Individual differences in premotor and motor recruitment during speech perception

Medical Research Council, Cognition and Brain Sciences Unit, 15 Chaucer Road, Cambridge CB2 7EF, England, UK.
Neuropsychologia (Impact Factor: 3.3). 04/2012; 50(7):1380-92. DOI: 10.1016/j.neuropsychologia.2012.02.023
Source: PubMed


Although activity in premotor and motor cortices is commonly observed in neuroimaging studies of spoken language processing, the degree to which this activity is an obligatory part of everyday speech comprehension remains unclear. We hypothesised that rather than being a unitary phenomenon, the neural response to speech perception in motor regions would differ across listeners as a function of individual cognitive ability. To examine this possibility, we used functional magnetic resonance imaging (fMRI) to investigate the neural processes supporting speech perception by comparing active listening to pseudowords with matched tasks that involved reading aloud or repetition, all compared to acoustically matched control stimuli and matched baseline tasks. At a whole-brain level there was no evidence for recruitment of regions in premotor or motor cortex during speech perception. A focused region of interest analysis similarly failed to identify significant effects, although a subset of regions approached significance, with notable variability across participants. We then used performance on a battery of behavioural tests that assessed meta-phonological and verbal short-term memory abilities to investigate the reasons for this variability, and found that individual differences in particular in low phonotactic probability pseudoword repetition predicted participants' neural activation within regions in premotor and motor cortices during speech perception. We conclude that normal listeners vary in the degree to which they recruit premotor and motor cortex as a function of short-term memory ability. This is consistent with a resource-allocation approach in which recruitment of the dorsal speech processing pathway depends on both individual abilities and specific task demands.

