Inter‐subject synchronization of brain responses during natural music listening

Music is a cultural universal and a rich part of the human experience. However, little is known about common brain systems that support the processing and integration of extended, naturalistic ‘real‐world’ music stimuli. We examined this question by presenting extended excerpts of symphonic music, and two pseudomusical stimuli in which the temporal and spectral structure of the Natural Music condition were disrupted, to non‐musician participants undergoing functional brain imaging and analysing synchronized spatiotemporal activity patterns between listeners. We found that music synchronizes brain responses across listeners in bilateral auditory midbrain and thalamus, primary auditory and auditory association cortex, right‐lateralized structures in frontal and parietal cortex, and motor planning regions of the brain. These effects were greater for natural music compared to the pseudo‐musical control conditions. Remarkably, inter‐subject synchronization in the inferior colliculus and medial geniculate nucleus was also greater for the natural music condition, indicating that synchronization at these early stages of auditory processing is not simply driven by spectro‐temporal features of the stimulus. Increased synchronization during music listening was also evident in a right‐hemisphere fronto‐parietal attention network and bilateral cortical regions involved in motor planning. While these brain structures have previously been implicated in various aspects of musical processing, our results are the first to show that these regions track structural elements of a musical stimulus over extended time periods lasting minutes. Our results show that a hierarchical distributed network is synchronized between individuals during the processing of extended musical sequences, and provide new insight into the temporal integration of complex and biologically salient auditory sequences.

[1]  M M Merzenich,et al.  Representation of a species-specific vocalization in the primary auditory cortex of the common marmoset: temporal and spectral characteristics. , 1995, Journal of neurophysiology.

[2]  S. Koelsch Neural substrates of processing syntax and semantics in music , 2005, Current Opinion in Neurobiology.

[3]  D. Poeppel,et al.  Stimulus context affects auditory cortical responses to changes in interaural correlation. , 2007, Journal of neurophysiology.

[4]  Gianluca Valenti D. J. Levitin, The World in Six Songs, Dutton/Penguin, New York 2008 , 2010 .

[5]  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.

[6]  T. Picton,et al.  Human Cortical Responses to the Speech Envelope , 2008, Ear and hearing.

[7]  Theiler,et al.  Generating surrogate data for time series with several simultaneously measured variables. , 1994, Physical review letters.

[8]  Jonathan Berger,et al.  Neural Dynamics of Event Segmentation in Music: Converging Evidence for Dissociable Ventral and Dorsal Networks , 2007, Neuron.

[9]  Katrin Amunts,et al.  The human inferior parietal cortex: Cytoarchitectonic parcellation and interindividual variability , 2006, NeuroImage.

[10]  N. Kraus,et al.  Context-Dependent Encoding in the Human Auditory Brainstem Relates to Hearing Speech in Noise: Implications for Developmental Dyslexia , 2009, Neuron.

[11]  Thomas E. Nichols,et al.  Nonparametric permutation tests for functional neuroimaging: A primer with examples , 2002, Human brain mapping.

[12]  N. Kraus,et al.  Reversal of age-related neural timing delays with training , 2013, Proceedings of the National Academy of Sciences.

[13]  Henning Scheich,et al.  Left Auditory Cortex Specialization for Vertical Harmonic Structure of Chords , 2005, Annals of the New York Academy of Sciences.

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

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

[16]  Timothy D. Griffiths,et al.  Orthogonal representation of sound dimensions in the primate midbrain , 2011, Nature Neuroscience.

[17]  S. Scott,et al.  Positive Emotions Preferentially Engage an Auditory–Motor “Mirror” System , 2006, The Journal of Neuroscience.

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

[19]  C. Schreiner,et al.  Thalamocortical transformation of responses to complex auditory stimuli , 2004, Experimental Brain Research.

[20]  C. Schreiner,et al.  Periodicity coding in the inferior colliculus of the cat. I. Neuronal mechanisms. , 1988, Journal of neurophysiology.

[21]  Aniruddh D. Patel,et al.  Human pitch perception is reflected in the timing of stimulus-related cortical activity , 2001, Nature Neuroscience.

[22]  C. Torrence,et al.  A Practical Guide to Wavelet Analysis. , 1998 .

[23]  Jessica A. Grahn,et al.  Feeling the Beat: Premotor and Striatal Interactions in Musicians and Nonmusicians during Beat Perception , 2009, The Journal of Neuroscience.

[24]  Istvan Molnar-Szakacs,et al.  Beyond superior temporal cortex: intersubject correlations in narrative speech comprehension. , 2008, Cerebral cortex.

[25]  C E Schreiner,et al.  Neural processing of amplitude-modulated sounds. , 2004, Physiological reviews.

[26]  J. Rauschecker,et al.  Brain Activation during Anticipation of Sound Sequences , 2009, The Journal of Neuroscience.

[27]  S. Scott,et al.  Identification of a pathway for intelligible speech in the left temporal lobe. , 2000, Brain : a journal of neurology.

[28]  D. Heeger,et al.  Reliability of cortical activity during natural stimulation , 2010, Trends in Cognitive Sciences.

