The effect of music on corticospinal excitability is related to the perceived emotion: A transcranial magnetic stimulation study

Transcranial magnetic stimulation (TMS) and neuroimaging studies suggest a functional link between the emotion-related brain areas and the motor system. It is not well understood, however, whether the motor cortex activity is modulated by specific emotions experienced during music listening. In 23 healthy volunteers, we recorded the motor evoked potentials (MEP) following TMS to investigate the corticospinal excitability while subjects listened to music pieces evoking different emotions (happiness, sadness, fear, and displeasure), an emotionally neutral piece, and a control stimulus (musical scale). Quality and intensity of emotions were previously rated in an additional group of 30 healthy subjects. Fear-related music significantly increased the MEP size compared to the neutral piece and the control stimulus. This effect was not seen with music inducing other emotional experiences and was not related to changes in autonomic variables (respiration rate, heart rate). Current data indicate that also in a musical context, the excitability of the corticomotoneuronal system is related to the emotion expressed by the listened piece.

[1]  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.

[2]  J. Sloboda,et al.  Emotions in everyday listening to music. , 2001 .

[3]  N. Davey,et al.  Musical beat influences corticospinal drive to ankle flexor and extensor muscles in man. , 2002, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[4]  G. Zaccara,et al.  Mild cognitive impairment , 2009, Neurology.

[5]  Ulf Ziemann,et al.  Modulation of interhemispheric inhibition by volitional motor activity: an ipsilateral silent period study , 2009, The Journal of physiology.

[6]  P. Gomez,et al.  Relationships between musical structure and psychophysiological measures of emotion. , 2007, Emotion.

[7]  Carlos M. Coelho,et al.  Increased corticospinal excitability induced by unpleasant visual stimuli , 2010, Neuroscience Letters.

[8]  P. Brown,et al.  Effects of combined cortical and acoustic stimuli on muscle activity , 2004, Experimental Brain Research.

[9]  Michael J. Martinez,et al.  Passive music listening spontaneously engages limbic and paralimbic systems , 2004, Neuroreport.

[10]  M. Jahanshahi,et al.  Changes in corticospinal motor excitability induced by non-motor linguistic tasks , 2003, Experimental Brain Research.

[11]  R. Zatorre,et al.  Intensely pleasurable responses to music correlate with activity in brain regions implicated in reward and emotion , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[12]  A. Damasio.  Descarte's error : emotion, reason, and the human brain , 1994 .

[13]  Steven C. R. Williams,et al.  A functional MRI study of happy and sad affective states induced by classical music , 2007, Human brain mapping.

[14]  A. Friederici,et al.  Investigating emotion with music: An fMRI study , 2006, Human brain mapping.

[15]  A. Serino,et al.  Motor Properties of Peripersonal Space in Humans , 2009, PloS one.

[16]  P. Schyns,et al.  A mechanism for impaired fear recognition after amygdala damage , 2005, Nature.

[17]  E. Altenmüller,et al.  Emotions over time: synchronicity and development of subjective, physiological, and facial affective reactions to music. , 2007, Emotion.

[18]  L. Nadel,et al.  Cognitive neuroscience of emotion , 2000 .

[19]  C. Babiloni,et al.  Influence of the supplementary motor area on primary motor cortex excitability during movements triggered by neutral or emotionally unpleasant visual cues , 2003, Experimental Brain Research.

[20]  U. Ziemann,et al.  Hysteresis effects on the input–output curve of motor evoked potentials , 2009, Clinical Neurophysiology.

[21]  Talma Hendler,et al.  Eyes Wide Shut: Amygdala Mediates Eyes-Closed Effect on Emotional Experience with Music , 2009, PloS one.

[22]  Lutz Jäncke,et al.  Modulation of corticospinal activity by strong emotions evoked by pictures and classical music: a transcranial magnetic stimulation study , 2007, Neuroreport.

