Neuro-oscillatory tracking of low- and high-level musico-acoustic features during naturalistic music listening: Insights from an intracranial electroencephalography study.

Studies investigating the neural processing of musico-acoustic features have tended to do so using highly controlled musical stimuli. However, it is increasingly argued that failing to use naturalistic stimuli limits the extent to which findings from lab studies can be extrapolated to rich and varied real-world experiences. Here, we recorded electrical brain activity from 8 epileptic patients, implanted for pre-surgical evaluation with Stereo-encephalography (SEEG), while they listened to pieces from the western tonal music repertoire. We estimated the sound intensity and key and pulse clarity of the stimuli using a toolbox for automatic extraction of musico-acoustic features. We then used partial-correlation analyses to examine the patterns of neuro-oscillatory activity associated with the processing of these features. Our results showed clear tracking of sound intensity in high-gamma and alpha frequency bands in posterior superior temporal gyrus, reflecting neural firing and the transfer of auditory information from the thalamus to auditory cortices, respectively. Patterns of partial correlations, in line with our hypotheses, also suggested limbic and inferior frontal cortical tracking of tonal and rhythmic uncertainty, albeit without the robustness shown for sound intensity tracking in auditory areas. The study provides an important contribution to the existing literature in its adherence to the call for a greater use of ecologically valid stimuli in neuroscientific investigations of music listening. Our results, specifically, have implications for research on the neural processing of musical uncertainty and for future studies seeking to use intracranial EEG to examine naturalistic music processing.

[1]  Leonard B. Meyer Emotion and Meaning in Music , 1957 .

[2]  F. D. da Silva,et al.  Organization of thalamic and cortical alpha rhythms: spectra and coherences. , 1973, Electroencephalography and clinical neurophysiology.

[3]  Ray Jackendoff,et al.  An overview of hierarchical structure in music , 1983 .

[4]  M. R. Jones,et al.  Dynamic attending and responses to time. , 1989, Psychological review.

[5]  W. Fries,et al.  Disturbance of rhythm sense following right hemisphere damage , 1990, Neuropsychologia.

[6]  Eugene Narmour,et al.  The Analysis and Cognition of Basic Melodic Structures: The Implication-Realization Model , 1990 .

[7]  James Theiler,et al.  Testing for nonlinearity in time series: the method of surrogate data , 1992 .

[8]  M. Besson,et al.  AN EVENT-RELATED POTENTIAL (ERP) STUDY OF MUSICAL EXPECTANCY : COMPARISON OF MUSICIANS WITH NONMUSICIANS , 1995 .

[9]  Peter Q. Pfordresher,et al.  Tracking Musical Patterns using Joint Accent Structure , 1997 .

[10]  D. Harrington,et al.  Temporal processing in the basal ganglia. , 1998, Neuropsychology.

[11]  F. L. D. Silva,et al.  Event-related EEG/MEG synchronization and desynchronization: basic principles , 1999, Clinical Neurophysiology.

[12]  Alan C. Evans,et al.  Emotional responses to pleasant and unpleasant music correlate with activity in paralimbic brain regions , 1999, Nature Neuroscience.

[13]  R. Burkard,et al.  The functional anatomy of the normal human auditory system: responses to 0.5 and 4.0 kHz tones at varied intensities. , 1999, Cerebral cortex.

[14]  E. Large,et al.  The dynamics of attending: How people track time-varying events. , 1999 .

[15]  A. Friederici,et al.  Time Perception and Motor Timing: A Common Cortical and Subcortical Basis Revealed by fMRI , 2000, NeuroImage.

[16]  A. Friederici,et al.  Musical syntax is processed in Broca's area: an MEG study , 2001, Nature Neuroscience.

[17]  A. Lehmann,et al.  Tracking Performance Correlates of Changes in Perceived Intensity of Emotion During Different Interpretations of a Chopin Piano Prelude , 2001 .

[18]  A. Friederici,et al.  Differentiating ERAN and MMN: An ERP study , 2001, Neuroreport.

[19]  Stephen M. Rao,et al.  The evolution of brain activation during temporal processing , 2001, Nature Neuroscience.

[20]  H. Critchley,et al.  Neural Activity in the Human Brain Relating to Uncertainty and Arousal during Anticipation , 2001, Neuron.

[21]  Marc Leman,et al.  The Cortical Topography of Tonal Structures Underlying Western Music , 2002, Science.

[22]  M. Jones,et al.  Temporal Aspects of Stimulus-Driven Attending in Dynamic Arrays , 2002, Psychological science.

[23]  D. V. Cramon,et al.  Predicting Perceptual Events Activates Corresponding Motor Schemes in Lateral Premotor Cortex: An fMRI Study , 2002, NeuroImage.

[24]  E. Schröger,et al.  Preattentive Memory-Based Comparison of Sound Intensity , 2003, Audiology and Neurotology.

[25]  C. Krumhansl,et al.  Measuring and Modeling Real-Time Responses to Music: The Dynamics of Tonality Induction , 2003, Perception.

