Inferior frontal sensitivity to common speech sounds is amplified by increasing word intelligibility

The left inferior frontal gyrus (LIFG) exhibits increased responsiveness when people listen to words composed of speech sounds that frequently co-occur in the English language (Vaden, Piquado, & Hickok, 2011), termed high phonotactic frequency (Vitevitch & Luce, 1998). The current experiment aimed to further characterize the relation of phonotactic frequency to LIFG activity by manipulating word intelligibility in participants of varying age. Thirty six native English speakers, 19-79 years old (mean=50.5, sd=21.0) indicated with a button press whether they recognized 120 binaurally presented consonant-vowel-consonant words during a sparse sampling fMRI experiment (TR=8 s). Word intelligibility was manipulated by low-pass filtering (cutoff frequencies of 400 Hz, 1000 Hz, 1600 Hz, and 3150 Hz). Group analyses revealed a significant positive correlation between phonotactic frequency and LIFG activity, which was unaffected by age and hearing thresholds. A region of interest analysis revealed that the relation between phonotactic frequency and LIFG activity was significantly strengthened for the most intelligible words (low-pass cutoff at 3150 Hz). These results suggest that the responsiveness of the left inferior frontal cortex to phonotactic frequency reflects the downstream impact of word recognition rather than support of word recognition, at least when there are no speech production demands.

[1]  W. Marslen-Wilson.  Functional parallelism in spoken word-recognition , 1987, Cognition.

[2]  N Makris,et al.  Analysis of lesions by MRI in stroke patients with acoustic‐phonetic processing deficits , 1995, Neurology.

[3]  Elizabeth K. Johnson,et al.  Statistical learning of tone sequences by human infants and adults , 1999, Cognition.

[4]  Gregory Hickok,et al.  Phonological repetition-suppression in bilateral superior temporal sulci , 2010, NeuroImage.

[5]  Jason A. Tourville,et al.  Neural mechanisms underlying auditory feedback control of speech , 2008, NeuroImage.

[6]  David A. Medler,et al.  Neural correlates of sensory and decision processes in auditory object identification , 2004, Nature Neuroscience.

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

[8]  Wolfram Ziegler,et al.  Syllable frequency and syllable structure in apraxia of speech , 2004, Brain and Language.

[9]  David B Pisoni,et al.  Perception of Wordlikeness: Effects of Segment Probability and Length on the Processing of Nonwords. , 2000, Journal of memory and language.

[10]  M. Folstein,et al.  The Mini-Mental State Examination. , 1983, Archives of general psychiatry.

[11]  Jeffery A. Jones,et al.  Perceptual calibration of F0 production: evidence from feedback perturbation. , 2000, The Journal of the Acoustical Society of America.

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

[13]  Michael S Vitevitch,et al.  The influence of sublexical and lexical representations on the processing of spoken words in English , 2003, Clinical linguistics & phonetics.

[14]  L E Humes,et al.  Speech identification difficulties of hearing-impaired elderly persons: the contributions of auditory processing deficits. , 1991, Journal of speech and hearing research.

[15]  Jeffery A. Jones,et al.  Learning to produce speech with an altered vocal tract: the role of auditory feedback. , 2003, The Journal of the Acoustical Society of America.

[16]  S. Goldinger,et al.  Phonetic priming, neighborhood activation, and PARSYN , 2000, Perception & psychophysics.

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

[18]  C Büchel,et al.  Brain regions involved in articulation , 1999, The Lancet.

[19]  J. McQueen.  Segmentation of Continuous Speech Using Phonotactics , 1998 .

[20]  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.

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

[22]  P. Luce,et al.  Phonotactics, density, and entropy in spoken word recognition , 2001 .

[23]  Stephen M. Wilson,et al.  Speech perception when the motor system is compromised , 2009, Trends in Cognitive Sciences.

[24]  Raymond D. Kent,et al.  Phonetic development in identical twins differing in auditory function. , 1987, The Journal of speech and hearing disorders.

[25]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

[26]  P. Wong,et al.  Aging and cortical mechanisms of speech perception in noise , 2009, Neuropsychologia.

[27]  D. Dirks,et al.  Examination of the Neighborhood Activation Theory in Normal and Hearing-Impaired Listeners , 2001, Ear and hearing.

[28]  Gregory Hickok,et al.  Neural correlates of word production stages delineated by parametric modulation of psycholinguistic variables , 2009, Human brain mapping.

[29]  Adam R. Walczak,et al.  At the heart of the ventral attention system: The right anterior insula , 2009, Human brain mapping.

