Article

Anatomically distinct dopamine release during anticipation and experience of peak emotion to music

Received:
Accepted:
Published online:

Abstract

Music, an abstract stimulus, can arouse feelings of euphoria and craving, similar to tangible rewards that involve the striatal dopaminergic system. Using the neurochemical specificity of [11C]raclopride positron emission tomography scanning, combined with psychophysiological measures of autonomic nervous system activity, we found endogenous dopamine release in the striatum at peak emotional arousal during music listening. To examine the time course of dopamine release, we used functional magnetic resonance imaging with the same stimuli and listeners, and found a functional dissociation: the caudate was more involved during the anticipation and the nucleus accumbens was more involved during the experience of peak emotional responses to music. These results indicate that intense pleasure in response to music can lead to dopamine release in the striatal system. Notably, the anticipation of an abstract reward can result in dopamine release in an anatomical pathway distinct from that associated with the peak pleasure itself. Our results help to explain why music is of such high value across all human societies.

  • Subscribe to Nature Neuroscience for full access:

    $59

    Subscribe

Additional access options:

Already a subscriber?  Log in  now or  Register  for online access.

References

  1. 1.

    et al. The dopaminergic basis of human behaviors: a review of molecular imaging studies. Neurosci. Biobehav. Rev. 33, 1109–1132 (2009).

  2. 2.

    & The content and structure of laypeople's concept of pleasure. Cogn. Emot. 17, 263–295 (2003).

  3. 3.

    & Psychological perspectives on music and emotion. in Music and Emotion: Theory and Research (ed. Sloboda, J.) 71–104 (Oxford University Press, Oxford, 2001).

  4. 4.

    An exploratory study of musical emotions and psychophysiology. Can. J. Exp. Psychol. 51, 336–353 (1997).

  5. 5.

    & 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).

  6. 6.

    & The rewards of music listening: response and physiological connectivity of the mesolimbic system. Neuroimage 28, 175–184 (2005).

  7. 7.

    , , , & Investigating emotion with music: an fMRI study. Hum. Brain Mapp. 27, 239–250 (2006).

  8. 8.

    , , , & A functional MRI study of happy and sad affective states induced by classical music. Hum. Brain Mapp. 28, 1150–1162 (2007).

  9. 9.

    & Linking nucelus accumbens dopamine and blood oxygenation. Psychopharmacology (Berl.) 191, 813–822 (2007).

  10. 10.

    Imaging synaptic neurotransmission with in vivo binding competition techniques: a critical review. J. Cereb. Blood Flow Metab. 20, 423–451 (2000).

  11. 11.

    & Musical expectancy and thrills. in Music and Emotion (eds. Juslin, P.N. & Sloboda, J.) (Oxford University Press, New York, 2009).

  12. 12.

    , , & Emotions over time: synchronicity and development of subjective, physiological, and facial affective reactions to music. Emotion 7, 774–788 (2007).

  13. 13.

    The emotional source of “chills” induced by music. Music Percept. 13, 171–207 (1995).

  14. 14.

    Music structure and emotional response: some empirical findings. Psychol. Music 19, 110–120 (1991).

  15. 15.

    , , , & The rewarding aspects of music listening are related to degree of emotional arousal. PLoS ONE 4, e7487 (2009).

  16. 16.

    , , & Neural responses during anticipation of a primary taste reward. Neuron 33, 815–826 (2002).

  17. 17.

    , & A neural substrate of prediction and reward. Science 275, 1593–1599 (1997).

  18. 18.

    Dopamine, learning and motivation. Nat. Rev. Neurosci. 5, 483–494 (2004).

  19. 19.

    Sweet Anticipation: Music and the Psychology of Expectation (MIT Press, Cambridge, Massachusetts, 2006).

  20. 20.

    Emotion and Meaning in Music. (University of Chicago Press, Chicago, 1956).

  21. 21.

    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).

  22. 22.

    , , & Circular analysis in systems neuroscience: the dangers of double dipping. Nat. Neurosci. 12, 535–540 (2009).

  23. 23.

    et al. Relationship between subjective effects of cocaine and dopamine transporter occupancy. Nature 386, 827–830 (1997).

  24. 24.

    & The reward circuit: linking primate anatomy and human imaging. Neuropharmacology 35, 4–26 (2010).

  25. 25.

    , , & Reward-related cortical inputs define a large striatal region in primates that interface with associative cortical connections, providing a substrate for incentive-based learning. J. Neurosci. 26, 8368–8376 (2006).

  26. 26.

    & Overlapping prediction errors in dorsal striatum during instrumental learning with juice and money reward in the human brain. J. Neurophysiol. 102, 3384–3391 (2009).

  27. 27.

    , & Feeding-induced dopamine release in dorsal striatum correlates with meal pleasantness ratings in healthy human volunteers. Neuroimage 19, 1709–1715 (2003).

  28. 28.

    et al. Modeling sensiitization to stimulants in humans: an [11C]raclopride/positron emission tomography study in healthy men. Arch. Gen. Psychiatry 63, 1386–1395 (2006).

  29. 29.

    , , , & The hedonic response to cigarette smoking is proportional to dopamine release in the human striatum as measured by positron emission tomography and [11C]raclopride. Synapse 54, 65–71 (2004).

