Cortical differentiation of speech and nonspeech sounds at 100 ms: implications for dyslexia.

Neurophysiological measures indicate cortical sensitivity to speech sounds by 150 ms after stimulus onset. In this time window dyslexic subjects start to show abnormal cortical processing. We investigated whether phonetic analysis is reflected in the robust auditory cortical activation at approximately 100 ms (N100m), and whether dyslexic subjects show abnormal N100m responses to speech or nonspeech sounds. We used magnetoencephalography to record auditory responses of 10 normally reading and 10 dyslexic adults. The speech stimuli were synthetic Finnish speech sounds (/a/, /u/, /pa/, /ka/). The nonspeech stimuli were complex nonspeech sounds and simple sine wave tones, composed of the F1+F2+F3 and F2 formant frequencies of the speech sounds, respectively. All sounds evoked a prominent N100m response in the bilateral auditory cortices. The N100m activation was stronger to speech than nonspeech sounds in the left but not in the right auditory cortex, in both subject groups. The leftward shift of hemispheric balance for speech sounds is likely to reflect analysis at the phonetic level. In dyslexic subjects the overall interhemispheric amplitude balance and timing were altered for all sound types alike. Dyslexic individuals thus seem to have an unusual cortical organization of general auditory processing in the time window of speech-sensitive analysis.

[1]  P. Alku,et al.  Electromagnetic recordings reveal latency differences in speech and tone processing in humans. , 1999, Brain research. Cognitive brain research.

[2]  R. Näätänen Attention and brain function , 1992 .

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

[4]  M. Studdert-Kennedy,et al.  Auditory temporal perception deficits in the reading-impaired: A critical review of the evidence , 1995, Psychonomic bulletin & review.

[5]  Maryanne Wolf,et al.  Rapid alternating stimulus naming in the developmental dyslexias , 1986, Brain and Language.

[6]  C Pantev,et al.  Magnetic and electric brain activity evoked by the processing of tone and vowel stimuli , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  Heikki Lyytinen,et al.  Heterogeneity in adult dyslexic readers: Relating processing skills to the speed and accuracy of oral text reading , 2001 .

[8]  K. Wiik,et al.  Finnish and English vowels , 1965 .

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

[10]  M. Denckla,et al.  Rapid ‘automatized’ naming (R.A.N.): Dyslexia differentiated from other learning disabilities , 1976, Neuropsychologia.

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

[12]  Bernd Lütkenhöner,et al.  High-Precision Neuromagnetic Study of the Functional Organization of the Human Auditory Cortex , 1998, Audiology and Neurotology.

[13]  G. Hynd,et al.  Brain morphology in developmental dyslexia and attention deficit disorder/hyperactivity. , 1990, Archives of neurology.

[14]  H. Renvall,et al.  Auditory Cortical Responses to Speech-Like Stimuli in Dyslexic Adults , 2002, Journal of Cognitive Neuroscience.

[15]  Bertrand Delgutte,et al.  Auditory Neural Processing of Speech , 2002 .

[16]  I. Johnsrude,et al.  Relationships between Human Auditory Cortical Structure and Function , 2003, Audiology and Neurotology.

[17]  P. Kuhl A new view of language acquisition. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[18]  C. Elberling,et al.  Auditory magnetic fields from the human cerebral cortex: Location and strength of an equivalent current dipole , 1982, Acta neurologica Scandinavica.

[19]  R. Hari,et al.  Responses of the human auditory cortex to vowel onset after fricative consonants , 2004, Experimental Brain Research.

[20]  R Hari,et al.  Neuromagnetic auditory evoked responses after a stroke in the right temporal lobe. , 1992, Neuroreport.

[21]  J. Connolly,et al.  Event-Related Potential Components Reflect Phonological and Semantic Processing of the Terminal Word of Spoken Sentences , 1994, Journal of Cognitive Neuroscience.

[22]  N. Geschwind,et al.  Developmental dyslexia: Four consecutive patients with cortical anomalies , 1985, Annals of neurology.

[23]  N. Yamada,et al.  Interhemispheric connection of auditory neural pathways assessed by auditory evoked magnetic fields in patients with fronto-temporal lobe infarction , 2002, Neuroscience Research.

[24]  Riitta Salmelin,et al.  Hemispheric balance in processing attended and non-attended vowels and complex tones. , 2003, Brain research. Cognitive brain research.

[25]  M. Eckert,et al.  Structural imaging in dyslexia: the planum temporale. , 2000, Mental retardation and developmental disabilities research reviews.

[26]  R. Hari The neuromagnetic method in the study of the human auditory cortex , 1990 .

[27]  R. Salmelin,et al.  Cortical processing of change detection: dissociation between natural vowels and two-frequency complex tones. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[28]  J. Rumsey,et al.  Failure to activate the left temporoparietal cortex in dyslexia. An oxygen 15 positron emission tomographic study. , 1992, Archives of neurology.