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

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

[32]  James L. McClelland,et al.  The TRACE model of speech perception , 1986, Cognitive Psychology.

[33]  R. C. Oldfield.  The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[34]  E. Newport,et al.  PSYCHOLOGICAL SCIENCE Research Article INCIDENTAL LANGUAGE LEARNING: Ustening (and Learning) out of the Comer of Your Ear , 2022 .

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

[36]  Paul C. Locasto,et al.  A systematic investigation of the functional neuroanatomy of auditory and visual phonological processing , 2005, NeuroImage.

[37]  D. Norris,et al.  Shortlist B: a Bayesian model of continuous speech recognition. , 2008, Psychological review.

[38]  P. Kuhl,et al.  Birdsong and human speech: common themes and mechanisms. , 1999, Annual review of neuroscience.

[39]  P Sterzer,et al.  Contributions of sensory input, auditory search and verbal comprehension to cortical activity during speech processing. , 2004, Cerebral cortex.

[40]  R. Baayen,et al.  Mixed-effects modeling with crossed random effects for subjects and items , 2008 .

[41]  Laurence White,et al.  Integration of multiple speech segmentation cues: a hierarchical framework. , 2005, Journal of experimental psychology. General.

[42]  Vince D. Calhoun,et al.  Age-Related Changes in Processing Speed: Unique Contributions of Cerebellar and Prefrontal Cortex , 2010, Front. Hum. Neurosci..

[43]  L. Tan,et al.  Distinct brain regions associated with syllable and phoneme , 2003, Human brain mapping.

[44]  Mitchell S. Sommers,et al.  The structural organization of the mental lexicon and its contribution to age-related declines in spoken-word recognition. , 1996 .

[45]  Chris Rorden,et al.  Speech apraxia without oral apraxia: can normal brain function explain the physiopathology? , 2006, Neuroreport.

[46]  P. Luce,et al.  When Words Compete: Levels of Processing in Perception of Spoken Words , 1998 .

[47]  G. Glover,et al.  Dissociable Intrinsic Connectivity Networks for Salience Processing and Executive Control , 2007, The Journal of Neuroscience.

[48]  Barry Horwitz,et al.  From phonemes to articulatory codes: an fMRI study of the role of Broca's area in speech production. , 2009, Cerebral cortex.

[49]  Karl J. Friston,et al.  Hemodynamic correlates of epileptiform discharges: An EEG-fMRI study of 63 patients with focal epilepsy , 2006, Brain Research.

[50]  D. Pisoni,et al.  Phonotactics, Neighborhood Activation, and Lexical Access for Spoken Words , 1999, Brain and Language.

[51]  Eveline Geiser,et al.  Segmental processing in the human auditory dorsal stream , 2008, Brain Research.

[52]  M. Merzenich,et al.  Modulation of the Auditory Cortex during Speech: An MEG Study , 2002, Journal of Cognitive Neuroscience.

[53]  M. Sommers.  The structural organization of the mental lexicon and its contribution to age-related declines in spoken-word recognition. , 1995, Psychology and aging.

[54]  B. Balas,et al.  Personal Familiarity Influences the Processing of Upright and Inverted Faces in Infants , 2009, Front. Hum. Neurosci..

[55]  Norbert Kathmann,et al.  Neural correlates of error awareness , 2007, NeuroImage.

[56]  Rajesh Kumar,et al.  A method for removal of global effects from fMRI time series , 2004, NeuroImage.

[57]  Jonathan H. Venezia,et al.  Hierarchical organization of human auditory cortex: evidence from acoustic invariance in the response to intelligible speech. , 2010, Cerebral cortex.

[58]  Adam R. Walczak,et al.  Age-related Effects on Word Recognition: Reliance on Cognitive Control Systems with Structural Declines in Speech-responsive Cortex , 2008, Journal of the Association for Research in Otolaryngology.

[59]  N. Dronkers.  A new brain region for coordinating speech articulation , 1996, Nature.

[60]  W Melnick,et al.  American National Standard specifications for audiometers. , 1971, ASHA.

[61]  F. Dick,et al.  Voxel-based lesion–symptom mapping , 2003, Nature Neuroscience.

[62]  M. Farah,et al.  Role of left inferior prefrontal cortex in retrieval of semantic knowledge: a reevaluation. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[63]  Chris Rorden,et al.  Neural recruitment for the production of native and novel speech sounds , 2009, NeuroImage.

[64]  P. Jusczyk,et al.  Do infants segment words or recurring contiguous patterns? , 2001, Journal of experimental psychology. Human perception and performance.

