Abstract
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.






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References
Arnfred SM, Eder DN, Hemmingsen RP, Glenthoj BY, Chen ACN (2001) Gating of the vertex somatosensory and auditory evoked potential p50 and the correlation to skin conductance orienting response in healthy men. Psychiatry Res 101:221–235
Benjamini Y, Yekutieli D (2001) The control of the false discovery rate in multiple testing under dependency. Ann Stat 29:1165–1188
Blumenfeld LD, Clementz BA (2001) Response to the first stimulus determines reduced auditory evoked response suppression in schizophrenia: single trials analysis using MEG. Clin Neurophysiol 112:1650–1659
Boutros NN, Belger A (1999) Midlatency evoked potentials attenuation and augmentation reflect different aspects of sensory gating. Biol Psychiatry 45:917–922
Boutros NN, Gjini K, Urbach H, Pflieger ME (2011) Mapping repetition suppression of the n100 evoked response to the human cerebral cortex. Biol Psychiatry 69:883–889
Brinkman MJR, Stauder JEA (2007) Development and gender in the p50 paradigm. Clin Neurophysiol 118:1517–1524
Bruneau N, Roux S, Guerin P, Barthelemy C, Lelord G (1997) Temporal prominence of auditory evoked potentials (n1 wave) in 4–8-year-old children. Psychophysiology 34:32–38
Buchwald JS, Rubinstein EH, Schwafel J, Strandburg RJ (1991) Midlatency auditory evoked-responses—differential-effects of a cholinergic agonist and antagonist. Electroencephalogr Clin Neurophysiol 80:303–309
Buchwald JS, Erwin R, Vanlancker D, Guthrie D, Schwafel J, Tanguay P (1992) Midlatency auditory evoked-responses: p1 abnormalities in adult autistic subjects. Electroencephalogr Clin Neurophysiol 84:164–171
Budd TW, Barry RJ, Gordon E, Rennie C, Michie PT (1998) Decrement of the n1 auditory event-related potential with stimulus repetition: habituation vs refractoriness. Int J Psychophysiol 31:51–68
Burgund ED, Kang HC, Kelly JE, Buckner RL, Snyder AZ, Petersen SE, Schlaggar BL (2002) The feasibility of a common stereotactic space for children and adults in fMRI studies of development. Neuroimage 17:184–200
Cacace AT, Satyamurti S, Wolpaw JR (1990) Human middle-latency auditory evoked-potentials—vertex and temporal components. Electroencephalogr Clin Neurophysiol 77:6–18
Cardy JEO, Ferrari P, Flagg EJ, Roberts W, Roberts TPL (2004) Prominence of m50 auditory evoked response over m100 in childhood and autism. Neuroreport 15:1867–1870
Cardy JEO, Flagg EJ, Roberts W, Roberts TPL (2008) Auditory evoked fields predict language ability and impairment in children. Int J Psychophysiol 68:170–175
Ceponiene R, Rinne T, Naatanen R (2002) Maturation of cortical sound processing as indexed by event-related potentials. Clin Neurophysiol 113:870–882
Chait M, Simon JZ, Poeppel D (2004) Auditory m50 and m100 responses to broadband noise: functional implications. Neuroreport 15:2455–2458
Corbetta M, Patel G, Shulman GL (2008) The reorienting system of the human brain: from environment to theory of mind. Neuron 58:306–324
Dale AM, Fischl B, Sereno MI (1999) Cortical surface-based analysis—I. Segmentation and surface reconstruction. Neuroimage 9:179–194
Dale AM, Liu AK, Fischl BR, Buckner RL, Belliveau JW, Lewine JD, Halgren E (2000) Dynamic statistical parametric mapping: combining fMRI and MEG for high-resolution imaging of cortical activity. Neuron 26:55–67
Delorme A, Makeig S (2004) Eeglab: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods 134:9–21
Dorman MF, Sharma A, Gilley P, Martin K, Roland P (2007) Central auditory development: evidence from CAEP measurements in children fit with cochlear implants. J Commun Disord 40:284–294
