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Sensory–motor transformations for speech occur bilaterally

Abstract

Historically, the study of speech processing has emphasized a strong link between auditory perceptual input and motor production output1,2,3,4. A kind of ‘parity’ is essential, as both perception- and production-based representations must form a unified interface to facilitate access to higher-order language processes such as syntax and semantics, believed to be computed in the dominant, typically left hemisphere5,6. Although various theories have been proposed to unite perception and production2,7, the underlying neural mechanisms are unclear. Early models of speech and language processing proposed that perceptual processing occurred in the left posterior superior temporal gyrus (Wernicke’s area) and motor production processes occurred in the left inferior frontal gyrus (Broca’s area)8,9. Sensory activity was proposed to link to production activity through connecting fibre tracts, forming the left lateralized speech sensory–motor system10. Although recent evidence indicates that speech perception occurs bilaterally11,12,13, prevailing models maintain that the speech sensory–motor system is left lateralized11,14,15,16,17,18 and facilitates the transformation from sensory-based auditory representations to motor-based production representations11,15,16. However, evidence for the lateralized computation of sensory–motor speech transformations is indirect and primarily comes from stroke patients that have speech repetition deficits (conduction aphasia) and studies using covert speech and haemodynamic functional imaging16,19. Whether the speech sensory–motor system is lateralized, like higher-order language processes, or bilateral, like speech perception, is controversial. Here we use direct neural recordings in subjects performing sensory–motor tasks involving overt speech production to show that sensory–motor transformations occur bilaterally. We demonstrate that electrodes over bilateral inferior frontal, inferior parietal, superior temporal, premotor and somatosensory cortices exhibit robust sensory–motor neural responses during both perception and production in an overt word-repetition task. Using a non-word transformation task, we show that bilateral sensory–motor responses can perform transformations between speech-perception- and speech-production-based representations. These results establish a bilateral sublexical speech sensory–motor system.

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Figure 1: Behavioural tasks and example neural activations.
Figure 2: Topography of neural responses and bilateral activation.
Figure 3: Neural decoding of words.
Figure 4: Listen–speak transformation task.

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Acknowledgements

We would like to thank A. Weiss, J. MacArthur and L. Frank for developing the data acquisition hardware and software; O. Felsovalyi, E. Londen, P. Purushothaman, L. Melloni, C. Boomhaur and A. Trongnetrpunya for technical assistance; and D. Poeppel and C. Brody for comments on the manuscript. This work was supported, in part, by R03-DC010475 from the NIDCD, a Career Award in the Biomedical Sciences from the Burroughs Wellcome Fund (B.P.), a Watson Investigator Program Award from NYSTAR (B.P.), a McKnight Scholar Award (B.P.) and a Sloan Research Fellowship (B.P.).

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G.B.C. designed the experiment, performed the research, analysed the data and wrote the manuscript. T.T. and O.D. performed the research and wrote the manuscript. C.C. and W.D. performed the research. B.P. designed the experiment, performed the research, analysed the data and wrote the manuscript.

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Correspondence to Bijan Pesaran.

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The authors declare no competing financial interests.

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This file contains a Supplementary Discussion, Supplementary Tables 1-2, Supplementary Figures 1-11 and additional references. (PDF 2214 kb)

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Cogan, G., Thesen, T., Carlson, C. et al. Sensory–motor transformations for speech occur bilaterally. Nature 507, 94–98 (2014). https://doi.org/10.1038/nature12935

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