Dissociating speech perception and comprehension at reduced levels of awareness

Medical Research Council Cognition and Brain Sciences Unit, 15 Chaucer Road, Cambridge CB2 7EF, United Kingdom.
Proceedings of the National Academy of Sciences (Impact Factor: 9.67). 11/2007; 104(41):16032-7. DOI: 10.1073/pnas.0701309104
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ABSTRACT We used functional MRI and the anesthetic agent propofol to assess the relationship among neural responses to speech, successful comprehension, and conscious awareness. Volunteers were scanned while listening to sentences containing ambiguous words, matched sentences without ambiguous words, and signal-correlated noise (SCN). During three scanning sessions, participants were nonsedated (awake), lightly sedated (a slowed response to conversation), and deeply sedated (no conversational response, rousable by loud command). Bilateral temporal-lobe responses for sentences compared with signal-correlated noise were observed at all three levels of sedation, although prefrontal and premotor responses to speech were absent at the deepest level of sedation. Additional inferior frontal and posterior temporal responses to ambiguous sentences provide a neural correlate of semantic processes critical for comprehending sentences containing ambiguous words. However, this additional response was absent during light sedation, suggesting a marked impairment of sentence comprehension. A significant decline in postscan recognition memory for sentences also suggests that sedation impaired encoding of sentences into memory, with left inferior frontal and temporal lobe responses during light sedation predicting subsequent recognition memory. These findings suggest a graded degradation of cognitive function in response to sedation such that "higher-level" semantic and mnemonic processes can be impaired at relatively low levels of sedation, whereas perceptual processing of speech remains resilient even during deep sedation. These results have important implications for understanding the relationship between speech comprehension and awareness in the healthy brain in patients receiving sedation and in patients with disorders of consciousness.

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Available from: Matthew H Davis, Sep 27, 2015
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    • "work ( FPN ) , dorsal attention network ( DAN ) , and language network ( LAN ) were left not investi - gated . Given that drug - induced sedation / anesthesia signifi - cantly impairs executive control , attention , explicit memory / working memory , and semantic processing / language [ Adapa et al . , 2014 ; Buffett - Jerrott and Stewart , 2002 ; Davis et al . , 2007 ; Fisher et al . , 2006 ; Millar et al , 2007 ] , as well as the correspon - dence between these cognitive functions with higher - order RSNs , we hypothesize that in contrast to placebo , midazolam may significantly reduce the network integrity of higher - order brain networks , including DMN , ECN , SN as well as bilateral FPN , DAN ,"
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    ABSTRACT: This work examines the effect of midazolam-induced light sedation on intrinsic functional connectivity of human brain, using a randomized, double-blind, placebo-controlled, cross-over, within-subject design. Fourteen healthy young subjects were enrolled and midazolam (0.03 mg/kg of the participant's body mass, to a maximum of 2.5 mg) or saline were administrated with an interval of one week. Resting-state fMRI was conducted before and after administration for each subject. We focus on two types of networks: sensory related lower-level functional networks and higher-order functions related ones. Independent component analysis (ICA) was used to identify these resting-state functional networks. We hypothesize that the sensory (visual, auditory, and sensorimotor) related networks will be intact under midazolam-induced light sedation while the higher-order (default mode, executive control, salience networks, etc.) networks will be functionally disconnected. It was found that the functional integrity of the lower-level networks was maintained, while that of the higher-level networks was significantly disrupted by light sedation. The within-network connectivity of the two types of networks was differently affected in terms of direction and extent. These findings provide direct evidence that higher-order cognitive functions including memory, attention, executive function, and language were impaired prior to lower-level sensory responses during sedation. Our result also lends support to the information integration model of consciousness. Hum Brain Mapp, 2015. © 2015 Wiley Periodicals, Inc. © 2015 Wiley Periodicals, Inc.
    Human Brain Mapping 08/2015; DOI:10.1002/hbm.22914 · 5.97 Impact Factor
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    • "Schiff and colleagues revealed activations of widely distributed cortical systems in some MCS patients in response to meaningful language compared to meaningless time-reversed stimuli (Schiff et al., 2005). Davis et al. designed a hierarchy of contrasts probing different stages of semantic processing, including the perception of ambiguous words within a contextual sentence (Davis et al., 2007). During propofol sedation, superior temporal areas were still responding to sentences versus noise. "
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    ABSTRACT: Our ability to identify covert cognitive abilities in non-communicating patients is of prime importance to improve diagnosis, to guide therapeutic decisions and to better predict their cognitive outcome. In the present study, we used a basic and rigorous paradigm contrasting pairs of words orthogonally. This paradigm enables the probing of semantic processing by comparing neural activity elicited by similar words delivered in various combinations. We describe the respective timing, topography and estimated cortical sources of two successive event-related potentials (ERP) components (N400 and late positive component (LPC)) using high-density EEG in conscious controls (N=20) and in minimally conscious (MCS; N=15) and vegetative states (VS; N=15) patients recorded at bedside. Whereas N400-like ERP components could be observed in the VS, MCS and conscious groups, only MCS and conscious groups showed a LPC response, suggesting that this late effect could be a potential specific marker of conscious semantic processing. This result is coherent with recent findings disentangling early and local non-conscious responses (e.g.: MMN in odd-ball paradigms, N400 in semantic violation paradigms) from late, distributed and conscious responses (e.g.: P3b to auditory rule violation) in controls and in patients with disorders of consciousness. However, N400 and LPC responses were not easily observed at the individual level, – even in conscious controls – , with standard ERP analyses, which is a limiting factor for its clinical use. Of potential interest, the only 3 patients presenting both significant N400 and LPC effects were MCS, and 2 of them regained consciousness and functional language abilities.
    Neuropsychologia 01/2015; 66:279–292. DOI:10.1016/j.neuropsychologia.2014.10.014 · 3.30 Impact Factor
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    • "For example, the authors Heinke et al. (2004) reported dose-dependent effects of propofol on temporo-frontal regions involved in auditory language processing using passive fMRI in healthy volunteers, albeit these effects were most marked in frontal rather than temporal regions. Moreover, an fMRI study of controls by Davis et al. (2007) found that despite impairment of semantic and mnemonic processes at low levels of propofol sedation, perceptual processing of speech at even high levels of sedation is preserved, as characterized by engagement of temporal lobe regions previously implicated in receptive language processing. "
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    ABSTRACT: Non-invasive assessment of hemispheric dominance for receptive language using magnetoencephalography (MEG) is now a well-established procedure used across several epilepsy centers in the context of pre-surgical evaluation of children and adults while awake, alert and attentive. However, the utility of MEG for the same purpose, in cases of sedated patients, is contested. Establishment of the efficiency of MEG is especially important in the case of children who, for a number of reasons, must be assessed under sedation. Here we explored the efficacy of MEG language mapping under sedation through retrospective review of 95 consecutive pediatric patients, who underwent our receptive language test as part of routine clinical evaluation. Localization of receptive language cortex and subsequent determination of laterality was successfully completed in 78% (n = 36) and 55% (n = 27) of non-sedated and sedated patients, respectively. Moreover, the proportion of patients deemed left hemisphere dominant for receptive language did not differ between non-sedated and sedated patients, exceeding 90% in both groups. Considering the challenges associated with assessing brain function in pediatric patients, the success of passive MEG in the context of the cases reviewed in this study support the utility of this method in pre-surgical receptive language mapping.
    Frontiers in Human Neuroscience 08/2014; 8:657. DOI:10.3389/fnhum.2014.00657 · 2.99 Impact Factor
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