Eggermont JJ, Ponton CW (2003) Auditory-evoked potential studies of cortical maturation in normal hearing and implanted children: correlations with changes in structure and speech perception. Acta Otolaryngol 123:249–252
Elberling C, Bak C, Kofoed B, Lebech J, Saermark K (1982) Auditory magnetic fields from the human cerebral cortex: location and strength of an equivalent current dipole. Acta Neurol Scand 65:553–569
Fischl B, Sereno MI, Dale AM (1999) Cortical surface-based analysis. II: inflation, flattening, and a surface-based coordinate system. Neuroimage 9:195–207
Fox AM, Anderson M, Reid C, Smith T, Bishop DVM (2010) Maturation of auditory temporal integration and inhibition assessed with event-related potentials (ERPs). BMC Neurosci 16:11–49
Fujioka T, Ross B, Kakigi R, Pantev C, Trainor LJ (2006) One year of musical training affects development of auditory cortical-evoked fields in young children. Brain 129:2593–2608
Gage NM, Siegel B, Roberts TPL (2003) Cortical auditory system maturational abnormalities in children with autism disorder: an MEG investigation. Dev Brain Res 144:201–209
Ghosh SS, Kakunoori S, Augustinack J, Nieto-Castanon A, Kovelman I, Gaab N, Christodoulou JA, Triantafyllou C, Gabrieli JDE, Fischl B (2010) Evaluating the validity of volume-based and surface-based brain image registration for developmental cognitive neuroscience studies in children 4 to 11 years of age. Neuroimage 53:85–93
Gilley PM, Sharma A, Dorman M, Martin K (2005) Developmental changes in refractoriness of the cortical auditory evoked potential. Clin Neurophysiol 116:648–657
Gootjes L, Raiji T, Salmelin R, Hari R (1999) Left-hemisphere dominance for processing of vowels: a whole-scalp neuromagnetic study. NeuroReport 10:2987–2991
Grill-Spector K, Henson R, Martin A (2006) Repetition and the brain: neural models of stimulus-specific effects. Trends Cogn Sci 10:14–23
Hamalainen MS, Ilmoniemi RJ (1994) Interpreting magnetic-fields of the brain: minimum norm estimates. Med Biol Eng Comput 32:35–42
Hamalainen MS, Sarvas J (1989) Realistic conductivity geometry model of the human head for interpretation of neuromagnetic data. IEEE Trans Biomed Eng 36:165–171
Hanlon FM, Miller GA, Thoma RJ, Irwin J, Jones A, Moses SN, Huang MX, Weisend MP, Paulson KM, Edgar JC, Adler LE, Canive JM (2005) Distinct m50 and m100 auditory gating deficits in schizophrenia. Psychophysiology 42:417–427
Hari R, Pelizzone M, Makela J, Hallstrom J, Leinonen L, Lounasmaa OV (1987) Neuromagnetic responses of the human auditory cortex to on- and offsets of noise bursts. Audiology 26:31–43
Hauk O, Wakeman DG, Henson R (2011) Comparison of noise-normalized minimum norm estimates for MEG analysis using multiple resolution metrics. Neuroimage 54:1966–1974
Hine J, Debener S (2007) Late auditory evoked potentials asymmetry revisited. Clin Neurophysiol 118:1274–1285
Howard MF, Poeppel D (2009) Hemispheric asymmetry in mid and long latency neuromagnetic responses to single clicks. Hear Res 257:41–52
Huang MX, Edgar JC, Thoma RJ, Hanlon FM, Moses SN, Lee RR, Paulson KM, Weisend MP, Irwin JG, Bustillo JR, Adler LE, Miller GA, Canive JM (2003) Predicting EEG responses using MEG sources in superior temporal gyrus reveals source asynchrony in patients with schizophrenia. Clin Neurophysiol 114:835–850
Hunter SK, Corral N, Ponicsan H, Ross RG (2008) Reliability of p50 auditory sensory gating measures in infants during active sleep. NeuroReport 19:79–82
Jaaskelainen IP, Ahveninen J, Bonmassar G, Dale AM, Ilmoniemi RJ, Levanen S, Lin FH, May P, Melcher J, Stufflebeam S, Tiitinen H, Belliveau JW (2004) Human posterior auditory cortex gates novel sounds to consciousness. Proc Natl Acad Sci USA 101:6809–6814
