Short-term Music Training Enhances Complex, Distributed Neural Communication during Music and Linguistic Tasks

Musical training is frequently associated with benefits to linguistic abilities, and recent focus has been placed on possible benefits of bilingualism to lifelong executive functions; however, the neural mechanisms for such effects are unclear. The aim of this study was to gain better understanding of the whole-brain functional effects of music and second-language training that could support such previously observed cognitive transfer effects. We conducted a 28-day longitudinal study of monolingual English-speaking 4- to 6-year-old children randomly selected to receive daily music or French language training, excluding weekends. Children completed passive EEG music note and French vowel auditory oddball detection tasks before and after training. Brain signal complexity was measured on source waveforms at multiple temporal scales as an index of neural information processing and network communication load. Comparing pretraining with posttraining, musical training was associated with increased EEG complexity at coarse temporal scales during the music and French vowel tasks in widely distributed cortical regions. Conversely, very minimal decreases in complexity at fine scales and trends toward coarse-scale increases were displayed after French training during the tasks. Spectral analysis failed to distinguish between training types and found overall theta (3.5–7.5 Hz) power increases after all training forms, with spatially fewer decreases in power at higher frequencies (>10 Hz). These findings demonstrate that musical training increased diversity of brain network states to support domain-specific music skill acquisition and music-to-language transfer effects.

[1]  D. Schön,et al.  Musician Children Detect Pitch Violations in Both Music and Language Better than Nonmusician Children: Behavioral and Electrophysiological Approaches , 2006 .

[2]  Madalena Costa,et al.  Multiscale entropy analysis of complex physiologic time series. , 2002, Physical review letters.

[3]  L. Aftanas,et al.  Human anterior and frontal midline theta and lower alpha reflect emotionally positive state and internalized attention: high-resolution EEG investigation of meditation , 2001, Neuroscience Letters.

[4]  Anthony Randal McIntosh,et al.  Partial least squares analysis of neuroimaging data: applications and advances , 2004, NeuroImage.

[5]  L. Trainor,et al.  Cortical Plasticity in 4-Month-Old Infants: Specific Effects of Experience with Musical Timbres , 2011, Brain Topography.

[6]  Sylvain Moreno Can Music Influence Language and Cognition? , 2009 .

[7]  L. Trainor,et al.  Associations Between Length of Music Training and Reading Skills in Children , 2011 .

[8]  W. Klimesch EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis , 1999, Brain Research Reviews.

[9]  Anthony Randal McIntosh,et al.  Relating brain signal variability to knowledge representation , 2012, NeuroImage.

[10]  A. Meltzoff,et al.  Bilingual experience and executive functioning in young children. , 2008, Developmental science.

[11]  F. Craik,et al.  Bilingual Minds , 2009, Psychological science in the public interest : a journal of the American Psychological Society.

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

[13]  M. Cheung,et al.  Music training improves verbal memory , 1998, Nature.

[14]  Robert Tibshirani,et al.  Bootstrap Methods for Standard Errors, Confidence Intervals, and Other Measures of Statistical Accuracy , 1986 .

[15]  N. Kraus,et al.  Music training for the development of auditory skills , 2010, Nature Reviews Neuroscience.

[16]  I. Johnsrude,et al.  Spectral and temporal processing in human auditory cortex. , 2002, Cerebral cortex.

[17]  Robert J. Zatorre,et al.  Neural networks involved in voluntary and involuntary vocal pitch regulation in experienced singers , 2010, Neuropsychologia.

[18]  A. von Stein,et al.  Different frequencies for different scales of cortical integration: from local gamma to long range alpha/theta synchronization. , 2000, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[19]  Gavin M. Bidelman,et al.  Brain signal variability as a window into the bidirectionality between music and language processing: moving from a linear to a nonlinear model , 2013, Front. Psychol..

[20]  E. Altenmüller,et al.  The musician's brain as a model of neuroplasticity , 2002, Nature Reviews Neuroscience.

[21]  Jason D. Zevin,et al.  The neural basis of non-native speech perception in bilingual children , 2013, NeuroImage.

[22]  Anthony R. McIntosh,et al.  Coordinated Information Generation and Mental Flexibility: Large-Scale Network Disruption in Children with Autism , 2014, Cerebral cortex.

[23]  I. Nelken,et al.  Modeling the auditory scene: predictive regularity representations and perceptual objects , 2009, Trends in Cognitive Sciences.

[24]  M. Freedman,et al.  Bilingualism as a protection against the onset of symptoms of dementia , 2007, Neuropsychologia.

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

[26]  E. Bialystok,et al.  Short-term second language and music training induces lasting functional brain changes in early childhood. , 2015, Child development.

[27]  Luc H. Arnal,et al.  Asymmetric Function of Theta and Gamma Activity in Syllable Processing: An Intra-Cortical Study , 2012, Front. Psychology.

[28]  A. McIntosh,et al.  The co-occurrence of multisensory facilitation and cross-modal conflict in the human brain. , 2011, Journal of neurophysiology.

[29]  O. Sporns,et al.  Rich-Club Organization of the Human Connectome , 2011, The Journal of Neuroscience.

[30]  V. Schmithorst,et al.  A longitudinal functional magnetic resonance imaging study of language development in children 5 to 11 years old , 2006, Annals of neurology.

[31]  D. Green,et al.  Control mechanisms in bilingual language production: Neural evidence from language switching studies , 2008 .

