Infant Auditory Processing and Event-related Brain Oscillations

Gabriella Musacchia, Silvia Ortiz-Mantilla, Teresa Realpe-Bonilla, Cynthia P Roesler, April A Benasich, Gabriella Musacchia, Silvia Ortiz-Mantilla, Teresa Realpe-Bonilla, Cynthia P Roesler, April A Benasich

Abstract

Rapid auditory processing and acoustic change detection abilities play a critical role in allowing human infants to efficiently process the fine spectral and temporal changes that are characteristic of human language. These abilities lay the foundation for effective language acquisition; allowing infants to hone in on the sounds of their native language. Invasive procedures in animals and scalp-recorded potentials from human adults suggest that simultaneous, rhythmic activity (oscillations) between and within brain regions are fundamental to sensory development; determining the resolution with which incoming stimuli are parsed. At this time, little is known about oscillatory dynamics in human infant development. However, animal neurophysiology and adult EEG data provide the basis for a strong hypothesis that rapid auditory processing in infants is mediated by oscillatory synchrony in discrete frequency bands. In order to investigate this, 128-channel, high-density EEG responses of 4-month old infants to frequency change in tone pairs, presented in two rate conditions (Rapid: 70 msec ISI and Control: 300 msec ISI) were examined. To determine the frequency band and magnitude of activity, auditory evoked response averages were first co-registered with age-appropriate brain templates. Next, the principal components of the response were identified and localized using a two-dipole model of brain activity. Single-trial analysis of oscillatory power showed a robust index of frequency change processing in bursts of Theta band (3 - 8 Hz) activity in both right and left auditory cortices, with left activation more prominent in the Rapid condition. These methods have produced data that are not only some of the first reported evoked oscillations analyses in infants, but are also, importantly, the product of a well-established method of recording and analyzing clean, meticulously collected, infant EEG and ERPs. In this article, we describe our method for infant EEG net application, recording, dynamic brain response analysis, and representative results.

