Discriminating between Auditory and Motor Cortical Responses to Speech and Nonspeech Mouth Sounds

Several perspectives on speech perception posit a central role for the representation of articulations in speech comprehension, supported by evidence for premotor activation when participants listen to speech. However, no experiments have directly tested whether motor responses mirror the profile of selective auditory cortical responses to native speech sounds or whether motor and auditory areas respond in different ways to sounds. We used fMRI to investigate cortical responses to speech and nonspeech mouth (ingressive click) sounds. Speech sounds activated bilateral superior temporal gyri more than other sounds, a profile not seen in motor and premotor cortices. These results suggest that there are qualitative differences in the ways that temporal and motor areas are activated by speech and click sounds: Anterior temporal lobe areas are sensitive to the acoustic or phonetic properties, whereas motor responses may show more generalized responses to the acoustic stimuli.

[1]  E. Jung,et al.  Improving the spatial accuracy in functional magnetic resonance imaging (fMRI) based on the blood oxygenation level dependent (BOLD) effect: benefits from parallel imaging and a 32-channel head array coil at 1.5 Tesla. , 2009, Clinical hemorheology and microcirculation.

[2]  Friedemann Pulvermüller,et al.  Motor cortex maps articulatory features of speech sounds , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[3]  P T Parikh,et al.  Evaluation of Image Quality of a 32-Channel versus a 12-Channel Head Coil at 1.5T for MR Imaging of the Brain , 2011, American Journal of Neuroradiology.

[4]  Sophie K. Scott,et al.  A little more conversation, a little less action — candidate roles for the motor cortex in speech perception , 2009, Nature Reviews Neuroscience.

[5]  Sophie K. Scott,et al.  Neural Correlates of Sublexical Processing in Phonological Working Memory , 2011, Journal of Cognitive Neuroscience.

[6]  Jesper Andersson,et al.  Valid conjunction inference with the minimum statistic , 2005, NeuroImage.

[7]  David A. Medler,et al.  Cerebral Cortex doi:10.1093/cercor/bhi040 Cerebral Cortex Advance Access published February 9, 2005 , 2022 .

[8]  Cathy J. Price,et al.  A review and synthesis of the first 20 years of PET and fMRI studies of heard speech, spoken language and reading , 2012, NeuroImage.

[9]  S K Scott,et al.  Are articulatory commands automatically and involuntarily activated during speech perception? , 2010, Proceedings of the National Academy of Sciences.

[10]  G. Rizzolatti,et al.  Speech listening specifically modulates the excitability of tongue muscles: a TMS study , 2002, The European journal of neuroscience.

[11]  Catherine T. Best,et al.  Left-Hemisphere Advantage for Click Consonants is Determined by Linguistic Significance and Experience , 1999 .

[12]  J Bamford,et al.  The BKB (Bamford-Kowal-Bench) sentence lists for partially-hearing children. , 1979, British journal of audiology.

[13]  H. Pashler,et al.  Puzzlingly High Correlations in fMRI Studies of Emotion, Personality, and Social Cognition 1 , 2009, Perspectives on psychological science : a journal of the Association for Psychological Science.

[14]  J Ashburner,et al.  Functional neuroimaging of speech perception in six normal and two aphasic subjects. , 1999, The Journal of the Acoustical Society of America.

[15]  M. Iacoboni,et al.  Listening to speech activates motor areas involved in speech production , 2004, Nature Neuroscience.

[16]  C. Heyes Where do mirror neurons come from? , 2010, Neuroscience & Biobehavioral Reviews.

[17]  D. LeBihan,et al.  Phonological Grammar Shapes the Auditory Cortex: A Functional Magnetic Resonance Imaging Study , 2003, The Journal of Neuroscience.

[18]  D. Poeppel,et al.  Towards a functional neuroanatomy of speech perception , 2000, Trends in Cognitive Sciences.

[19]  S. Scott,et al.  The neuroanatomical and functional organization of speech perception , 2003, Trends in Neurosciences.

[20]  Vincent L. Gracco,et al.  A mediating role of the premotor cortex in phoneme segmentation , 2009, Brain and Language.

[21]  Matthew H. Davis,et al.  Hierarchical Processing in Spoken Language Comprehension , 2003, The Journal of Neuroscience.

[22]  P. Denes On the Motor Theory of Speech Perception , 1965 .

[23]  P. Matthews,et al.  Defining a left-lateralized response specific to intelligible speech using fMRI. , 2003, Cerebral cortex.

