Segregation of Vowels and Consonants in Human Auditory Cortex: Evidence for Distributed Hierarchical Organization

The speech signal consists of a continuous stream of consonants and vowels, which must be de- and encoded in human auditory cortex to ensure the robust recognition and categorization of speech sounds. We used small-voxel functional magnetic resonance imaging to study information encoded in local brain activation patterns elicited by consonant-vowel syllables, and by a control set of noise bursts. First, activation of anterior–lateral superior temporal cortex was seen when controlling for unspecific acoustic processing (syllables versus band-passed noises, in a “classic” subtraction-based design). Second, a classifier algorithm, which was trained and tested iteratively on data from all subjects to discriminate local brain activation patterns, yielded separations of cortical patches discriminative of vowel category versus patches discriminative of stop-consonant category across the entire superior temporal cortex, yet with regional differences in average classification accuracy. Overlap (voxels correctly classifying both speech sound categories) was surprisingly sparse. Third, lending further plausibility to the results, classification of speech–noise differences was generally superior to speech–speech classifications, with the no\ exception of a left anterior region, where speech–speech classification accuracies were significantly better. These data demonstrate that acoustic–phonetic features are encoded in complex yet sparsely overlapping local patterns of neural activity distributed hierarchically across different regions of the auditory cortex. The redundancy apparent in these multiple patterns may partly explain the robustness of phonemic representations.

[1]  S. Blumstein,et al.  Perceptual invariance and onset spectra for stop consonants in different vowel environments. , 1980, The Journal of the Acoustical Society of America.

[2]  P. Tallal,et al.  Rate of acoustic change may underlie hemispheric specialization for speech perception , 1980, Science.

[3]  S. Blumstein,et al.  A reconsideration of acoustic invariance for place of articulation in diffuse stop consonants: evidence from a cross-language study. , 1981, The Journal of the Acoustical Society of America.

[4]  M M Merzenich,et al.  Representation of a species-specific vocalization in the primary auditory cortex of the common marmoset: temporal and spectral characteristics. , 1995, Journal of neurophysiology.

[5]  C. Schroeder,et al.  Tonotopic organization of responses reflecting stop consonant place of articulation in primary auditory cortex (A1) of the monkey , 1995, Brain Research.

[6]  P. Tallal,et al.  Neurobiology of speech perception. , 1997, Annual review of neuroscience.

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

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

[9]  A. Caramazza,et al.  Separable processing of consonants and vowels , 2000, Nature.

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

[11]  X. Wang,et al.  On cortical coding of vocal communication sounds in primates. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[12]  A. Friederici,et al.  Auditory Language Comprehension: An Event-Related fMRI Study on the Processing of Syntactic and Lexical Information , 2000, Brain and Language.

[13]  J. Rauschecker,et al.  Hierarchical Organization of the Human Auditory Cortex Revealed by Functional Magnetic Resonance Imaging , 2001, Journal of Cognitive Neuroscience.

[14]  R. Zatorre,et al.  Spectral and temporal processing in human auditory cortex. , 2001, Cerebral cortex.

[15]  A. Ishai,et al.  Distributed and Overlapping Representations of Faces and Objects in Ventral Temporal Cortex , 2001, Science.

[16]  P. Morosan,et al.  Probabilistic Mapping and Volume Measurement of Human Primary Auditory Cortex , 2001, NeuroImage.

[17]  P. Morosan,et al.  Human Primary Auditory Cortex: Cytoarchitectonic Subdivisions and Mapping into a Spatial Reference System , 2001, NeuroImage.

[18]  J. Rauschecker,et al.  Functional Specialization in Rhesus Monkey Auditory Cortex , 2001, Science.

[19]  Christoph E Schreiner,et al.  Functional architecture of auditory cortex , 2002, Current Opinion in Neurobiology.

[20]  Thomas E. Nichols,et al.  Thresholding of Statistical Maps in Functional Neuroimaging Using the False Discovery Rate , 2002, NeuroImage.

