The Mysterious Island: Insula and Its Dual Function in Sleep and Wakefulness

• Main Authors: Ekaterina V. Levichkina, Irina I. Busygina, Marina L. Pigareva, Ivan N. Pigarev
• Format: Article
• Language: English
• Published: Frontiers Media S.A. 2021-02-01
• Series: Frontiers in Systems Neuroscience
• Subjects: insular cortex; wakefulness; sleep; visceral regulation; visceral theory of sleep; gut-brain communication
• Online Access: https://www.frontiersin.org/articles/10.3389/fnsys.2020.592660/full

In the recent sleep studies, it was shown that afferentation of many cortical areas switches during sleep to the interoceptive one. However, it was unclear whether the insular cortex, which is often considered as the main cortical visceral representation, maintains the same effective connectivity in both states of vigilance, or processes interoceptive information predominantly in one state. We investigated neuronal responses of the cat insular cortex to electrical stimulations of the intestinal wall delivered during wakefulness and natural sleep. Marked increase was observed in the number of insular neurons responding to this stimulation in sleep comparing to wakefulness, and enlarged amplitudes of evoked local field potentials were found as well. Moreover, most of the cells responding to intestinal stimulation in wakefulness never responded to identical stimuli during sleep and vice versa. It was also shown that applied low intensity intestinal stimulations had never compromised sleep quality. In addition, experiments with microstimulation of the insular cortex and recording of intestinal myoelectric activity demonstrated that effective insula-to-gut propagation also happened only during sleep. On the other hand, the same insular stimulations in wakefulness led to contractions of orofacial muscles. The evoked face movements gradually disappeared in the course of sleep development. These findings demonstrate that pattern of efficient afferent and efferent connections of the insular cortex changes with transition from wakefulness to sleep.