Dynamic speech representations in the human temporal lobe

Speech perception requires rapid integration of acoustic input with context-dependent knowledge. Recent methodological advances have allowed researchers to identify underlying information representations in primary and secondary auditory cortex and to examine how context modulates these representations. We review recent studies that focus on contextual modulations of neural activity in the superior temporal gyrus (STG), a major hub for spectrotemporal encoding. Recent findings suggest a highly interactive flow of information processing through the auditory ventral stream, including influences of higher-level linguistic and metalinguistic knowledge, even within individual areas. Such mechanisms may give rise to more abstract representations, such as those for words. We discuss the importance of characterizing representations of context-dependent and dynamic patterns of neural activity in the approach to speech perception research.

[1]  Karl J. Friston The free-energy principle: a unified brain theory? , 2010, Nature Reviews Neuroscience.

[2]  J. Elman On the Meaning of Words and Dinosaur Bones: Lexical Knowledge Without a Lexicon , 2009, Cogn. Sci..

[3]  I. Nelken,et al.  Processing of low-probability sounds by cortical neurons , 2003, Nature Neuroscience.

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

[5]  Lori L. Holt,et al.  Are there interactive processes in speech perception? , 2006, Trends in Cognitive Sciences.

[6]  Mitchell Steinschneider,et al.  Intracranial study of speech-elicited activity on the human posterolateral superior temporal gyrus. , 2011, Cerebral cortex.

[7]  I. Nelken,et al.  Sensitivity to Complex Statistical Regularities in Rat Auditory Cortex , 2012, Neuron.

[8]  J. Simon,et al.  Emergence of neural encoding of auditory objects while listening to competing speakers , 2012, Proceedings of the National Academy of Sciences.

[9]  Karl J. Friston,et al.  The Cortical Dynamics of Intelligible Speech , 2008, The Journal of Neuroscience.

[10]  J. McQueen,et al.  Changing only the probability that spoken words will be distorted changes how they are recognized. , 2012, Journal of the Acoustical Society of America.

[11]  Jeffrey R. Binder,et al.  Attentional and linguistic interactions in speech perception , 2008, NeuroImage.

[12]  Antoine J. Shahin,et al.  Attentional Gain Control of Ongoing Cortical Speech Representations in a “Cocktail Party” , 2010, The Journal of Neuroscience.

[13]  Kristofer E. Bouchard,et al.  Functional Organization of Human Sensorimotor Cortex for Speech Articulation , 2013, Nature.

[14]  Sarah C. Creel,et al.  How Talker Identity Relates to Language Processing , 2011, Lang. Linguistics Compass.

[15]  Rutvik H. Desai,et al.  Specialization along the Left Superior Temporal Sulcus for Auditory Categorization , 2010, Cerebral cortex.

[16]  Risto Näätänen,et al.  Training the Brain to Weight Speech Cues Differently: A Study of Finnish Second-language Users of English , 2010, Journal of Cognitive Neuroscience.

[17]  David Poeppel,et al.  What Does the Right Hemisphere Know about Phoneme Categories? , 2011, Journal of Cognitive Neuroscience.

[18]  S. Scott,et al.  The Pathways for Intelligible Speech: Multivariate and Univariate Perspectives , 2013, Cerebral cortex.

[19]  Elia Formisano,et al.  Processing of Natural Sounds in Human Auditory Cortex: Tonotopy, Spectral Tuning, and Relation to Voice Sensitivity , 2012, The Journal of Neuroscience.

[20]  A. Clark Whatever next? Predictive brains, situated agents, and the future of cognitive science. , 2013, The Behavioral and brain sciences.

[21]  Bruce D. McCandliss,et al.  Brain mechanisms implicated in the preattentive categorization of speech sounds revealed using FMRI and a short-interval habituation trial paradigm. , 2007, Cerebral cortex.

[22]  Mitchell Steinschneider,et al.  Coding of repetitive transients by auditory cortex on Heschl's gyrus. , 2009, Journal of neurophysiology.

[23]  Anne Cutler,et al.  Are there really interactive processes in speech perception? , 2006, Trends in Cognitive Sciences.

[24]  Feng Rong,et al.  Sensorimotor Integration in Speech Processing: Computational Basis and Neural Organization , 2011, Neuron.

[25]  Timothy D. Griffiths,et al.  A unified framework for the organization of the primate auditory cortex , 2013, Front. Syst. Neurosci..

[26]  Mitchell Steinschneider,et al.  Spectrotemporal analysis of evoked and induced electroencephalographic responses in primary auditory cortex (A1) of the awake monkey. , 2008, Cerebral cortex.

