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Modulating musical reward sensitivity up and down with transcranial magnetic stimulation

Nature Human Behaviour volume 2, pages 27–32 (2018)Cite this article

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Abstract

Humans have the unique capacity to experience pleasure from aesthetic stimuli, such as art and music. Recent neuroimaging findings with music have led to a model in which mesolimbic striatal circuits interact with cortical systems to generate expectancies leading to pleasure1,2. However, neuroimaging approaches are correlational. Here, we provide causal evidence for the model by combining transcranial magnetic stimulation over the left dorsolateral prefrontal cortex to directly modulate fronto-striatal function3 bidirectionally together with measures of pleasure and motivation during music listening. Our results show that perceived pleasure, psychophysiological measures of emotional arousal, and the monetary value assigned to music, are all significantly increased by exciting fronto-striatal pathways, whereas inhibition of this system leads to decreases in all of these variables compared with sham stimulation. These findings support the hypothesis that fronto-striatal function causally mediates both the affective responses and motivational aspects of music-induced reward, and provide insights into how aesthetic responses emerge in the human brain.

The ability to experience pleasure is considered an evolutionary mechanism to ensure the pursuit of basic biological needs, such as food or sex4,5. However, humans are also able to experience pleasure with more abstract, aesthetic rewards that lack a clear physiological benefit, such as music. In contrast to primary rewards, the hedonic impact of music listening is driven by its intrinsic ability to change emotional arousal6. Indeed, music may evoke a large variety of emotions, from happiness to sadness, and all of them (independently of their valence) may be associated with some sort of pleasure7,8,9,10. Several music theorists have suggested that the emotions evoked by music may arise, among other aspects, from structural and temporal features of music, such as anticipation and expectancy11,12.

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Fig. 1: Schematic of the experimental approach used.
Fig. 2: Schematic of the experimental paradigm.
Fig. 3: Main results of the study.

References

  1. Salimpoor, V. N. et al. Interactions between the nucleus accumbens and auditory cortices predict music reward value. Science 340, 216–219 (2013).

    Article  CAS  PubMed  Google Scholar 

  2. Martinez-Molina, N., Mas-Herrero, E., Rodriguez-Fornells, A., Zatorre, R. J. & Marco-Pallarés, J. The broken link in specific musical anhedonia: ventral striatum activation and functional connectivity with auditory cortex. Proc. Natl Acad. Sci. USA  113, E7337–E7345 (2016).

  3. Strafella, A. P., Paus, T., Barrett, J. & Dagher, A. Repetitive transcranial magnetic stimulation of the human prefrontal cortex induces dopamine release in the caudate nucleus. J. Neurosci. 21, RC157 (2001).

    CAS  PubMed  Google Scholar 

  4. Berridge, K. C. & Kringelbach, M. L. Affective neuroscience of pleasure: reward in humans and animals. Psychopharmacology 199, 457–480 (2008).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  5. Darwin, C. The Expression of the Emotions in Man and Animals (J. Murray, London, 1872).

  6. Salimpoor, V. N., Benovoy, M., Longo, G., Cooperstock, J. R. & Zatorre, R. J. The rewarding aspects of music listening are related to degree of emotional arousal. PLoS ONE 4, e7487 (2009).

    Article  PubMed Central  PubMed  Google Scholar 

  7. Zentner, M., Grandjean, D. & Scherer, K. R. Emotions evoked by the sound of music: characterization, classification, and measurement. Emotion 8, 494–521 (2008).

    Article  PubMed  Google Scholar 

  8. Kawakami, A., Furukawa, K., Katahira, K. & Okanoya, K. Sad music induces pleasant emotion. Front. Psychol. 4, 311 (2013).

    Article  PubMed Central  PubMed  Google Scholar 

  9. Taruffi, L. & Koelsch, S. The paradox of music-evoked sadness: an online survey. PLoS ONE 9, e110490 (2014).

    Article  PubMed Central  PubMed  Google Scholar 

  10. Sachs, M. E., Damasio, A. & Habibi, A. The pleasures of sad music: a systematic review. Front. Hum. Neurosci. 9, 404 (2015).

    Article  PubMed Central  PubMed  Google Scholar 

  11. Meyer, L. B. Emotion and Meaning in Music (Univ. Chicago Press, Chicago and London, 1956).

    Google Scholar 

  12. Huron, D. B. Sweet Anticipation: Music and the Psychology of Expectation (MIT Press, Cambridge, 2006).

  13. Zatorre, R. J. & Halpern, A. R. Mental concerts: musical imagery and auditory cortex. Neuron 47, 9–12 (2005).

    Article  CAS  PubMed  Google Scholar 

  14. Peretz, I. et al. Music lexical networks: the cortical organization of music recognition. Ann. NY Acad. Sci. 1169, 256–265 (2009).

