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      Categorical Speech Representation in Human Superior Temporal Gyrus

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          Abstract

          Speech perception requires the rapid and effortless extraction of meaningful phonetic information from a highly variable acoustic signal. A powerful example of this phenomenon is categorical speech perception, in which a continuum of acoustically varying sounds is transformed into perceptually distinct phoneme categories. Here we show that the neural representation of speech sounds is categorically organized in the human posterior superior temporal gyrus. Using intracranial high-density cortical surface arrays, we found that listening to synthesized speech stimuli varying in small and acoustically equal steps evoked distinct and invariant cortical population response patterns that were organized by their sensitivities to critical acoustic features. Phonetic category boundaries were similar between neurometric and psychometric functions. While speech-sound responses were distributed, spatially discrete cortical loci were found to underlie specific phonetic discrimination. Thus, we demonstrate direct evidence for acoustic-to-higher order phonetic level encoding of speech sounds in human language receptive cortex.

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          Most cited references25

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          Dorsal and ventral streams: a framework for understanding aspects of the functional anatomy of language.

          Despite intensive work on language-brain relations, and a fairly impressive accumulation of knowledge over the last several decades, there has been little progress in developing large-scale models of the functional anatomy of language that integrate neuropsychological, neuroimaging, and psycholinguistic data. Drawing on relatively recent developments in the cortical organization of vision, and on data from a variety of sources, we propose a new framework for understanding aspects of the functional anatomy of language which moves towards remedying this situation. The framework posits that early cortical stages of speech perception involve auditory fields in the superior temporal gyrus bilaterally (although asymmetrically). This cortical processing system then diverges into two broad processing streams, a ventral stream, which is involved in mapping sound onto meaning, and a dorsal stream, which is involved in mapping sound onto articulatory-based representations. The ventral stream projects ventro-laterally toward inferior posterior temporal cortex (posterior middle temporal gyrus) which serves as an interface between sound-based representations of speech in the superior temporal gyrus (again bilaterally) and widely distributed conceptual representations. The dorsal stream projects dorso-posteriorly involving a region in the posterior Sylvian fissure at the parietal-temporal boundary (area Spt), and ultimately projecting to frontal regions. This network provides a mechanism for the development and maintenance of "parity" between auditory and motor representations of speech. Although the proposed dorsal stream represents a very tight connection between processes involved in speech perception and speech production, it does not appear to be a critical component of the speech perception process under normal (ecologically natural) listening conditions, that is, when speech input is mapped onto a conceptual representation. We also propose some degree of bi-directionality in both the dorsal and ventral pathways. We discuss some recent empirical tests of this framework that utilize a range of methods. We also show how damage to different components of this framework can account for the major symptom clusters of the fluent aphasias, and discuss some recent evidence concerning how sentence-level processing might be integrated into the framework.
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            Multidimensional scaling, tree-fitting, and clustering.

            American mathematical psychologists have developed computer-based methods for constructing representations of the psychological structure of a set of stimuli on the basis of pairwise measures of similarity or confusability. Applications to perceptual and semantic data illustrate how complementary aspects of the underlying psychological structure are revealed by different types of representations, including multidimensional spatial configurations and nondimensional tree-structures or clusterings.
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              Neural substrates of phonemic perception.

              The temporal lobe in the left hemisphere has long been implicated in the perception of speech sounds. Little is known, however, regarding the specific function of different temporal regions in the analysis of the speech signal. Here we show that an area extending along the left middle and anterior superior temporal sulcus (STS) is more responsive to familiar consonant-vowel syllables during an auditory discrimination task than to comparably complex auditory patterns that cannot be associated with learned phonemic categories. In contrast, areas in the dorsal superior temporal gyrus bilaterally, closer to primary auditory cortex, are activated to the same extent by the phonemic and nonphonemic sounds. Thus, the left middle/anterior STS appears to play a role in phonemic perception. It may represent an intermediate stage of processing in a functional pathway linking areas in the bilateral dorsal superior temporal gyrus, presumably involved in the analysis of physical features of speech and other complex non-speech sounds, to areas in the left anterior STS and middle temporal gyrus that are engaged in higher-level linguistic processes.
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                Author and article information

                Journal
                9809671
                21092
                Nat Neurosci
                Nature neuroscience
                1097-6256
                1546-1726
                26 August 2010
                3 October 2010
                November 2010
                1 May 2011
                : 13
                : 11
                : 1428-1432
                Affiliations
                [1 ]Department of Neurological Surgery, University of California San Francisco
                [2 ]Helen Wills Neuroscience Institute, University of California Berkeley
                [3 ]Department of Psychology, University of California, Berkeley
                [4 ]Department of Neurology, Otto-von-Guericke University, Magdeburg, Germany
                [5 ]Department of Linguistics, University of California Berkeley
                Author notes
                Correspondence to: Edward F. Chang, MD, W.M. Keck Foundation Center for Integrative Neuroscience, Departments of Neurological Surgery and Physiology, University of California, San Francisco, 505 Parnassus Avenue, M779, San Francisco, CA 94143, (Fax) 415 353-3907, (Phone) 415 385-5280, changed@ 123456neurosurg.ucsf.edu , Jochem W. Rieger, PhD, Klinik für Neurology, Otto-von-Guericke Universität, Leipzigerstr. 44, 39120 Magdeburg, Germany, (Fax) +49 39167290224, (Phone) +49 3916117511, jochem.rieger@ 123456med.ovgu.de
                [*]

                these authors contributed equally to this manuscript

                Article
                nihpa231455
                10.1038/nn.2641
                2967728
                20890293
                c8368f21-3415-4c77-a81b-d42501a04707

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                History
                Funding
                Funded by: National Institute of Neurological Disorders and Stroke : NINDS
                Award ID: R00 NS065120-03 ||NS
                Funded by: National Institute of Neurological Disorders and Stroke : NINDS
                Award ID: R00 NS065120-02 ||NS
                Funded by: National Institute of Neurological Disorders and Stroke : NINDS
                Award ID: L30 NS060463-02 ||NS
                Funded by: National Institute of Neurological Disorders and Stroke : NINDS
                Award ID: L30 NS060463-01 ||NS
                Funded by: National Institute of Neurological Disorders and Stroke : NINDS
                Award ID: K99 NS065120-01A1 ||NS
                Funded by: National Institute of Neurological Disorders and Stroke : NINDS
                Award ID: F32 NS061552-01 ||NS
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                Neurosciences
                Neurosciences

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