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Available from: Matthew H Davis, Jan 14, 2014
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    • "Increased temporal precision also may enhance understanding of the functional role of dorsal stream activity observed during speech perception. While dorsal stream activity is not typically observed during ''passive'' listening tasks (Scott et al., 2009; Szenkovits et al., 2012; Bowers et al., 2013), it has been reported in a variety of more challenging ''active'' perception tasks, such as discrimination of foreign phonemes (Callan et al., 2006), segmentation (Burton et al., 2000; LoCasto et al., 2004), and discrimination of speech in noise (Bowers et al., 2013, 2014). These mixed findings leave unanswered questions regarding the extent to which auditoryto-motor mapping functionally supports accurate perception vs. being merely a by-product of increased processing. "
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    ABSTRACT: Sensorimotor integration (SMI) across the dorsal stream enables online monitoring of speech. Jenson et al. (2014) used independent component analysis (ICA) and event related spectral perturbation (ERSP) analysis of electroencephalography (EEG) data to describe anterior sensorimotor (e.g., premotor cortex, PMC) activity during speech perception and production. The purpose of the current study was to identify and temporally map neural activity from posterior (i.e., auditory) regions of the dorsal stream in the same tasks. Perception tasks required "active" discrimination of syllable pairs (/ba/ and /da/) in quiet and noisy conditions. Production conditions required overt production of syllable pairs and nouns. ICA performed on concatenated raw 68 channel EEG data from all tasks identified bilateral "auditory" alpha (α) components in 15 of 29 participants localized to pSTG (left) and pMTG (right). ERSP analyses were performed to reveal fluctuations in the spectral power of the α rhythm clusters across time. Production conditions were characterized by significant α event related synchronization (ERS; pFDR < 0.05) concurrent with EMG activity from speech production, consistent with speech-induced auditory inhibition. Discrimination conditions were also characterized by α ERS following stimulus offset. Auditory α ERS in all conditions temporally aligned with PMC activity reported in Jenson et al. (2014). These findings are indicative of speech-induced suppression of auditory regions, possibly via efference copy. The presence of the same pattern following stimulus offset in discrimination conditions suggests that sensorimotor contributions following speech perception reflect covert replay, and that covert replay provides one source of the motor activity previously observed in some speech perception tasks. To our knowledge, this is the first time that inhibition of auditory regions by speech has been observed in real-time with the ICA/ERSP technique.
    Full-text · Article · Oct 2015 · Frontiers in Human Neuroscience
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    • "These conditions typically have been those in which task demands are increased and include categorical discrimination of foreign phonemes (Callan et al., 2006), phoneme segmentation (Burton et al., 2000; Locasto et al., 2004; Burton and Small, 2006), and speech in noise (Osnes et al., 2011; Alho et al., 2012; D'Ausilio et al., 2012). Thus, motor system activity in speech perception may be context dependent, in addition to being variable across individuals (Szenkovits et al., 2012). Given equivocal findings, the role of the motor system in speech perception is hotly debated. "
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    ABSTRACT: Activity in anterior sensorimotor regions is found in speech production and some perception tasks. Yet, how sensorimotor integration supports these functions is unclear due to a lack of data examining the timing of activity from these regions. Beta (~20 Hz) and alpha (~10 Hz) spectral power within the EEG μ rhythm are considered indices of motor and somatosensory activity, respectively. In the current study, perception conditions required discrimination (same/different) of syllables pairs (/ba/ and /da/) in quiet and noisy conditions. Production conditions required covert and overt syllable productions and overt word production. Independent component analysis was performed on EEG data obtained during these conditions to (1) identify clusters of μ components common to all conditions and (2) examine real-time event-related spectral perturbations (ERSP) within alpha and beta bands. 17 and 15 out of 20 participants produced left and right μ-components, respectively, localized to precentral gyri. Discrimination conditions were characterized by significant (pFDR < 0.05) early alpha event-related synchronization (ERS) prior to and during stimulus presentation and later alpha event-related desynchronization (ERD) following stimulus offset. Beta ERD began early and gained strength across time. Differences were found between quiet and noisy discrimination conditions. Both overt syllable and word productions yielded similar alpha/beta ERD that began prior to production and was strongest during muscle activity. Findings during covert production were weaker than during overt production. One explanation for these findings is that μ-beta ERD indexes early predictive coding (e.g., internal modeling) and/or overt and covert attentional/motor processes. μ-alpha ERS may index inhibitory input to the premotor cortex from sensory regions prior to and during discrimination, while μ-alpha ERD may index sensory feedback during speech rehearsal and production.
    Full-text · Article · Jul 2014 · Frontiers in Psychology
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    • "The left inferior frontal region is commonly reported in language processing including premotor speech, subvocalization, learning new words and encoding during speech production(e.g. Veroude et al., 2010; Szenkovits et al., 2012), suggesting that old adults tested in the afternoon, and to a lesser extent old adults tested in the morning were attending far more to the language component of the task than young adults. More activity in this region suggests that old adults, particularly when tested in the afternoon, tend to preferentially attend to highly salient word or word-like stimuli. "
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    ABSTRACT: Behavioral evidence suggests that the attention-based ability to regulate distraction varies across the day in synchrony with a circadian arousal rhythm that changes across the life span. Using functional magnetic resonance imaging (fMRI), we assessed whether neural activity in an attention control network also varies across the day and with behavioral markers. We tested older adults in the morning or afternoon and younger adults tested in the afternoon using a 1-back task with superimposed distractors, followed by an implicit test for the distractors. Behavioral results replicated earlier findings with older adults tested in the morning better able to ignore distraction than those tested in the afternoon. Imaging results showed that time of testing modulates task-related fMRI signals in older adults and that age differences were reduced when older adults are tested at peak times of day. In particular, older adults tested in the morning activated similar cognitive control regions to those activated by young adults (rostral prefrontal and superior parietal cortex), whereas older adults tested in the afternoon were reliably different; furthermore, the degree to which participants were able to activate the control regions listed above correlated with the ability to suppress distracting information. (PsycINFO Database Record (c) 2014 APA, all rights reserved).
    Full-text · Article · Jul 2014 · Psychology and Aging
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