    Article  PubMed  Google Scholar 

  15. Janata, P. Acuity of mental representations of pitch. Ann. NY Acad. Sci. 1252, 214–221 (2012).

    Article  PubMed  Google Scholar 

  16. Zatorre, R. J. & Salimpoor, V. N. From perception to pleasure: music and its neural substrates. Proc. Natl Acad. Sci. USA 110 (Suppl. 2), 10430–10437 (2013).

    Article  Google Scholar 

  17. Salimpoor, V. N., Zald, D. H., Zatorre, R. J., Dagher, A. & McIntosh, A. R. Predictions and the brain: how musical sounds become rewarding. Trends Cogn. Sci. 19, 86–91 (2015).

    Article  PubMed  Google Scholar 

  18. Zhang, L. I., Bao, S. & Merzenich, M. M. Persistent and specific influences of early acoustic environments on primary auditory cortex. Nat. Neurosci. 4, 1123–1130 (2001).

    Article  CAS  PubMed  Google Scholar 

  19. Köver, H., Gill, K., Tseng, Y.-T. L. & Bao, S. Perceptual and neuronal boundary learned from higher-order stimulus probabilities. J. Neurosci. 33, 3699–3705 (2013).

    Article  PubMed Central  PubMed  Google Scholar 

  20. Bao, S. Perceptual learning in the developing auditory cortex. Eur. J. Neurosci. 41, 718–724 (2015).

    Article  PubMed Central  PubMed  Google Scholar 

  21. Albouy, P., Mattout, J., Sanchez, G., Tillmann, B. & Caclin, A. Altered retrieval of melodic information in congenital amusia: insights from dynamic causal modeling of MEG data. Front. Hum. Neurosci. 9, 20 (2015).

    Article  PubMed Central  PubMed  Google Scholar 

  22. Bastos, A. M. et al. Canonical microcircuits for predictive coding. Neuron 76, 695–711 (2012).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  23. Tillmann, B. et al. Cognitive priming in sung and instrumental music: activation of inferior frontal cortex. NeuroImage 31, 1771–1782 (2006).

    Article  CAS  PubMed  Google Scholar 

  24. Rohrmeier, M. A. & Koelsch, S. Predictive information processing in music cognition. Acritical review. Int. J. Psychophysiol. 83, 164–175 (2012).

    Article  PubMed  Google Scholar 

  25. Blood, A. J. & Zatorre, R. J. Intensely pleasurable responses to music correlate with activity in brain regions implicated in reward and emotion. Proc. Natl Acad. Sci. USA 98, 11818–11823 (2001).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  26. Salimpoor, V. N., Benovoy, M., Larcher, K., Dagher, A. & Zatorre, R. J. Anatomically distinct dopamine release during anticipation and experience of peak emotion to music. Nat. Neurosci. 14, 257–262 (2011).

    Article  CAS  PubMed  Google Scholar 

  27. Koelsch, S. Brain correlates of music-evoked emotions. Nat. Rev. Neurosci. 15, 170–180 (2014).

    Article  CAS  PubMed  Google Scholar 

  28. Critchley, H. D., Mathias, C. J. & Dolan, R. J. Neural activity in the human brain relating to uncertainty and arousal during anticipation. Neuron 29, 537–545 (2001).

    Article  CAS  PubMed  Google Scholar 

  29. Knutson, B., Adams, C. M., Fong, G. W. & Hommer, D. Anticipation of increasing monetary reward selectively recruits nucleus accumbens. J. Neurosci. 21, RC159 (2001).

    CAS  PubMed  Google Scholar 

  30. Ito, R., Dalley, J. W., Robbins, T. W. & Everitt, B. J. Dopamine release in the dorsal striatum during cocaine-seeking behavior under the control of a drug-associated cue. J. Neurosci. 22, 6247–6253 (2002).

    CAS  PubMed  Google Scholar 

  31. O’Doherty, J. P., Deichmann, R., Critchley, H. D. & Dolan, R. J. Neural responses during anticipation of a primary taste reward. Neuron 33, 815–826 (2002).

    Article  PubMed  Google Scholar 

  32. Wallis, J. D. & Miller, E. K. Neuronal activity in primate dorsolateral and orbital prefrontal cortex during performance of a reward preference task. Eur. J. Neurosci. 18, 2069–2081 (2003).

