Abstract
Speaking is one of the most complex actions that we perform, but nearly all of us learn to do it effortlessly. Production of fluent speech requires the precise, coordinated movement of multiple articulators (for example, the lips, jaw, tongue and larynx) over rapid time scales. Here we used high-resolution, multi-electrode cortical recordings during the production of consonant-vowel syllables to determine the organization of speech sensorimotor cortex in humans. We found speech-articulator representations that are arranged somatotopically on ventral pre- and post-central gyri, and that partially overlap at individual electrodes. These representations were coordinated temporally as sequences during syllable production. Spatial patterns of cortical activity showed an emergent, population-level representation, which was organized by phonetic features. Over tens of milliseconds, the spatial patterns transitioned between distinct representations for different consonants and vowels. These results reveal the dynamic organization of speech sensorimotor cortex during the generation of multi-articulator movements that underlies our ability to speak.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Levelt, W. J. M. Speaking: From Intention to Articulation (MIT Press, 1993)
Ladefoged, P. & Johnson, K. A Course in Phonetics (Wadsworth Publishing, 2010)
Browman, C. P. & Goldstein, L. Articulatory gestures as phonological units. Haskins Laboratories Status Report on Speech Research 99, 69–101 (1989)
Fowler, C. A., Rubin, P. E., Remez, R. E. & Turvey, M. T. in Language Production: Speech and Talk Vol. 1 (ed. Butterworth, B. ) 373–420 (Academic Press, 1980)
Gracco, V. L. & Lofqvist, A. Speech motor coordination and control: evidence from lip, jaw, and laryngeal movements. J. Neurosci. 14, 6585–6597 (1994)
Schöner, G. & Kelso, J. A. Dynamic pattern generation in behavioral and neural systems. Science 239, 1513–1520 (1988)
Franklin, D. W. & Wolpert, D. M. Computational mechanisms of sensorimotor control. Neuron 72, 425–442 (2011)
Brown, S. et al. The somatotopy of speech: phonation and articulation in the human motor cortex. Brain Cogn. 70, 31–41 (2009)
Guenther, F. H., Ghosh, S. S. & Tourville, J. A. Neural modeling and imaging of the cortical interactions underlying syllable production. Brain Lang. 96, 280–301 (2006)
Schulz, G. M., Varga, M., Jeffires, K., Ludlow, C. L. & Braun, A. R. Functional neuroanatomy of human vocalization: an H215O PET study. Cereb. Cortex 15, 1835–1847 (2005)
Jürgens, U. Neural pathways underlying vocal control. Neurosci. Biobehav. Rev. 26, 235–258 (2002)
Kuypers, H. G. Corticobular connexions to the pons and lower brain-stem in man: an anatomical study. Brain 81, 364–388 (1958)
Brodmann, K. Vergleichende Lokalisationslehre der Grosshirnrinde in ihren Prinzipien dargestellt auf Grund des Zellenbaues (Smith-Gordon, 1994)
Penfield, W. & Boldrey, E. Somatic motor and sensory representation in the cerebral cortex of man studied by electrical stimulation. Brain 60, 389–443 (1937)
Foerster, O. The cerebral cortex in man. Lancet 221, 309–312 (1931)
Penfield, W. & Roberts, R. Speech and Brain: Mechanisms. (Princeton, 1959)
Saltzman, E. & Munhall, K. A dynamical approach to gestural patterning in speech production. Ecol. Psychol. 1, 333–382 (1989)
Clements, G. N. & Hume, E. in The Handbook of Phonological Theory (ed. Goldsmith, J. A. ) 245–306 (Basil Blackwell, 1995)
Chomsky, N. & Halle, M. The Sound Pattern of English (MIT Press, 1991)
Mesgarani, N. & Chang, E. F. Selective cortical representation of attended speaker in multi-talker speech perception. Nature 485, 233–236 (2012)
Crone, N. E., Miglioretti, D. L., Gordon, B. & Lesser, R. P. Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. II. Event-related synchronization in the gamma band. Brain 121, 2301–2315 (1998)
Edwards, E. et al. Spatiotemporal imaging of cortical activation during verb generation and picture naming. Neuroimage 50, 291–301 (2010)
Ray, S. & Maunsell, J. H. Different origins of gamma rhythm and high-gamma activity in macaque visual cortex. PLoS Biol. 9, e1000610 (2011)
Kent, R. D. in The Production of Speech (ed. MacNeilage, P. F. ) (Springer-Verlag, 1983)
McCarthy, G., Allison, T. & Spencer, D. D. Localization of the face area of human sensorimotor cortex by intracranial recording of somatosensory evoked potentials. J. Neurosurg. 79, 874–884 (1993)
Afshar, A. et al. Single-trial neural correlates of arm movement preparation. Neuron 71, 555–564 (2011)
