Dopamine Release during Anticipation and Experience of Emotion to Music

 

Nature NEUROSCIENCE. VOLUME 14, NUMBER 2, FEBRUARY 2011, p.257

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

Valorie N Salimpoor, et.al.

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

International Laboratory for Brain, Music and Sound Research, Montreal, Quebec, Canada

Centre for Interdisciplinary Research in Music Media and Technology, Montreal, Quebec, Canada

Centre for Intelligent Machines, McGill University, Montreal, Quebec, Canada

[paraphrase]

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.

 Humans experience intense pleasure to certain stimuli, such as food, psychoactive drugs and money; these rewards are largely mediated by dopaminergic activity in the mesolimbic system, which has been implicated in reinforcement and motivation. These rewarding stimuli are either biological reinforcers that are necessary for survival, synthetic chemicals that directly promote dopaminergic neurotransmission, or tangible items that are secondary rewards. However, humans have the ability to obtain pleasure from more abstract stimuli, such as music and art, which are not directly essential for survival and cannot be considered to be secondary or conditioned reinforcers. These stimuli have persisted through cultures and generations and are pre-eminent in most people’s lives. Notably, the experience of pleasure to these abstract stimuli is highly specific to cultural and personal preferences, which can vary tremendously across individuals.

Most people agree that music is an especially potent pleasurable stimulus that is frequently used to affect emotional states. It has been empirically demonstrated that music can effectively elicit highly pleasurable emotional responses and previous neuroimaging stud­ies have implicated emotion and reward circuits of the brain during pleasurable music listening, particularly the ventral striatum, suggesting the possible involvement of dopaminergic mechanisms. However, the role of dopamine has never been directly tested. We used ligand-based positron emission tomography (PET) scanning to estimate dopamine release specifically in the striatum on the basis of the competition between endogenous dopamine and [11C]raclopride for binding to dopamine D2 receptors. Pleasure is a subjective phenomenon that is difficult to assess objectively. However, physiological changes occur during moments of extreme pleasure, which can be used to index pleasurable states in response to music. We used the ‘chills’ or ‘musical frisson’11 response, a well-established marker of peak emotional responses to music. Chills involve a clear and discrete pattern of autonomic nervous system (ANS) arousal, which allows for objective verification through psychophysiological meas­urements. Thus, the chills response can be used to objectively index pleasure, a subjective phenomenon that would otherwise be difficult to operationalize, and allows us to pinpoint the precise time of maxi­mal pleasure.

Research study — Neuronal Imaging of Dopamine Dynamics

 

DISCUSSION

Our results provide, to the best of our knowledge, the first direct evidence that the intense pleasure experienced when listening to music is associated with dopamine activity in the mesolimbic reward system, including both dorsal and ventral striatum. This phylogenetically ancient circuitry has evolved to reinforce basic biological behaviors with high adaptive value. However, the rewarding qualities of music listening are not obviously directly adaptive. That is, musical stimuli, similar to other aesthetic stimuli, are perceived as being rewarding by the listener, rather than exerting a direct biological or chemical influence. Furthermore, the perception that results in a rewarding response is relatively specific to the listener, as there is large vari­ability in musical preferences amongst individuals. Thus, through complex cognitive mechanisms, humans are able to obtain pleasure from music2, a highly abstract reward consisting of just a sequence of tones unfolding over time, which is comparable to the pleasure experienced from more basic biological stimuli.

One explanation for this phenomenon is that it is related to enhance­ment of emotions. The emotions induced by music are evoked, among other things, by temporal phenomena, such as expectations, delay, tension, resolution, prediction, surprise and anticipation. Indeed, we found a temporal dissociation between distinct regions of the striatum while listening to pleasurable music. The combined psychophysiological, neurochemical and hemodynamic procedure that we used revealed that peaks of ANS activity that reflect the expe­rience of the most intense emotional moments are associated with dopamine release in the NAcc. This region has been implicated in the euphoric component of psychostimulants such as cocaine and is highly interconnected with limbic regions that mediate emotional responses, such as the amygdala, hippocampus, cingulate and ven­tromedial prefrontal cortex. In contrast, immediately before the climax of emotional responses there was evidence for relatively greater dopamine activity in the caudate. This subregion of the striatum is interconnected with sensory, motor and associative regions of the brain and has been typically implicated in learning of stimulus-response associations and in mediating the reinforcing qualities of rewarding stimuli such as food. Our findings indicate that a sense of emotional expectation, prediction and anticipation in response to abstract pleasure can also result in dopamine release, but primarily in the dorsal striatum. Previous studies have found that amphetamine-induced dopamine release in the NAcc spreads to more dorsal regions after repeated exposure to the drug, which suggests that this area may be involved in improved predictability and anticipation of a reward. Similarly, previous studies involving rewards such as food and smoking that contain a number of contextual predicting cues (for example, odor and taste) also found dorsal striatum dopamine release. Conversely, in studies in which there were no contextual cues or experience with the drugs involved, dopamine release was largely observed in the ventral striatum. Finally, evidence from animal research also suggests that, as rewards become better pre­dicted, the responses that initiated in the ventral regions move more dorsally in the striatum. These results are consistent with a model in which repeated exposure to rewards associated with a specific context gradually shift the response from ventral to dorsal and further suggest that contextual cues that allow prediction of a reward, in our case the sequences of tones leading up to the peak pleasure moments, may also act as reward predictors mediated via the dorsal striatum.