[26]  T. Shallice,et al.  Human cingulate cortex and autonomic control: converging neuroimaging and clinical evidence. , 2003, Brain : a journal of neurology.

[27]  R. Malach,et al.  Intersubject Synchronization of Cortical Activity During Natural Vision , 2004, Science.

[28]  A. Schnider,et al.  Receptive amusia: temporal auditory processing deficit in a professional musician following a left temporo-parietal lesion , 2004, Neuropsychologia.

[29]  G. Ojemann,et al.  Neuronal activity in the human lateral temporal lobe , 2004, Experimental Brain Research.

[30]  P. Janata Brain Networks That Track Musical Structure , 2005, Annals of the New York Academy of Sciences.

[31]  Raymond J. Dolan,et al.  Information theory, novelty and hippocampal responses: unpredicted or unpredictable? , 2005, Neural Networks.

[32]  Justyna Humięcka-Jakubowska,et al.  Sweet Anticipation : Music and , 2006 .

[33]  I. Peretz,et al.  Musical scale properties are automatically processed in the human auditory cortex , 2006, Brain Research.

[34]  T. Zanto,et al.  Neural correlates of rhythmic expectancy , 2006 .

[35]  W. Thompson,et al.  A Comparison of Acoustic Cues in Music and Speech for Three Dimensions of Affect , 2006 .

[36]  Robert J. Zatorre,et al.  Interactions between auditory and dorsal premotor cortex during synchronization to musical rhythms , 2006, NeuroImage.

[37]  Stefan Koelsch,et al.  Cognitive priming in sung and instrumental music: Activation of inferior frontal cortex , 2006, NeuroImage.

[38]  Stefan Koelsch,et al.  The Role of Harmonic Expectancy Violations in Musical Emotions: Evidence from Subjective, Physiological, and Neural Responses , 2006, Journal of Cognitive Neuroscience.

[39]  Ingo Fründ,et al.  Stimulus intensity affects early sensory processing: sound intensity modulates auditory evoked gamma-band activity in human EEG. , 2007, International Journal of Psychophysiology.

[40]  M. Grigutsch,et al.  Music and emotion: electrophysiological correlates of the processing of pleasant and unpleasant music. , 2007, Psychophysiology.

[41]  G. Glover,et al.  Dissociable Intrinsic Connectivity Networks for Salience Processing and Executive Control , 2007, The Journal of Neuroscience.

[42]  José Fornari,et al.  Multi-Feature Modeling of Pulse Clarity: Design, Validation and Optimization , 2008, ISMIR.

[43]  C. Schroeder,et al.  Neuronal Mechanisms of Cortical Alpha Oscillations in Awake-Behaving Macaques , 2008, The Journal of Neuroscience.

[44]  D. Västfjäll,et al.  Emotional responses to music: the need to consider underlying mechanisms. , 2008, The Behavioral and brain sciences.

[45]  B. Ross,et al.  Beta and Gamma Rhythms in Human Auditory Cortex during Musical Beat Processing , 2009, Annals of the New York Academy of Sciences.

[46]  J. Devin McAuley,et al.  Neural bases of individual differences in beat perception , 2009, NeuroImage.

[47]  Fred L. Steinberg,et al.  Dynamic Emotional and Neural Responses to Music Depend on Performance Expression and Listener Experience , 2010, PloS one.

[48]  H. Eichenbaum,et al.  Measuring phase-amplitude coupling between neuronal oscillations of different frequencies. , 2010, Journal of neurophysiology.

[49]  T. Jung,et al.  Electroencephalographic dynamics of musical emotion perception revealed by independent spectral components , 2010, Neuroreport.

[50]  K. Miller Broadband Spectral Change: Evidence for a Macroscale Correlate of Population Firing Rate? , 2010, The Journal of Neuroscience.

[51]  Anthony Randal McIntosh,et al.  A common functional brain network for autobiographical, episodic, and semantic memory retrieval , 2010, NeuroImage.

[52]  G. Rauchs,et al.  When Music and Long-Term Memory Interact: Effects of Musical Expertise on Functional and Structural Plasticity in the Hippocampus , 2010, PloS one.

[53]  J. Maunsell,et al.  Different Origins of Gamma Rhythm and High-Gamma Activity in Macaque Visual Cortex , 2011, PLoS biology.

[54]  Robert Oostenveld,et al.  FieldTrip: Open Source Software for Advanced Analysis of MEG, EEG, and Invasive Electrophysiological Data , 2010, Comput. Intell. Neurosci..

[55]  T. Egner,et al.  Emotional processing in anterior cingulate and medial prefrontal cortex , 2011, Trends in Cognitive Sciences.

[56]  V. Menon,et al.  Decoding temporal structure in music and speech relies on shared brain resources but elicits different fine-scale spatial patterns. , 2011, Cerebral cortex.

[57]  R. Romo,et al.  α-Oscillations in the monkey sensorimotor network influence discrimination performance by rhythmical inhibition of neuronal spiking , 2011, Proceedings of the National Academy of Sciences.

