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      Is the Sensorimotor Cortex Relevant for Speech Perception and Understanding? An Integrative Review

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          Abstract

          In the neuroscience of language, phonemes are frequently described as multimodal units whose neuronal representations are distributed across perisylvian cortical regions, including auditory and sensorimotor areas. A different position views phonemes primarily as acoustic entities with posterior temporal localization, which are functionally independent from frontoparietal articulatory programs. To address this current controversy, we here discuss experimental results from functional magnetic resonance imaging (fMRI) as well as transcranial magnetic stimulation (TMS) studies. On first glance, a mixed picture emerges, with earlier research documenting neurofunctional distinctions between phonemes in both temporal and frontoparietal sensorimotor systems, but some recent work seemingly failing to replicate the latter. Detailed analysis of methodological differences between studies reveals that the way experiments are set up explains whether sensorimotor cortex maps phonological information during speech perception or not. In particular, acoustic noise during the experiment and ‘motor noise’ caused by button press tasks work against the frontoparietal manifestation of phonemes. We highlight recent studies using sparse imaging and passive speech perception tasks along with multivariate pattern analysis (MVPA) and especially representational similarity analysis (RSA), which succeeded in separating acoustic-phonological from general-acoustic processes and in mapping specific phonological information on temporal and frontoparietal regions. The question about a causal role of sensorimotor cortex on speech perception and understanding is addressed by reviewing recent TMS studies. We conclude that frontoparietal cortices, including ventral motor and somatosensory areas, reflect phonological information during speech perception and exert a causal influence on language understanding.

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          Most cited references96

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          Distributed and overlapping representations of faces and objects in ventral temporal cortex.

          The functional architecture of the object vision pathway in the human brain was investigated using functional magnetic resonance imaging to measure patterns of response in ventral temporal cortex while subjects viewed faces, cats, five categories of man-made objects, and nonsense pictures. A distinct pattern of response was found for each stimulus category. The distinctiveness of the response to a given category was not due simply to the regions that responded maximally to that category, because the category being viewed also could be identified on the basis of the pattern of response when those regions were excluded from the analysis. Patterns of response that discriminated among all categories were found even within cortical regions that responded maximally to only one category. These results indicate that the representations of faces and objects in ventral temporal cortex are widely distributed and overlapping.
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            Meta-analyzing left hemisphere language areas: phonology, semantics, and sentence processing.

            The advent of functional neuroimaging has allowed tremendous advances in our understanding of brain-language relationships, in addition to generating substantial empirical data on this subject in the form of thousands of activation peak coordinates reported in a decade of language studies. We performed a large-scale meta-analysis of this literature, aimed at defining the composition of the phonological, semantic, and sentence processing networks in the frontal, temporal, and inferior parietal regions of the left cerebral hemisphere. For each of these language components, activation peaks issued from relevant component-specific contrasts were submitted to a spatial clustering algorithm, which gathered activation peaks on the basis of their relative distance in the MNI space. From a sample of 730 activation peaks extracted from 129 scientific reports selected among 260, we isolated 30 activation clusters, defining the functional fields constituting three distributed networks of frontal and temporal areas and revealing the functional organization of the left hemisphere for language. The functional role of each activation cluster is discussed based on the nature of the tasks in which it was involved. This meta-analysis sheds light on several contemporary issues, notably on the fine-scale functional architecture of the inferior frontal gyrus for phonological and semantic processing, the evidence for an elementary audio-motor loop involved in both comprehension and production of syllables including the primary auditory areas and the motor mouth area, evidence of areas of overlap between phonological and semantic processing, in particular at the location of the selective human voice area that was the seat of partial overlap of the three language components, the evidence of a cortical area in the pars opercularis of the inferior frontal gyrus dedicated to syntactic processing and in the posterior part of the superior temporal gyrus a region selectively activated by sentence and text processing, and the hypothesis that different working memory perception-actions loops are identifiable for the different language components. These results argue for large-scale architecture networks rather than modular organization of language in the left hemisphere.
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              Active perception: sensorimotor circuits as a cortical basis for language.

              Action and perception are functionally linked in the brain, but a hotly debated question is whether perception and comprehension of stimuli depend on motor circuits. Brain language mechanisms are ideal for addressing this question. Neuroimaging investigations have found specific motor activations when subjects understand speech sounds, word meanings and sentence structures. Moreover, studies involving transcranial magnetic stimulation and patients with lesions affecting inferior frontal regions of the brain have shown contributions of motor circuits to the comprehension of phonemes, semantic categories and grammar. These data show that language comprehension benefits from frontocentral action systems, indicating that action and perception circuits are interdependent.
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                Author and article information

                Contributors
                Journal
                Front Hum Neurosci
                Front Hum Neurosci
                Front. Hum. Neurosci.
                Frontiers in Human Neuroscience
                Frontiers Media S.A.
                1662-5161
                21 September 2016
                2016
                : 10
                : 435
                Affiliations
                [1] 1Brain Language Laboratory, Department of Philosophy and Humanities, Freie Universität Berlin Berlin, Germany
                [2] 2Berlin School of Mind and Brain, Humboldt-Universität zu Berlin Berlin, Germany
                Author notes

                Edited by: Nathalie Tzourio-Mazoyer, CNRS, CEA and Bordeaux University, France

                Reviewed by: Roel M. Willems, Radboud University Nijmegen, Netherlands; Monica Baciu, Université Pierre Mendès-France, France

                *Correspondence: Malte R. Schomers m.schomers@ 123456fu-berlin.de Friedemann Pulvermüller friedemann.pulvermuller@ 123456fu-berlin.de
                Article
                10.3389/fnhum.2016.00435
                5030253
                27708566
                4f33ef50-0563-4d10-b3ce-9745cfe36c57
                Copyright © 2016 Schomers and Pulvermüller.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution and reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 26 May 2016
                : 15 August 2016
                Page count
                Figures: 4, Tables: 1, Equations: 0, References: 134, Pages: 18, Words: 13055
                Funding
                Funded by: Deutsche Forschungsgemeinschaft 10.13039/501100001659
                Award ID: Pu 97/16-1
                Funded by: Freie Universität Berlin 10.13039/501100007537
                Categories
                Neuroscience
                Review

                Neurosciences
                speech perception,sensorimotor integration of speech,motor cortex,somatosensory cortex,articulatory features,multivariate pattern analysis (mvpa),transcranial magnetic stimulation (tms),embodied cognition

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