Infants’ brain responses to speech suggest Analysis by Synthesis

Significance Infants discriminate speech sounds universally until 8 mo of age, then native discrimination improves and nonnative discrimination declines. Using magnetoencephalography, we investigate the contribution of auditory and motor brain systems to this developmental transition. We show that 7-mo-old infants activate auditory and motor brain areas similarly for native and nonnative sounds; by 11–12 mo, greater activation in auditory brain areas occurs for native sounds, whereas greater activation in motor brain areas occurs for nonnative sounds, matching the adult pattern. We posit that hearing speech invokes an Analysis by Synthesis process: auditory analysis of speech is coupled with synthesis that predicts the motor plans necessary to produce it. Both brain systems contribute to the developmental transition in infant speech perception. Historic theories of speech perception (Motor Theory and Analysis by Synthesis) invoked listeners’ knowledge of speech production to explain speech perception. Neuroimaging data show that adult listeners activate motor brain areas during speech perception. In two experiments using magnetoencephalography (MEG), we investigated motor brain activation, as well as auditory brain activation, during discrimination of native and nonnative syllables in infants at two ages that straddle the developmental transition from language-universal to language-specific speech perception. Adults are also tested in Exp. 1. MEG data revealed that 7-mo-old infants activate auditory (superior temporal) as well as motor brain areas (Broca’s area, cerebellum) in response to speech, and equivalently for native and nonnative syllables. However, in 11- and 12-mo-old infants, native speech activates auditory brain areas to a greater degree than nonnative, whereas nonnative speech activates motor brain areas to a greater degree than native speech. This double dissociation in 11- to 12-mo-old infants matches the pattern of results obtained in adult listeners. Our infant data are consistent with Analysis by Synthesis: auditory analysis of speech is coupled with synthesis of the motor plans necessary to produce the speech signal. The findings have implications for: (i) perception-action theories of speech perception, (ii) the impact of “motherese” on early language learning, and (iii) the “social-gating” hypothesis and humans’ development of social understanding.

[1]  K. Stevens,et al.  Linguistic experience alters phonetic perception in infants by 6 months of age. , 1992, Science.

[2]  Toshiaki Imada,et al.  Age-Specific Average Head Template for Typically Developing 6-Month-Old Infants , 2013, PloS one.

[3]  Martin Luessi,et al.  MNE software for processing MEG and EEG data , 2014, NeuroImage.

[4]  L. Fadiga,et al.  Active perception: sensorimotor circuits as a cortical basis for language , 2010, Nature Reviews Neuroscience.

[5]  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.

[6]  H. Helmholtz Handbuch der physiologischen Optik , 2015 .

[7]  R D Pascual-Marqui,et al.  Standardized low-resolution brain electromagnetic tomography (sLORETA): technical details. , 2002, Methods and findings in experimental and clinical pharmacology.

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

[9]  S. Taulu,et al.  Suppression of Interference and Artifacts by the Signal Space Separation Method , 2003, Brain Topography.

[10]  Bart de Boer,et al.  Investigating the role of infant-directed speech with a computer model , 2003 .

[11]  M. Arbib,et al.  Language within our grasp , 1998, Trends in Neurosciences.

[12]  P. Kuhl Early language acquisition: cracking the speech code , 2004, Nature Reviews Neuroscience.

[13]  Patricia K. Kuhl,et al.  Brain Responses to Words in 2-Year-Olds with Autism Predict Developmental Outcomes at Age 6 , 2013, PloS one.

[14]  J. Houk,et al.  The Role of the Basal Ganglia and Cerebellum in Language Processing , 2006 .

[15]  R. Ilmoniemi,et al.  Magnetoencephalography-theory, instrumentation, and applications to noninvasive studies of the working human brain , 1993 .

[16]  R. Ilmoniemi,et al.  Responses of the primary auditory cortex to pitch changes in a sequence of tone pips: Neuromagnetic recordings in man , 1984, Neuroscience Letters.

[17]  W J Levelt,et al.  Spoken word production: A theory of lexical access , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[18]  Shinobu Masaki,et al.  Learning-induced neural plasticity associated with improved identification performance after training of a difficult second-language phonetic contrast , 2003, NeuroImage.

