Individual differences in premotor and motor recruitment during speech perception

Although activity in premotor and motor cortices is commonly observed in neuroimaging studies of spoken language processing, the degree to which this activity is an obligatory part of everyday speech comprehension remains unclear. We hypothesised that rather than being a unitary phenomenon, the neural response to speech perception in motor regions would differ across listeners as a function of individual cognitive ability. To examine this possibility, we used functional magnetic resonance imaging (fMRI) to investigate the neural processes supporting speech perception by comparing active listening to pseudowords with matched tasks that involved reading aloud or repetition, all compared to acoustically matched control stimuli and matched baseline tasks. At a whole-brain level there was no evidence for recruitment of regions in premotor or motor cortex during speech perception. A focused region of interest analysis similarly failed to identify significant effects, although a subset of regions approached significance, with notable variability across participants. We then used performance on a battery of behavioural tests that assessed meta-phonological and verbal short-term memory abilities to investigate the reasons for this variability, and found that individual differences in particular in low phonotactic probability pseudoword repetition predicted participants' neural activation within regions in premotor and motor cortices during speech perception. We conclude that normal listeners vary in the degree to which they recruit premotor and motor cortex as a function of short-term memory ability. This is consistent with a resource-allocation approach in which recruitment of the dorsal speech processing pathway depends on both individual abilities and specific task demands.

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

[2]  Karl J. Friston,et al.  Unified segmentation , 2005, NeuroImage.

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

[4]  Régine Kolinsky,et al.  Perception and awareness in phonological processing: the case of the phoneme , 1994, Cognition.

[5]  M. Beckman,et al.  The interaction between vocabulary size and phonotactic probability effects on children's production accuracy and fluency in nonword repetition. , 2004, Journal of speech, language, and hearing research : JSLHR.

[6]  Lori L. Holt,et al.  Reflections on mirror neurons and speech perception , 2009, Trends in Cognitive Sciences.

[7]  J. Ashburner,et al.  Multimodal Image Coregistration and Partitioning—A Unified Framework , 1997, NeuroImage.

[8]  Derek Besner,et al.  Phonology, Lexical Access in Reading, and Articulatory Suppression: A Critical Review , 1987 .

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

[10]  M. D’Esposito Working memory. , 2008, Handbook of clinical neurology.

[11]  N. Cowan The magical number 4 in short-term memory: A reconsideration of mental storage capacity , 2001, Behavioral and Brain Sciences.

[12]  Jennifer M. Rodd,et al.  The functional organisation of the fronto-temporal language system: Evidence from syntactic and semantic ambiguity , 2010, Neuropsychologia.

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

[14]  S. Blumstein,et al.  The Role of Segmentation in Phonological Processing: An fMRI Investigation , 2000, Journal of Cognitive Neuroscience.

[15]  K. Berman,et al.  Human Dorsal and Ventral Auditory Streams Subserve Rehearsal-Based and Echoic Processes during Verbal Working Memory , 2005, Neuron.

[16]  Masa-aki Sato,et al.  Premotor cortex mediates perceptual performance , 2010, NeuroImage.

[17]  Sophie K. Scott,et al.  The functional neuroanatomy of prelexical processing in speech perception , 2004, Cognition.

[18]  M. Masson,et al.  Using confidence intervals in within-subject designs , 1994, Psychonomic bulletin & review.

[19]  A. Baddeley,et al.  The role of phonological memory in vocabulary acquisition: A study of young children learning new names , 1990 .

[20]  D. Poeppel,et al.  Dorsal and ventral streams: a framework for understanding aspects of the functional anatomy of language , 2004, Cognition.

[21]  James S. Hyde,et al.  Strategies for block-design fMRI experiments during task-related motion of structures of the oral cavity , 2006, NeuroImage.

[22]  Steven L. Small,et al.  Repetition Suppression for Spoken Sentences and the Effect of Task Demands , 2006, Journal of Cognitive Neuroscience.

[23]  Matthew H. Davis,et al.  Hearing speech sounds: Top-down influences on the interface between audition and speech perception , 2007, Hearing Research.

[24]  A. Benton,et al.  On Aphasia , 1874, British medical journal.

[25]  Kevin G. Munhall,et al.  Functional Overlap between Regions Involved in Speech Perception and in Monitoring One's Own Voice during Speech Production , 2010, Journal of Cognitive Neuroscience.

[26]  Colin Humphries,et al.  Role of left posterior superior temporal gyrus in phonological processing for speech perception and production , 2001, Cogn. Sci..

[27]  G. Hickok,et al.  Auditory–Motor Interaction Revealed by fMRI: Speech, Music, and Working Memory in Area Spt , 2003 .

[28]  Matthew H. Davis,et al.  The neural mechanisms of speech comprehension: fMRI studies of semantic ambiguity. , 2005, Cerebral cortex.

[29]  M. Vitevitch,et al.  Sublexical and lexical representations in speech production: effects of phonotactic probability and onset density. , 2004, Journal of experimental psychology. Learning, memory, and cognition.