    Article  PubMed  Google Scholar 

  33. Tsujimoto, S. & Sawaguchi, T. Neuronal activity representing temporal prediction of reward in the primate prefrontal cortex. J. Neurophysiol. 93, 3687–3692 (2005).

    Article  PubMed  Google Scholar 

  34. Beiser, D. G. & Houk, J. C. Model of cortical-basal ganglionic processing: encoding the serial order of sensory events. J. Neurophysiol. 79, 3168–3188 (1998).

    Article  CAS  PubMed  Google Scholar 

  35. Grahn, J. A. & Rowe, J. B. Finding and feeling the musical beat: striatal dissociations between detection and prediction of regularity. Cereb. Cortex 23, 913–921 (2013).

    Article  Google Scholar 

  36. Gebauer, L., Kringelbach, M. L. & Vuust, P. Ever-changing cycles of musical pleasure: The role of dopamine and anticipation. Psychomusicol. Music Mind Brain 22, 152–167 (2012).

    Article  Google Scholar 

  37. Pogarell, O. et al. Striatal dopamine release after prefrontal repetitive transcranial magnetic stimulation in major depression: preliminary results of a dynamic [123I] IBZM SPECT study. J. Psychiat. Res. 40, 307–314 (2006).

    Article  PubMed  Google Scholar 

  38. Pogarell, O. et al. Acute prefrontal rTMS increases striatal dopamine to a similar degree as D-amphetamine. Psychiat. Res. 156, 251–255 (2007).

    Article  CAS  Google Scholar 

  39. Ko, J. H. et al. Theta burst stimulation-induced inhibition of dorsolateral prefrontal cortex reveals hemispheric asymmetry in striatal dopamine release during a set-shifting task: a TMS-[(11)C]raclopride PET study. Eur. J. Neurosci. 28, 2147–2155 (2008).

    Article  PubMed Central  PubMed  Google Scholar 

  40. Hayashi, T., Ko, J. H., Strafella, A. P. & Dagher, A. Dorsolateral prefrontal and orbitofrontal cortex interactions during self-control of cigarette craving. Proc. Natl Acad. Sci. USA 110, 4422–4427 (2013).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  41. Haber, S. N. & Knutson, B. The reward circuit: linking primate anatomy and human imaging. Neuropsychopharmacology 35, 4–26 (2010).

    Article  PubMed  Google Scholar 

  42. Keck, M. E. et al. Repetitive transcranial magnetic stimulation increases the release of dopamine in the mesolimbic and mesostriatal system. Neuropharmacology 43, 101–109 (2002).

    Article  CAS  PubMed  Google Scholar 

  43. Zangen, A. & Hyodo, K. Transcranial magnetic stimulation induces increases in extracellular levels of dopamine and glutamate in the nucleus accumbens. NeuroReport 13, 2401–2405 (2002).

    Article  CAS  PubMed  Google Scholar 

  44. Erhardt, A. et al. Repetitive transcranial magnetic stimulation increases the release of dopamine in the nucleus accumbens shell of morphine-sensitized rats during abstinence. Neuropsychopharmacology 29, 2074–2080 (2004).

    Article  CAS  PubMed  Google Scholar 

  45. Kanno, M., Matsumoto, M., Togashi, H., Yoshioka, M. & Mano, Y. Effects of acute repetitive transcranial magnetic stimulation on dopamine release in the rat dorsolateral striatum. J. Neurol. Sci. 217, 73–81 (2004).

    Article  CAS  PubMed  Google Scholar 

  46. Huang, Y.-Z., Edwards, M. J., Rounis, E., Bhatia, K. P. & Rothwell, J. C. Theta burst stimulation of the human motor cortex. Neuron 45, 201–206 (2005).

    Article  CAS  PubMed  Google Scholar 

  47. Di Lazzaro, V. et al. Theta-burst repetitive transcranial magnetic stimulation suppresses specific excitatory circuits in the human motor cortex. J. Physiol. 565, 945–950 (2005).

    Article  PubMed Central  PubMed  Google Scholar 

  48. Mas-Herrero, E., Zatorre, R. J., Rodriguez-Fornells, A. & Marco-Pallarés, J. Dissociation between musical and monetary reward responses in specific musical anhedonia. Curr. Biol. 24, 699–704 (2014).

    Article  CAS  PubMed  Google Scholar 

  49. Grewe, O., Nagel, F., Kopiez, R. & Altenmüller, E. How does music arouse ‘chills’? Investigating strong emotions, combining psychological, physiological, and psychoacoustical methods. Ann. NY Acad. Sci. 1060, 446–449 (2005).

