Passive listening to preferred motor tempo modulates corticospinal excitability

Rhythms are an essential characteristic of our lives, and auditory-motor coupling affects a variety of behaviors. Previous research has shown that the neural regions associated with motor system processing are coupled to perceptual rhythmic and melodic processing such that the perception of rhythmic stimuli can entrain motor system responses. However, the degree to which individual preference modulates the motor system is unknown. Recent work has shown that passively listening to metrically strong rhythms increases corticospinal excitability, as indicated by transcranial magnetic stimulation (TMS). Furthermore, this effect is modulated by high-groove music, or music that inspires movement, while neuroimaging evidence suggests that premotor activity increases with tempos occurring within a preferred tempo (PT) category. PT refers to the rate of a hypothetical endogenous oscillator that may be indicated by spontaneous motor tempo (SMT) and preferred perceptual tempo (PPT) measurements. The present study investigated whether listening to a rhythm at an individual’s PT preferentially modulates motor system excitability. SMT was obtained in human participants through a tapping task in which subjects were asked to tap a response key at their most comfortable rate. Subjects listened a 10-beat tone sequence at 11 log-spaced tempos and rated their preference for each (PPT). We found that SMT and PPT measurements were correlated, indicating that preferred and produced tempos occurred at a similar rate. Crucially, single-pulse TMS delivered to left M1 during PPT judgments revealed that corticospinal excitability, measured by motor-evoked potentials (MEPs), was modulated by tempos traveling closer to individual PT. However, the specific nature of this modulation differed across individuals, with some exhibiting an increase in excitability around PT and others exhibiting a decrease. These findings suggest that auditory-motor coupling induced by rhythms is preferentially modulated by rhythms occurring at a preferred rate, and that individual differences can alter the nature of this coupling.

[1]  Bruno Nettl An ethnomusicologist contemplates universals in musical sound and musical culture , 2000 .

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

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

[4]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[5]  I. Winkler,et al.  Auditory organization of sound sequences by a temporal or numerical regularity--a mismatch negativity study comparing musicians and non-musicians. , 2005, Brain research. Cognitive brain research.

[6]  Neil G. Muggleton,et al.  Modulation of Motor Excitability by Metricality of Tone Sequences , 2012 .

[7]  L. Barsalou Grounded cognition. , 2008, Annual review of psychology.

[8]  Alan C. Evans,et al.  Musical Training Shapes Structural Brain Development , 2009, The Journal of Neuroscience.

[9]  Hans Forssberg,et al.  Listening to rhythms activates motor and premotor cortices , 2009, Cortex.

[10]  Robert J. Zatorre,et al.  Moving on Time: Brain Network for Auditory-Motor Synchronization is Modulated by Rhythm Complexity and Musical Training , 2008, Journal of Cognitive Neuroscience.

[11]  Martin Wiener,et al.  Double Dissociation of Dopamine Genes and Timing in Humans , 2011, Journal of Cognitive Neuroscience.

[12]  S. Bestmann,et al.  Variability of Human Corticospinal Excitability Tracks the State of Action Preparation , 2013, The Journal of Neuroscience.

[13]  G. Schlaug,et al.  Brain Structures Differ between Musicians and Non-Musicians , 2003, The Journal of Neuroscience.

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

[15]  K. Stefan,et al.  Modulation of associative human motor cortical plasticity by attention. , 2004, Journal of neurophysiology.

[16]  Ricarda I Schubotz,et al.  Inhibitory stimulation of the ventral premotor cortex temporarily interferes with musical beat rate preference , 2011, Human brain mapping.

[17]  M. Thaut,et al.  Rhythmic auditory-motor facilitation of gait patterns in patients with Parkinson's disease. , 1997, Journal of neurology, neurosurgery, and psychiatry.

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

[19]  Jochen Kaiser,et al.  Auditory–motor synchronization facilitates attention allocation , 2013, NeuroImage.

[20]  L. Craighero,et al.  Corticospinal excitability is specifically modulated by motor imagery: a magnetic stimulation study , 1998, Neuropsychologia.

[21]  Longqi Liu,et al.  Cell reprogramming: Into the groove. , 2013, Nature materials.

[22]  Takashi Hanakawa,et al.  Stimulus-response profile during single-pulse transcranial magnetic stimulation to the primary motor cortex. , 2009, Cerebral cortex.

[23]  S. Rossi,et al.  Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research , 2009, Clinical Neurophysiology.

[24]  M. Thaut,et al.  Rhythmic facilitation of gait training in hemiparetic stroke rehabilitation , 1997, Journal of the Neurological Sciences.

[25]  C. Gallistel,et al.  Toward a neurobiology of temporal cognition: advances and challenges , 1997, Current Opinion in Neurobiology.

[26]  Eckart Altenmüller,et al.  Annals of the New York Academy of Sciences the Involvement of Audio–motor Coupling in the Music-supported Therapy Applied to Stroke Patients , 2022 .

[27]  C. Drake,et al.  The “Ticktock” of Our Internal Clock , 2003, Psychological science.

[28]  Jonathan Westley Peirce,et al.  Neuroinformatics Original Research Article Generating Stimuli for Neuroscience Using Psychopy , 2022 .

[29]  Stefan Skare,et al.  See Blockindiscussions, Blockinstats, Blockinand Blockinauthor Blockinprofiles Blockinfor Blockinthis Blockinpublication Extensive Blockinpiano Blockinpracticing Blockinhas Blockinregionally Specific Blockineffects Blockinon Blockinwhite Blockinmatter Blockindevelopment , 2022 .

[30]  Fred Charatan Into the groove , 2008, BMJ : British Medical Journal.

[31]  Jessica A. Grahn,et al.  Into the groove: Can rhythm influence Parkinson's disease? , 2013, Neuroscience & Biobehavioral Reviews.

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

[33]  L. Jäncke,et al.  Cortical activations in primary and secondary motor areas for complex bimanual movements in professional pianists. , 2000, Brain research. Cognitive brain research.

[34]  Simone Rossi,et al.  The effect of music on corticospinal excitability is related to the perceived emotion: A transcranial magnetic stimulation study , 2013, Cortex.

[35]  Michael J. Hove,et al.  Musical groove modulates motor cortex excitability: A TMS investigation , 2013, Brain and Cognition.

[36]  D Yves von Cramon,et al.  Tuning‐in to the beat: Aesthetic appreciation of musical rhythms correlates with a premotor activity boost , 2009, Human brain mapping.

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

[38]  Nathaniel S. Miller,et al.  The time of our lives: life span development of timing and event tracking. , 2006, Journal of experimental psychology. General.

[39]  M. Magistris,et al.  The size of motor-evoked potentials: influencing parameters and quantification , 2008 .