[24]  David J. Ostry,et al.  Auditory plasticity and speech motor learning , 2009, Proceedings of the National Academy of Sciences.

[25]  S. Scott,et al.  Identification of a pathway for intelligible speech in the left temporal lobe. , 2000, Brain : a journal of neurology.

[26]  Marco Iacoboni,et al.  Neural responses to non-native phonemes varying in producibility: Evidence for the sensorimotor nature of speech perception , 2006, NeuroImage.

[27]  R. Wise,et al.  Sounds do-able: auditory–motor transformations and the posterior temporal plane , 2005, Trends in Neurosciences.

[28]  R J Wise,et al.  Separate neural subsystems within 'Wernicke's area'. , 2001, Brain : a journal of neurology.

[29]  D. Poeppel,et al.  The cortical organization of speech processing , 2007, Nature Reviews Neuroscience.

[30]  J. Thiran,et al.  Distinct Pathways Involved in Sound Recognition and Localization: A Human fMRI Study , 2000, NeuroImage.

[31]  M. Turvey,et al.  The motor theory of speech perception reviewed , 2006, Psychonomic bulletin & review.

[32]  Maneesh C. Patel,et al.  Perceptual Systems Controlling Speech Production , 2008, The Journal of Neuroscience.

[33]  Marco Iacoboni,et al.  The Essential Role of Premotor Cortex in Speech Perception , 2007, Current Biology.

[34]  Tony Ro,et al.  Neural Substrates of Sound–Touch Synesthesia after a Thalamic Lesion , 2008, The Journal of Neuroscience.

[35]  A. Liberman,et al.  The motor theory of speech perception revised , 1985, Cognition.

[36]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[37]  G. Rizzolatti,et al.  The mirror-neuron system. , 2004, Annual review of neuroscience.

[38]  T. Paus,et al.  Seeing and hearing speech excites the motor system involved in speech production , 2003, Neuropsychologia.

[39]  L. Fadiga,et al.  The Motor Somatotopy of Speech Perception , 2009, Current Biology.

[40]  R. Zatorre,et al.  Voice-selective areas in human auditory cortex , 2000, Nature.

[41]  G. Rizzolatti,et al.  Neurophysiological mechanisms underlying the understanding and imitation of action , 2001, Nature Reviews Neuroscience.

[42]  R. Zatorre,et al.  Adaptation to speaker's voice in right anterior temporal lobe , 2003, Neuroreport.

[43]  John F. Houde There's more to speech perception than meets the ear , 2009, Proceedings of the National Academy of Sciences.

[44]  Paul Boersma,et al.  Praat, a system for doing phonetics by computer , 2002 .

[45]  Sophie K. Scott,et al.  Cortical asymmetries in speech perception: what's wrong, what's right and what's left? , 2012, Trends in Cognitive Sciences.

[46]  Kayoko Okada,et al.  Area Spt in the Human Planum Temporale Supports Sensory-motor Integration for Speech Processing Establishing the Existence of Distinct Sen- Sory versus Motor Activation Patterns Would Establish That , 2022 .

[47]  Paul Boersma,et al.  Praat: doing phonetics by computer , 2003 .

[48]  E. T. Possing,et al.  Human temporal lobe activation by speech and nonspeech sounds. , 2000, Cerebral cortex.

[49]  Jonas Obleser,et al.  Magnetic Brain Response Mirrors Extraction of Phonological Features from Spoken Vowels , 2004, Journal of Cognitive Neuroscience.

[50]  Jean-Luc Anton,et al.  Region of interest analysis using an SPM toolbox , 2010 .

[51]  C. Best,et al.  Examination of perceptual reorganization for nonnative speech contrasts: Zulu click discrimination by English-speaking adults and infants. , 1988, Journal of experimental psychology. Human perception and performance.

[52]  G. Rizzolatti,et al.  Action recognition in the premotor cortex. , 1996, Brain : a journal of neurology.

[53]  Stuart Rosen,et al.  Neural correlates of intelligibility in speech investigated with noise vocoded speech--a positron emission tomography study. , 2006, The Journal of the Acoustical Society of America.

[54]  R J Wise,et al.  Cerebral areas associated with motor control of speech in humans. , 1997, Journal of applied physiology.

[55]  W. K. Simmons,et al.  Circular analysis in systems neuroscience: the dangers of double dipping , 2009, Nature Neuroscience.

[56]  M. Schroeder Reference Signal for Signal Quality Studies , 1968 .