Auditory Evoked Responses in Musicians during Passive Vowel Listening Are Modulated by Functional Connectivity between Bilateral Auditory-related Brain Regions

Currently, there is striking evidence showing that professional musical training can substantially alter the response properties of auditory-related cortical fields. Such plastic changes have previously been shown not only to abet the processing of musical sounds, but likewise spectral and temporal aspects of speech. Therefore, here we used the EEG technique and measured a sample of musicians and nonmusicians while the participants were passively exposed to artificial vowels in the context of an oddball paradigm. Thereby, we evaluated whether increased intracerebral functional connectivity between bilateral auditory-related brain regions may promote sensory specialization in musicians, as reflected by altered cortical N1 and P2 responses. This assumption builds on the reasoning that sensory specialization is dependent, at least in part, on the amount of synchronization between the two auditory-related cortices. Results clearly revealed that auditory-evoked N1 responses were shaped by musical expertise. In addition, in line with our reasoning musicians showed an overall increased intracerebral functional connectivity (as indexed by lagged phase synchronization) in theta, alpha, and beta bands. Finally, within-group correlative analyses indicated a relationship between intracerebral beta band connectivity and cortical N1 responses, however only within the musicians' group. Taken together, we provide first electrophysiological evidence for a relationship between musical expertise, auditory-evoked brain responses, and intracerebral functional connectivity among auditory-related brain regions.

[1]  H. Wimmer,et al.  Theta band power changes in normal and dyslexic children , 2001, Clinical Neurophysiology.

[2]  P. Hagoort,et al.  Event-related theta power increases in the human EEG during online sentence processing , 2002, Neuroscience Letters.

[3]  G. D. Rosen,et al.  Interhemispheric connections differ between symmetrical and asymmetrical brain regions , 1989, Neuroscience.

[4]  M. Besson,et al.  Twelve Months of Active Musical Training in 8- to 10-Year-Old Children Enhances the Preattentive Processing of Syllabic Duration and Voice Onset Time , 2014 .

[5]  M. Fuchs,et al.  A standardized boundary element method volume conductor model , 2002, Clinical Neurophysiology.

[6]  L. Jäncke,et al.  Interhemispheric transcallosal connectivity between the left and right planum temporale predicts musicianship, performance in temporal speech processing, and functional specialization , 2014, Brain Structure and Function.

[7]  K. Hong,et al.  Lateralization of music processing with noises in the auditory cortex: an fNIRS study , 2014, Front. Behav. Neurosci..

[8]  Alan C. Evans,et al.  Neuroanatomical correlates of musicianship as revealed by cortical thickness and voxel-based morphometry. , 2009, Cerebral cortex.

[9]  B. Ross,et al.  COGNITIVE NEUROSCIENCE AND NEUROPSYCHOLOGY: Timbre-specific enhancement of auditory cortical representations in musicians , 2022 .

[10]  Lutz Jäncke,et al.  The encoding of vowels and temporal speech cues in the auditory cortex of professional musicians: An EEG study , 2013, Neuropsychologia.

[11]  Rolando J. Biscay-Lirio,et al.  Assessing interactions in the brain with exact low-resolution electromagnetic tomography , 2011, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[12]  Roger D. Traub,et al.  Self-Organized Synaptic Plasticity Contributes to the Shaping of γ and β Oscillations In Vitro , 2001, The Journal of Neuroscience.

[13]  Lutz Jäncke,et al.  Enhancement of Auditory-evoked Potentials in Musicians Reflects an Influence of Expertise but not Selective Attention , 2008, Journal of Cognitive Neuroscience.

[14]  E. Seifritz,et al.  Psilocybin-induced spiritual experiences and insightfulness are associated with synchronization of neuronal oscillations , 2015, Psychopharmacology.

[15]  C. Pantev.  Evoked and induced gamma-band activity of the human cortex , 2005, Brain Topography.

[16]  M. Sams,et al.  Musicians have enhanced subcortical auditory and audiovisual processing of speech and music , 2007, Proceedings of the National Academy of Sciences.

[17]  J. Martinerie,et al.  The brainweb: Phase synchronization and large-scale integration , 2001, Nature Reviews Neuroscience.

[18]  Dietrich Lehmann,et al.  Coherence and phase locking in the scalp EEG and between LORETA model sources, and microstates as putative mechanisms of brain temporo-spatial functional organization , 2006, Journal of Physiology-Paris.

[19]  W. Ritter,et al.  The sources of auditory evoked responses recorded from the human scalp. , 1970, Electroencephalography and clinical neurophysiology.

[20]  R. Näätänen,et al.  The mismatch negativity (MMN): towards the optimal paradigm , 2004, Clinical Neurophysiology.

