Maturation of auditory temporal integration and inhibition assessed with event-related potentials (ERPs)

BackgroundWe examined development of auditory temporal integration and inhibition by assessing electrophysiological responses to tone pairs separated by interstimulus intervals (ISIs) of 25, 50, 100, 200, 400, and 800 ms in 28 children aged 7 to 9 years, and 15 adults.ResultsIn adults a distinct neural response was elicited to tones presented at ISIs of 25 ms or longer, whereas in children this was only seen in response to tones presented at ISIs above 100 ms. In adults, late N1 amplitude was larger for the second tone of the tone pair when separated by ISIs as short as 100 ms, consistent with the perceptual integration of successive stimuli within the temporal window of integration. In contrast, children showed enhanced negativity only when tone pairs were separated by ISIs of 200 ms. In children, the amplitude of the P1 component was attenuated at ISIs below 200 ms, consistent with a refractory process.ConclusionsThese results indicate that adults integrate sequential auditory information into smaller temporal segments than children. These results suggest that there are marked maturational changes from childhood to adulthood in the perceptual processes underpinning the grouping of incoming auditory sensory information, and that electrophysiological measures provide a sensitive, non-invasive method allowing further examination of these changes.

[1]  R. J. Irwin,et al.  The development of auditory temporal acuity in children. , 1985, Child development.

[2]  H. Semlitsch,et al.  A solution for reliable and valid reduction of ocular artifacts, applied to the P300 ERP. , 1986, Psychophysiology.

[3]  J. Richard Jennings,et al.  Editorial Policy on Analyses of Variance With Repeated Measures , 1987 .

[4]  J. Thayer,et al.  The continuing problem of false positives in repeated measures ANOVA in psychophysiology: a multivariate solution. , 1987, Psychophysiology.

[5]  T. Picton,et al.  The N1 wave of the human electric and magnetic response to sound: a review and an analysis of the component structure. , 1987, Psychophysiology.

[6]  D. Guthrie,et al.  Significance testing of difference potentials. , 1991, Psychophysiology.

[7]  T. Bullock,et al.  Induced Rhythms in the Brain , 1992, Brain Dynamics.

[8]  Erol Başar,et al.  Evoked Potentials: Ensembles of Brain Induced Rhythmicities in the Alpha, Theta and Gamma Ranges , 1992 .

[9]  M. Woldorff,et al.  Distortion of ERP averages due to overlap from temporally adjacent ERPs: analysis and correction. , 2007, Psychophysiology.

[10]  B A Schneider,et al.  Gap detection in infants, children, and adults. , 1995, The Journal of the Acoustical Society of America.

[11]  D. Woods The component structure of the N1 wave of the human auditory evoked potential. , 1995, Electroencephalography and clinical neurophysiology. Supplement.

[12]  V. Jousmäki,et al.  Temporal integration in auditory sensory memory: neuromagnetic evidence. , 1996, Electroencephalography and clinical neurophysiology.

[13]  Dorothy V. M. Bishop,et al.  Uncommon Understanding: Development and Disorders of Language Comprehension in Children , 1997 .

[14]  C. Barthélémy,et al.  Temporal prominence of auditory evoked potentials (N1 wave) in 4-8-year-old children. , 1997, Psychophysiology.

[15]  L. McEvoy,et al.  Temporal characteristics of auditory sensory memory: neuromagnetic evidence. , 1997, Psychophysiology.

[16]  H. Keselman Testing treatment effects in repeated measures designs: an update for psychophysiological researchers. , 1998, Psychophysiology.

[17]  R. Näätänen,et al.  Interstimulus interval and auditory event-related potentials in children: evidence for multiple generators. , 1998, Electroencephalography and clinical neurophysiology.

[18]  M. Taylor,et al.  Tracking the development of the N1 from age 3 to adulthood: an examination of speech and non-speech stimuli , 2000, Clinical Neurophysiology.

[19]  Margot J. Taylor,et al.  Guidelines for using human event-related potentials to study cognition: recording standards and publication criteria. , 2000, Psychophysiology.