Another noteworthy finding is the correspondence between behavio­ral and imaging results, which strengthens the evidence for the distinct roles of dorsal and ventral striatum. We found a positive correlation between subject-reported intensity of chills and dopamine release in the NAcc during [11C]raclopride PET scanning, which confirms the fMRI results that peak pleasure responses are associated with this region. Furthermore, the number of chills reported by listeners during the PET scan was correlated with dopamine release in the caudate, which is consistent with the fMRI results showing increased activity in this region during anticipation of peak emotional responses; as greater number of chills suggests increased incidence of anticipation, greater dopamine release would be expected in this area.

It is important to note that chills are not necessarily pleasurable per se, as they can be unpleasant in other contexts (for example, as a result of intense fear). Instead, chills are physiological markers of intense ANS arousal, which in turn is believed to underlie peak pleasure during music listening; we used chills here only to allow objective quantification of a highly subjective response that would be otherwise difficult to measure and because they afford preci­sion as to the time at which the peak pleasure occurred. As such, chills are byproducts, and not a cause of the emotional responses. Thus, it is important to clarify that, although chills index peak emotional responses in this group of people, the specific experience of chills is not necessary to result in neural activity in the striatum, a finding that is consistent with less-specific analyses performed in previous studies. This conclusion is confirmed by our findings that, even when the chills epochs were excluded from the analysis, there was still a significant linear relationship between increases in self-reported pleasure and increases in hemodynamic activity in the regions that showed dopamine release. Furthermore, when chills were reported, maximal signal was seen in the NAcc voxels that showed a linear increase as participants progressed from neutral to low pleasure to high pleasure, further confirming that chills represented the peak of pleasure in this group. This finding is also consistent with the finding that the degree of binding potential decrease in the NAcc for each participant was positively correlated with the degree of pleasure reported from listening to the musical excerpts, irrespective of the number of chills that were experienced.

It should be noted that there was some activity in the ventral stria­tum during the anticipation phase at lower statistical thresholds, consistent with other studies using different stimuli. However, we found that, during the anticipatory phase, there was also increased BOLD response in the caudate (more so than the NAcc), which then shifted more ventromedially as participants reported experiencing peak reward. This is an important finding because the stimu­lus that we are using is a dynamic reward with a temporal component, allowing examination of the reward in real time as it progresses from anticipation to peak pleasure states, which is generally not possible because of limitations with movement inside the PET scanner. Some studies administered the pleasurable stimulus (for example, food) immediately before the scan and measured subsequent dopamine release, in which case anticipation and consumption cannot be dis­tinguished. Other studies measured the anticipation phase online, with the promise of the delivery of the tangible reward after the scan, in which case the consumption phase is missed. Music is a unique reward that allows assessment of all reward phases online, from the point that a single note is heard to the point at which maximum pleasure is reached.

The anatomical dissociation between the anticipatory and consum­matory phases during intensely pleasurable music listening suggests that distinct mechanisms are involved. This distinction may map onto the ‘wanting’ and ‘liking’ phases of a reward in an error prediction model. The anticipatory phase, set off by temporal cues signaling that a potentially pleasurable auditory sequence is coming, can trigger expectations of euphoric emotional states and create a sense of want­ing and reward prediction. This reward is entirely abstract and may involve such factors as suspended expectations and a sense of resolu­tion. Indeed, composers and performers frequently take advantage of such phenomena, and manipulate emotional arousal by violating expectations in certain ways or by delaying the predicted outcome (for example, by inserting unexpected notes or slowing tempo) before the resolution to heighten the motivation for completion. The peak emotional response evoked by hearing the desired sequence would represent the consummatory or liking phase, representing fulfilled expectations and accurate reward prediction. We propose that each of these phases may involve dopamine release, but in different sub­circuits of the striatum, which have different connectivity and func­tional roles.

The notion that dopamine can be released in anticipation of an abstract reward (a series of tones) has important implications for understanding how music has become pleasurable. However, the pre­cise source of the anticipation requires further investigation. A sense of anticipation may arise through one’s familiarity with the rules that underlie musical structure, such that listeners are anticipating the next note that may violate or confirm their expectations, in turn leading to emotional arousal, or alternatively it may arise through familiarity with a specific piece and knowing that a particularly pleasant section is coming up. These components are not mutually exclusive, as the second likely evolves from the first, and the overall anticipation is likely to be a combination of both. Nonetheless, the subtle differences that exist between them will need to be disentangled through future experiments that are specifically designed to parse out this distinc­tion. Abstract rewards are largely cognitive in nature and our results pave the way for future work to examine nontangible rewards that humans consider rewarding for complex reasons.

Dopamine is pivotal for establishing and maintaining behavior. If music-induced emotional states can lead to dopamine release, as our findings indicate, it may begin to explain why musical experiences are so valued. These results further speak to why music can be effec­tively used in rituals, marketing or film to manipulate hedonic states. Our findings provide neurochemical evidence that intense emotional responses to music involve ancient reward circuitry and serve as a starting point for more detailed investigations of the biological sub­strates that underlie abstract forms of pleasure.

 

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