[27]  Ping Li,et al.  Cortical Dynamics of Acoustic and Phonological Processing in Speech Perception , 2011, PloS one.

[28]  J. Maunsell,et al.  Different Origins of Gamma Rhythm and High-Gamma Activity in Macaque Visual Cortex , 2011, PLoS biology.

[29]  A. Samuel,et al.  Perceptual learning for speech: Is there a return to normal? , 2005, Cognitive Psychology.

[30]  A. Lotto,et al.  Speech Perception Within an Auditory Cognitive Science Framework , 2008, Current directions in psychological science.

[31]  Sarah C. Creel,et al.  Heeding the voice of experience: The role of talker variation in lexical access , 2008, Cognition.

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

[33]  I. Fried,et al.  Coupling Between Neuronal Firing, Field Potentials, and fMRI in Human Auditory Cortex , 2005, Science.

[34]  H. Coslett,et al.  Localization of sublexical speech perception components , 2010, Brain and Language.

[35]  David Poeppel,et al.  The analysis of speech in different temporal integration windows: cerebral lateralization as 'asymmetric sampling in time' , 2003, Speech Commun..

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

[37]  C. Honey,et al.  Topographic Mapping of a Hierarchy of Temporal Receptive Windows Using a Narrated Story , 2011, The Journal of Neuroscience.

[38]  Brian H Scott,et al.  Transformation of temporal processing across auditory cortex of awake macaques. , 2011, Journal of neurophysiology.

[39]  J. Rauschecker,et al.  Phoneme and word recognition in the auditory ventral stream , 2012, Proceedings of the National Academy of Sciences.

[40]  Ingrid S. Johnsrude,et al.  Human auditory cortex is sensitive to the perceived clarity of speech , 2012, NeuroImage.

[41]  Friedemann Pulvermüller,et al.  Rapid Cortical Plasticity Underlying Novel Word Learning , 2010, The Journal of Neuroscience.

[42]  Stefan J Kiebel,et al.  How the Human Brain Recognizes Speech in the Context of Changing Speakers , 2010, The Journal of Neuroscience.

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

[44]  A. Pouget,et al.  Probabilistic brains: knowns and unknowns , 2013, Nature Neuroscience.

[45]  W. Marslen-Wilson,et al.  Neural dynamics of inflectional and derivational processing in spoken word comprehension: laterality and automaticity , 2013, Front. Hum. Neurosci..

[46]  Roy D. Patterson,et al.  Direct Recordings of Pitch Responses from Human Auditory Cortex , 2010, Current Biology.

[47]  Sophie K. Scott,et al.  Hemispheric Asymmetries in Speech Perception: Sense, Nonsense and Modulations , 2011, PloS one.

[48]  T. Hackett Information flow in the auditory cortical network , 2011, Hearing Research.

[49]  Y. Cohen,et al.  Representation of speech categories in the primate auditory cortex. , 2011, Journal of neurophysiology.

[50]  Brian N. Pasley,et al.  Reconstructing Speech from Human Auditory Cortex , 2012, PLoS biology.

[51]  Kirill V. Nourski,et al.  Representation of speech in human auditory cortex: Is it special? , 2013, Hearing Research.

[52]  C. Wernicke Der aphasische Symptomencomplex: Eine psychologische Studie auf anatomischer Basis , 1874 .

[53]  M. Gaskell,et al.  Acquiring Novel Words and Their Past Tenses: Evidence from Lexical Effects on Phonetic Categorisation. , 2012 .

[54]  Keith Johnson,et al.  Phonetic Feature Encoding in Human Superior Temporal Gyrus , 2014, Science.

[55]  D. Poeppel,et al.  Mechanisms Underlying Selective Neuronal Tracking of Attended Speech at a “Cocktail Party” , 2013, Neuron.

[56]  N. Geschwind Disconnexion syndromes in animals and man. I. , 1965, Brain : a journal of neurology.

[57]  Christopher K. Kovach,et al.  Coding of repetitive transients by auditory cortex on posterolateral superior temporal gyrus in humans: an intracranial electrophysiology study. , 2013, Journal of neurophysiology.

[58]  Matthew H. Davis,et al.  Predictive Top-Down Integration of Prior Knowledge during Speech Perception , 2012, The Journal of Neuroscience.

[59]  E. Chang,et al.  Categorical Speech Representation in Human Superior Temporal Gyrus , 2010, Nature Neuroscience.

[60]  N. Mesgarani,et al.  Selective cortical representation of attended speaker in multi-talker speech perception , 2012, Nature.

