The discrimination of and orienting to speech and non-speech sounds in children with autism

The present study aimed to find out how different stages of cortical auditory processing (sound encoding, discrimination, and orienting) are affected in children with autism. To this end, auditory event-related potentials (ERP) were studied in 15 children with autism and their controls. Their responses were recorded for pitch, duration, and vowel changes in speech stimuli, and for corresponding changes in the non-speech counterparts of the stimuli, while the children watched silent videos and ignored the stimuli. The responses to sound repetition were diminished in amplitude in the children with autism, reflecting impaired sound encoding. The mismatch negativity (MMN), an ERP indexing sound discrimination, was enhanced in the children with autism as far as pitch changes were concerned. This is consistent with earlier studies reporting auditory hypersensitivity and good pitch-processing abilities, as well as with theories proposing enhanced perception of local stimulus features in individuals with autism. The discrimination of duration changes was impaired in these children, however. Finally, involuntary orienting to sound changes, as reflected by the P3a ERP, was more impaired for speech than non-speech sounds in the children with autism, suggesting deficits particularly in social orienting. This has been proposed to be one of the earliest symptoms to emerge, with pervasive effects on later development.

[1]  H. Tager-Flusberg,et al.  Identifying neurocognitive phenotypes in autism. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[2]  Stephen McAdams,et al.  The neuroanatomical substrate of sound duration discrimination , 2002, Neuropsychologia.

[3]  P. Alku,et al.  Children's Auditory Event-Related Potentials Index Sound Complexity and “Speechness” , 2001, The International journal of neuroscience.

[4]  I. Peretz,et al.  Enhanced Pitch Sensitivity in Individuals with Autism: A Signal Detection Analysis , 2003, Journal of Cognitive Neuroscience.

[5]  F. Volkmar,et al.  The enactive mind, or from actions to cognition: lessons from autism. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[6]  I. Peretz,et al.  Local and global processing of music in high-functioning persons with autism: beyond central coherence? , 2000, Journal of child psychology and psychiatry, and allied disciplines.

[7]  Jean-Baptiste Poline,et al.  Perception of complex sounds: abnormal pattern of cortical activation in autism. , 2003, The American journal of psychiatry.

[8]  Chantal Kemner,et al.  Auditory event-related brain potentials in autistic children and three different control groups , 1995, Biological Psychiatry.

[9]  R Näätänen,et al.  Mismatch negativity outside strong attentional focus: a commentary on Woldorff et al. (1991) , 1991, Psychophysiology.

[10]  C. Gillberg,et al.  Biology of the Autistic Syndromes , 1994 .

[11]  R Galambos,et al.  Autism: processing of novel auditory information assessed by event-related brain potentials. , 1984, Electroencephalography and clinical neurophysiology.

[12]  B. Hermelin,et al.  Musical Processing in High Functioning Children with Autism , 2001, Annals of the New York Academy of Sciences.

[13]  R Näätänen,et al.  The mismatch negativity as an index of temporal processing in audition , 2001, Clinical Neurophysiology.

[14]  R V Shannon,et al.  Speech Recognition with Primarily Temporal Cues , 1995, Science.

[15]  E. Pang,et al.  Cortical auditory evoked potentials in autism: a review. , 2004, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[16]  R. Ilmoniemi,et al.  Processing of novel sounds and frequency changes in the human auditory cortex: magnetoencephalographic recordings. , 1998, Psychophysiology.

[17]  J. Burack,et al.  Enhanced perceptual functioning in the development of autism. , 2001 .

[18]  Bartolo Lanuzza,et al.  The mismatch negativity and the P3a components of the auditory event-related potentials in autistic low-functioning subjects , 2003, Clinical Neurophysiology.

[19]  Sue Peppé,et al.  Prosody in autism spectrum disorders: a critical review. , 2003, International journal of language & communication disorders.

[20]  Eric Courchesne,et al.  Brainstem, cerebellar and limbic neuroanatomical abnormalities in autism , 1997, Current Opinion in Neurobiology.

[21]  L. Gustafsson.  Inadequate cortical feature maps: A neural circuit theory of autism , 1997, Biological Psychiatry.

[22]  C. Escera,et al.  The accuracy of sound duration representation in the human brain determines the accuracy of behavioural perception , 2000, The European journal of neuroscience.

[23]  Stefano Seri,et al.  Autism in tuberous sclerosis: evoked potential evidence for a deficit in auditory sensory processing , 1999, Clinical Neurophysiology.

[24]  S. Hillyard,et al.  The effects of channel-selective attention on the mismatch negativity wave elicited by deviant tones. , 1991, Psychophysiology.

[25]  A. Meltzoff,et al.  Children with Autism Fail to Orient to Naturally Occurring Social Stimuli , 1998, Journal of autism and developmental disorders.

[26]  Edward G. Blackstock,et al.  Cerebral asymmetry and the development of early infantile autism , 1978, Journal of autism and childhood schizophrenia.

[27]  R Näätänen,et al.  Event-related brain potentials reveal covert distractibility in closed head injuries. , 1999, Neuroreport.

[28]  R. Ivry,et al.  The neural representation of time , 2004, Current Opinion in Neurobiology.

[29]  R. Näätänen,et al.  Early selective-attention effect on evoked potential reinterpreted. , 1978, Acta psychologica.

[30]  George McCloskey,et al.  Leiter International Performance Scale , 1987 .

