Ontogenetic development of ponto-geniculo-occipital waves during paradoxical sleep in kittens

Ponto-geniculo-occipital (PGO) waves are a hallmark feature of paradoxical sleep (PS), emerging just before PS onset during the transition from slow-wave sleep (SWS) to PS (TSWS-PS) and persisting throughout the PS phase in adult cats. These waves are considered a biomarker for the maturation of PS. However, their developmental trajectory in mammals remains poorly understood. This study investigated the emergence and maturation of PGO waves during PS in developing kittens.

Electrodes were stereotaxically implanted into the lateral geniculate nucleus, accurately localized using magnetic resonance imaging. Recording included cortical electroencephalogram, nuchal muscle activity, PGO waves, and rapid eye movements (REMs).

Despite the presence of abundant PS and frequent muscle twitches accompanied by REMs in neonatal kittens, PGO spikes were first detected at postnatal day (PND) 16, with an average onset at PND 19. Initially, these waves appeared with lower density and amplitude during the TSWS-PS and PS phases. Over the following weeks, PGO wave density and amplitude increased, along with prolonged durations during both TSWS-PS and PS. Type I waves (singlet and bigeminy) predominated during TSWS-PS, while type II waves (clusters) were more frequent during PS. The proportion of type II waves and their co-occurrence with REMs increased with age. The adult-like pattern of PGO waves was fully established by PND 50.

The emergence and maturation of PGO waves during PS are closely linked to the development of the sleep-wake cycle and may play a role in learning and memory processes.