    Article  PubMed  Google Scholar 

  50. Mas-Herrero, E., Marco-Pallares, J., Lorenzo-Seva, U., Zatorre, R. J. & Rodriguez-Fornells, A. Individual differences in music reward experiences. Music Percept. Interdiscip. J. 31, 118–138 (2013).

    Article  Google Scholar 

  51. Schellenberg, E. G., Peretz, I. & Vieillard, S. Liking for happy- and sad-sounding music: Effects of exposure. Cogn. Emot. 22, 218–237 (2008).

    Article  Google Scholar 

  52. van den Bosch, I., Salimpoor, V. N. & Zatorre, R. J. Familiarity mediates the relationship between emotional arousal and pleasure during music listening. Front. Hum. Neurosci. 7, (2013).

  53. Pereira, C. S. et al. Music and emotions in the brain: familiarity matters. PLoS ONE 6, e27241 (2011).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  54. Peretz, I., Gaudreau, D. & Bonnel, A. M. Exposure effects on music preference and recognition. Mem. Cogn. 26, 884–902 (1998).

    Article  CAS  Google Scholar 

  55. Sescousse, G., Caldú, X., Segura, B. & Dreher, J.-C. Processing of primary and secondary rewards: a quantitative meta-analysis and review of human functional neuroimaging studies. Neurosci. Biobehav. Rev. 37, 681–696 (2013).

    Article  PubMed  Google Scholar 

  56. Schultz, W., Dayan, P. & Montague, P. R. A neural substrate of prediction and reward. Science 275, 1593–1599 (1997).

    Article  CAS  PubMed  Google Scholar 

  57. Waelti, P., Dickinson, A. & Schultz, W. Dopamine responses comply with basic assumptions of formal learning theory. Nature 412, 43–48 (2001).

    Article  CAS  PubMed  Google Scholar 

  58. Pan, W.-X., Schmidt, R., Wickens, J. R. & Hyland, B. I. Dopamine cells respond to predicted events during classical conditioning: evidence for eligibility traces in the reward-learning network. J. Neurosci. 25, 6235–6242 (2005).

    Article  CAS  PubMed  Google Scholar 

  59. Schott, B. H. et al. Mesolimbic functional magnetic resonance imaging activations during reward anticipation correlate with reward-related ventral striatal dopamine release. J. Neurosci. 28, 14311–14319 (2008).

    Article  CAS  PubMed  Google Scholar 

  60. D’Ardenne, K., McClure, S. M., Nystrom, L. E. & Cohen, J. D. BOLD responses reflecting dopaminergic signals in the human ventral tegmental area. Science 319, 1264–1267 (2008).

    Article  PubMed  Google Scholar 

  61. Hart, A. S., Rutledge, R. B., Glimcher, P. W. & Phillips, P. E. M. Phasic dopamine release in the rat nucleus accumbens symmetrically encodes a reward prediction error term. J. Neurosci. 34, 698–704 (2014).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  62. Chang, C. Y. et al. Brief optogenetic inhibition of dopamine neurons mimics endogenous negative reward prediction errors. Nat. Neurosci. 19, 111–116 (2016).

    Article  CAS  PubMed  Google Scholar 

  63. Volkow, N. D. et al. ‘Nonhedonic’ food motivation in humans involves dopamine in the dorsal striatum and methylphenidate amplifies this effect. Synapse 44, 175–180 (2002).

    Article  CAS  PubMed  Google Scholar 

  64. Volkow, N. D. et al. Cocaine cues and dopamine in dorsal striatum: mechanism of craving in cocaine addiction. J. Neurosci. 26, 6583–6588 (2006).

    Article  CAS  PubMed  Google Scholar 

  65. Vanderschuren, L. J. M. J., Di Ciano, P. & Everitt, B. J. Involvement of the dorsal striatum in cue-controlled cocaine seeking. J. Neurosci. 25, 8665–8670 (2005).

    Article  CAS  PubMed  Google Scholar 

  66. Letchworth, S. R., Nader, M. A., Smith, H. R., Friedman, D. P. & Porrino, L. J. Progression of changes in dopamine transporter binding site density as a result of cocaine self-administration in rhesus monkeys. J. Neurosci. 21, 2799–2807 (2001).

