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: 9.81). 11/2007; 104(41):16032-7. DOI: 10.1073/pnas.0701309104
Source: PubMed

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, Aug 27, 2015
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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 · 3.45 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 · 2.90 Impact Factor
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    • "In the temporal lobe, statistically robust activation for the semantically ambiguous sentences was located in the left posterior inferior temporal cortex (pIT), specifically in the occipitotemporal sulcus and inferior temporal gyrus. This is in a similar location to that found by Rodd et al. (2012) and Bekinschtein et al. (2011), but is more inferior than other studies where activation centers around pMTG/ITG (Rodd et al., 2005; Davis et al., 2007; Zempleni et al., 2007). "
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    ABSTRACT: Semantic ambiguity resolution is an essential and frequent part of speech comprehension because many words map onto multiple meanings (e.g., "bark," "bank"). Neuroimaging research highlights the importance of the left inferior frontal gyrus (LIFG) and the left posterior temporal cortex in this process but the roles they serve in ambiguity resolution are uncertain. One possibility is that both regions are engaged in the processes of semantic reinterpretation that follows incorrect interpretation of an ambiguous word. Here we used fMRI to investigate this hypothesis. 20 native British English monolinguals were scanned whilst listening to sentences that contained an ambiguous word. To induce semantic reinterpretation, the disambiguating information was presented after the ambiguous word and delayed until the end of the sentence (e.g., "the teacher explained that the BARK was going to be very damp"). These sentences were compared to well-matched unambiguous sentences. Supporting the reinterpretation hypothesis, these ambiguous sentences produced more activation in both the LIFG and the left posterior inferior temporal cortex. Importantly, all but one subject showed ambiguity-related peaks within both regions, demonstrating that the group-level results were driven by high inter-subject consistency. Further support came from the finding that activation in both regions was modulated by meaning dominance. Specifically, sentences containing biased ambiguous words, which have one more dominant meaning, produced greater activation than those with balanced ambiguous words, which have two equally frequent meanings. Because the context always supported the less frequent meaning, the biased words require reinterpretation more often than balanced words. This is the first evidence of dominance effects in the spoken modality and provides strong support that frontal and temporal regions support the updating of semantic representations during speech comprehension.
    Frontiers in Human Neuroscience 07/2014; 8:530. DOI:10.3389/fnhum.2014.00530 · 2.90 Impact Factor
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