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

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.

[1]  C. Aring,et al.  A CRITICAL REVIEW , 1939, Journal of neurology and psychiatry.

[2]  Some Empirical Findings , 1984 .

[3]  J. Sloboda.  Music Structure and Emotional Response: Some Empirical Findings , 1991 .

[4]  J. Litton,et al.  Saturation Analysis in PET—Analysis of Errors Due to Imperfect Reference Regions , 1994, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[5]  D. Collins,et al.  Automatic 3D Intersubject Registration of MR Volumetric Data in Standardized Talairach Space , 1994, Journal of computer assisted tomography.

[6]  J. Panksepp.  The emotional sources of "chills" induced by music. , 1995 .

[7]  A. Lammertsma,et al.  Simplified Reference Tissue Model for PET Receptor Studies , 1996, NeuroImage.

[8]  Karl J. Friston,et al.  A unified statistical approach for determining significant signals in images of cerebral activation , 1996, Human brain mapping.

[9]  Peter Dayan,et al.  A Neural Substrate of Prediction and Reward , 1997, Science.

[10]  Vincent J. Cunningham,et al.  Parametric Imaging of Ligand-Receptor Binding in PET Using a Simplified Reference Region Model , 1997, NeuroImage.

[11]  D. Louis Collins,et al.  Animal: Validation and Applications of Nonlinear Registration-Based Segmentation , 1997, Int. J. Pattern Recognit. Artif. Intell..

[12]  C. Krumhansl.  An exploratory study of musical emotions and psychophysiology. , 1997, Canadian journal of experimental psychology = Revue canadienne de psychologie experimentale.

[13]  W C Eckelman,et al.  Kinetic Modeling of [11C]Raclopride: Combined PET-Microdialysis Studies , 1997, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[14]  S. J. Gatley,et al.  Relationship between subjective effects of cocaine and dopamine transporter occupancy , 1997, Nature.

[15]  D. Brooks,et al.  Evidence for striatal dopamine release during a video game , 1998, Nature.

[16]  Alan C. Evans,et al.  Automatic Quantification of MS Lesions in 3D MRI Brain Data Sets: Validation of INSECT , 1998, MICCAI.

[17]  K. Worsley,et al.  A Statistical Method for the Analysis of Positron Emission Tomography Neuroreceptor Ligand Data , 2000, NeuroImage.

[18]  M. Laruelle.  Imaging Synaptic Neurotransmission with in Vivo Binding Competition Techniques: A Critical Review , 2000, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[19]  J. Sloboda,et al.  Psychological perspectives on music and emotion , 2001 .

[20]  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.

[21]  A. Dagher,et al.  Amphetamine-Induced Increases in Extracellular Dopamine, Drug Wanting, and Novelty Seeking: A PET/[11C]Raclopride Study in Healthy Men , 2002, Neuropsychopharmacology.

[22]  Alan C. Evans,et al.  A General Statistical Analysis for fMRI Data , 2000, NeuroImage.

[23]  J. O'Doherty,et al.  Neural Responses during Anticipation of a Primary Taste Reward , 2002, Neuron.

[24]  A. Dagher,et al.  Alcohol promotes dopamine release in the human nucleus accumbens , 2003, Synapse.

[25]  Alain Dagher,et al.  Feeding-induced dopamine release in dorsal striatum correlates with meal pleasantness ratings in healthy human volunteers , 2003, NeuroImage.

[26]  Laurette Dubé,et al.  The content and structure of laypeople's concept of pleasure , 2003, Cognition & emotion.

[27]  R. Wise.  Dopamine, learning and motivation , 2004, Nature Reviews Neuroscience.

[28]  N. Rickard.  Intense emotional responses to music: a test of the physiological arousal hypothesis , 2004 .

[29]  F. McGlone,et al.  Dopamine Transmission in the Human Striatum during Monetary Reward Tasks , 2004, The Journal of Neuroscience.

[30]  Alain Dagher,et al.  The hedonic response to cigarette smoking is proportional to dopamine release in the human striatum as measured by positron emission tomography and [11C]raclopride , 2004, Synapse.

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

[32]  T. Robbins,et al.  Neural systems of reinforcement for drug addiction: from actions to habits to compulsion , 2005, Nature Neuroscience.

[33]  S. Haber,et al.  Reward-Related Cortical Inputs Define a Large Striatal Region in Primates That Interface with Associative Cortical Connections, Providing a Substrate for Incentive-Based Learning , 2006, The Journal of Neuroscience.

[34]  Brian Knutson,et al.  Linking nucleus accumbens dopamine and blood oxygenation , 2007, Psychopharmacology.

[35]  T. Robbins,et al.  Erratum: Neural systems of reinforcement for drug addition: from actions to habits to compulsion , 2006, Nature Neuroscience.

[36]  Alain Dagher,et al.  Modeling sensitization to stimulants in humans: an [11C]raclopride/positron emission tomography study in healthy men. , 2006, Archives of general psychiatry.

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

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

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

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

[41]  H. Heinze,et al.  Mesolimbic Functional Magnetic Resonance Imaging Activations during Reward Anticipation Correlate with Reward-Related Ventral Striatal Dopamine Release , 2008, The Journal of Neuroscience.

[42]  W. Dowling.  Emotion and Meaning in Music , 2008 .

[43]  Eckart Altenmüller,et al.  Chills As an Indicator of Individual Emotional Peaks , 2009, Annals of the New York Academy of Sciences.

[44]  R. Zatorre,et al.  The Rewarding Aspects of Music Listening Are Related to Degree of Emotional Arousal , 2009, PloS one.

[45]  W. K. Simmons,et al.  Circular analysis in systems neuroscience: the dangers of double dipping , 2009, Nature Neuroscience.

[46]  E. Kim,et al.  A review of molecular imaging studies reaching the clinical stage. , 2009, European journal of radiology.

[47]  D. Louis Collins,et al.  Motion correction of multi-frame PET data in neuroreceptor mapping: Simulation based validation , 2009, NeuroImage.

[48]  Mitul A. Mehta,et al.  The dopaminergic basis of human behaviors: A review of molecular imaging studies , 2009, Neuroscience & Biobehavioral Reviews.

[49]  Vivian V. Valentin,et al.  Overlapping prediction errors in dorsal striatum during instrumental learning with juice and money reward in the human brain. , 2009, Journal of neurophysiology.

[50]  Mark Slifstein,et al.  Striatal and extrastriatal dopamine release measured with PET and [18F] fallypride , 2010, Synapse.

[51]  S. Haber,et al.  The Reward Circuit: Linking Primate Anatomy and Human Imaging , 2010, Neuropsychopharmacology.

[52]  David Margulis,et al.  Musical expectancy and thrills , 2011 .