Intracerebral recordings of slow wave and rapid eye-movement sleep in naturally sleeping pigeons

Mammals and birds both show sleep-related slow oscillations (SO) of neuronal activity, which are thought to be involved in processing hippocampal memories at the systems level in mammals. However, unlike the mammalian hippocampus which receives input from most of the cortex, input to the avian hippocampus is restricted to olfactory and visual information, the latter coming from the hyperpallium. This variation in brain connectivity between mammals and birds may be an indication of fundamental differences in the manner of information processing at the systems level during sleep. Therefore, examining sleep-related brain activity at the systems level in birds provides us with an opportunity to test models proposed in mammals, and to reveal fundamental principles that could expand our understanding of mammalian sleep. The aim of the current study was to explore activity in the avian hyperpallium during both natural slow wave sleep (SWS) and rapid eye-movement (REM) sleep, and to compare this to activity recorded under anesthesia. We used a 32-channel silicon probe connected to a transmitter to make intracerebral recordings of the hyperpallium in naturally sleeping and isoflurane anesthetized pigeons (Columba livia) based on a within-bird design. Local field potential (LFP) recordings reveal high amplitude SO (<2Hz) across most recordingsites during natural SWS. These oscillations show diverse propagation patterns (i.e. slow waves) across the recording array. Similar results are found under anesthesia, with the exception that the SO show higher amplitude and SO activity seems more synchronized between electrode sites. In contrast, LFP recordings during REM sleep show a reduced amount of slow wave activity and lack the traveling SO seen during SWS. In conclusion, this study shows that the traveling nature of slow waves can be found in the avian hyperpallium during both natural SWS and anesthesia. As traveling slow waves have also been described in mammals, this appears to be a fundamental feature of slow wave sleep. However, simultaneous recordings of the hyperpallium and hippocampus during natural sleep are needed to evaluate the potential role that these slow waves play in processing information at a systems level in the avian brain.