Kanno A, Nakasato N, Murayama N, Yoshimoto T (2000) Middle and long latency peak sources in auditory evoked magnetic fields for tone bursts in humans. Neurosci Lett 293:187–190
Kisley MA, Noecker TL, Guinther PM (2004) Comparison of sensory gating to mismatch negativity and self-reported perceptual phenomena in healthy adults. Psychophysiology 41:604–612
Kodera K, Hink RF, Yamada O, Suzuki JI (1979) Effects of rise time on simultaneously recorded auditory-evoked potentials from the early, middle and late ranges. Audiology 18:395–402
Korzyukov O, Pflieger ME, Wagner M, Bowyer SM, Rosburg T, Sundaresan K, Elger CE, Boutros NN (2007) Generators of the intracranial p50 response in auditory sensory gating. Neuroimage 35:814–826
Korzyukov O, Asano E, Gumenyuk V, Juhasz C, Wagner M, Rothermel RD, Chugani HT (2009) Intracranial recording and source localization of auditory brain responses elicited at the 50 ms latency in three children aged from 3 to 16 years. Brain Topogr 22:166–175
Kotecha R, Pardos M, Wang YY, Wu T, Horn P, Brown D, Rose D, DeGrauw T, Xiang J (2009) Modeling the developmental patterns of auditory evoked magnetic fields in children. PLoS ONE 4:e4811
Kral A, Eggermont JJ (2007) What’s to lose and what’s to learn: development under auditory deprivation, cochlear implants and limits of cortical plasticity. Brain Res Rev 56:259–269
Lavikainen J, Tiitinen H, May P, Naatanen R (1997) Binaural interaction in the human brain can be non-invasively accessed with long-latency event-related potentials. Neurosci Lett 222:37–40
Lin FH, Belliveau JW, Dale AM, Hamalainen MS (2006a) Distributed current estimates using cortical orientation constraints. Hum Brain Mapp 27:1–13
Lin FH, Witzel T, Ahlfors SP, Stufflebeam SM, Belliveau JW, Hamalainen MS (2006b) Assessing and improving the spatial accuracy in MEG source localization by depth-weighted minimum-norm estimates. Neuroimage 31:160–171
Loveless N, Levanen S, Jousmaki V, Sams M, Hari R (1996) Temporal integration in auditory sensory memory: neuromagnetic evidence. Evoked potential-electroencephalogr. Clin Neurophysiol 100:220–228
Makela JP, Ahonen A, Hamalainen M, Hari R, Ilmoniemi R, Kajola M, Knuutila J, Lounasmaa OV, McEvoy L, Salmelin R, Sams M, Salonen, Simola J, Tesche C, Vasama J (1993) Functional differences between auditory cortices of the two hemispheres revealed by whole-head neuromagnetic recordings. Hum Brain Mapp 1:48–56
Marshall PJ, Bar-Haim Y, Fox NA (2004) The development of p50 suppression in the auditory event-related potential. Int J Psychophysiol 51:135–141
Matsuzaki J, Kagitani-Shimono K, Goto T, Sanefuji W, Yamamoto T, Sakai S, Uchida H, Hirata M, Mohri I, Yorifuji S, Taniike M (2012) Differential responses of primary auditory cortex in autistic spectrum disorder with auditory hypersensitivity. Neuroreport 23:113–118
Moore JK, Linthicum FH (2007) The human auditory system: a timeline of development. Int J Audiol 46:460–478
Orekhova EV, Stroganova TA, Prokofyev AO, Nygren G, Gillberg C, Elam M (2008) Sensory gating in young children with autism: relation to age, IQ, and EEG gamma oscillations. Neurosci Lett 434:218–223
Orekhova EV, Stroganova TA, Prokofiev A, Nygren G, Gillberg C, Elam M (2009) The right hemisphere fails to respond to temporal novelty in autism: evidence from an ERP study. Clin Neurophysiol 120:520–529
Paetau R, Ahonen A, Salonen O, Sams M (1995) Auditory-evoked magnetic-fields to tones and pseudowords in healthy-children and adults. J Clin Neurophysiol 12:177–185
Pantev C, Lutkenhoner B, Hoke M, Lehnertz K (1986) Comparison between simultaneously recorded auditory-evoked magnetic fields and potentials elicited by ipsilateral, contralateral and binaural tone burst stimulation. Audiology 25:54–61