[19]  C. Fowler Compensation for coarticulation reflects gesture perception, not spectral contrast , 2006, Perception & psychophysics.

[20]  P. Kuhl,et al.  Cross-language analysis of phonetic units in language addressed to infants. , 1997, Science.

[21]  A. Yuille,et al.  Opinion TRENDS in Cognitive Sciences Vol.10 No.7 July 2006 Special Issue: Probabilistic models of cognition Vision as Bayesian inference: analysis by synthesis? , 2022 .

[22]  I. Sigel,et al.  HANDBOOK OF CHILD PSYCHOLOGY , 2006 .

[23]  Patricia K Kuhl,et al.  Look who's talking: speech style and social context in language input to infants are linked to concurrent and future speech development. , 2014, Developmental science.

[24]  P. Kuhl Is speech learning 'gated' by the social brain? , 2007, Developmental science.

[25]  R. Oostenveld,et al.  Nonparametric statistical testing of EEG- and MEG-data , 2007, Journal of Neuroscience Methods.

[26]  P. Kuhl,et al.  Impact of second-language experience in infancy: brain measures of first- and second-language speech perception. , 2011, Developmental science.

[27]  D. Yarnitsky,et al.  Neurophysiology of the cortical pain network: revisiting the role of S1 in subjective pain perception via standardized low-resolution brain electromagnetic tomography (sLORETA). , 2008, Journal of Pain.

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

[29]  J. Rauschecker,et al.  Maps and streams in the auditory cortex: nonhuman primates illuminate human speech processing , 2009, Nature Neuroscience.

[30]  J. Decety,et al.  The Oxford handbook of social neuroscience , 2011 .

[31]  P. Kuhl,et al.  Infant speech perception activates Broca's area: a developmental magnetoencephalography study , 2006, Neuroreport.

[32]  P. Kuhl,et al.  Enhanced discriminability at the phonetic boundaries for the place feature in macaques. , 1983, The Journal of the Acoustical Society of America.

[33]  Nancy Kanwisher,et al.  Functional specificity for high-level linguistic processing in the human brain , 2011, Proceedings of the National Academy of Sciences.

[34]  Terrence J Sejnowski,et al.  Foundations for a New Science of Learning , 2009, Science.

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

[36]  M. Sigman,et al.  Functional organization of perisylvian activation during presentation of sentences in preverbal infants , 2006, Proceedings of the National Academy of Sciences.

[37]  Marco Iacoboni,et al.  The role of premotor cortex in speech perception: Evidence from fMRI and rTMS , 2008, Journal of Physiology-Paris.

[38]  P. Kuhl,et al.  Foreign-language experience in infancy: Effects of short-term exposure and social interaction on phonetic learning , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[39]  A. Liberman,et al.  Parametrically Dissociating Speech and Nonspeech Perception in the Brain Using fMRI , 2001, Brain and Language.

[40]  Robert J Zatorre,et al.  Learning new sounds of speech: reallocation of neural substrates , 2004, NeuroImage.

[41]  Anders M. Dale,et al.  Automatic parcellation of human cortical gyri and sulci using standard anatomical nomenclature , 2010, NeuroImage.

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

[43]  P. Kuhl,et al.  Infants show a facilitation effect for native language phonetic perception between 6 and 12 months. , 2006, Developmental science.

[44]  Andrew N Meltzoff,et al.  Neural mirroring mechanisms and imitation in human infants , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[45]  A. Meltzoff,et al.  Infant vocalizations in response to speech: vocal imitation and developmental change. , 1996, The Journal of the Acoustical Society of America.

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

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

[48]  P. Kuhl,et al.  Brain potentials to native and non-native speech contrasts in 7- and 11-month-old American infants. , 2005, Developmental science.

[49]  J. D. Miller,et al.  Speech perception by the chinchilla: voiced-voiceless distinction in alveolar plosive consonants , 1975, Science.

[50]  Pienie Zwitserlood,et al.  Plasticity of the human auditory cortex induced by discrimination learning of non-native, mora-timed contrasts of the Japanese language. , 2002, Learning & memory.