[31]  G. Dawson,et al.  Early social attention impairments in autism: social orienting, joint attention, and attention to distress. , 2004, Developmental psychology.

[32]  R. Näätänen,et al.  Maturation of cortical sound processing as indexed by event-related potentials , 2002, Clinical Neurophysiology.

[33]  I. Winkler,et al.  Involuntary Attention and Distractibility as Evaluated with Event-Related Brain Potentials , 2000, Audiology and Neurotology.

[34]  Ami Klin,et al.  Young autistic children's listening preferences in regard to speech: A possible characterization of the symptom of social withdrawal , 1991, Journal of autism and developmental disorders.

[35]  R. Erwin,et al.  Midlatency auditory evoked responses: P1 abnormalities in adult autistic subjects. , 1992, Electroencephalography and clinical neurophysiology.

[36]  Risto Näätänen,et al.  Brain activity index of distractibility in normal school-age children , 2001, Neuroscience Letters.

[37]  U. Frith,et al.  Autism and Asperger Syndrome , 1992 .

[38]  P. Heaton,et al.  Pitch memory, labelling and disembedding in autism. , 2003, Journal of child psychology and psychiatry, and allied disciplines.

[39]  E Courchesne,et al.  Attention function and dysfunction in autism. , 2001, Frontiers in bioscience : a journal and virtual library.

[40]  R. Knight,et al.  Neural Mechanisms of Involuntary Attention to Acoustic Novelty and Change , 1998, Journal of Cognitive Neuroscience.

[41]  T. Nicol,et al.  Speech-Evoked Neurophysiologic Responses in Children with Learning Problems: Development and Behavioral Correlates of Perception , 2000, Ear and hearing.

[42]  C. Escera,et al.  Activation of brain mechanisms of attention switching as a function of auditory frequency change , 2001, Neuroreport.

[43]  I. Peretz,et al.  Absolute pitch in autism: A case study , 1999 .

[44]  C. Escera,et al.  Electrophysiological evidence of abnormal activation of the cerebral network of involuntary attention in alcoholism , 2003, Clinical Neurophysiology.

[45]  R. Näätänen,et al.  Speech–sound-selective auditory impairment in children with autism: They can perceive but do not attend , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[46]  Andrew E. Switala,et al.  Minicolumnar pathology in autism , 2002, Neurology.

[47]  T. Charman,et al.  The Development of Autism : Perspectives From Theory and Research , 2001 .

[48]  Geraldine Dawson,et al.  Links between social and linguistic processing of speech in preschool children with autism: behavioral and electrophysiological measures. , 2005, Developmental science.

[49]  Manuel F. Casanova,et al.  Clinical and Macroscopic Correlates of Minicolumnar Pathology in Autism , 2002, Journal of child neurology.

[50]  Geraldine Dawson,et al.  Neural correlates of face and object recognition in young children with autism spectrum disorder, developmental delay, and typical development. , 2002, Child development.

[51]  Jean-Louis Adrien,et al.  Hypersensitivity to acoustic change in children with autism: electrophysiological evidence of left frontal cortex dysfunctioning. , 2002, Psychophysiology.

[52]  N. Bruneau,et al.  Blood flow response to auditory stimulations in normal, mentally retarded, and autistic children: A preliminary transcranial Doppler ultrasonographic study of the middle cerebral arteries , 1992, Biological Psychiatry.

[53]  Y. Samson,et al.  Perception of complex sounds in autism: abnormal auditory cortical processing in children. , 2004, The American journal of psychiatry.

[54]  R. Knight.  Decreased response to novel stimuli after prefrontal lesions in man. , 1984, Electroencephalography and clinical neurophysiology.

[55]  N. Squires,et al.  Two varieties of long-latency positive waves evoked by unpredictable auditory stimuli in man. , 1975, Electroencephalography and clinical neurophysiology.

[56]  P. Alku,et al.  A method for generating natural-sounding speech stimuli for cognitive brain research , 1999, Clinical Neurophysiology.

[57]  Francesca Pei,et al.  Attentional skills during the first 6 months of age in autism spectrum disorder. , 2002, Journal of the American Academy of Child and Adolescent Psychiatry.

[58]  G. Baird,et al.  The frequency and distribution of spontaneous attention shifts between social and nonsocial stimuli in autistic, typically developing, and nonautistic developmentally delayed infants. , 1998, Journal of child psychology and psychiatry, and allied disciplines.

[59]  Robert Jones,et al.  Sensory-Perceptual Abnormalities in Autism: A Case For More Research? , 1997, Journal of autism and developmental disorders.

[60]  I. Rapin,et al.  Update on the language disorders of individuals on the autistic spectrum , 2003, Brain and Development.

[61]  Pascal Belin,et al.  Abnormal cortical voice processing in autism , 2004, Nature Neuroscience.

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

[63]  A. Neal,et al.  Neural plasticity, joint attention, and a transactional social-orienting model of autism* , 2000 .

[64]  Mm. Liabre.  Standard Progressive Matrices , 1984 .

[65]  R. Müller,et al.  Brain Mapping of Language and Auditory Perception in High-Functioning Autistic Adults: A PET Study , 1999, Journal of autism and developmental disorders.

[66]  J Townsend,et al.  Impairment in shifting attention in autistic and cerebellar patients. , 1994, Behavioral neuroscience.