Figures

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References

    1. Gou Z, Choudhury N, Benasich AA. Resting frontal gamma power at 16, 24 and 36 months predicts individual differences in language and cognition at 4 and 5 years. Behavioural brain research. 2011;220:263–270.
    1. Uhlhaas PJ, Roux F, Rodriguez E, Rotarska-Jagiela A, Singer W. Neural synchrony and the development of cortical networks. Trends in cognitive sciences. 2010;14:72–80.
    1. Singer W. Development and plasticity of cortical processing architectures. Science. 1995;270:758–764.
    1. Singer W. Mechanisms of experience dependent self-organization of neuronal assemblies in the mammalian visual system. Archivos de biologia y medicina experimentales. 1983;16:317–327.
    1. Lakatos P, et al. An oscillatory hierarchy controlling neuronal excitability and stimulus processing in the auditory cortex. Journal of neurophysiology. 2005;94:1904–1911.
    1. Jacobs J, Kahana MJ, Ekstrom AD, Fried I. Brain oscillations control timing of single-neuron activity in humans. The Journal of neuroscience. 2007;27:3839–3844.
    1. Schroeder CE, Lakatos P. Low-frequency neuronal oscillations as instruments of sensory selection. Trends Neurosci. 2009;32:9–18.
    1. Schroeder CE, Lakatos P, Kajikawa Y, Partan S, Puce A. Neuronal oscillations and visual amplification of speech. Trends in cognitive sciences. 2008;12:106–113.
    1. Basar E. Oscillations in 'brain-body-mind'-A holistic view including the autonomous system. Brain Res. 2008;1235:2–11.
    1. Buzsaki G. Large-scale recording of neuronal ensembles. Nature. 2004;7:446–451.
    1. Aslin RN. Discrimination of frequency transitions by human infants. The Journal of the Acoustical Society of America. 1989;86:582–590.
    1. Eilers RE, Morse PA, Gavin WJ, Oller DK. Discrimination of voice onset time in infancy. The Journal of the Acoustical Society of America. 1981;70:955–965.
    1. Irwin RJ, Ball AK, Kay N, Stillman JA, Rosser J. The development of auditory temporal acuity in children. Child development. 1985;56:614–620.
    1. Jusczyk PW, Pisoni DB, Walley A, Murray J. Discimination of relative onset time of two-component tones by infants. The Journal of the Acoustical Society of America. 1980;67:262–270.
    1. Bishop DVM, Hardiman MJ, Barry JG. Auditory Deficit as a Consequence Rather than Endophenotype of Specific Language Impairment Electrophysiological Evidence. Plos One. 2012;7:e35851.
    1. Benasich AA, et al. The infant as a prelinguistic model for language learning impairments: Predicting from event-related potentials to behavior. Neuropsychologia. 2006;44:396–411.
    1. Choudhury N, Benasich AA. Maturation of auditory evoked potentials from 6 to 48 months: prediction to 3 and 4 year language and cognitive abilities. Clinical neurophysiology : official journal of the International Federation of Clinical Neurophysiology. 2011;122:320–338.
    1. Lakatos P, et al. Timing of pure tone and noise-evoked responses in macaque auditory cortex. Neuroreport. 2005;16:933–937.
    1. Shah AS, et al. Neural dynamics and the fundamental mechanisms of event-related brain potentials. Cerebral cortex. 2004;14:476–483.
    1. Fries P. A mechanism for cognitive dynamics: neuronal communication through neuronal coherence. Trends Cogn Sci. 2005;9:474–480.
    1. Buzsaki G. Rhythms of the Brain. New York: Oxford University Press; 2006.
    1. Buzsaki G, Draguhn A. Neuronal oscillations in cortical networks. Science. 2004;304:1926–1929.
    1. Whittingstall K, Logothetis NK. Frequency-band coupling in surface EEG reflects spiking activity in monkey visual cortex. Neuron. 2009;64:281–289.
    1. Ortiz-Mantilla S, Hämäläinen JA, Musacchia G, Benasich AA. Enhancement of gamma oscillations indicates preferential processing of native over foreign phonemic contrasts in infants. The Journal of neuroscience : the official journal of the Society for Neuroscience. 2013;33:18746–18754.
    1. Palmer SB, Fais L, Golinkoff RM, Werker JF. Perceptual narrowing of linguistic sign occurs in the 1st year of life. Child. 2012;83:543–553.
    1. Werker JF, Tees RC. Speech perception as a window for understanding plasticity and commitment in language systems of the brain. Dev Psychobiol. 2005;46:233–251.
    1. Benasich AA. Impaired processing of brief, rapidly presented auditory cues in infants with a family history of autoimmune disorder. Developmental neuropsychology. 2002;22:351–372.
    1. Benasich AA, Tallal P. Infant discrimination of rapid auditory cues predicts later language impairment. Behavioural brain research. 2002;136:31–49.
    1. Lopez-Calderon J, Luck SJ. ERPLAB: an open-source toolbox for the analysis of event-related potentials. Front Hum. Neurosci. 2014;8:213.
    1. Delorme A, Sejnowski T, Makeig S. Enhanced detection of artifacts in EEG data using higher-order statistics and independent component analysis. NeuroImage. 2007;34(4):1443–1449.
    1. Hämäläinen JA, Ortiz-Mantilla S, Benasich AA. Source localization of event-related potentials to pitch change mapped onto age-appropriate MRIs at 6 months of age. NeuroImage. 2011;54:1910–1918.
    1. Ortiz-Mantilla S, Hämäläinen JA, Benasich AA. Time course of ERP generators to syllables in infants: A source localization study using age-appropriate brain templates. NeuroImage. 2012;59:3275–3287.
    1. Canolty RT, et al. High gamma power is phase-locked to theta oscillations in human neocortex. Science. 2006;313:1626–1628.
    1. Delorme A, Makeig S. EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. Journal of neuroscience. 2004;134:9–21.
    1. Delorme A, et al. ERICA: new tools for advanced EEG processing. Computational intelligence and neuroscience. 2011;2011:130714.
    1. Makeig S. Auditory event-related dynamics of the EEG spectrum and effects of exposure to tones. Electroencephalography and clinical neurophysiology. 1993;86:283–293.
    1. Hoechstetter K, et al. BESA source coherence: a new method to study cortical oscillatory coupling. Brain topography. 2004;16:233–238.
    1. Papp N, Ktonas P. Critical evaluation of complex demodulation techniques for the quantification of bioelectrical activity. Biomedical sciences instrumentation. 1977;13:135–145.
    1. Yoon H, Yeom W, Kang S, Hong J, Park K. A multiple phase demodulation method for high resolution of the laser scanner. The Review of scientific instruments. 2009;80:056106.
    1. Wang Z, Maier A, Leopold DA, Logothetis NK, Liang H. Single-trial evoked potential estimation using wavelets. Comput Biol Med. 2007;37(4):463–473.
    1. Kramer MA, Tort AB, Kopell NJ. Sharp edge artifacts and spurious coupling in EEG frequency comodulation measures. J Neurosci Methods. 2008;170(2):352–357.
    1. Kriegeskorte N, Simmons WK, Bellgowan PS, Baker CI. Circular analysis in systems neuroscience: the dangers of double dipping. Nat Neurosci. 2009;12(5):535–540.
    1. Musacchia G, et al. Oscillatory support for rapid frequency change processing in infants. Neuropsychologia. 2013;51:2812–2824.
    1. Boer T, Scott LS, Nelson CA. In: Infant EEG and Event-Related Potentials.Studies in Developmental Psychology. Hann M, editor. Washington D.C: Psychology Press; 2007. pp. 5–39.
    1. Basar E, Schurmann M, Demiralp T, Basar-Eroglu C, Ademoglu A. Event-related oscillations are 'real brain responses' - wavelet analysis and new strategies. Int J Psychophysiol. 2001;39:91–127.

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