Human temporal lobe activation by speech and nonspeech sounds.

Functional organization of the lateral temporal cortex in humans is not well understood. We recorded blood oxygenation signals from the temporal lobes of normal volunteers using functional magnetic resonance imaging during stimulation with unstructured noise, frequency-modulated (FM) tones, reversed speech, pseudowords and words. For all conditions, subjects performed a material-nonspecific detection response when a train of stimuli began or ceased. Dorsal areas surrounding Heschl's gyrus bilaterally, particularly the planum temporale and dorsolateral superior temporal gyrus, were more strongly activated by FM tones than by noise, suggesting a role in processing simple temporally encoded auditory information. Distinct from these dorsolateral areas, regions centered in the superior temporal sulcus bilaterally were more activated by speech stimuli than by FM tones. Identical results were obtained in this region using words, pseudowords and reversed speech, suggesting that the speech-tones activation difference is due to acoustic rather than linguistic factors. In contrast, previous comparisons between word and nonword speech sounds showed left-lateralized activation differences in more ventral temporal and temporoparietal regions that are likely involved in processing lexical-semantic or syntactic information associated with words. The results indicate functional subdivision of the human lateral temporal cortex and provide a preliminary framework for understanding the cortical processing of speech sounds.

[1]  R G Shulman,et al.  Functional magnetic resonance imaging assessment of the human brain auditory cortex response to increasing word presentation rates. , 1997, Journal of neurophysiology.

[2]  William D Marslen-Wilson,et al.  Processing interactions and lexical access during word recognition in continuous speech , 1978, Cognitive Psychology.

[3]  J. Rauschecker,et al.  Processing of complex sounds in the macaque nonprimary auditory cortex. , 1995, Science.

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

[5]  B H Repp,et al.  Relative Amplitude of Aspiration Noise as a Voicing Cue for Syllable-Initial Stop Consonants , 1979, Language and speech.

[6]  G. A. Miller,et al.  The intelligibility of speech as a function of the context of the test materials. , 1951, Journal of experimental psychology.

[7]  L. Lisker,et al.  A Cross-Language Study of Voicing in Initial Stops: Acoustical Measurements , 1964 .

[8]  E. Cornish,et al.  The Percentile Points of Distributions Having Known Cumulants , 1960 .

[9]  Jemett L. Desmond,et al.  Semantic encoding and retrieval in the left inferior prefrontal cortex: a functional MRI study of task difficulty and process specificity , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  Richard S. J. Frackowiak,et al.  Functional anatomy of a common semantic system for words and pictures , 1996, Nature.

[11]  S. Petersen,et al.  PET activation of posterior temporal regions during auditory word presentation and verb generation. , 1996, Cerebral cortex.

[12]  Y. Tanaka,et al.  Pure word deafness following bilateral lesions. A psychophysical analysis. , 1987, Brain : a journal of neurology.

[13]  A. Galaburda,et al.  Cytoarchitectonic organization of the human auditory cortex , 1980, The Journal of comparative neurology.

[14]  S. Henschen,et al.  On the hearing Sphere , 1918 .

[15]  Colin M. Macleod Half a century of research on the Stroop effect: an integrative review. , 1991, Psychological bulletin.

[16]  Philip Lieberman,et al.  Speech Physiology, Speech Perception, and Acoustic Phonetics , 1988 .

[17]  D. Massaro,et al.  Evaluation and integration of acoustic features in speech perception. , 1980, The Journal of the Acoustical Society of America.

[18]  Paul J. Abbas,et al.  A chronic microelectrode investigation of the tonotopic organization of human auditory cortex , 1996, Brain Research.

[19]  P. Kuhl Human adults and human infants show a “perceptual magnet effect” for the prototypes of speech categories, monkeys do not , 1991, Perception & psychophysics.

[20]  Alan D. Baddeley,et al.  Working memory and stimulus-independent thought: Effects of memory load and presentation rate , 1993 .

[21]  Emmanuel Dupoux,et al.  Brain processing of native and foreign languages. , 1996 .

[22]  S. F. Witelson,et al.  Sylvian fissure morphology and asymmetry in men and women: Bilateral differences in relation to handedness in men , 1992, The Journal of comparative neurology.

[23]  G. V. van Orden A ROWS is a ROSE: spelling, sound, and reading. , 1987, Memory & cognition.

[24]  S. Posse,et al.  Intensity coding of auditory stimuli: an fMRI study , 1998, Neuropsychologia.

[25]  J P Rauschecker,et al.  Processing of frequency-modulated sounds in the cat's posterior auditory field. , 1994, Journal of neurophysiology.

[26]  D. Symmes,et al.  On the use of natural stimuli in neurophysiological studies of audition , 1981, Hearing Research.

[27]  M M Mesulam,et al.  Large‐scale neurocognitive networks and distributed processing for attention, language, and memory , 1990, Annals of neurology.

[28]  Daniel S. O'Leary,et al.  A Positron Emission Tomography Study of Binaurally and Dichotically Presented Stimuli: Effects of Level of Language and Directed Attention , 1996, Brain and Language.

