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.

Figures at a glance

leftFigure 1: Positive correlation between emotional arousal and intensity of chills during PET scanning.
The mean intensity of chills reported by each participant during the PET scanning session was significantly correlated with psychophysiological measurements that were also acquired during the scan. These are indicative of increased sympathetic nervous system activity, suggesting that the intensity of chills is a good marker of peak emotional arousal (Supplementary Table 1). The y axis represents standardized z scores for each biosignal. See main text for P-values.

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Figure 2: Evidence for dopamine release during pleasurable music listening.
(a) Statistical parametric maps (t statistic on sagittal, coronal and axial slices) reveal significant (P < 0.001) [11C]raclopride binding potential (BP) decreases bilaterally in the caudate, putamen and NAcc (white arrows) during pleasurable compared with neutral music listening (Supplementary Table 2), indicating increased dopamine release during pleasurable music. (b) Changes in binding potential (BP) values plotted separately for each individual; note that the change was consistent for the majority of people at each site.

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Figure 3: Combined fMRI and PET results reveal temporal distinctions in regions showing dopamine release.
(a) [11C]raclopride PET scan results were spatially conjoined with the fMRI results by creating a mask of significant dopamine release overlayed on BOLD response t maps during each condition. (b) Hemodynamic responses and dopamine activity were maximal in the caudate during anticipatory phases, but shifted more ventrally to NAcc during peak emotional responses. (c) Percent signal change in BOLD response relative to the mean was calculated from the peak voxel of the caudate and NAcc clusters based on the [11C]raclopride PET data. Voxels showing maximum dopamine release in the caudate and NAcc (Supplementary Table 2) were identified and percent BOLD signal change was calculated during the fMRI epochs associated with peak emotional responses; values were interpolated for each second preceding this response for each individual, up to 15 s, which was defined as the anticipatory period based on previous findings15 (see Online Methods for additional details). We found increased activity during anticipation (A1-A15) and decreased activity during peak emotional response (C1-C4) for the caudate, but a continuous increase in activity in NAcc with a maximum during peak emotional responses. The mean signal for neutral epochs for the NAcc and caudate clusters are also plotted for reference, as are the 5 s preceding the anticipation epochs.

For the entire article, and picture scans of the brain (figures mentioned above) in this study, go to:
http://www.nature.com/neuro/journal/vaop/ncurrent/full/nn.2726.html