[61]  Ferath Kherif,et al.  Does Semantic Context Benefit Speech Understanding through “Top–Down” Processes? Evidence from Time-resolved Sparse fMRI , 2011, Journal of Cognitive Neuroscience.

[62]  I. Nelken,et al.  Processing of complex sounds in the auditory system , 2008, Current Opinion in Neurobiology.

[63]  D. Gow The cortical organization of lexical knowledge: A dual lexicon model of spoken language processing , 2012, Brain and Language.

[64]  M. Tanenhaus,et al.  Time Course of Frequency Effects in Spoken-Word Recognition: Evidence from Eye Movements , 2001, Cognitive Psychology.

[65]  D. Poeppel,et al.  Processing Asymmetry of Transitions between Order and Disorder in Human Auditory Cortex , 2007, The Journal of Neuroscience.

[66]  R. Goebel,et al.  Processing of Natural Sounds: Characterization of Multipeak Spectral Tuning in Human Auditory Cortex , 2013, The Journal of Neuroscience.

[67]  C. Atencio,et al.  Hierarchical representations in the auditory cortex , 2011, Current Opinion in Neurobiology.

[68]  J. Elman An alternative view of the mental lexicon , 2004, Trends in Cognitive Sciences.

[69]  D Norris,et al.  Merging information in speech recognition: Feedback is never necessary , 2000, Behavioral and Brain Sciences.

[70]  Joachim Gross,et al.  Phase-Locked Responses to Speech in Human Auditory Cortex are Enhanced During Comprehension , 2012, Cerebral cortex.

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

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

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

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

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

[76]  Mark A. Chevillet,et al.  Functional Correlates of the Anterolateral Processing Hierarchy in Human Auditory Cortex , 2011, The Journal of Neuroscience.

[77]  M. Schönwiesner,et al.  Spectro-temporal modulation transfer function of single voxels in the human auditory cortex measured with high-resolution fMRI , 2009, Proceedings of the National Academy of Sciences.

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

[79]  Jeffrey L. Elman,et al.  Language Proficiency Modulates the Recruitment of Non-Classical Language Areas in Bilinguals , 2011, PloS one.

[80]  Matthew K. Leonard,et al.  Independence of early speech processing from word meaning. , 2013, Cerebral cortex.

[81]  D. T. Ives,et al.  Bihemispheric foundations for human speech comprehension , 2010, Proceedings of the National Academy of Sciences.

[82]  Mitchell Steinschneider,et al.  Phonemic Representations and Categories , 2013 .

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

[84]  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.

[85]  Jonas Obleser,et al.  Bilateral Speech Comprehension Reflects Differential Sensitivity to Spectral and Temporal Features , 2008, The Journal of Neuroscience.

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

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

[88]  J. Simon,et al.  Neural coding of continuous speech in auditory cortex during monaural and dichotic listening. , 2012, Journal of neurophysiology.

[89]  S. Dehaene,et al.  Cortical representation of the constituent structure of sentences , 2011, Proceedings of the National Academy of Sciences.

[90]  Y. Cohen,et al.  Neural Correlates of Auditory Cognition , 2013, Springer Handbook of Auditory Research.

[91]  B. Gordon,et al.  Induced electrocorticographic gamma activity during auditory perception , 2001, Clinical Neurophysiology.

[92]  Rainer Goebel,et al.  "Who" Is Saying "What"? Brain-Based Decoding of Human Voice and Speech , 2008, Science.

[93]  Christoph E. Schreiner,et al.  Auditory Cortex Mapmaking: Principles, Projections, and Plasticity , 2007, Neuron.

[94]  Stefan J. Kiebel,et al.  From Birdsong to Human Speech Recognition: Bayesian Inference on a Hierarchy of Nonlinear Dynamical Systems , 2013, PLoS Comput. Biol..

[95]  Matthew H. Davis,et al.  A complementary systems account of word learning: neural and behavioural evidence , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

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

[97]  Mitchell Steinschneider,et al.  Spectral organization of the human lateral superior temporal gyrus revealed by intracranial recordings. , 2014, Cerebral cortex.

[98]  I. Fried,et al.  Ultra-fine frequency tuning revealed in single neurons of human auditory cortex , 2008, Nature.

[99]  Matthew H. Davis,et al.  Temporal Predictive Codes for Spoken Words in Auditory Cortex , 2012, Current Biology.

[100]  Sachiko Koyama,et al.  Comprehension of degraded speech sounds with m-sequence modulation: An fMRI study , 2010, NeuroImage.