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. 2021 Apr 28;41(17):3889-3899.
doi: 10.1523/JNEUROSCI.0727-20.2020. Epub 2021 Mar 29.

Unraveling the Temporal Dynamics of Reward Signals in Music-Induced Pleasure with TMS

Ernest Mas-Herrero  1   2 , Alain Dagher  3 , Marcel Farrés-Franch  3   4 , Robert J Zatorre  5   4   6
Affiliations

Unraveling the Temporal Dynamics of Reward Signals in Music-Induced Pleasure with TMS

Ernest Mas-Herrero et al. J Neurosci. .

Abstract

Music's ability to induce feelings of pleasure has been the subject of intense neuroscientific research lately. Prior neuroimaging studies have shown that music-induced pleasure engages cortico-striatal circuits related to the anticipation and receipt of biologically relevant rewards/incentives, but these reports are necessarily correlational. Here, we studied both the causal role of this circuitry and its temporal dynamics by applying transcranial magnetic stimulation (TMS) over the left dorsolateral PFC combined with fMRI in 17 male and female participants. Behaviorally, we found that, in accord with previous findings, excitation of fronto-striatal pathways enhanced subjective reports of music-induced pleasure and motivation, whereas inhibition of the same circuitry led to the reduction of both. fMRI activity patterns indicated that these behavioral changes were driven by bidirectional TMS-induced alteration of fronto-striatal function. Specifically, changes in activity in the NAcc predicted modulation of both hedonic and motivational responses, with a dissociation between pre-experiential versus experiential components of musical reward. In addition, TMS-induced changes in the fMRI functional connectivity between the NAcc and frontal and auditory cortices predicted the degree of modulation of hedonic responses. These results indicate that the engagement of cortico-striatal pathways and the NAcc, in particular, is indispensable to experience rewarding feelings from music.SIGNIFICANCE STATEMENT Neuroimaging studies have shown that music-induced pleasure engages cortico-striatal circuits involved in the processing of biologically relevant rewards. Yet, these reports are necessarily correlational. Here, we studied both the causal role of this circuitry and its temporal dynamics by combining brain stimulation over the frontal cortex with functional imaging. Behaviorally, we found that excitation and inhibition of fronto-striatal pathways enhanced and disrupted, respectively, subjective reports of music-induced pleasure and motivation. These changes were associated with changes in NAcc activity and NAcc coupling with frontal and auditory cortices, dissociating between pre-experimental versus experiential components of musical reward. These results indicate that the engagement of cortico-striatal pathways, and the NAcc in particular, is indispensable to experience rewarding feeling from music.

Keywords: NAcc; TMS; motivation; music; pleasure; reward.

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Figures

Figure 1.
Figure 1.
Schematic of the experimental paradigm. Each trial started with a fixation cross lasting 20 s, followed by a musical excerpt (with a duration of 45 s, in the figure represented by the power spectral density of an audio track). While listening to music, the participants had to rate the degree of pleasure they were experiencing in real time by pressing the corresponding button. Real-time ratings of pleasure were used to identify Pre-experience and Experience time periods. The Experience phase was modeled as events time-locked to the moment at which a participant pressed a button to indicate a change in pleasure ratings. The green line is only for illustrative purposes since durations were set to 0 (see Materials and Methods). The Pre-experience epochs were defined as the 10 s before a button press. At the end of each excerpt, participants had to indicate the amount of money they were willing to pay (only for the experimenter-selected excerpts), the familiarity, and the arousal. Pre, Pre-experience; Exp., Experience.
Figure 2.
Figure 2.
Main behavioral results of the study. Change with respect to the Sham condition following both iTBS and cTBS for liking rates (illustrating the main effect of TMS session from the repeated-measures ANOVA, averaged across self- and experimenter-selected excerpts, d = 0.81) (a), the money spent to buy experimenter-selected music (d = 0.50) (b), and the number (d = 0.51) (c) and time (d = 0.57) (d) reporting chills. In all four variables, the excitatory iTBS condition leads to positive change, whereas the inhibitory cTBS condition has the opposite effect. Violin plots represent kernel probability density. White circle dots represent the average. White error bars indicate SD.
Figure 3.
Figure 3.
Main fMRI results. a, b, Left, Graph represents the parametric effect of SHVs (top, Pre-experience; bottom, Experience) on percent signal change for the reward circuitry (including bilateral NAcc, caudate, putamen, and vmPFC). Note the linear increase in percent signal change as the pleasure increase during both the Pre-experience and the Experience following iTBS and Sham sessions, but not cTBS. Middle, Bar graph represents the resulting slopes (individual and the average) of the SHV regressor for each session and phase. Right, Contrast estimates reflecting the slopes of the SHVs regressors following either iTBS or cTBS with respect to Sham for each of the ROIs and reward phase. c, Reward-related ROIs included in the study. NP, No pleasure; LP, low pleasure; HP, high pleasure; CH, chills.
Figure 4.
Figure 4.
Robust regression analysis. Scatter plots represent the relationship between individual differences in TMS modulation of subjective reports of pleasure and motivation, on the one hand, and subject-specific TMS-induced changes in the NAcc activity during both the Pre-experience and Experience phases. *Pbonf < 0.05.
Figure 5.
Figure 5.
Functional connectivity using the left dlPFC as a seed. Scatter plots represent the significant relationships between individual differences in TMS modulation of subjective reports of pleasure and TMS-induced changes in the functional connectivity strength between the dlPFC and reward circuit in the Pre-experience phase.
Figure 6.
Figure 6.
Functional connectivity using the right and left STG as a seed. Scatter plots represent the relationship between individual differences in TMS modulation of subjective reports of pleasure and TMS-induced changes in the functional connectivity strength between the right (top) and the left (bottom) STG and the NAcc in the Experience phase. Only changes in functional connectivity between the right STG and the right NAcc were associated with changes in subjective reports of pleasure. *Pbonf < 0.05.
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References

    1. Albouy P, Mattout J, Sanchez G, Tillmann B, Caclin A (2015) Altered retrieval of melodic information in congenital amusia: insights from dynamic causal modeling of MEG data. Front Hum Neurosci 9:20. 10.3389/fnhum.2015.00020 - DOI - PMC - PubMed
    1. Bartra O, McGuire JT, Kable JW (2013) The valuation system: a coordinate-based meta-analysis of BOLD fMRI experiments examining neural correlates of subjective value. Neuroimage 76:412–427. 10.1016/j.neuroimage.2013.02.063 - DOI - PMC - PubMed
    1. Bastos AM, Usrey WM, Adams RA, Mangun GR, Fries P, Friston KJ (2012) Canonical microcircuits for predictive coding. Neuron 76:695–711. 10.1016/j.neuron.2012.10.038 - DOI - PMC - PubMed
    1. Berridge KC, Kringelbach ML (2008) Affective neuroscience of pleasure: reward in humans and animals. Psychopharmacology (Berl) 199:457–480. 10.1007/s00213-008-1099-6 - DOI - PMC - PubMed
    1. Berridge KC, Kringelbach ML (2015) Pleasure systems in the brain. Neuron 86:646–664. 10.1016/j.neuron.2015.02.018 - DOI - PMC - PubMed

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