Abrupt and gradual changes in neuronal processing upon falling asleep and awakening

Abstract

The neural processes that change when falling asleep are only partially understood. At the cortical level, features of both spontaneous neural activity and sensory responses change between wakefulness and sleep. For example, in early auditory cortex, sleep increases the occurrence of post-onset silent (OFF) periods and elevates population synchrony. However, it remains unknown whether such changes occur abruptly or gradually around sleep onset and awakening. Here, we recorded spontaneous and sound-evoked neuronal spiking activity in early auditory cortex along with polysomnography during thousands of episodes when male rats fell asleep or woke up. We found that when falling asleep, stimulus-induced neuronal silent periods (OFF periods), characteristic of non-rapid eye movement (NREM) sleep, increased within few seconds around sleep onset. By contrast, a gradual increase in neuronal population synchrony built up over tens of seconds until reaching maximal levels. EEG auditory-evoked potentials likely representing stimulus-triggered "K complexes" changed along with post-onset neuronal firing, whereas ongoing EEG slow wave activity was associated with neuronal population synchrony. Similar effects, but with opposite direction, were observed around awakenings. The results highlight late stimulus-induced neuronal silence as a key feature changing abruptly around transitions between vigilance states, likely reflecting neuronal bistability and manifesting also in EEG evoked potentials. More generally, these findings emphasize the added value of going beyond monitoring ongoing activity and perturbing the nervous system to reveal its state - an insight that could also help guide development of more sensitive non-invasive monitors of falling asleep in humans.