation of young juveniles, and was stable or declined at older ages. Synchronous activity during sleep was larger for recording sites in the left hemisphere for both juveniles and adults, and generally intra-hemispheric synchrony was larger than inter-hemispheric synchrony during sleep. A graph theory analysis revealed that in adults, highly correlated EEG activity tends to be distributed across fewer networks that are spread across a wider area of the brain, whereas in juveniles, highly correlated EEG activity is distributed across more numerous, albeit smaller, networks in the brain. Overall, our results reveal significant changes in the neural signatures of sleep during maturation in an avian brain.