  30. 30.

    et al. Amphetamine-induced increases in extracellular dopamine, drug wanting, and novelty seeking: a PET/[11C]raclopride study in healthy men. Neuropsychopharmacology 27, 1027–1035 (2002).

  31. 31.

    et al. Alcohol promotes dopamine release in the human nuclus accumbens. Synapse 49, 226–231 (2003).

  32. 32.

    & Neural systems of reinforcement for drug addiction: from actions to habits to compulsion. Nat. Neurosci. 8, 1481–1489 (2005).

  33. 33.

    Intense emotional responses to music: a test of the physiological arousal hypothesis. Psychol. Music 32, 371–388 (2004).

  34. 34.

    , & Chills as an indicator of individual emotional peaks. Ann. NY Acad. Sci. 1169, 351–354 (2009).

  35. 35.

    et al. Dopamine transmission in the human striatum during monetary reward tasks. J. Neurosci. 24, 4105–4112 (2004).

  36. 36.

    et al. Evidence for striatal dopamine release during a video game. Nature 393, 266–268 (1998).

  37. 37.

    & On music and reward. in The Neurobiology of Sensation and Reward (ed. Gottfried, J.A.) (CRC Press, 2011).

  38. 38.

    et al. Motion correction of multi-frame PET data in neuroreceptor mapping: simulation based validation. Neuroimage 47, 1496–1505 (2009).

  39. 39.

    , & Automatic 3D intersubject registration of MR volumetric data in standardized Talirach space. J. Comput. Assist. Tomogr. 18, 192–205 (1994).

  40. 40.

    , , & Parametric imaging of ligand-receptor binding in PET using a simplified reference region model. Neuroimage 6, 279–287 (1997).

  41. 41.

    & Simplified reference tissue model for PET receptor studies. Neuroimage 4, 153–158 (1996).

  42. 42.

    , & Saturation analysis in PET-analysis of errors due to non-perfect reference regions. J. Cereb. Blood Flow Metab. 14, 358–361 (1994).

  43. 43.

    & ANIMAL: Validation and application of nonlinear registration-based segmentation. Intern. J. Pattern Recognit. Artif. Intell. 11, 1271–1294 (1997).

  44. 44.

    , & Automatic quantification of MS lesions in 3D MRI Brain data sets: validation of INSECT. in Medical Image Computing and Computer-Assisted Intervention (eds. Wells, W.M., Colchester, A. & Delp, S.) 439–448 (Springer-Verlag, Cambridge, Massachusetts, 1998).

  45. 45.

    et al. A statistical method for the analysis of positron emission tomography neuroreceptor ligand data. Neuroimage 12, 245–256 (2000).

  46. 46.

    et al. Kinetic modeling of [11C]raclopride: combined PET microdialysis studies. J. Cereb. Blood Flow Metab. 17, 932–942 (1997).

  47. 47.

    et al. A unified statistical approach for determining significant signals in images of cerebral activation. Hum. Brain Mapp. 4, 58–73 (1996).

  48. 48.

    et al. A general statistical analysis for fMRI data. Neuroimage 15, 1–15 (2002).

  49. 49.

    et al. Striatal and extrastriatal dopamine release measured with PET and [(18)F]fallypride. Synapse 64, 350–362 (2010).

Download references

Acknowledgements

We thank the staff of the Montreal Neurological Institute PET and MR Units and the staff of the Centre for Interdisciplinary Research in Music Media and Technology for help with data acquisition, M. Ferreira and M. Bouffard for their assistance with data analysis, and G. Longo for assistance with stimulus preparation. This research was supported by funding from the Canadian Institutes of Health Research to R.J.Z., a Natural Science and Engineering Research Council stipend to V.N.S., a Jeanne Timmins Costello award to V.N.S. and Centre for Interdisciplinary Research in Music Media and Technology awards to V.N.S. and M.B.

Author information

Affiliations

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

    • Valorie N Salimpoor
    • , Kevin Larcher
    • , Alain Dagher
    •  & Robert J Zatorre
  2. International Laboratory for Brain, Music and Sound Research, Montreal, Quebec, Canada.

    • Valorie N Salimpoor
    •  & Robert J Zatorre
  3. Centre for Interdisciplinary Research in Music Media and Technology, Montreal, Quebec, Canada.

    • Valorie N Salimpoor
    • , Mitchel Benovoy
    •  & Robert J Zatorre
  4. Centre for Intelligent Machines, McGill University, Montreal, Quebec, Canada.

    • Mitchel Benovoy

Authors

  1. Search for Valorie N Salimpoor in:

  2. Search for Mitchel Benovoy in:

  3. Search for Kevin Larcher in:

  4. Search for Alain Dagher in:

  5. Search for Robert J Zatorre in:

Contributions

V.N.S., R.J.Z. and A.D. designed the study. V.N.S. and M.B. performed all experiments. V.N.S., M.B. and K.L. analyzed the data. V.N.S. and R.J.Z. wrote the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Valorie N Salimpoor or Robert J Zatorre.

Supplementary information

PDF files

  1. 1.

    Supplementary Text and Figures

    Supplementary Figures 1–3 and Supplementary Tables 1–4