[29]  Christiana M. Leonard,et al.  Planum temporale asymmetry and language dominance , 1994, Neuropsychologia.

[30]  J. Binder,et al.  Functional magnetic resonance imaging of human auditory cortex , 1994, Annals of neurology.

[31]  M. Mintun,et al.  Regional cerebral blood flow during word and nonword reading , 1997, Human brain mapping.

[32]  J. Kaas,et al.  Subdivisions of AuditoryCortex and Levels of Processing in Primates , 1998, Audiology and Neurotology.

[33]  J. Rauschecker,et al.  Attention‐related modulation of activity in primary and secondary auditory cortex , 1997, Neuroreport.

[34]  N. Geschwind,et al.  Human Brain: Left-Right Asymmetries in Temporal Speech Region , 1968, Science.

[35]  J P Rauschecker,et al.  Processing of frequency-modulated sounds in the cat's anterior auditory field. , 1994, Journal of neurophysiology.

[36]  C. Wernicke Der aphasische Symptomenkomplex , 1974 .

[37]  C. Leonard,et al.  Anomalous cerebral structure in dyslexia revealed with magnetic resonance imaging. , 1993, Archives of neurology.

[38]  Allan Collins,et al.  A spreading-activation theory of semantic processing , 1975 .

[39]  A. Syrota,et al.  The Cortical Representation of Speech , 1993, Journal of Cognitive Neuroscience.

[40]  W. Glaser,et al.  Context effects in stroop-like word and picture processing. , 1989, Journal of experimental psychology. General.

[41]  Richard S. J. Frackowiak,et al.  Noun and verb retrieval by normal subjects. Studies with PET. , 1996, Brain : a journal of neurology.

[42]  M. Posner,et al.  Positron Emission Tomographic Studies of the Processing of Singe Words , 1989, Journal of Cognitive Neuroscience.

[43]  M. Mendez,et al.  Cortical auditory disorders: clinical and psychoacoustic features. , 1988, Journal of neurology, neurosurgery, and psychiatry.

[44]  J. Kaas,et al.  Tonotopic organization, architectonic fields, and connections of auditory cortex in macaque monkeys , 1993, The Journal of comparative neurology.

[45]  P A Bandettini,et al.  Effects of stimulus rate on signal response during functional magnetic resonance imaging of auditory cortex. , 1994, Brain research. Cognitive brain research.

[46]  G. Celesia Organization of auditory cortical areas in man. , 1976, Brain : a journal of neurology.

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

[48]  J. D. Waggener,et al.  A cortical auditory disorder , 1973, Neurology.

[49]  J. A. Frost,et al.  Conceptual Processing during the Conscious Resting State: A Functional MRI Study , 1999, Journal of Cognitive Neuroscience.

[50]  T. Carr,et al.  Words, pictures, and priming: on semantic activation, conscious identification, and the automaticity of information processing. , 1982, Journal of experimental psychology. Human perception and performance.

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

[52]  D. Pisoni Auditory and phonetic memory codes in the discrimination of consonants and vowels , 1973, Perception & psychophysics.

[53]  Dani Byrd,et al.  Auditory Selective Attention: An fMRI Investigation , 1996, NeuroImage.

[54]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[55]  Karl J. Friston,et al.  Distribution of cortical neural networks involved in word comprehension and word retrieval. , 1991, Brain : a journal of neurology.

[56]  Karl J. Friston,et al.  Subtractions, conjunctions, and interactions in experimental design of activation studies , 1997, Human brain mapping.

[57]  A. Galaburda,et al.  Topographical variation of the human primary cortices: implications for neuroimaging, brain mapping, and neurobiology. , 1993, Cerebral cortex.

[58]  Kenneth S. Pope,et al.  Regulation of the Stream of Consciousness: Toward a Theory of Ongoing Thought , 1978 .

[59]  R. Glushko The Organization and Activation of Orthographic Knowledge in Reading Aloud. , 1979 .

[60]  A G Samuel,et al.  Phonetic prototypes , 1982, Perception & psychophysics.

[61]  Albert M. Barrett,et al.  A CASE OF PURE WORD–DEAFNESS WITH AUTOPSY , 1910 .

[62]  J. Millichap,et al.  Brain Activity During Reading , 1995 .

[63]  J. Rauschecker Cortical processing of complex sounds , 1998, Current Opinion in Neurobiology.

[64]  Karl J. Friston,et al.  The cortical localization of the lexicons. Positron emission tomography evidence. , 1992, Brain : a journal of neurology.

[65]  Jeffrey L. Elman,et al.  Interactive processes in speech perception: the TRACE model , 1986 .

[66]  Richard S. J. Frackowiak,et al.  Differential activation of right and left posterior sylvian regions by semantic and phonological tasks: a positron-emission tomography study in normal human subjects , 1994, Neuroscience Letters.

[67]  P F Liddle,et al.  The role of the left prefrontal cortex in verbal processing: semantic processing or willed action? , 1994, Neuroreport.

[68]  P. Chauvel,et al.  Localization of the primary auditory area in man. , 1991, Brain : a journal of neurology.

