Abstract
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.
Highlights
Insular cortex is often considered as the main representation of the visceral systems at the cortical level (Saper, 2002; Aleksandrov and Fedorova, 2003; Bagaev and Aleksandrov, 2006; Craig, 2009; Nieuwenhuys, 2012), following a common approach to classification of the cortical areas according to the dominant input from a particular sensory modality, e.g., visual, auditory, visceral, etc.the current map of the cortical functions is dramatically different from the one widely accepted by the middle of the twentieth century, when proportionally more of the physiological studies were devoted to the investigation of various visceral systems and their cortical representations
Sleep is characterized by increased delta and spindle activity while increased gamma is common for wakefulness (Contreras and Steriade, 1996; Destexhe et al, 1999)
We found that in all recordings in both cats delta and spindle range power spectral density values in EEG were significantly higher in sleep while power in gamma range was always higher in wakefulness (Wilcoxon Rank Sum test p < 0.001)
Summary
The current map of the cortical functions is dramatically different from the one widely accepted by the middle of the twentieth century, when proportionally more of the physiological studies were devoted to the investigation of various visceral systems and their cortical representations In these early experiments, performed in acute conditions under general anesthesia, responses to stimulation of internal organs and visceral nerves were found in frontal, Insular Cortex in Wakefulness and Sleep parietal, and temporal cortices (Amassian, 1951; Chernigovskii and Musiashchikova, 1965; historic overview of the frontal cortex involvement in visceral control is presented in the review by Neafsey, 1990). This view at that time was not considered surprising, given a huge number of interoreceptors distributed in various visceral organs (e.g., Chernigovskii, 1960, 1967)
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