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

[22]  J. Hart,et al.  Distinct prefrontal cortex activity associated with item memory and source memory for visual shapes. , 2003, Brain research. Cognitive brain research.

[23]  Jonas Obleser,et al.  Auditory-evoked magnetic field codes place of articulation in timing and topography around 100 milliseconds post syllable onset , 2003, NeuroImage.

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

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

[26]  R. Zatorre,et al.  Sensitivity to Auditory Object Features in Human Temporal Neocortex , 2004, The Journal of Neuroscience.

[27]  Elvira Brattico,et al.  Orderly cortical representation of vowel categories presented by multiple exemplars. , 2004, Brain research. Cognitive brain research.

[28]  M. Mishkin,et al.  Species-specific calls evoke asymmetric activity in the monkey's temporal poles , 2004, Nature.

[29]  Jonas Obleser,et al.  Attentional influences on functional mapping of speech sounds in human auditory cortex , 2004, BMC Neuroscience.

[30]  A. R. Jennings,et al.  Analysis of the spectral envelope of sounds by the human brain , 2005, NeuroImage.

[31]  Y. Benjamini,et al.  False Discovery Rate–Adjusted Multiple Confidence Intervals for Selected Parameters , 2005 .

[32]  G. Rees,et al.  Predicting the orientation of invisible stimuli from activity in human primary visual cortex , 2005, Nature Neuroscience.

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

[34]  M. Schönwiesner,et al.  Hemispheric asymmetry for spectral and temporal processing in the human antero‐lateral auditory belt cortex , 2005, The European journal of neuroscience.

[35]  J. Rauschecker,et al.  Vowel sound extraction in anterior superior temporal cortex , 2006, Human brain mapping.

[36]  Rainer Goebel,et al.  Information-based functional brain mapping. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[37]  Sean M. Polyn,et al.  Beyond mind-reading: multi-voxel pattern analysis of fMRI data , 2006, Trends in Cognitive Sciences.

[38]  Rajeev D. S. Raizada,et al.  Selective Amplification of Stimulus Differences during Categorical Processing of Speech , 2007, Neuron.

[39]  Nikolaus Kriegeskorte,et al.  Combining the tools: Activation- and information-based fMRI analysis , 2007, NeuroImage.

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

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

[42]  Rainer Goebel,et al.  Combining multivariate voxel selection and support vector machines for mapping and classification of fMRI spatial patterns , 2008, NeuroImage.

[43]  M. Kilgard,et al.  Cortical activity patterns predict speech discrimination ability , 2008, Nature Neuroscience.

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

[45]  N. Logothetis,et al.  A voice region in the monkey brain , 2008, Nature Neuroscience.

[46]  N. Logothetis,et al.  Where Are the Human Speech and Voice Regions, and Do Other Animals Have Anything Like Them? , 2009, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[47]  Gregory Hickok,et al.  Selective attention to semantic and syntactic features modulates sentence processing networks in anterior temporal cortex. , 2009, Cerebral cortex.

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

[49]  John-Dylan Haynes,et al.  Decoding visual consciousness from human brain signals , 2009, Trends in Cognitive Sciences.

[50]  J. Obleser,et al.  Pre-lexical abstraction of speech in the auditory cortex , 2009, Trends in Cognitive Sciences.

[51]  Nikolaus Kriegeskorte,et al.  Comparison of multivariate classifiers and response normalizations for pattern-information fMRI , 2010, NeuroImage.

[52]  Daniel Recasens,et al.  Coarticulation and Connected Speech Processes , 2010 .

[53]  J. Rauschecker,et al.  Cortical Representation of Natural Complex Sounds: Effects of Acoustic Features and Auditory Object Category , 2010, The Journal of Neuroscience.

[54]  Colin Humphries,et al.  Tonotopic organization of human auditory cortex , 2010, NeuroImage.

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

[56]  R. Malach,et al.  Syntactic structure building in the anterior temporal lobe during natural story listening , 2012, Brain and Language.

[57]  J. Obleser,et al.  Dissociable neural imprints of perception and grammar in auditory functional imaging , 2012, Human brain mapping.