Pantev C, Ross B, Berg P, Elbert T, Rockstroh B (1998) Study of the human auditory cortices using a whole-head magnetometer: left versus right hemisphere and ipsilateral versus contralateral stimulation. Audiol Neurootol 3:183–190
Poeppel D, Yellin E, Phillips C, Roberts TPL, Rowley HA, Wexler K, Marantz A (1996) Task-induced asymmetry of the auditory evoked m100 neuromagnetic field elicited by speech sounds. Brain Res Cogn Brain Res 4:231–242
Ponton C, Eggermont JJ, Khosla D, Kwong B, Don M (2002) Maturation of human central auditory system activity: separating auditory evoked potentials by dipole source modeling. Clin Neurophysiol 113:407–420
Potter D, Summerfelt A, Gold J, Buchanan RW (2006) Review of clinical correlates of p50 sensory gating abnormalities in patients with schizophrenia. Schizophr Bull 32:692–700
Reite M, Zimmerman JT, Zimmerman JE (1981) Magnetic auditory evoked fields: interhemispheric asymmetry. Electroencephalogr Clin Neurophysiol 51:388–392
Rosburg T, Trautner P, Boutros NN, Korzyukov OA, Schaller C, Elger CE, Kurthen M (2006) Habituation of auditory evoked potentials in intracranial and extracranial recordings. Psychophysiology 43:137–144
Rosburg T, Zimmerer K, Huonker R (2010) Short-term habituation of auditory evoked potential and neuromagnetic field components in dependence of the interstimulus interval. Exp Brain Res 205:559–570
Ruhnau P, Herrmann B, Maess B, Schroger E (2011) Maturation of obligatory auditory responses and their neural sources: evidence from EEG and MEG. Neuroimage 58:630–639
Sable JJ, Low KA, Maclin EL, Fabiani M, Gratton G (2004) Latent inhibition mediates n1 attenuation to repeating sounds. Psychophysiology 41:636–642
Sharma A, Gilley PM, Dormant MF, Baldwin R (2007) Deprivation-induced cortical reorganization in children with cochlear implants. Int J Audiol 46:494–499
Sharma A, Cardon G, Henion K, Roland P (2011) Cortical maturation and behavioral outcomes in children with auditory neuropathy spectrum disorder. Int J Audiol 50:98–106
Sturm W, Willmes K (2001) On the functional neuroanatomy of intrinsic and phasic alertness. Neuroimage 14:S76–S84
Sussman E, Stemschneider M, Gumenyuk V, Grushko J, Lawson K (2008) The maturation of human evoked brain potentials to sounds presented at different stimulus rates. Hear Res 236:61–79
Thoma RJ, Hanlon FM, Moses SN, Edgar JC, Huang MX, Weisend MP, Irwin J, Sherwood A, Paulson K, Bustillo J, Adler LE, Miller GA, Canive JM (2003) Lateralization of auditory sensory gating and neuropsychological dysfunction in schizophrenia. Am J Psychiatry 160:1595–1605
Tonnquist-Uhlen I, Ponton CW, Eggermont JJ, Kwong B, Don M (2003) Maturation of human central auditory system activity: the T-complex. Clin Neurophysiol 114:685–701
Weiland BJ, Boutros NN, Moran JM, Tepley N, Bowyer SM (2008) Evidence for a frontal cortex role in both auditory and somatosensory habituation: a MEG study. Neuroimage 42:827–835
Acknowledgments
This research was supported by grant # 2009-3765 from the Swedish Research Council and by grant # 16.518.11.7088 from the Russian Ministry of Science and Education. We are grateful to all participants and to the families of the children for their contribution.
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Orekhova, E.V., Butorina, A.V., Tsetlin, M.M. et al. Auditory Magnetic Response to Clicks in Children and Adults: Its Components, Hemispheric Lateralization and Repetition Suppression Effect. Brain Topogr 26, 410–427 (2013). https://doi.org/10.1007/s10548-012-0262-x
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DOI: https://doi.org/10.1007/s10548-012-0262-x