[20]  B A Wright,et al.  Age-related improvements in auditory backward and simultaneous masking in 6- to 10-year-old children. , 2000, Journal of speech, language, and hearing research : JSLHR.

[21]  R. Uwer,et al.  The development of auditory evoked dipole source activity from childhood to adulthood , 2000, Clinical Neurophysiology.

[22]  J. Eggermont,et al.  Maturation of human central auditory system activity: separating auditory evoked potentials by dipole source modeling , 2002, Clinical Neurophysiology.

[23]  Jos J. Eggermont,et al.  Auditory-evoked Potential Studies of Cortical Maturation in Normal Hearing and Implanted Children: Correlations with Changes in Structure and Speech Perception , 2003, Acta oto-laryngologica.

[24]  Katrin Krumbholz,et al.  Microsecond temporal resolution in monaural hearing without spectral cues? , 2003, The Journal of the Acoustical Society of America.

[25]  C. Tenke,et al.  Optimizing PCA methodology for ERP component identification and measurement: theoretical rationale and empirical evaluation , 2003, Clinical Neurophysiology.

[26]  I. Kirk,et al.  Age-related improvements in auditory temporal resolution in reading-impaired children. , 2003, Dyslexia.

[27]  T. Griffiths,et al.  What is an auditory object? , 2004, Nature Reviews Neuroscience.

[28]  G. McArthur,et al.  Immature cortical responses to auditory stimuli in specific language impairment: evidence from ERPs to rapid tone sequences. , 2004, Developmental science.

[29]  Kathy A. Low,et al.  Latent inhibition mediates N1 attenuation to repeating sounds. , 2004, Psychophysiology.

[30]  E. Sussman,et al.  The development of the length of the temporal window of integration for rapidly presented auditory information as indexed by MMN , 2005, Clinical Neurophysiology.

[31]  E. Schröger,et al.  Auditory streaming affects the processing of successive deviant and standard sounds. , 2005, Psychophysiology.

[32]  H. Neville,et al.  Auditory and visual refractory period effects in children and adults: An ERP study , 2005, Clinical Neurophysiology.

[33]  C. Tenke,et al.  Trusting in or breaking with convention: Towards a renaissance of principal components analysis in electrophysiology , 2005, Clinical Neurophysiology.

[34]  Dorothy V. M. Bishop,et al.  Individual Differences in Auditory Processing in Specific Language Impairment: A Follow-Up Study using Event-Related Potentials and Behavioural Thresholds , 2005, Cortex.

[35]  Kerry M. M. Walker,et al.  Development of perceptual correlates of reading performance , 2006, Brain Research.

[36]  Terence W. Picton,et al.  Effects of Attention on Neuroelectric Correlates of Auditory Stream Segregation , 2006, Journal of Cognitive Neuroscience.

[37]  D. Shore,et al.  The development of temporal resolution: between-channel gap detection in infants and adults. , 2006, Journal of speech, language, and hearing research : JSLHR.

[38]  Jennifer J. Lister,et al.  Cortical Evoked Response to Gaps in Noise: Within-Channel and Across-Channel Conditions , 2007, Ear and hearing.

[39]  E. Sussman,et al.  Processing intensity at rapid rates: evidence from auditory evoked potentials in 9-11-year-old children. , 2008, International journal of pediatric otorhinolaryngology.

[40]  M. Steinschneider,et al.  The maturation of human evoked brain potentials to sounds presented at different stimulus rates , 2008, Hearing Research.

[41]  P. Dawes,et al.  Maturation of visual and auditory temporal processing in school-aged children. , 2008, Journal of speech, language, and hearing research : JSLHR.

[42]  A. Mouraux,et al.  The Enhancement of the N1 Wave Elicited by Sensory Stimuli Presented at Very Short Inter-Stimulus Intervals Is a General Feature across Sensory Systems , 2008, PloS one.

[43]  M. Steinschneider,et al.  Attention effects on auditory scene analysis in children , 2009, Neuropsychologia.

[44]  R. Draganova,et al.  Hemispheric asymmetry of auditory evoked fields elicited by spectral versus temporal stimulus change. , 2009, Cerebral cortex.