Preferential Inhibition of Frontal-to-Parietal Feedback Connectivity Is a Neurophysiologic Correlate of General Anesthesia in Surgical Patients

Ku, Seung Woo; Lee, UnCheol; Noh, Gyu Jeong; Jun, In Gu; Mashour, George A.

doi:10.1371/journal.pone.0025155

Cited by 196 publications

(198 citation statements)

References 42 publications

(46 reference statements)

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“…1). 13,14,18,19,21 The results of these studies are in line with earlier electrophysiological work in animals 22 and humans, 23 which demonstrated a loss of neural synchronization, under general anesthesia, between anterior and posterior parts of the brain. The work of John et al 23 is particularly noteworthy in this regard because they analyzed electroencephalography data from a total of 176 surgical patients anesthetized with a wide variety of pharmacological agents (induction of anesthesia with propofol, thiopental, or etomidate; maintenance of anesthesia with propofol, isoflurane, desflurane, or sevoflurane).…”

Section: " H Ow Do General Anesthetics Work?" In 2005supporting

confidence: 87%

“…1). 13,14,18,19,21 The results of these studies are in line with earlier electrophysiological work in animals 22 …”

supporting

confidence: 88%

“…Several recent studies-carried out in both humans and animals, and using a variety of different anesthetic agents-have investigated differences in directional corticocortical connectivity between the awake state and anesthesia-induced unconsciousness. [12][13][14][15][16][17][18][19][20][21] Intriguingly, the vast majority of these studies [12][13][14]16,[18][19][20][21] (two exceptions 15,17 shall be discussed later in this section) indicate that connectivity along the sensory pathways, under general anesthesia, is reduced primarily in the top-down direction. In other words, unconsciousness, which is the anesthetic endpoint this article is exclusively concerned with, appears to be correlated with reduced signaling from higher-order association cortices to early sensory cortices (table 1 and fig.…”

Section: " H Ow Do General Anesthetics Work?" In 2005mentioning

confidence: 99%

“…1B). 13,14,18,19,21 Recall that this asymmetry disappears when consciousness is lost due to a selective anesthetic suppression of top-down information flow. Thus, in terms of hierarchical predictive coding, anesthesia-induced unconsciousness would be caused by a breakdown of the top-down predictive process.…”

Section: Prediction As the Central Element Of Conscious Perceptionmentioning

confidence: 99%

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The Role of Dendritic Signaling in the Anesthetic Suppression of Consciousness

Meyer

2015

Anesthesiology

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Despite considerable progress in the identification of the molecular targets of general anesthetics, it remains unclear how these drugs affect the brain at the systems level to suppress consciousness. According to recent proposals, anesthetics may achieve this feat by interfering with corticocortical topdown processes, that is, by interrupting information flow from association to early sensory cortices. Such a view entails two immediate questions. First, at which anatomical site, and by virtue of which physiological mechanism, do anesthetics interfere with top-down signals? Second, why does a breakdown of top-down signaling cause unconsciousness? While an answer to the first question can be gleaned from emerging neurophysiological evidence on dendritic signaling in cortical pyramidal neurons, a response to the second is offered by increasingly popular theoretical frameworks that place the element of prediction at the heart of conscious perception. Science magazine posed this question in a special section titled "What don't we know?," dedicated to the greatest challenges of contemporary science. 1 "Scientists are chipping away at the drugs' effects on individual neurons," the article reads, "but understanding how they render us unconscious will be a tougher nut to crack." This prediction proved correct: a decade later, we have expanded considerably our knowledge of the molecular targets of general anesthetics, but it remains enigmatic how these drugs affect the brain at the systems level. Why does the potentiation of γ-aminobutyric acid (GABA) receptors caused by propofol or desflurane cause unconsciousness? How are the brain's computational processes affected by this and other molecular mechanisms of anesthetics, so that patients undergoing surgery cease to experience their surrounds in terms of sight, sound, and touch? Anesthesiologists and cognitive neuroscientists alike have been captivated by these questions and have proposed a number of models in an attempt to answer them, such as Flohr's "information processing theory of anesthesia," 2 Alkire's "thalamic consciousness switch hypothesis," 3-6 Mashour's "cognitive unbinding paradigm," 7,8 John and Prichep's "anesthetic cascade," 9 or Hudetz's "forgotten present." 10,11 We shall return to some of these frameworks in a later section of the article.One recent development is particularly intriguing. Given that the most striking feature of general anesthesia is an interruption of the patient's ability to perceive the environment, it would appear intuitive for anesthetics to interfere primarily with bottom-up information flow along the sensory pathways, that is, with the signals that carry perceptual information from the thalamus to the primary sensory cortices and on to unimodal and multimodal association cortices. However, the very opposite appears to be the case. Several recent studies-carried out in both humans and animals, and using a variety of different anesthetic agents-have investigated differences in directional corticocortical connectivity bet...