    CAS  PubMed  Google Scholar 

  67. Porrino, L. J., Lyons, D., Smith, H. R., Daunais, J. B. & Nader, M. A. Cocaine self-administration produces a progressive involvement of limbic, association, and sensorimotor striatal domains. J. Neurosci. 24, 3554–3562 (2004).

    Article  CAS  PubMed  Google Scholar 

  68. Sloboda, J. A. & O’Neill, S. A. in Music and Emotion: Theory and Research (eds Juslin, P. N. & Sloboda, J. A.) 415–429 (Oxford Univ. Press, Oxford, 2001).

  69. Chamorro-Premuzic, T. & Furnham, A. Personality and music: can traits explain how people use music in everyday life? Br. J. Psychol. 98, 175–185 (2007).

    Article  PubMed  Google Scholar 

  70. Cho, S. S. & Strafella, A. P. rTMS of the left dorsolateral prefrontal cortex modulates dopamine release in the ipsilateral anterior cingulate cortex and orbitofrontal cortex. PLoS ONE 4, e6725 (2009).

    Article  PubMed Central  PubMed  Google Scholar 

  71. Lan, M. J., Chhetry, B. T., Liston, C., Mann, J. J. & Dubin, M. Transcranial magnetic stimulation of left dorsolateral prefrontal cortex induces brain morphological changes in regions associated with a treatment resistant major depressive episode: an exploratory analysis. Brain Stimulat. 9, 577–583 (2016).

    Article  Google Scholar 

  72. Pujara, M. S., Philippi, C. L., Motzkin, J. C., Baskaya, M. K. & Koenigs, M. Ventromedial prefrontal cortex damage is associated with decreased ventral striatum volume and response to reward. J. Neurosci. 36, 5047–5054 (2016).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  73. Liu, X., Hairston, J., Schrier, M. & Fan, J. Common and distinct networks underlying reward valence and processing stages: a meta-analysis of functional neuroimaging studies. Neurosci. Biobehav. Rev. 35, 1219–1236 (2011).

    Article  PubMed  Google Scholar 

  74. Samanez-Larkin, G. R. et al. Anticipation of monetary gain but not loss in healthy older adults. Nat. Neurosci. 10, 787–791 (2007).

    Article  PubMed Central  PubMed  Google Scholar 

  75. Treadway, M. T. & Zald, D. H. Reconsidering anhedonia in depression: lessons from translational neuroscience. Neurosci. Biobehav. Rev. 35, 537–555 (2011).

    Article  PubMed  Google Scholar 

  76. Jordan, L. L., Zahodne, L. B., Okun, M. S. & Bowers, D. Hedonic and behavioral deficits associated with apathy in Parkinson’s disease: potential treatment implications. Mov. Disord. 28, 1301–1304 (2013).

    Article  PubMed Central  PubMed  Google Scholar 

  77. Rossi, S., Hallett, M., Rossini, P. M., Pascual-Leone, A. & Safety of TMS Consensus Group. Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin. Neurophysiol. 120, 2008–2039 (2009).

  78. Rossini, P. M. 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. Electroencephalogr. Clin. Neurophysiol. 91, 79–92 (1994).

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Acknowledgements

R.J.Z. is supported by funds from the Canadian Institutes of Health Research (CIHR), the Natural Sciences and Engineering Research Council of Canada, and the Canada Fund for Innovation. A.D is funded by the CIHR Foundation Grant. E.M.-H. was supported by the Jeanne Timmins Costello Fellowship and the CIBC Fellowship in Brain Imaging from the Montreal Neurological Institute. The funders had no role in the conceptualization, design, data collection, analysis, decision to publish or preparation of the manuscript.

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Authors and Affiliations

  1. Montreal Neurological Institute, McGill University, Montreal, QC, Canada

    Ernest Mas-Herrero, Alain Dagher & Robert J. Zatorre

  2. International Laboratory for Brain, Music, and Sound Research (BRAMS), Montreal, QC, Canada

    Ernest Mas-Herrero & Robert J. Zatorre

  3. Centre for Research on Brain, Language and Music (CRBLM), Montreal, QC, Canada

    Ernest Mas-Herrero & Robert J. Zatorre

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E.M.-H., A.D. and R.J.Z. designed the experiment. E.M.-H. ran and analysed the data (with the supervision of A.D. and R.J.Z). All authors wrote the manuscript.

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Correspondence to Robert J. Zatorre.

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Mas-Herrero, E., Dagher, A. & Zatorre, R.J. Modulating musical reward sensitivity up and down with transcranial magnetic stimulation. Nat Hum Behav 2, 27–32 (2018). https://doi.org/10.1038/s41562-017-0241-z

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