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

[52]  P. D. Eimas,et al.  Speech Perception in Infants , 1971, Science.

[53]  Stephen José Hanson,et al.  Foundational issues in human brain mapping , 2010 .

[54]  J. Hirsch,et al.  fMRI Evidence for Cortical Modification during Learning of Mandarin Lexical Tone , 2003, Journal of Cognitive Neuroscience.

[55]  L. Carver,et al.  Reward anticipation and processing of social versus nonsocial stimuli in children with and without autism spectrum disorders. , 2014, Journal of child psychology and psychiatry, and allied disciplines.

[56]  Jeffery A. Jones,et al.  Phonetic perceptual identification by native- and second-language speakers differentially activates brain regions involved with acoustic phonetic processing and those involved with articulatory–auditory/orosensory internal models , 2004, NeuroImage.

[57]  Toshiaki Imada,et al.  Theta brain rhythms index perceptual narrowing in infant speech perception , 2013, Front. Psychol..

[58]  Wilhelm von Humboldt,et al.  On Language: The Diversity of Human Language-Structure and Its Influence on the Mental Development of Mankind , 1988 .

[59]  L. Carver,et al.  Research review: Social motivation and oxytocin in autism--implications for joint attention development and intervention. , 2013, Journal of child psychology and psychiatry, and allied disciplines.

[60]  Norman J. Lass,et al.  Speech and Language: Advances in Basic Research and Practice , 1979 .

[61]  J. Werker,et al.  Cross-language speech perception: Evidence for perceptual reorganization during the first year of life , 1984 .

[62]  David Poeppel,et al.  Feedforward and feedback in speech perception: Revisiting analysis by synthesis , 2011 .

[63]  Karl J. Friston,et al.  The problem of low variance voxels in statistical parametric mapping; a new hat avoids a ‘haircut’ , 2012, NeuroImage.

[64]  D. Poeppel,et al.  Speech perception at the interface of neurobiology and linguistics , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[65]  R. Ilmoniemi,et al.  Language-specific phoneme representations revealed by electric and magnetic brain responses , 1997, Nature.

[66]  P. Kuhl Brain Mechanisms in Early Language Acquisition , 2010, Neuron.

[67]  Weiant Wathen-Dunn,et al.  Models for the perception of speech and visual form : proceedings of a symposium , 1967 .

[68]  A M Liberman,et al.  Perception of the speech code. , 1967, Psychological review.

[69]  P. Kuhl,et al.  Phonetic learning as a pathway to language: new data and native language magnet theory expanded (NLM-e) , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

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

[71]  S. Taulu,et al.  Spatiotemporal signal space separation method for rejecting nearby interference in MEG measurements , 2006, Physics in medicine and biology.

[72]  Richard S. J. Frackowiak,et al.  The anatomy of phonological and semantic processing in normal subjects. , 1992, Brain : a journal of neurology.

[73]  S. Dehaene,et al.  Anatomical variability in the cortical representation of first and second language , 1997, Neuroreport.

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

[75]  R. Hari,et al.  Brain basis of human social interaction: from concepts to brain imaging. , 2009, Physiological reviews.

[76]  James L. McClelland,et al.  Unsupervised learning of vowel categories from infant-directed speech , 2007, Proceedings of the National Academy of Sciences.

[77]  Toshio Inui,et al.  A functional magnetic resonance imaging study of listening comprehension of languages in human at 3 tesla-comprehension level and activation of the language areas , 1999, Neuroscience Letters.

[78]  Jessica Maye,et al.  Infant sensitivity to distributional information can affect phonetic discrimination , 2002, Cognition.

[79]  Alan C. Evans,et al.  Lateralization of phonetic and pitch discrimination in speech processing. , 1992, Science.

[80]  Patricia K. Kuhl,et al.  Early gray-matter and white-matter concentration in infancy predict later language skills: A whole brain voxel-based morphometry study , 2013, Brain and Language.

[81]  A. Meltzoff,et al.  The bimodal perception of speech in infancy. , 1982, Science.

[82]  Robert J. Zatorre,et al.  12 – Functional and Structural Imaging of the Human Auditory System , 2000 .