Auditory Magnetic Response to Clicks in Children and Adults: Its Components, Hemispheric Lateralization and Repetition Suppression Effect

The auditory magnetic event-related fields (ERF) qualitatively change through the child development, reflecting maturation of auditory cortical areas. Clicks presented with long inter-stimulus interval produce distinct ERF components, and may appear useful to characterize immature EFR morphology in children. The present study is aimed to investigate morphology of the auditory ERFs in school-age children, as well as lateralization and repetition suppression of ERF components evoked by the clicks. School-age children and adults passively listened to pairs of click presented to the right ear, left ear or binaurally, with 8–11 s intervals between the pairs and a 1 s interval within a pair. Adults demonstrated a typical P50m/N100m response. Unlike adults, children had two distinct components preceding the N100m–P50m (at ~65 ms) and P100m (at ~100 ms). The P100m dominated the child ERF, and was most prominent in response to binaural stimulation. The N100m in children was less developed than in adults and partly overlapped in time with the P100m, especially in response to monaural clicks. Strong repetition suppression was observed for P50m both in children and adults, P100m in children and N100m in adults. Both children and adults demonstrated ERF amplitude and/or latency right hemispheric advantage effects that may reflect right hemisphere dominance for preattentive arousal processes. Our results contribute to the knowledge concerning development of auditory processing and its lateralization in children and have implications for investigation of the auditory evoked fields in developmental disorders.

[1]  M. Dorman,et al.  Deprivation-induced cortical reorganization in children with cochlear implants , 2007, International journal of audiology.

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

[3]  J. Eggermont,et al.  What's to lose and what's to learn: Development under auditory deprivation, cochlear implants and limits of cortical plasticity , 2007, Brain Research Reviews.

[4]  Mingxiong Huang,et al.  Distinct M50 and M100 auditory gating deficits in schizophrenia. , 2005, Psychophysiology.

[5]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

[6]  T. Yoshimoto,et al.  Middle and long latency peak sources in auditory evoked magnetic fields for tone bursts in humans , 2000, Neuroscience Letters.

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

[8]  Timothy P L Roberts,et al.  Cortical auditory system maturational abnormalities in children with autism disorder: an MEG investigation. , 2003, Brain research. Developmental brain research.

[9]  Andrew C. N. Chen,et al.  Gating of the vertex somatosensory and auditory evoked potential P50 and the correlation to skin conductance orienting response in healthy men , 2001, Psychiatry Research.

[10]  M. Dorman,et al.  Developmental changes in refractoriness of the cortical auditory evoked potential , 2005, Clinical Neurophysiology.

[11]  R. Ross,et al.  Reliability of P50 auditory sensory gating measures in infants during active sleep , 2008, Neuroreport.

[12]  Seppo P. Ahlfors,et al.  Assessing and improving the spatial accuracy in MEG source localization by depth-weighted minimum-norm estimates , 2006, NeuroImage.

[13]  K. Lehnertz,et al.  Comparison between simultaneously recorded auditory-evoked magnetic fields and potentials elicited by ipsilateral, contralateral and binaural tone burst stimulation. , 1986, Audiology : official organ of the International Society of Audiology.

[14]  A. Dale,et al.  Cortical Surface-Based Analysis II: Inflation, Flattening, and a Surface-Based Coordinate System , 1999, NeuroImage.

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

[16]  Nash N. Boutros,et al.  Evidence for a frontal cortex role in both auditory and somatosensory habituation: A MEG study , 2008, NeuroImage.

[17]  R. Ilmoniemi,et al.  Interpreting magnetic fields of the brain: minimum norm estimates , 2006, Medical and Biological Engineering and Computing.

[18]  R. Näätänen,et al.  Binaural interaction in the human brain can be non-invasively accessed with long-latency event-related potentials , 1997, Neuroscience Letters.

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

[20]  M. Dorman,et al.  Central auditory development: evidence from CAEP measurements in children fit with cochlear implants. , 2007, Journal of communication disorders.

[21]  M. Kisley,et al.  Comparison of sensory gating to mismatch negativity and self-reported perceptual phenomena in healthy adults. , 2004, Psychophysiology.

[22]  Garrett Cardon,et al.  Cortical maturation and behavioral outcomes in children with auditory neuropathy spectrum disorder , 2011, International journal of audiology.

[23]  J. Eggermont,et al.  Maturation of human central auditory system activity: the T-complex , 2003, Clinical Neurophysiology.

[24]  W. Sanefuji,et al.  Differential responses of primary auditory cortex in autistic spectrum disorder with auditory hypersensitivity , 2012, Neuroreport.

[25]  R. Kotecha,et al.  Modeling the Developmental Patterns of Auditory Evoked Magnetic Fields in Children , 2009, PloS one.

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

[27]  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.

[28]  J. Suzuki,et al.  Effects of rise time on simultaneously recorded auditory-evoked potentials from the early, middle and late ranges. , 1979, Audiology : official organ of the International Society of Audiology.

[29]  C. Rennie,et al.  Decrement of the N1 auditory event-related potential with stimulus repetition: habituation vs. refractoriness. , 1998, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[30]  Brett A Clementz,et al.  Response to the first stimulus determines reduced auditory evoked response suppression in schizophrenia: single trials analysis using MEG , 2001, Clinical Neurophysiology.

[31]  R. Rothermel,et al.  Intracranial Recording and Source Localization of Auditory Brain Responses Elicited at the 50 ms Latency in Three Children Aged from 3 to 16 Years , 2009, Brain Topography.

[32]  T. A. Stroganova,et al.  The right hemisphere fails to respond to temporal novelty in autism: Evidence from an ERP study , 2009, Clinical Neurophysiology.