[21]  A. Galaburda,et al.  Individual variability in cortical organization: Its relationship to brain laterality and implications to function , 1990, Neuropsychologia.

[22]  Roberto D. Pascual-Marqui,et al.  Discrete, 3D distributed, linear imaging methods of electric neuronal activity. Part 1: exact, zero error localization , 2007, 0710.3341.

[23]  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.

[24]  Lutz Jäncke,et al.  Electrical brain imaging reveals spatio-temporal dynamics of timbre perception in humans , 2006, NeuroImage.

[25]  Claude Alain,et al.  Perceptual learning modulates sensory evoked response during vowel segregation. , 2003, Brain research. Cognitive brain research.

[26]  W. Klimesch,et al.  EEG alpha oscillations: The inhibition–timing hypothesis , 2007, Brain Research Reviews.

[27]  K. Wehrmann,et al.  Transfer of Training , 2002, Journal of health & social policy.

[28]  M. Scherg,et al.  Morphology of Heschl's gyrus reflects enhanced activation in the auditory cortex of musicians , 2002, Nature Neuroscience.

[29]  R. Pascual-Marqui,et al.  Resting-State EEG Source Localization and Functional Connectivity in Schizophrenia-Like Psychosis of Epilepsy , 2011, PloS one.

[30]  David C. Alsop,et al.  Differentiating maturational and training influences on fMRI activation during music processing , 2012, NeuroImage.

[31]  Joachim Lange,et al.  Audio–visual congruency alters power and coherence of oscillatory activity within and between cortical areas , 2013, NeuroImage.

[32]  André Brechmann,et al.  Hemispheric shifts of sound representation in auditory cortex with conceptual listening. , 2005, Cerebral cortex.

[33]  M. Whittington,et al.  Gamma and beta frequency oscillations in response to novel auditory stimuli: A comparison of human electroencephalogram (EEG) data with in vitro models. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[34]  Lutz Jäncke,et al.  Increased cortical surface area of the left planum temporale in musicians facilitates the categorization of phonetic and temporal speech sounds , 2013, Cortex.

[35]  Antoine J. Shahin,et al.  Enhancement of Neuroplastic P2 and N1c Auditory Evoked Potentials in Musicians , 2003, The Journal of Neuroscience.

[36]  D. Poeppel,et al.  The cortical organization of speech processing , 2007, Nature Reviews Neuroscience.

[37]  M. Besson,et al.  Musical training influences linguistic abilities in 8-year-old children: more evidence for brain plasticity. , 2009, Cerebral cortex.

[38]  Lutz Jäncke,et al.  Processing of Voiced and Unvoiced Acoustic Stimuli in Musicians , 2011, Front. Psychology.

[39]  J Mazziotta,et al.  A probabilistic atlas and reference system for the human brain: International Consortium for Brain Mapping (ICBM). , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[40]  L. Jäncke,et al.  Intracerebral functional connectivity-guided neurofeedback as a putative rehabilitative intervention for ameliorating auditory-related dysfunctions , 2014, Front. Psychol..

[41]  Lutz Jäncke,et al.  Musicianship Boosts Perceptual Learning of Pseudoword-Chimeras: An Electrophysiological Approach , 2012, Brain Topography.

[42]  Richard S. J. Frackowiak,et al.  Endogenous Cortical Rhythms Determine Cerebral Specialization for Speech Perception and Production , 2007, Neuron.

[43]  W. Klimesch,et al.  What does phase information of oscillatory brain activity tell us about cognitive processes? , 2008, Neuroscience & Biobehavioral Reviews.

[44]  J. Staiger,et al.  Increased corpus callosum size in musicians , 1995, Neuropsychologia.

[45]  T. Sejnowski,et al.  Removal of eye activity artifacts from visual event-related potentials in normal and clinical subjects , 2000, Clinical Neurophysiology.

[46]  H. Pratt,et al.  High-resolution time course of hemispheric dominance revealed by low-resolution electromagnetic tomography , 2003, Clinical Neurophysiology.

[47]  Changle Zhou,et al.  Graph theoretical analysis of EEG functional connectivity during music perception , 2012, Brain Research.

[48]  R. Oostenveld,et al.  Neuronal Dynamics Underlying High- and Low-Frequency EEG Oscillations Contribute Independently to the Human BOLD Signal , 2011, Neuron.

[49]  W. Singer,et al.  Dynamic predictions: Oscillations and synchrony in top–down processing , 2001, Nature Reviews Neuroscience.