[29]  D. Abrams,et al.  Abnormal Cortical Processing of the Syllable Rate of Speech in Poor Readers , 2009, The Journal of Neuroscience.

[30]  Evan Balaban,et al.  Multivariate activation and connectivity patterns discriminate speech intelligibility in Wernicke's, Broca's, and Geschwind's areas. , 2013, Cerebral cortex.

[31]  J. Kaas,et al.  Subdivisions of auditory cortex and processing streams in primates. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[32]  D. Abrams,et al.  Right-Hemisphere Auditory Cortex Is Dominant for Coding Syllable Patterns in Speech , 2008, The Journal of Neuroscience.

[33]  E. Dissanayake,et al.  "The World in Six Songs: How the Musical Brain Created Human Nature" , 2011 .

[34]  Pascal Belin,et al.  Is voice processing species-specific in human auditory cortex? An fMRI study , 2004, NeuroImage.

[35]  Erika Skoe,et al.  Plasticity in the Adult Human Auditory Brainstem following Short-term Linguistic Training , 2008, Journal of Cognitive Neuroscience.

[36]  E Ahissar,et al.  Speech comprehension is correlated with temporal response patterns recorded from auditory cortex , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[37]  William A. Sethares,et al.  Rhythm and Transforms , 2007 .

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

[39]  A. Boemio,et al.  Hierarchical and asymmetric temporal sensitivity in human auditory cortices , 2005, Nature Neuroscience.

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

[41]  C. Rorden,et al.  Stereotaxic display of brain lesions. , 2000, Behavioural neurology.

[42]  R. Patterson,et al.  Encoding of the temporal regularity of sound in the human brainstem , 2001, Nature Neuroscience.

[43]  Clara E. James,et al.  Degree of musical expertise modulates higher order brain functioning. , 2013, Cerebral cortex.

[44]  C. Schreiner,et al.  Representation of spectral and temporal envelope of twitter vocalizations in common marmoset primary auditory cortex. , 2002, Journal of neurophysiology.

[45]  Mark W. Woolrich,et al.  Advances in functional and structural MR image analysis and implementation as FSL , 2004, NeuroImage.

[46]  Erika Skoe,et al.  A Little Goes a Long Way: How the Adult Brain Is Shaped by Musical Training in Childhood , 2012, The Journal of Neuroscience.

[47]  Pascal Belin,et al.  The Relationship of Lyrics and Tunes in the Processing of Unfamiliar Songs: A Functional Magnetic Resonance Adaptation Study , 2010, The Journal of Neuroscience.

[48]  André Brechmann,et al.  Auditory stream segregation relying on timbre involves left auditory cortex , 2004, Neuroreport.

[49]  R. Zatorre,et al.  When the brain plays music: auditory–motor interactions in music perception and production , 2007, Nature Reviews Neuroscience.

[50]  G. Glover,et al.  Self‐navigated spiral fMRI: Interleaved versus single‐shot , 1998, Magnetic resonance in medicine.

[51]  J. Snyder,et al.  Gamma-band activity reflects the metric structure of rhythmic tone sequences. , 2005, Brain research. Cognitive brain research.

[52]  V. Menon,et al.  The Neural Locus of Temporal Structure and Expectancies in Music: Evidence From Functional Neuroimaging At 3 Tesla , 2005, Music Perception.

[53]  N. Kraus,et al.  Human inferior colliculus activity relates to individual differences in spoken language learning. , 2012, Journal of neurophysiology.

[54]  B Blesser,et al.  Speech perception under conditions of spectral transformation. I. Phonetic characteristics. , 1972, Journal of speech and hearing research.

[55]  Gary H. Glover,et al.  Neural Correlates of Timbre Change in Harmonic Sounds , 2002, NeuroImage.

[56]  J P Rauschecker,et al.  Structural brain changes in tinnitus. , 2006, Cerebral cortex.

[57]  C. Stevens,et al.  Sweet Anticipation: Music and the Psychology of Expectation, by David Huron . Cambridge, Massachusetts: MIT Press, 2006 , 2007 .

[58]  Francis Eustache,et al.  Semantic and episodic memory of music are subserved by distinct neural networks , 2003, NeuroImage.

[59]  Nina Kraus,et al.  Assistive listening devices drive neuroplasticity in children with dyslexia , 2012, Proceedings of the National Academy of Sciences.

[60]  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.

[61]  Aslak Grinsted,et al.  Nonlinear Processes in Geophysics Application of the Cross Wavelet Transform and Wavelet Coherence to Geophysical Time Series , 2022 .

[62]  William H. McNeill,et al.  Keeping Together in Time: Dance and Drill in Human History. , 1995 .

[63]  Vinod Menon,et al.  Musical structure is processed in “language” areas of the brain: a possible role for Brodmann Area 47 in temporal coherence , 2003, NeuroImage.

[64]  N. Kraus,et al.  Learning to Encode Timing: Mechanisms of Plasticity in the Auditory Brainstem , 2009, Neuron.

[65]  R. Zatorre,et al.  Listening to musical rhythms recruits motor regions of the brain. , 2008, Cerebral cortex.

[66]  Adrian Rees,et al.  Responses of neurons in the inferior colliculus of the rat to AM and FM tones , 1983, Hearing Research.