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Arousal transitions in sleep, wakefulness, and anesthesia are characterized by an orderly sequence of cortical events.

ABSTRACT: Many aspects of brain function are influenced by modulatory processes, including arousal. The most abrupt changes in arousal occur at the wake-sleep transition and at the induction of anesthetic conditions. They are accompanied by major electrophysiological changes, including an emergence of low-frequency (sleep-like) activity and a loss of mid-frequency (wake-like) activity that has been linked to feedback processes of the brain. Nevertheless, the causal relationship between these two types of electrophysiological changes, as well as the cortical mechanisms underlying changes in arousal and consciousness, remain poorly understood. To address this, we studied spontaneous electro-cortical activity during arousal changes in macaques. During sleep and at loss of consciousness induced by propofol anesthesia, we identified a prototypical sequence of cortical events in which the loss of mid-frequency activity preceded, by seconds, the increases in low-frequency activity. Furthermore, in visual areas, an influence of mid-frequency change onto high-frequency activity was observed across visual hierarchy. These results are consistent with the notion that drops in arousal and consciousness are facilitated by a release of feedback cortical inhibition.

SUBMITTER: Liu X

PROVIDER: S-EPMC4468021 | biostudies-literature | 2015 Aug

REPOSITORIES: biostudies-literature

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Arousal transitions in sleep, wakefulness, and anesthesia are characterized by an orderly sequence of cortical events.

Liu Xiao X Yanagawa Toru T Leopold David A DA Chang Catie C Ishida Hiroaki H Fujii Naotaka N Duyn Jeff H JH

NeuroImage 20150410

Many aspects of brain function are influenced by modulatory processes, including arousal. The most abrupt changes in arousal occur at the wake-sleep transition and at the induction of anesthetic conditions. They are accompanied by major electrophysiological changes, including an emergence of low-frequency (sleep-like) activity and a loss of mid-frequency (wake-like) activity that has been linked to feedback processes of the brain. Nevertheless, the causal relationship between these two types of ...[more]

PMID: 25865143

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Project description:Disruption of cortical connectivity likely contributes to loss of consciousness (LOC) during both sleep and general anesthesia, but the degree of overlap in the underlying mechanisms is unclear. Both sleep and anesthesia comprise states of varying levels of arousal and consciousness, including states of largely maintained conscious experience (sleep: N1, REM; anesthesia: sedated but responsive) as well as states of substantially reduced conscious experience (sleep: N2/N3; anesthesia: unresponsive). Here, we tested the hypotheses that (1) cortical connectivity will exhibit clear changes when transitioning into states of reduced consciousness, and (2) these changes will be similar for arousal states of comparable levels of consciousness during sleep and anesthesia. Using intracranial recordings from five adult neurosurgical patients, we compared resting state cortical functional connectivity (as measured by weighted phase lag index, wPLI) in the same subjects across arousal states during natural sleep [wake (WS), N1, N2, N3, REM] and propofol anesthesia [pre-drug wake (WA), sedated/responsive (S), and unresponsive (U)]. Analysis of alpha-band connectivity indicated a transition boundary distinguishing states of maintained and reduced conscious experience in both sleep and anesthesia. In wake states WS and WA, alpha-band wPLI within the temporal lobe was dominant. This pattern was largely unchanged in N1, REM, and S. Transitions into states of reduced consciousness N2, N3, and U were characterized by dramatic changes in connectivity, with dominant connections shifting to prefrontal cortex. Secondary analyses indicated similarities in reorganization of cortical connectivity in sleep and anesthesia. Shifts from temporal to frontal cortical connectivity may reflect impaired sensory processing in states of reduced consciousness. The data indicate that functional connectivity can serve as a biomarker of arousal state and suggest common mechanisms of LOC in sleep and anesthesia.