[32]  C. Price The anatomy of language: a review of 100 fMRI studies published in 2009 , 2010, Annals of the New York Academy of Sciences.

[33]  Margot J. Taylor,et al.  Brain noise is task dependent and region specific. , 2010, Journal of neurophysiology.

[34]  Stefan Koelsch,et al.  Musical training modulates the development of syntax processing in children , 2009, NeuroImage.

[35]  R D Pascual-Marqui,et al.  Standardized low-resolution brain electromagnetic tomography (sLORETA): technical details. , 2002, Methods and findings in experimental and clinical pharmacology.

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

[37]  Gorka Zamora-López,et al.  Cortical Hubs Form a Module for Multisensory Integration on Top of the Hierarchy of Cortical Networks , 2009, Front. Neuroinform..

[38]  Annemarie Seither-Preisler,et al.  Size and Synchronization of Auditory Cortex Promotes Musical, Literacy, and Attentional Skills in Children , 2014, The Journal of Neuroscience.

[39]  Albert Costa,et al.  Bilingualism aids conflict resolution: Evidence from the ANT task , 2008, Cognition.

[40]  Madalena Costa,et al.  Multiscale entropy analysis of biological signals. , 2005, Physical review. E, Statistical, nonlinear, and soft matter physics.

[41]  F. Rauscher,et al.  Music and spatial task performance , 1993, Nature.

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

[43]  Robert Oostenveld,et al.  The five percent electrode system for high-resolution EEG and ERP measurements , 2001, Clinical Neurophysiology.

[44]  Richard M. Leahy,et al.  Brainstorm: A User-Friendly Application for MEG/EEG Analysis , 2011, Comput. Intell. Neurosci..

[45]  Alan C. Evans,et al.  Neural mechanisms underlying melodic perception and memory for pitch , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[46]  R. Zatorre,et al.  A role for the intraparietal sulcus in transforming musical pitch information. , 2010, Cerebral cortex.

[47]  E. Glenn Schellenberg,et al.  Cognitive Performance After Listening to Music: A Review of the Mozart Effect , 2012 .

[48]  Chung-Kang Peng,et al.  Costa, Goldberger, and Peng Reply: , 2003 .

[49]  J. V. Haxby,et al.  Spatial Pattern Analysis of Functional Brain Images Using Partial Least Squares , 1996, NeuroImage.

[50]  Jessica A. Grahn,et al.  Putting brain training to the test , 2010, Nature.

[51]  E. Schellenberg,et al.  Music Lessons Enhance IQ , 2004, Psychological science.

[52]  F. Bookstein,et al.  Neurobehavioral effects of prenatal alcohol: Part II. Partial least squares analysis. , 1989, Neurotoxicology and teratology.

[53]  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.

[54]  Aniruddh D. Patel,et al.  Language, music, syntax and the brain , 2003, Nature Neuroscience.

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

[56]  G. Edelman,et al.  A measure for brain complexity: relating functional segregation and integration in the nervous system. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[57]  O. Sporns,et al.  Mapping the Structural Core of Human Cerebral Cortex , 2008, PLoS biology.

[58]  J. Richman,et al.  Physiological time-series analysis using approximate entropy and sample entropy. , 2000, American journal of physiology. Heart and circulatory physiology.

[59]  G. Deco,et al.  Emerging concepts for the dynamical organization of resting-state activity in the brain , 2010, Nature Reviews Neuroscience.

[60]  Natasa Kovacevic,et al.  Increased Brain Signal Variability Accompanies Lower Behavioral Variability in Development , 2008, PLoS Comput. Biol..

[61]  Viktor K. Jirsa,et al.  Noise during Rest Enables the Exploration of the Brain's Dynamic Repertoire , 2008, PLoS Comput. Biol..

[62]  Vesa Välimäki,et al.  Musical aptitude and second language pronunciation skills in school-aged children: Neural and behavioral evidence , 2008, Brain Research.

[63]  David Poeppel,et al.  The analysis of speech in different temporal integration windows: cerebral lateralization as 'asymmetric sampling in time' , 2003, Speech Commun..

[64]  P. Nunez,et al.  Spatial‐temporal structures of human alpha rhythms: Theory, microcurrent sources, multiscale measurements, and global binding of local networks , 2001, Human brain mapping.

[65]  Olaf Sporns,et al.  Network structure of cerebral cortex shapes functional connectivity on multiple time scales , 2007, Proceedings of the National Academy of Sciences.

[66]  R. Zatorre,et al.  Structure and function of auditory cortex: music and speech , 2002, Trends in Cognitive Sciences.

[67]  J. Kelso,et al.  Cortical coordination dynamics and cognition , 2001, Trends in Cognitive Sciences.

[68]  T. Klingberg,et al.  Increased prefrontal and parietal activity after training of working memory , 2004, Nature Neuroscience.

[69]  Vasily A. Vakorin,et al.  Variability of Brain Signals Processed Locally Transforms into Higher Connectivity with Brain Development , 2011, Journal of Neuroscience.

[70]  Egon Wanke,et al.  Mapping brains without coordinates , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[71]  Natasa Kovacevic,et al.  Brain signal variability relates to stability of behavior after recovery from diffuse brain injury , 2012, NeuroImage.

[72]  Jubin Abutalebi,et al.  The neural basis of first and second language processing , 2005, Current Opinion in Neurobiology.

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

[74]  S. Baron-Cohen,et al.  Atypical EEG complexity in autism spectrum conditions: A multiscale entropy analysis , 2011, Clinical Neurophysiology.