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

[31]  Gregory Hickok,et al.  Eight Problems for the Mirror Neuron Theory of Action Understanding in Monkeys and Humans , 2009, Journal of Cognitive Neuroscience.

[32]  K. Watkins,et al.  Motor Representations of Articulators Contribute to Categorical Perception of Speech Sounds , 2009, The Journal of Neuroscience.

[33]  C. Price The anatomy of language: a review of 100 fMRI studies published in 2009 , 2010, Annals of the New York Academy of Sciences.

[34]  Kayoko Okada,et al.  Bilateral capacity for speech sound processing in auditory comprehension: Evidence from Wada procedures , 2008, Brain and Language.

[35]  A. Baddeley Recent developments in working memory , 1998, Current Opinion in Neurobiology.

[36]  Gordon D. A. Brown Phonological coding in rhyming and homophony judgement. , 1987 .

[37]  Jeremy I. Skipper,et al.  Seeing Voices : How Cortical Areas Supporting Speech Production Mediate Audiovisual Speech Perception , 2007 .

[38]  Karl J. Friston,et al.  Comparing Functional (PET) Images: The Assessment of Significant Change , 1991, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

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

[40]  Kenneth I Forster,et al.  DMDX: A Windows display program with millisecond accuracy , 2003, Behavior research methods, instruments, & computers : a journal of the Psychonomic Society, Inc.

[41]  P. Luce,et al.  Increases in phonotactic probability facilitate spoken nonword repetition. , 2005 .

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

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

[44]  David Poeppel,et al.  Visual speech speeds up the neural processing of auditory speech. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

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

[46]  A. Baddeley,et al.  The phonological loop as a language learning device. , 1998, Psychological review.

[47]  C. Jarrold,et al.  Rehearsal and the development of working memory , 2010 .

[48]  Karl J. Friston,et al.  Spatial registration and normalization of images , 1995 .

[49]  Marc Brysbaert,et al.  Activation of articulatory information in speech perception , 2009, Proceedings of the National Academy of Sciences.

[50]  P. Bertelson,et al.  Literacy training and speech segmentation , 1986, Cognition.

[51]  T Shallice,et al.  The selective impairment of auditory verbal short-term memory. , 1969, Brain : a journal of neurology.

[52]  Volkmar Glauche,et al.  Ventral and dorsal pathways for language , 2008, Proceedings of the National Academy of Sciences.

[53]  Kenneth Hugdahl,et al.  Effective connectivity analysis demonstrates involvement of premotor cortex during speech perception , 2011, NeuroImage.

[54]  J. J. Ryan,et al.  Scoring Reliability on the Wechsler Adult Intelligence Scale-Third Edition (WAIS-III) , 2003, Assessment.

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

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

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

[58]  Karl J. Friston,et al.  Hearing and saying. The functional neuro-anatomy of auditory word processing. , 1996, Brain : a journal of neurology.

[59]  Jean-François Démonet,et al.  Left premotor cortex and allophonic speech perception in dyslexia: A PET study , 2009, NeuroImage.

[60]  C. Frankish,et al.  Phonotactic influences on short-term memory. , 1999, Journal of experimental psychology. Learning, memory, and cognition.

[61]  Cathy J. Price,et al.  Dissociating functional brain networks by decoding the between-subject variability , 2009, NeuroImage.

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

[63]  S. Scott,et al.  Functional Integration across Brain Regions Improves Speech Perception under Adverse Listening Conditions , 2007, The Journal of Neuroscience.

[64]  Joseph T. Devlin,et al.  Speech Perception: Motoric Contributions versus the Motor Theory , 2009, Current Biology.

[65]  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.

[66]  James S. Hyde,et al.  High spatial resolution increases the specificity of block-design BOLD fMRI studies of overt vowel production , 2008, NeuroImage.

[67]  Bradley R. Buchsbaum,et al.  Temporal lobe speech perception systems are part of the verbal working memory circuit: Evidence from two recent fMRI studies , 2003 .

[68]  P. Bertelson,et al.  Does awareness of speech as a sequence of phones arise spontaneously? , 1979, Cognition.

[69]  Gregory Hickok,et al.  The role of mirror neurons in speech perception and action word semantics , 2010 .

[70]  K. Sakai,et al.  Brain activations during conscious self‐monitoring of speech production with delayed auditory feedback: An fMRI study , 2003, Human brain mapping.

[71]  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.

[72]  Derek Besner,et al.  Reading for Meaning: The Effects of Concurrent Articulation* , 1981 .

[73]  John M Deeks,et al.  Simulations of cochlear implant hearing using filtered harmonic complexes: implications for concurrent sound segregation. , 2004, The Journal of the Acoustical Society of America.

[74]  J. Richardson Phonology and reading: The effects of articulatory suppression upon homophony and rhyme judgements , 1987 .

[75]  HighWire Press The journal of neuroscience : the official journal of the Society for Neuroscience. , 1981 .