Cortical functional connectivity indexes arousal state during sleep and anesthesia

Banks, Matthew I.; Krause, Bryan M.; Endemann, Christopher M.; Campbell, Declan; Kovach, Christopher K.; Dyken, Mark Eric; Kawasaki, Hiroto; Nourski, Kirill V.

doi:10.1016/j.neuroimage.2020.116627

Cited by 53 publications

(44 citation statements)

References 90 publications

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“…This is the most comprehensive and controlled study assessing cognitive recovery from the anesthetized state in healthy humans. Although there have been numerous studies of recovery from anesthetic-induced unconsciousness ( Långsjö et al, 2012 ; Purdon et al, 2013 ; Chennu et al, 2016 ; Kim et al, 2018 ; Banks et al, 2020 ; Scheinin et al, 2021 ), our investigation was unique in that the length and depth of general anesthesia was consistent with surgical conditions but the experimental paradigm did not include any surgical intervention. This allowed us to study cognitive reconstitution after a major perturbation of arousal state while also informing the ongoing controversy regarding the effects of general anesthesia on human cognition.…”

Section: Discussionmentioning

confidence: 99%

Recovery of consciousness and cognition after general anesthesia in humans

Mashour

Palanca

Basner

et al. 2021

eLife

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Understanding how the brain recovers from unconsciousness can inform neurobiological theories of consciousness and guide clinical investigation. To address this question, we conducted a multicenter study of 60 healthy humans, half of whom received general anesthesia for three hours and half of whom served as awake controls. We administered a battery of neurocognitive tests and recorded electroencephalography to assess cortical dynamics. We hypothesized that recovery of consciousness and cognition is an extended process, with differential recovery of cognitive functions that would commence with return of responsiveness and end with return of executive function, mediated by prefrontal cortex. We found that, just prior to the recovery of consciousness, frontal-parietal dynamics returned to baseline. Consistent with our hypothesis, cognitive reconstitution after anesthesia evolved over time. Contrary to our hypothesis, executive function returned first. Early engagement of prefrontal cortex in recovery of consciousness and cognition is consistent with global neuronal workspace theory.

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Section: Discussionmentioning

confidence: 99%

Recovery of consciousness and cognition after general anesthesia in humans

Mashour

Palanca

Basner

et al. 2021

eLife

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“…Experiments were conducted in the operating room immediately prior to and during induction of general anesthesia for electrode removal and seizure focus resection surgery. The experiments were part of a series of studies on auditory novelty detection and resting state connectivity across task conditions and arousal states (Nourski et al, 2018a(Nourski et al, ,b, 2021bBanks et al, 2020). Auditory stimuli were quintuples of vowels /A/ and /i/, presented in an LGD paradigm (Bekinschtein et al, 2009;Nourski et al, 2018a; Figure 1).…”

Section: Stimuli and Proceduresmentioning

confidence: 99%

“…The time course of induction of sedation followed by general anesthesia is shown for each subject in Figure 2. In all subjects except R413, the rate of infusion was increased every 10 min by 25 µg/kg/min, following the approach previously used by Nourski et al (2017Nourski et al ( ,2018bNourski et al ( ,2021b and Banks et al (2020). The duration of the infusion was 50 min with a maximum rate of 150 µg/kg/min.…”

Section: Stimuli and Proceduresmentioning

confidence: 99%

“…The transition from OAA/S = 3 ("responsive to loud or repeated command") to OAA/S = 2 ("unresponsive in the absence of mild prodding or shaking") (Chernik et al, 1990) was used as the threshold between sedation and LOC. LOC was thus approximated as the loss of responsiveness (Vanluchene et al, 2004;Nourski et al, 2018b;Banks et al, 2020). The depth of sedation was additionally assessed using EEG parameters: response entropy (RE) (E-ENTROPY module; Datex-Ohmeda, Madison, WI, United States) (Viertiö-Oja et al, 2004) in subject R369 and bispectral index (BIS) (BIS Complete 4-Channel Monitor; Medtronic, Fridley, MN, United States) (Gan et al, 1997) in all other subjects.…”

Section: Stimuli and Proceduresmentioning

confidence: 99%

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Arousal State-Dependence of Interactions Between Short- and Long-Term Auditory Novelty Responses in Human Subjects

Nourski

Steinschneider

Rhone

et al. 2021

Front. Hum. Neurosci.