[50]  M. Scherg,et al.  Structural and functional asymmetry of lateral Heschl's gyrus reflects pitch perception preference , 2005, Nature Neuroscience.

[51]  N. Weisz,et al.  Prestimulus beta power and phase synchrony influence the sound-induced flash illusion. , 2014, Cerebral cortex.

[52]  Robert J. Zatorre,et al.  Musical Training as a Framework for Brain Plasticity: Behavior, Function, and Structure , 2012, Neuron.

[53]  Giancarlo Valente,et al.  Dynamic and Task-Dependent Encoding of Speech and Voice by Phase Reorganization of Cortical Oscillations , 2009, The Journal of Neuroscience.

[54]  Yung-Yang Lin,et al.  Theta oscillation during auditory change detection: An MEG study , 2009, Biological Psychology.

[55]  C. Im,et al.  Theta Oscillation Related to the Auditory Discrimination Process in Mismatch Negativity: Oddball versus Control Paradigm , 2012, Journal of clinical neurology.

[56]  G. Bidelman,et al.  Examining neural plasticity and cognitive benefit through the unique lens of musical training , 2014, Hearing Research.

[57]  H. Petsche,et al.  Synchronization between prefrontal and posterior association cortex during human working memory. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[58]  David Poeppel,et al.  Cortical oscillations and speech processing: emerging computational principles and operations , 2012, Nature Neuroscience.

[59]  R. Traub,et al.  Self-organized synaptic plasticity contributes to the shaping of gamma and beta oscillations in vitro. , 2001, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[60]  Bernd Lütkenhöner,et al.  Piano tones evoke stronger magnetic fields than pure tones or noise, both in musicians and non-musicians , 2006, NeuroImage.

[61]  Mireille Besson,et al.  Musical and linguistic expertise influence pre-attentive and attentive processing of non-speech sounds , 2012, Cortex.

[62]  Jae-Jin Song,et al.  Tinnitus and musical hallucinosis: The same but more , 2013, NeuroImage.

[63]  M. Besson,et al.  Transfer of Training between Music and Speech: Common Processing, Attention, and Memory , 2011, Front. Psychology.

[64]  Peter Brown,et al.  Cortico-cortical coupling patterns during dual task performance , 2004, Experimental Brain Research.

[65]  E. Schellenberg,et al.  Short-Term Music Training Enhances Verbal Intelligence and Executive Function , 2011, Psychological science.

[66]  Ana P. Pinheiro,et al.  The music of language: An ERP investigation of the effects of musical training on emotional prosody processing , 2015, Brain and Language.

[67]  Marta Olivetti Belardinelli,et al.  Influence of Musical Expertise on Segmental and Tonal Processing in Mandarin Chinese , 2011, Journal of Cognitive Neuroscience.

[68]  S. Kuriki,et al.  Effects of Musical Experience on Different Components of MEG Responses Elicited by Sequential Piano-Tones and Chords , 2006, The Journal of Neuroscience.

[69]  G. Schlaug,et al.  In vivo evidence of structural brain asymmetry in musicians , 1995, Science.

[70]  T. Womelsdorf,et al.  The role of neuronal synchronization in selective attention , 2007, Current Opinion in Neurobiology.

[71]  Mireille Besson,et al.  Musicians and the Metric Structure of Words , 2011, Journal of Cognitive Neuroscience.

[72]  Mari Tervaniemi,et al.  Music Training Enhances Rapid Neural Plasticity of N1 and P2 Source Activation for Unattended Sounds , 2012, Front. Hum. Neurosci..

[73]  D. Bosnyak,et al.  Distributed auditory cortical representations are modified when non-musicians are trained at pitch discrimination with 40 Hz amplitude modulated tones. , 2004, Cerebral cortex.

[74]  R. Oostenveld,et al.  Increased auditory cortical representation in musicians , 1998, Nature.

[75]  D. Poeppel,et al.  Phase Patterns of Neuronal Responses Reliably Discriminate Speech in Human Auditory Cortex , 2007, Neuron.

[76]  Lutz Jäncke,et al.  Music and Language Expertise Influence the Categorization of Speech and Musical Sounds: Behavioral and Electrophysiological Measurements , 2014, Journal of Cognitive Neuroscience.

[77]  Nina Kraus,et al.  Biological impact of auditory expertise across the life span: Musicians as a model of auditory learning , 2014, Hearing Research.

[78]  Alan C. Evans,et al.  The Effects of Musical Training on Structural Brain Development , 2009, Annals of the New York Academy of Sciences.

[79]  Lutz Jäncke,et al.  Neurofunctional and behavioral correlates of phonetic and temporal categorization in musically trained and untrained subjects. , 2012, Cerebral cortex.