[29]  K. Kiehl,et al.  Detection of Sounds in the Auditory Stream: Event-Related fMRI Evidence for Differential Activation to Speech and Nonspeech , 2001, Journal of Cognitive Neuroscience.

[30]  S. Kuriki,et al.  Neuromagnetic study of the auditory responses in right and left hemispheres of the human brain evoked by pure tones and speech sounds , 2004, Experimental Brain Research.

[31]  Riitta Hari,et al.  Deficit of temporal auditory processing in dyslexic adults , 1996, Neuroscience Letters.

[32]  Uta Frith,et al.  Abnormal Functional Activation During a Simple Word Repetition Task: A PET Study of Adult Dyslexics , 2000, Journal of Cognitive Neuroscience.

[33]  J. Mäkelä,et al.  Functional differences between auditory cortices of the two hemispheres revealed by whole‐head neuromagnetic recordings , 1993 .

[34]  A. Galaburda Developmental dyslexia and animal studies: at the interface between cognition and neurology , 1994, Cognition.

[35]  Colin Phillips,et al.  Levels of representation in the electrophysiology of speech perception , 2001, Cogn. Sci..

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

[37]  Heikki Lyytinen,et al.  Cortical Activation during Spoken-Word Segmentation in Nonreading-Impaired and Dyslexic Adults , 2002, The Journal of Neuroscience.

[38]  M M Merzenich,et al.  Auditory processing parallels reading abilities in adults. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

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

[40]  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.

[41]  S. Crain,et al.  Cognitive Profiles of Reading-Disabled Children: Comparison of Language Skills in Phonology, Morphology, and Syntax , 1995 .

[42]  Heikki Lyytinen,et al.  Abnormal Auditory Cortical Activation in Dyslexia 100 msec after Speech Onset , 2002, Journal of Cognitive Neuroscience.

[43]  N. Suga,et al.  Cortical neurons sensitive to combinations of information-bearing elements of biosonar signals in the mustache bat. , 1978, Science.

[44]  T. Baldeweg,et al.  Impaired auditory frequency discrimination in dyslexia detected with mismatch evoked potentials , 1999, Annals of neurology.

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

[46]  P. Bryant,et al.  Categorizing sounds and learning to read—a causal connection , 1983, Nature.

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

[48]  Scott T. Grafton,et al.  Automated image registration: I. General methods and intrasubject, intramodality validation. , 1998, Journal of computer assisted tomography.

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

[50]  Mateo Obregón,et al.  Early naming deficits, developmental dyslexia, and a specific deficit hypothesis , 1992, Brain and Language.

[51]  M. Merzenich,et al.  Cortical auditory signal processing in poor readers. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

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

[53]  R Salmelin,et al.  Left-hemisphere dominance for processing of vowels: a whole-scalp neuromagnetic study. , 1999, Neuroreport.

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

[55]  Karl Zilles,et al.  A New Approach to Fast Elastic Alignment with Applications to Human Brain , 1996, VBC.

[56]  H. Remschmidt,et al.  Speech perception deficit in dyslexic adults as measured by mismatch negativity (MMN). , 2001, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

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

[58]  Dennis H. Klatt,et al.  Software for a cascade/parallel formant synthesizer , 1980 .

[59]  R Näätänen,et al.  Phonetic invariance in the human auditory cortex. , 1993, Neuroreport.

[60]  D. Poeppel,et al.  Auditory Cortex Accesses Phonological Categories: An MEG Mismatch Study , 2000, Journal of Cognitive Neuroscience.

[61]  J N Giedd,et al.  A magnetic resonance imaging study of planum temporale asymmetry in men with developmental dyslexia. , 1997, Archives of neurology.

[62]  A. Galaburda Neuroanatomic basis of developmental dyslexia. , 1993, Neurologic clinics.

[63]  S. Palva,et al.  Discrimination of Speech and of Complex Nonspeech Sounds of Different Temporal Structure in the Left and Right Cerebral Hemispheres , 2000, NeuroImage.

[64]  A Schnitzler,et al.  Native language, gender, and functional organization of the auditory cortex. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[65]  K. Alho Cerebral Generators of Mismatch Negativity (MMN) and Its Magnetic Counterpart (MMNm) Elicited by Sound Changes , 1995, Ear and hearing.

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

[67]  P. Tallal,et al.  Neurobiological Basis of Speech: A Case for the Preeminence of Temporal Processing , 1993, Annals of the New York Academy of Sciences.

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

[69]  J M Badier,et al.  Evoked potentials recorded from the auditory cortex in man: evaluation and topography of the middle latency components. , 1994, Electroencephalography and clinical neurophysiology.

[70]  M. Studdert-Kennedy,et al.  Speech perception deficits in poor readers: auditory processing or phonological coding? , 1997, Journal of experimental child psychology.

[71]  K. Stevens Acoustic correlates of some phonetic categories. , 1979, The Journal of the Acoustical Society of America.