[69]  W. James The principles of psychology , 1983 .

[70]  G. Wohlfart,et al.  Clinical picture and morbid anatomy in a case of pure word deafness. , 1952, The Journal of nervous and mental disease.

[71]  Stephen M. Rao,et al.  Human Brain Language Areas Identified by Functional Magnetic Resonance Imaging , 1997, The Journal of Neuroscience.

[72]  F. Fazio,et al.  Brain processing of native and foreign languages , 1996, NeuroImage.

[73]  W. Ganong Phonetic categorization in auditory word perception. , 1980, Journal of experimental psychology. Human perception and performance.

[74]  A. Buchman,et al.  Word deafness: one hundred years later. , 1986, Journal of neurology, neurosurgery, and psychiatry.

[75]  A M Galaburda,et al.  The intrinsic architectonic and connectional organization of the superior temporal region of the rhesus monkey , 1983, The Journal of comparative neurology.

[76]  M. Alexander,et al.  Pure word deafness. Analysis of a case with bilateral lesions and a defect at the prephonemic level. , 1982, Brain : a journal of neurology.

[77]  N. Cowan,et al.  The cocktail party phenomenon revisited: attention and memory in the classic selective listening procedure of Cherry (1953). , 1995, Journal of experimental psychology. General.

[78]  J. Kaas,et al.  Subdivisions of auditory cortex and ipsilateral cortical connections of the parabelt auditory cortex in macaque monkeys , 1998, The Journal of comparative neurology.

[79]  D. Klatt Review of selected models of speech perception , 1989 .

[80]  D. Spalding The Principles of Psychology , 1873, Nature.

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

[82]  M. Studdert-Kennedy,et al.  Stop-consonant recognition: Release bursts and formant transitions as functionally equivalent, context-dependent cues , 1977 .

[83]  R. Dodge The apperception of the spoken sentence: A study in the psychology of language. , 2022 .

[84]  James L. McClelland,et al.  An interactive activation model of context effects in letter perception: part 1.: an account of basic findings , 1988 .

[85]  M. Mishkin,et al.  Serial and parallel processing in rhesus monkey auditory cortex , 1997, The Journal of comparative neurology.

[86]  J. Antrobus,et al.  Studies in the stream of consciousness: Experimental enhancement and suppression of spontaneous cognitive processes , 1966 .

[87]  Lutz Jäncke,et al.  Anatomical left‐right asymmetry of language‐related temporal cortex is different in left‐ and right‐handers , 1991, Annals of neurology.

[88]  A. Marcel Conscious and unconscious perception: Experiments on visual masking and word recognition , 1983, Cognitive Psychology.

[89]  R. M. Warren,et al.  Speech perception and phonemic restorations , 1971 .

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

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

[92]  G. Humphreys,et al.  Segregating Semantic from Phonological Processes during Reading , 1997, Journal of Cognitive Neuroscience.

[93]  Richard S. J. Frackowiak,et al.  Brain activity during reading. The effects of exposure duration and task. , 1994, Brain : a journal of neurology.

[94]  R. Frackowiak,et al.  Demonstrating the implicit processing of visually presented words and pseudowords. , 1996, Cerebral cortex.

[95]  James L. McClelland,et al.  An interactive activation model of context effects in letter perception: I. An account of basic findings. , 1981 .

[96]  A Jesmanowicz,et al.  Lateralized human brain language systems demonstrated by task subtraction functional magnetic resonance imaging. , 1995, Archives of neurology.

[97]  M. E. Raichle,et al.  PET Studies of Auditory and Phonological Processing: Effects of Stimulus Characteristics and Task Demands , 1995, Journal of Cognitive Neuroscience.

[98]  J. Talairach,et al.  Co-Planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging , 1988 .

[99]  N. Geschwind,et al.  Current concepts: aphasia. , 1971, The New England journal of medicine.

[100]  N. Geschwind,et al.  Right-left asymmetrics in the brain. , 1978, Science.

[101]  Alan C. Evans,et al.  Interhemispheric anatomical differences in human primary auditory cortex: probabilistic mapping and volume measurement from magnetic resonance scans. , 1996, Cerebral cortex.

[102]  J. A. Frost,et al.  Function of the left planum temporale in auditory and linguistic processing , 1996, NeuroImage.

[103]  J. Bogen,et al.  WERNICKE'S REGION–WHERE IS IT? , 1976, Annals of the New York Academy of Sciences.

[104]  B. Repp Phonetic trading relations and context effects: new experimental evidence for a speech mode of perception. , 1982, Psychological bulletin.

[105]  Q. Summerfield,et al.  On the dissociation of spectral and temporal cues to the voicing distinction in initial stop consonants. , 1977, The Journal of the Acoustical Society of America.

[106]  P. T. Fox,et al.  Positron emission tomographic studies of the cortical anatomy of single-word processing , 1988, Nature.

[107]  G. C. Orden,et al.  Word identification in reading proceeds from spelling to sound to meaning. , 1988, Journal of experimental psychology. Learning, memory, and cognition.