[33]  E. Halgren,et al.  Dynamic Statistical Parametric Mapping Combining fMRI and MEG for High-Resolution Imaging of Cortical Activity , 2000, Neuron.

[34]  G. A. Miller,et al.  Predicting EEG responses using MEG sources in superior temporal gyrus reveals source asynchrony in patients with schizophrenia , 2003, Clinical Neurophysiology.

[35]  Abraham Z. Snyder,et al.  The Feasibility of a Common Stereotactic Space for Children and Adults in fMRI Studies of Development , 2002, NeuroImage.

[36]  K. Grill-Spector,et al.  Repetition and the brain: neural models of stimulus-specific effects , 2006, Trends in Cognitive Sciences.

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

[38]  M. Hämäläinen,et al.  Realistic conductivity geometry model of the human head for interpretation of neuromagnetic data , 1989, IEEE Transactions on Biomedical Engineering.

[39]  G. A. Miller,et al.  Lateralization of auditory sensory gating and neuropsychological dysfunction in schizophrenia. , 2003, The American journal of psychiatry.

[40]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

[41]  R. Kakigi,et al.  One year of musical training affects development of auditory cortical-evoked fields in young children. , 2006, Brain : a journal of neurology.

[42]  Ann Summerfelt,et al.  Review of clinical correlates of P50 sensory gating abnormalities in patients with schizophrenia. , 2005, Schizophrenia bulletin.

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

[44]  J. Mäkelä,et al.  Neuromagnetic responses of the human auditory cortex to on- and offsets of noise bursts. , 1987, Audiology : official organ of the International Society of Audiology.

[45]  F. Linthicum,et al.  The human auditory system: A timeline of development , 2007, International journal of audiology.

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

[47]  W. Roberts,et al.  Prominence of M50 auditory evoked response over M100 in childhood and autism , 2004, Neuroreport.

[48]  J R Wolpaw,et al.  Human middle-latency auditory evoked potentials: vertex and temporal components. , 1990, Electroencephalography and clinical neurophysiology.

[49]  David Poeppel,et al.  Auditory M50 and M100 responses to broadband noise: functional implications , 2004, Neuroreport.

[50]  M. Reite,et al.  Magnetic auditory evoked fields: interhemispheric asymmetry. , 1981, Electroencephalography and clinical neurophysiology.

[51]  Oleg Korzyukov,et al.  Generators of the intracranial P50 response in auditory sensory gating , 2007, NeuroImage.

[52]  D. Bishop,et al.  Maturation of auditory temporal integration and inhibition assessed with event-related potentials (ERPs) , 2010, BMC Neuroscience.

[53]  Mary F. Howard,et al.  Hemispheric asymmetry in mid and long latency neuromagnetic responses to single clicks , 2009, Hearing Research.

[54]  Olaf Hauk,et al.  Comparison of noise-normalized minimum norm estimates for MEG analysis using multiple resolution metrics , 2011, NeuroImage.

[55]  G. Nygren,et al.  Sensory gating in young children with autism: Relation to age, IQ, and EEG gamma oscillations , 2008, Neuroscience Letters.

[56]  T. Rosburg,et al.  Short-term habituation of auditory evoked potential and neuromagnetic field components in dependence of the interstimulus interval , 2010, Experimental Brain Research.

[57]  B. Rockstroh,et al.  Study of the Human Auditory Cortices Using a Whole-Head Magnetometer: Left vs. Right Hemisphere and Ipsilateral vs. Contralateral Stimulation , 1998, Audiology and Neurotology.

[58]  Y. Benjamini,et al.  THE CONTROL OF THE FALSE DISCOVERY RATE IN MULTIPLE TESTING UNDER DEPENDENCY , 2001 .

[59]  C. Elger,et al.  Habituation of auditory evoked potentials in intracranial and extracranial recordings. , 2006, Psychophysiology.

[60]  A. Belger,et al.  Midlatency evoked potentials attenuation and augmentation reflect different aspects of sensory gating , 1999, Biological Psychiatry.

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

[62]  Wendy Roberts,et al.  Auditory evoked fields predict language ability and impairment in children. , 2008, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[63]  A. Dale,et al.  Human posterior auditory cortex gates novel sounds to consciousness. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[64]  O. Salonen,et al.  Auditory Evoked Magnetic Fields to Tones and Pseudowords in Healthy Children and Adults , 1995, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[65]  Erich Schröger,et al.  Maturation of obligatory auditory responses and their neural sources: Evidence from EEG and MEG , 2011, NeuroImage.

[66]  K. Willmes,et al.  On the Functional Neuroanatomy of Intrinsic and Phasic Alertness , 2001, NeuroImage.

[67]  J S Buchwald,et al.  Midlatency auditory evoked responses: differential effects of a cholinergic agonist and antagonist. , 1991, Electroencephalography and clinical neurophysiology.

[68]  J. Stauder,et al.  Development and gender in the P50 paradigm , 2007, Clinical Neurophysiology.

[69]  N. Fox,et al.  The development of P50 suppression in the auditory event-related potential. , 2003, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[70]  D. Poeppel,et al.  Task-induced asymmetry of the auditory evoked M100 neuromagnetic field elicited by speech sounds. , 1996, Brain research. Cognitive brain research.

[71]  Nash N. Boutros,et al.  Mapping Repetition Suppression of the N100 Evoked Response to the Human Cerebral Cortex , 2011, Biological Psychiatry.

[72]  A. Dale,et al.  Distributed current estimates using cortical orientation constraints , 2006, Human brain mapping.

[73]  M. Corbetta,et al.  The Reorienting System of the Human Brain: From Environment to Theory of Mind , 2008, Neuron.

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

[75]  S. Debener,et al.  Late auditory evoked potentials asymmetry revisited , 2007, Clinical Neurophysiology.