Dataset Information

FMRI investigation of unexpected somatosensory feedback perturbation during speech.

ABSTRACT: Somatosensory feedback plays a critical role in the coordination of articulator movements for speech production. In response to unexpected resistance to lip or jaw movements during speech, fluent speakers can use the difference between the somatosensory expectations of a speech sound and the actual somatosensory feedback to adjust the trajectories of functionally relevant but unimpeded articulators. In an effort to investigate the neural substrates underlying the somatosensory feedback control of speech, we used an event-related sparse sampling functional magnetic resonance imaging paradigm and a novel pneumatic device that unpredictably blocked subjects' jaw movements. In comparison to speech, perturbed speech, in which jaw perturbation prompted the generation of compensatory speech motor commands, demonstrated increased effects in bilateral ventral motor cortex, right-lateralized anterior supramarginal gyrus, inferior frontal gyrus pars triangularis and ventral premotor cortex, and bilateral inferior posterior cerebellum (lobule VIII). Structural equation modeling revealed a significant increased influence from left anterior supramarginal gyrus to right anterior supramarginal gyrus and from left anterior supramarginal gyrus to right ventral premotor cortex as well as a significant increased reciprocal influence between right ventral premotor cortex and right ventral motor cortex and right anterior supramarginal gyrus and right inferior frontal gyrus pars triangularis for perturbed speech relative to speech. These results suggest that bilateral anterior supramarginal gyrus, right inferior frontal gyrus pars triangularis, right ventral premotor and motor cortices are functionally coupled and influence speech motor output when somatosensory feedback is unexpectedly perturbed during speech production.

SUBMITTER: Golfinopoulos E

PROVIDER: S-EPMC3065208 | biostudies-literature | 2011 Apr

REPOSITORIES: biostudies-literature

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fMRI investigation of unexpected somatosensory feedback perturbation during speech.

Golfinopoulos Elisa E Tourville Jason A JA Bohland Jason W JW Ghosh Satrajit S SS Nieto-Castanon Alfonso A Guenther Frank H FH

NeuroImage 20101230 3

Somatosensory feedback plays a critical role in the coordination of articulator movements for speech production. In response to unexpected resistance to lip or jaw movements during speech, fluent speakers can use the difference between the somatosensory expectations of a speech sound and the actual somatosensory feedback to adjust the trajectories of functionally relevant but unimpeded articulators. In an effort to investigate the neural substrates underlying the somatosensory feedback control o ...[more]

PMID: 21195191

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Project description:Successful perception depends on combining sensory input with prior knowledge. However, the underlying mechanism by which these two sources of information are combined is unknown. In speech perception, as in other domains, two functionally distinct coding schemes have been proposed for how expectations influence representation of sensory evidence. Traditional models suggest that expected features of the speech input are enhanced or sharpened via interactive activation (Sharpened Signals). Conversely, Predictive Coding suggests that expected features are suppressed so that unexpected features of the speech input (Prediction Errors) are processed further. The present work is aimed at distinguishing between these two accounts of how prior knowledge influences speech perception. By combining behavioural, univariate, and multivariate fMRI measures of how sensory detail and prior expectations influence speech perception with computational modelling, we provide evidence in favour of Prediction Error computations. Increased sensory detail and informative expectations have additive behavioural and univariate neural effects because they both improve the accuracy of word report and reduce the BOLD signal in lateral temporal lobe regions. However, sensory detail and informative expectations have interacting effects on speech representations shown by multivariate fMRI in the posterior superior temporal sulcus. When prior knowledge was absent, increased sensory detail enhanced the amount of speech information measured in superior temporal multivoxel patterns, but with informative expectations, increased sensory detail reduced the amount of measured information. Computational simulations of Sharpened Signals and Prediction Errors during speech perception could both explain these behavioural and univariate fMRI observations. However, the multivariate fMRI observations were uniquely simulated by a Prediction Error and not a Sharpened Signal model. The interaction between prior expectation and sensory detail provides evidence for a Predictive Coding account of speech perception. Our work establishes methods that can be used to distinguish representations of Prediction Error and Sharpened Signals in other perceptual domains.

Project description:Real-time functional magnetic resonance imaging (fMRI) is a promising non-invasive method for brain-computer interfaces (BCIs). BCIs translate brain activity into signals that allow communication with the outside world. Visual and motor imagery are often used as information-encoding strategies, but can be challenging if not grounded in recent experience in these modalities, e.g., in patients with locked-in-syndrome (LIS). In contrast, somatosensory imagery might constitute a more suitable information-encoding strategy as the somatosensory function is often very robust. Somatosensory imagery has been shown to activate the somatotopic cortex, but it has been unclear so far whether it can be reliably detected on a single-trial level and successfully classified according to specific somatosensory imagery content. Using ultra-high field 7-T fMRI, we show reliable and high-accuracy single-trial decoding of left-foot (LF) vs. right-hand (RH) somatosensory imagery. Correspondingly, higher decoding accuracies were associated with greater spatial separation of hand and foot decoding-weight patterns in the primary somatosensory cortex (S1). Exploiting these novel neuroscientific insights, we developed-and provide a proof of concept for-basic BCI communication by showing that binary (yes/no) answers encoded by somatosensory imagery can be decoded with high accuracy in simulated real-time (in 7 subjects) as well as in real-time (1 subject). This study demonstrates that body part-specific somatosensory imagery differentially activates somatosensory cortex in a topographically specific manner; evidence which was surprisingly still lacking in the literature. It also offers proof of concept for a novel somatosensory imagery-based fMRI-BCI control strategy, with particularly high potential for visually and motor-impaired patients. The strategy could also be transferred to lower MRI field strengths and to mobile functional near-infrared spectroscopy. Finally, given that communication BCIs provide the BCI user with a form of feedback based on their brain signals and can thus be considered as a specific form of neurofeedback, and that repeated use of a BCI has been shown to enhance underlying representations, we expect that the current BCI could also offer an interesting new approach for somatosensory rehabilitation training in the context of stroke and phantom limb pain.

Dataset Information

FMRI investigation of unexpected somatosensory feedback perturbation during speech.

Publications

fMRI investigation of unexpected somatosensory feedback perturbation during speech.

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