Project description:RationaleA total of 20-30% of respiratory events in obstructive sleep apnea are terminated without clear arousal. Arousals are thought to predispose to further events by promoting hyperventilation, hypocapnia, and upper-airway dilator muscle hypotonia. Therefore, events terminated without arousal may promote stable breathing.ObjectivesTo compare physiologic changes at respiratory event termination with American Sleep Disorders Association (ASDA) Arousal to No Arousal, and determine whether secondary respiratory events are less common and have higher dilator muscle activity after No Arousal compared with ASDA Arousal.MethodsPatients with obstructive sleep apnea wore sleep staging, genioglossus (EMG(GG)), and tensor palatini (EMG(TP)) electrodes plus a nasal mask and pneumotachograph. During stable sleep, continuous positive airway pressure (CPAP) was lowered for 3-minute periods to induce respiratory events. Physiologic variables were compared between events terminated with (1) ASDA Arousal, (2) No Arousal, or (3) sudden CPAP increase (CPAPinc, control).Measurements and main resultsSixteen subjects had adequate data. EMG(GG), EMG(TP), and heart rate increased after ASDA Arousal (340 ± 57%, 215 ± 28%, and 110.7 ± 2.3%) and No Arousal (185 ± 32%, 167 ± 15%, and 108.5 ± 1.6%) but not CPAPinc (90 ± 10%, 94 ± 11%, and 102.1 ± 1%). Ventilation increased more after ASDA Arousal than No Arousal and CPAPinc, but not after accounting for the severity of respiratory event. Fewer No Arousals were followed by secondary events than ASDA Arousals. However, low dilator muscle activity did not occur after ASDA Arousal or No Arousal (EMG(GG) rose from 75 ± 5 to 125 ± 7%) and secondary events were less severe than initial events (ventilation rose 4 ± 0.4 to 5.5 ± 0.51 L/min).ConclusionsRespiratory events that were terminated with ASDA Arousal were more severely flow-limited, had enhanced hyperventilation after event termination, and were more often followed by secondary events than No arousal. However, secondary events were not associated with low dilator muscle activity and airflow was improved after both No Arousal and ASDA Arousal.

Project description:Although at the organismal level sleep is defined as a behavioral state, at the level of the cerebral cortex sleep has a distinct local and use-dependent aspect. This observation raises the question whether sleep is a functional property of a complex brain or occurs at the level of neuronal assemblies with populations that were active more during wakefulness needing more intense sleep to recover. Here we show that primary cortical cultures have the capacity to change between sleep- and wake-like states that share key signatures with their in vivo counterparts. Cortical cultures initially exhibit random firing activity that is gradually replaced by a M-bM-^@M-^\sleep-likeM-bM-^@M-^] synchronized burst-pause firing activity as neurons mature and make connections. When stimulated with excitatory neurotransmitters, transient tonic firing is observed, followed by the reappearance of a M-bM-^@M-^\sleep-likeM-bM-^@M-^] state. Besides electrophysiological similarities also the transcriptional profile of stimulated cortical cultures greatly resembles that of the cortex of sleep deprived animals. We then used our in vitro model to map the metabolic pathways activated by the M-bM-^@M-^\wake-likeM-bM-^@M-^] state and found evidence for increased lysolipid release, strongly suggesting that sleep plays a role in neuronal membrane homeostasis. With our in vitro model the cellular and molecular consequences of sleep loss and the genetic determinants of disturbed sleep can now be investigated in a dish. Keywords: stress response For the in vivo transcriptome analyses mice were sleep deprived for 6 hours and brain harvested immediately afterwards. For the in vitro analyses, cortical cultures were stimulated with a neurotransmitter cocktail and cells harvested 3 hours afterwards. Control mice were kept undisturbed in their home cage and control cultures were sham stimulated with water. Also, another set of sleep deprived mice as well as stimulated cultures were allowed to recover before being sampled the next day at the time of day at which sleep deprivation or stimulation started the day before).

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Arousal transitions in sleep, wakefulness, and anesthesia are characterized by an orderly sequence of cortical events.

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Arousal transitions in sleep, wakefulness, and anesthesia are characterized by an orderly sequence of cortical events.

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