eNeuro. 2021 Nov 2:ENEURO.0194-21.2021. doi: 10.1523/ENEURO.0194-21.2021. Online ahead of print.
ABSTRACT
Studies in animals have demonstrated a strong relationship between cortical and hippocampal activity, and autonomic tone. However, the extent, distribution, and nature of this relationship have not been investigated with intracranial recordings in humans during sleep. Cortical and hippocampal population neuronal firing was estimated from high gamma band activity (HG) from 70 to 110 Hz in local field potentials recorded from 15 subjects (9 females) during non-rapid eye movement (NREM) sleep. Autonomic tone was estimated from heart rate variability (HRV). HG and HRV were significantly correlated in the hippocampus and multiple cortical sites in NREM stages N1-3. The average correlation between HG and HRV could be positive or negative across patients given anatomical location and sleep stage and was most profound in lateral temporal lobe in N3, suggestive of greater cortical activity associated with sympathetic tone. Patient-wide correlation was related to delta band activity (1-4 Hz), which is known to be correlated with high gamma activity during sleep. The percentage of statistically correlated channels was weaker in N1 and N2 as compared to N3, and was strongest in regions that have previously been associated with autonomic processes, such as anterior hippocampus and insula. The anatomical distribution of HRV-HG correlations during sleep did not reproduce those usually observed with PET or fMRI during waking. This study aims to characterize the relationship between autonomic tone and neuronal firing rate during sleep and further studies are needed to investigate finer temporal resolutions, denser coverages, and different frequency bands in both waking and sleep.Significance StatementStudies in animals have shown that the autonomic nervous system sets the operating mode of all the organ systems in the body, including the central nervous system. We show here that high gamma activity in widespread cortical and hippocampal regions is correlated with heart rate variability in humans during sleep. The correlation was especially profound in sites which have previously been associated with autonomic and emotional regulation. The direction of change varied between forebrain locations, indicating the existence of sympathetic and parasympathetic modulating structures. The percentage of correlated channels between autonomic tone and cortical activity was greatest in the deepest stages of slow-wave sleep. Overall, this study characterizes in humans a foundational link in the unity of mind and body.
PMID:34732536 | DOI:10.1523/ENEURO.0194-21.2021