Mazor, O. & Laurent, G. Transient dynamics versus fixed points in odor representations by locust antennal lobe projection neurons. Neuron 48, 661–673 (2005)
Sussillo, D. & Abbott, L. F. Generating coherent patterns of activity from chaotic neural networks. Neuron 63, 544–557 (2009)
Ahrens, M. B. et al. Brain-wide neuronal dynamics during motor adaptation in zebrafish. Nature 485, 471–477 (2012)
Churchland, M. M., Cunningham, J. P., Kaufman, M. T., Ryu, S. I. & Shenoy, K. V. Cortical preparatory activity: representation of movement or first cog in a dynamical machine? Neuron 68, 387–400 (2010)
McCarthy, J. J. Feature geometry and dependency: a review. Phonetica 45, 84–108 (1988)
Briggman, K. L. & Kristan, W. B. Multifunctional pattern-generating circuits. Annu. Rev. Neurosci. 31, 271–294 (2008)
Churchland, M. M. et al. Neural population dynamics during reaching. Nature 487, 51–56 (2012)
Brown, S., Ngan, E. & Liotti, M. A larynx area in the human motor cortex. Cereb. Cortex 18, 837–845 (2008)
Terumitsu, M., Fujii, Y., Suzuki, K., Kwee, I. L. & Nakada, T. Human primary motor cortex shows hemispheric specialization for speech. Neuroreport 17, 1091–1095 (2006)
Hast, M. H., Fischer, J. M., Wetzel, A. B. & Thompson, V. E. Cortical motor representation of the laryngeal muscles in Macaca mulatta. Brain Res. 73, 229–240 (1974)
Jürgens, U. On the elicitability of vocalization from the cortical larynx area. Brain Res. 81, 564–566 (1974)
Pruszynski, J. A. et al. Primary motor cortex underlies multi-joint integration for fast feedback control. Nature 478, 387–390 (2011)
Hatsopoulos, N. G. & Suminski, A. J. Sensing with the motor cortex. Neuron 72, 477–487 (2011)
Tremblay, S., Shiller, D. M. & Ostry, D. J. Somatosensory basis of speech production. Nature 423, 866–869 (2003)
Matyas, F. et al. Motor control by sensory cortex. Science 330, 1240–1243 (2010)
Rathelot, J. A. & Strick, P. L. Muscle representation in the macaque motor cortex: an anatomical perspective. Proc. Natl Acad. Sci. USA 103, 8257–8262 (2006)
Gracco, V. L. & Abbs, J. H. Dynamic control of the perioral system during speech: kinematic analyses of autogenic and nonautogenic sensorimotor processes. J. Neurophysiol. 54, 418–432 (1985)
Sherrington, C. S. The Integrative Action of the Nervous System (Yale University Press, 1911)
Jakobson, R., Fant, G. & Halle, M. Preliminaries to speech analysis: the distinctive features and their correlates (MIT Press, 1969)
Keating, P. A. The Window Model of Coarticulation: Articulatory Evidence (Cambridge Univ. Press, 1990)
Dell, G. S., Juliano, C. & Govindjee, A. Structure and content in language production: a theory of frame constraints in phonological speech errors. Cogn. Sci. 17, 149–195 (1993)
Mesgarani, N. & Chang, E. F. Selective cortical representation of attended speaker in multi-talker speech perception. Nature 485, 233–236 (2012)
Yang, X. et al. Auditory representations of acoustic signals. IEEE Transactions Inf. Theor. 38, 824–839 (1992)
International Phonetic Association Handbook of the International Phonetic Association (Cambridge Univ. Press, 1999)
Rousseeuw, P. Silhouettes: a graphical aid to the interpretation and validation of cluster analysis. J. Comput. Appl. Math. 20, 53–65 (1987)
Acknowledgements
We thank A. Ren for technical help with data collection and pre-processing, and M. Babiak for audio transcription. J. Houde, C. Niziolek, S. Lisberger, K. Chaisanguanthum, C. Cheung and I. Garner provided helpful comments on the manuscript. E.F.C. was funded by the US National Institutes of Health grants R00-NS065120, DP2-OD00862 and R01-DC012379, and the Ester A. and Joseph Klingenstein Foundation.
Author information
Authors and Affiliations
Contributions
E.F.C. conceived and collected the data for this project. K.E.B. designed and implemented the analysis with assistance from E.F.C. N.M. assisted with preliminary analysis. K.E.B. and E.F.C. wrote the manuscript. K.J. provided phonetic consultation on experimental design and interpretation of results. E.F.C. supervised the project.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Supplementary information
Supplementary Information
This file contains Supplementary Figures 1-13, Supplementary Table 1 and Supplementary Methods. (PDF 5017 kb)
Rights and permissions
About this article
Cite this article
Bouchard, K., Mesgarani, N., Johnson, K. et al. Functional organization of human sensorimotor cortex for speech articulation. Nature 495, 327–332 (2013). https://doi.org/10.1038/nature11911
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/nature11911
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.