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In everyday life, predictable sensory stimuli are generally not ecologically informative. By contrast, novel or unexpected stimuli signal ecologically salient changes in the environment. This idea forms the basis of the predictive coding hypothesis: efficient sensory encoding minimizes neural activity associated with predictable backgrounds and emphasizes detection of changes in the environment. In real life, the brain must resolve multiple unexpected sensory events occurring over different time scales. The local/global deviant experimental paradigm examines auditory predictive coding over multiple time scales. For short-term novelty [hundreds of milliseconds; local deviance (LD)], sequences of identical sounds (/xxxxx/) are interspersed with sequences that contain deviants (/xxxxy/). Long-term novelty [several seconds; global deviance (GD)] is created using either (a) frequent /xxxxx/ and infrequent /xxxxy/ sequences, or (b) frequent /xxxxy/ and infrequent /xxxxx/ sequences. In scenario (a), there is both an LD and a GD effect (LDGD, “double surprise”). In (b), the global deviant is a local standard, i.e., sequence of identical sounds (LSGD). Cortical responses reflecting LD and GD originate in different brain areas, have a different time course, and are differentially sensitive to general anesthesia. Neural processes underlying LD and GD have been shown to interact, reflecting overlapping networks subserving the detection of novel auditory stimuli. This study examined these interactions using intracranial electroencephalography in neurosurgical patients. Subjects performed a GD target detection task before and during induction of anesthesia with propofol. Recordings were made from the auditory cortex, surrounding auditory-related and prefrontal cortex in awake, sedated, and unresponsive states. High gamma activity was used to measure the neural basis of local-by-global novelty interactions. Positive interaction was defined as a greater response to the double surprise LDGD condition compared to LSGD. Negative interaction was defined as a weaker response to LDGD. Positive interaction was more frequent than negative interaction and was primarily found in auditory cortex. Negative interaction typically occurred in prefrontal cortex and was more sensitive to general anesthesia. Temporo-parietal auditory-related areas exhibited both types of interaction. These interactions may have relevance in a clinical setting as biomarkers of conscious perception in the assessment of depth of anesthesia and disorders of consciousness.

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“…However, in these clinical studies with surgical patients, it is difficult to dissociate the effects of general anesthesia from the surgical intervention, which can adversely affect cognition through pain, inflammation, and analgesic confounds. In most experimental studies that isolate the effects of general anesthesia alone in healthy volunteers, the anesthetic protocols either just cross the threshold of unresponsiveness (Långsjö et al, 2005 ; Purdon et al, 2013 ; Blain-Moraes et al, 2015 ; Chennu et al, 2016 ; Scheinin et al, 2021 ), or induce a more profound unconsciousness for a short period of time (Banks et al, 2020 ). While these experimental anesthetic protocols may be suitable for modeling light sedation procedures (Allampati et al, 2019 ), they do not model general anesthesia for a major surgery, which animal studies have suggested can immediately and persistently impair cognition in the post-anesthetic period (Valentim et al, 2008 ; Carr et al, 2011 ; Avidan and Evers, 2016 ; Jiang et al, 2017 ).…”

Section: Introductionmentioning

confidence: 99%

Distinct and Dissociable EEG Networks Are Associated With Recovery of Cognitive Function Following Anesthesia-Induced Unconsciousness

Rokos

Mišić

Berkun

et al. 2021

Front. Hum. Neurosci.

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The temporal trajectories and neural mechanisms of recovery of cognitive function after a major perturbation of consciousness is of both clinical and neuroscientific interest. The purpose of the present study was to investigate network-level changes in functional brain connectivity associated with the recovery and return of six cognitive functions after general anesthesia. High-density electroencephalograms (EEG) were recorded from healthy volunteers undergoing a clinically relevant anesthesia protocol (propofol induction and isoflurane maintenance), and age-matched healthy controls. A battery of cognitive tests (motor praxis, visual object learning test, fractal-2-back, abstract matching, psychomotor vigilance test, digital symbol substitution test) was administered at baseline, upon recovery of consciousness (ROC), and at half-hour intervals up to 3 h following ROC. EEG networks were derived using the strength of functional connectivity measured through the weighted phase lag index (wPLI). A partial least squares (PLS) analysis was conducted to assess changes in these networks: (1) between anesthesia and control groups; (2) during the 3-h recovery from anesthesia; and (3) for each cognitive test during recovery from anesthesia. Networks were maximally perturbed upon ROC but returned to baseline 30–60 min following ROC, despite deficits in cognitive performance that persisted up to 3 h following ROC. Additionally, during recovery from anesthesia, cognitive tests conducted at the same time-point activated distinct and dissociable functional connectivity networks across all frequency bands. The results highlight that the return of cognitive function after anesthetic-induced unconsciousness is task-specific, with unique behavioral and brain network trajectories of recovery.

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Cortical functional connectivity indexes arousal state during sleep and anesthesia

Cited by 53 publications

References 90 publications

Recovery of consciousness and cognition after general anesthesia in humans

Recovery of consciousness and cognition after general anesthesia in humans

Arousal State-Dependence of Interactions Between Short- and Long-Term Auditory Novelty Responses in Human Subjects

Distinct and Dissociable EEG Networks Are Associated With Recovery of Cognitive Function Following Anesthesia-Induced Unconsciousness

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