[23]  R. Sparing,et al.  Task‐dependent modulation of functional connectivity between hand motor cortices and neuronal networks underlying language and music: a transcranial magnetic stimulation study in humans , 2007, The European journal of neuroscience.

[24]  A. Gabrielsson.  Emotion perceived and emotion felt: Same or different? , 2001 .

[25]  Jejo D. Koola,et al.  Emotion facilitates action: a transcranial magnetic stimulation study of motor cortex excitability during picture viewing. , 2007, Psychophysiology.

[26]  R. Töpper,et al.  Motor cortex hand area and speech: implications for the development of language , 2003, Neuropsychologia.

[27]  E. Murray.  The amygdala, reward and emotion , 2007, Trends in Cognitive Sciences.

[28]  R. Adolphs,et al.  Amygdala damage impairs emotion recognition from music , 2007, Neuropsychologia.

[29]  Andrea A. Kühn,et al.  Motor cortex inhibition induced by acoustic stimulation , 2004, Experimental Brain Research.

[30]  G. Rizzolatti,et al.  Motor facilitation during action observation: a magnetic stimulation study. , 1995, Journal of neurophysiology.

[31]  R. Zatorre,et al.  Anatomically distinct dopamine release during anticipation and experience of peak emotion to music , 2011, Nature Neuroscience.

[32]  Gaspare Galati,et al.  Transcranial magnetic stimulation highlights the sensorimotor side of empathy for pain , 2005, Nature Neuroscience.

[33]  Franca Tecchio,et al.  Corticospinal excitability modulation during mental simulation of wrist movements in human subjects , 1998, Neuroscience Letters.

[34]  S. Koelsch.  Investigating Emotion with Music , 2005, Annals of the New York Academy of Sciences.

[35]  Lutz Jäncke,et al.  The emotional power of music: How music enhances the feeling of affective pictures , 2006, Brain Research.

[36]  Á. Pascual-Leone,et al.  Lateralized effects of self-induced sadness and happiness on corticospinal excitability , 1997, Neurology.

[37]  J. Rothwell,et al.  Speech‐induced changes in corticospinal excitability , 1996, Annals of neurology.

[38]  P. Pasqualetti,et al.  Are autonomic signals influencing cortico-spinal motor excitability? A study with transcranial magnetic stimulation , 2000, Brain Research.

[39]  S. Rossi,et al.  Distinct Olfactory Cross-Modal Effects on the Human Motor System , 2008, PLoS ONE.

[40]  S. Koelsch.  Towards a neural basis of music-evoked emotions , 2010, Trends in Cognitive Sciences.

[41]  Daniel Tranel,et al.  Cardiovascular and respiratory responses during musical mood induction. , 2006, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

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

[43]  I. Peretz,et al.  Impaired recognition of scary music following unilateral temporal lobe excision. , 2005, Brain : a journal of neurology.

[44]  Daniel J. Levitin,et al.  The rewards of music listening: Response and physiological connectivity of the mesolimbic system , 2005, NeuroImage.

[45]  David W. McNeal,et al.  Amygdala interconnections with the cingulate motor cortex in the rhesus monkey , 2007, The Journal of comparative neurology.

[46]  Sheng Li,et al.  Voluntary breathing influences corticospinal excitability of nonrespiratory finger muscles. , 2011, Journal of neurophysiology.

[47]  I. Peretz,et al.  Music and emotion: perceptual determinants, immediacy, and isolation after brain damage , 1998, Cognition.

[48]  P. Rossini,et al.  Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee. , 1994, Electroencephalography and clinical neurophysiology.

[49]  D. Levitin,et al.  Current Advances in the Cognitive Neuroscience of Music , 2009, Annals of the New York Academy of Sciences.

[50]  D. Schutter,et al.  Fearful faces selectively increase corticospinal motor tract excitability: a transcranial magnetic stimulation study. , 2008, Psychophysiology.

[51]  G. Rizzolatti,et al.  Listening to action-related sentences modulates the activity of the motor system: a combined TMS and behavioral study. , 2005, Brain research. Cognitive brain research.