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Section: " H Ow Do General Anesthetics Work?" In 2005supporting

confidence: 87%

“…1). 13,14,18,19,21 The results of these studies are in line with earlier electrophysiological work in animals 22 …”

supporting

confidence: 88%

Section: " H Ow Do General Anesthetics Work?" In 2005mentioning

confidence: 99%

Section: Prediction As the Central Element Of Conscious Perceptionmentioning

confidence: 99%

See 2 more Smart Citations

The Role of Dendritic Signaling in the Anesthetic Suppression of Consciousness

Meyer

2015

Anesthesiology

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“…One such process is access of sensory information to consciousness (Dehaene and Changeux, 2011) as implied by the disrupted fronto-parietal connectivity during anesthesia-induced loss of consciousness (Ferrarelli et al, 2010;Ku et al, 2011), early (80-130 ms) synchronization correlates of conscious detection (Melloni et al, 2007;Wyart et al, 2012), and currently found correlations with BIT scores in patients. However, the targetrelated decrease of beta synchronization in control participants contradicts this explanation.…”

Section: Fronto-parietal Beta Synchronization During Visual Processingmentioning

confidence: 99%

Synchronization of fronto-parietal beta and theta networks as a signature of visual awareness in neglect

et al. 2017

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The version presented here may differ from the published version or from the version of record. If you wish to cite this item you are advised to consult the publisher's version. Please see the repository url above for details on accessing the published version and note that access may require a subscription. In the neglect syndrome, the perceptual deficit for contra-lesional hemi-space is increasingly viewed as a dysfunction of fronto-parietal cortical networks, the disruption of which has been described in neuroanatomical and hemodynamic studies. Here we exploit the superior temporal resolution of electroencephalography (EEG) to study dynamic transient connectivity of fronto-parietal circuits at early stages of visual perception in neglect. As reflected by interregional phase synchronization in a full-field attention task, two functionally distinct frontoparietal networks, in beta (15-25 Hz) and theta (4-8 Hz) frequency bands, were related to stimulus discrimination within the first 200 ms of visual processing. Neglect pathology was specifically associated with significant suppressions of both beta and theta networks engaging right parietal regions. These connectivity abnormalities occurred in a pattern that was distinctly different from what was observed in right-hemisphere lesion patients without neglect. Also, both beta and theta abnormalities contributed additively to visual awareness decrease, quantified in the Behavioural Inattention Test. These results provide evidence for the impairment of fast dynamic fronto-parietal interactions during early stages of visual processing in neglect pathology. Also, they reveal that different modes of fronto-parietal dysfunction contribute independently to deficits in visual awareness at the behavioural level.

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No cognitive processing in the unconscious, anesthetic‐like, state of sleep

Vertes

Linley

2020

J of Comparative Neurology

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We review evidence challenging the hypothesis that memories are processed or consolidated in sleep. We argue that the brain is in an unconscious state in sleep, akin to general anesthesia (GA), and hence is incapable of meaningful cognitive processingthe sole purview of waking consciousness. At minimum, the encoding of memories in sleep would require that waking events are faithfully transferred to and reproduced in sleep. Remarkably, however, this has never been demonstrated, as waking experiences are never truly replicated in sleep but rather appear in very altered or distorted forms. General anesthetics (GAs) exert their effects through endogenous sleep-wake control systems and accordingly GA and sleep share several common features: sensory blockade, immobility, amnesia and lack of awareness (unconsciousness). The loss of consciousness in non-REM (NREM) sleep or to GAs is characterized by: (a) delta oscillations throughout the cortex; (b) marked reductions in neural activity (from waking) over widespread regions of the cortex, most pronounced in frontal and parietal cortices; and (c) a significant disruption of the functional connectivity of thalamocortical and corticocortical networks, particularly those involved in "higher order" cognitive functions. Several (experimental) reports in animals and humans have shown that disrupting the activity of the cortex, particularly the orbitofrontal cortex, severely impairs higher order cognitive and executive functions. The profound and widespread deactivation of the cortex in the unconscious states of NREM sleep or GA would be expected to produce an equivalent, or undoubtedly a much greater, disruptive effect on mnemonic and cognitive functions. In conclusion, we contend that the unconscious, severely altered state of the brain in NREM sleep would negate any possibility of cognitive processing in NREM sleep.

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Preferential Inhibition of Frontal-to-Parietal Feedback Connectivity Is a Neurophysiologic Correlate of General Anesthesia in Surgical Patients

Cited by 196 publications

References 42 publications

The Role of Dendritic Signaling in the Anesthetic Suppression of Consciousness

The Role of Dendritic Signaling in the Anesthetic Suppression of Consciousness

Synchronization of fronto-parietal beta and theta networks as a signature of visual awareness in neglect

No cognitive processing in the unconscious, anesthetic‐like, state of sleep

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