[65]  Holly L Storkel,et al.  Methods for minimizing the confounding effects of word length in the analysis of phonotactic probability and neighborhood density. , 2004, Journal of speech, language, and hearing research : JSLHR.

[66]  Carlo Caltagirone,et al.  Some aspects of phonological impairment in aphasia , 1980, Brain and Language.

[67]  Emily B. Myers,et al.  An event-related fMRI investigation of phonological–lexical competition , 2006, Neuropsychologia.

[68]  Chris Rorden,et al.  Modulation of frontal lobe speech areas associated with the production and perception of speech movements. , 2009, Journal of speech, language, and hearing research : JSLHR.

[69]  Raymond D. Kent,et al.  An auditory-feedback-based neural network model of speech production that is robust to developmental changes in the size and shape of the articulatory system. , 2000, Journal of speech, language, and hearing research : JSLHR.

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

[71]  J. Mills,et al.  Longitudinal changes in speech recognition in older persons. , 2008, The Journal of the Acoustical Society of America.

[72]  Meredith A. Shafto,et al.  Preserving Syntactic Processing across the Adult Life Span: The Modulation of the Frontotemporal Language System in the Context of Age-Related Atrophy , 2009, Cerebral cortex.

[73]  M. Eckert,et al.  Speech Recognition in Younger and Older Adults: A Dependency on Low-Level Auditory Cortex , 2009, The Journal of Neuroscience.

[74]  P. Jusczyk,et al.  Infants' sensitivity to phonotactic patterns in the native language. , 1994 .

[75]  Gregory Hickok,et al.  Sublexical Properties of Spoken Words Modulate Activity in Broca's Area but Not Superior Temporal Cortex: Implications for Models of Speech Recognition , 2011, Journal of Cognitive Neuroscience.

[76]  A. Hillis,et al.  Re-examining the brain regions crucial for orchestrating speech articulation. , 2004, Brain : a journal of neurology.

[77]  J. Dubno,et al.  Effects of age and mild hearing loss on speech recognition in noise. , 1984, The Journal of the Acoustical Society of America.

[78]  Elizabeth Bates,et al.  Exploring the processing continuum of single-word comprehension in aphasia. , 2005, Journal of speech, language, and hearing research : JSLHR.

[79]  Kristina M. Visscher,et al.  A Core System for the Implementation of Task Sets , 2006, Neuron.

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

[81]  A D Friederici,et al.  Phonological processing during language production: fMRI evidence for a shared production-comprehension network. , 2003, Brain research. Cognitive brain research.

[82]  Todd M. Bailey,et al.  Determinants of wordlikeness: Phonotactics or lexical neighborhoods? , 2001 .

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

[84]  A. Wingfield,et al.  Neural processing during older adults' comprehension of spoken sentences: age differences in resource allocation and connectivity. , 2010, Cerebral cortex.

[85]  Sharon L. Thompson-Schill,et al.  Prefrontal Cortical Response to Conflict during Semantic and Phonological Tasks , 2007, Journal of Cognitive Neuroscience.

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

[87]  Justin L. Vincent,et al.  Distinct brain networks for adaptive and stable task control in humans , 2007, Proceedings of the National Academy of Sciences.

[88]  E. Newport,et al.  WORD SEGMENTATION : THE ROLE OF DISTRIBUTIONAL CUES , 1996 .

[89]  G. Glover,et al.  Error‐related brain activation during a Go/NoGo response inhibition task , 2001, Human brain mapping.

[90]  V. Menon,et al.  Saliency, switching, attention and control: a network model of insula function , 2010, Brain Structure and Function.

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

[92]  H. Kucera,et al.  Computational analysis of present-day American English , 1967 .

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

[94]  P. Jusczyk,et al.  Infants′ Sensitivity to the Sound Patterns of Native Language Words , 1993 .

[95]  T. Tombaugh,et al.  The Mini‐Mental State Examination: A Comprehensive Review , 1992, Journal of the American Geriatrics Society.

[96]  John Ashburner,et al.  A fast diffeomorphic image registration algorithm , 2007, NeuroImage.

[97]  E. Nordeen,et al.  Auditory feedback is necessary for the maintenance of stereotyped song in adult zebra finches. , 1992, Behavioral and neural biology.

[98]  Sheila E. Blumstein,et al.  Neural Systems underlying Lexical Competition: An Eye Tracking and fMRI Study , 2010, Journal of Cognitive Neuroscience.

[99]  J. Mazziotta,et al.  Cracking the Language Code: Neural Mechanisms Underlying Speech Parsing , 2006, The Journal of Neuroscience.