[58]  Aniruddh D. Patel,et al.  The impact of basal ganglia lesions on sensorimotor synchronization, spontaneous motor tempo, and the detection of tempo changes , 2011, Behavioural Brain Research.

[59]  Luc H. Arnal,et al.  Cortical oscillations and sensory predictions , 2012, Trends in Cognitive Sciences.

[60]  S. Uppenkamp,et al.  Neural Coding of Sound Intensity and Loudness in the Human Auditory System , 2012, Journal of the Association for Research in Otolaryngology.

[61]  M. Pearce,et al.  Tracking of pitch probabilities in congenital amusia , 2012, Neuropsychologia.

[62]  Rinus G. Verdonschot,et al.  Neural mechanisms underlying the induction and relief of perceptual curiosity , 2012, Front. Behav. Neurosci..

[63]  Milan Sonka,et al.  3D Slicer as an image computing platform for the Quantitative Imaging Network. , 2012, Magnetic resonance imaging.

[64]  Gerwin Schalk,et al.  Dynamics of electrocorticographic (ECoG) activity in human temporal and frontal cortical areas during music listening , 2012, NeuroImage.

[65]  Mikko Sams,et al.  Large-scale brain networks emerge from dynamic processing of musical timbre, key and rhythm , 2012, NeuroImage.

[66]  S. Koelsch,et al.  Predictive information processing in music cognition. A critical review. , 2012, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[67]  Geraint A. Wiggins,et al.  Probabilistic models of expectation violation predict psychophysiological emotional responses to live concert music , 2013, Cognitive, Affective, & Behavioral Neuroscience.

[68]  Jessica A. Grahn,et al.  Finding and Feeling the Musical Beat: Striatal Dissociations between Detection and Prediction of Regularity , 2012, Cerebral cortex.

[69]  Stefan Koelsch,et al.  Co-localizing linguistic and musical syntax with intracranial EEG , 2013, NeuroImage.

[70]  M. Pearce,et al.  Electrophysiological correlates of melodic processing in congenital amusia , 2013, Neuropsychologia.

[71]  Robert T. Knight,et al.  Spatial and temporal relationships of electrocorticographic alpha and gamma activity during auditory processing , 2014, NeuroImage.

[72]  J. Numminen,et al.  Dynamics of brain activity underlying working memory for music in a naturalistic condition , 2014, Cortex.

[73]  G. Curio,et al.  ECoG high gamma activity reveals distinct cortical representations of lyrics passages, harmonic and timbre-related changes in a rock song , 2014, Front. Hum. Neurosci..

[74]  Maria A. G. Witek,et al.  Rhythmic complexity and predictive coding: a novel approach to modeling rhythm and meter perception in music , 2014, Front. Psychol..

[75]  S. Koelsch,et al.  Tension-related activity in the orbitofrontal cortex and amygdala: an fMRI study with music. , 2014, Social cognitive and affective neuroscience.

[76]  S. Koelsch Brain correlates of music-evoked emotions , 2014, Nature Reviews Neuroscience.

[77]  T. Koenig,et al.  Professional musicians listen differently to music , 2014, Neuroscience.

[78]  B. Ross,et al.  Beta-Band Oscillations Represent Auditory Beat and Its Metrical Hierarchy in Perception and Imagery , 2015, The Journal of Neuroscience.

[79]  M. Baulac,et al.  Intracranial markers of emotional valence processing and judgments in music , 2015, Cognitive neuroscience.

[80]  M. Baulac,et al.  An Intracranial EEG Study of the Neural Dynamics of Musical Valence Processing. , 2015, Cerebral cortex.

[81]  James I. Lubell,et al.  Amygdala and Orbitofrontal Engagement in Breach and Resolution of Expectancy: A Case Study , 2015 .

[82]  D. Poeppel,et al.  Cortical entrainment to music and its modulation by expertise , 2015, Proceedings of the National Academy of Sciences.

[83]  Diana Omigie,et al.  Dopamine and epistemic curiosity in music listening , 2015 .

[84]  Jan-Mathijs Schoffelen,et al.  A Tutorial Review of Functional Connectivity Analysis Methods and Their Interpretational Pitfalls , 2016, Front. Syst. Neurosci..

[85]  L. Trainor,et al.  Unpredicted Pitch Modulates Beta Oscillatory Power during Rhythmic Entrainment to a Tone Sequence , 2016, Front. Psychol..

[86]  Elke B Lange,et al.  Challenges and Opportunities of Predicting Musical Emotions with Perceptual and Automatized Features , 2018, Music Perception.

[87]  E. Brattico,et al.  Atonal Music: Can Uncertainty Lead to Pleasure? , 2019, Front. Neurosci..

[88]  Dominique Hasboun,et al.  Intracranial Recordings and Computational Modeling of Music Reveal the Time Course of Prediction Error Signaling in Frontal and Temporal Cortices , 2019, Journal of Cognitive Neuroscience.