Surprise-related activation in the nucleus accumbens interacts with music-induced pleasantness

Ofir Shany, Neomi Singer, Benjamin Paul Gold, Nori Jacoby, Ricardo Tarrasch, Talma Hendler, Roni Granot, Ofir Shany, Neomi Singer, Benjamin Paul Gold, Nori Jacoby, Ricardo Tarrasch, Talma Hendler, Roni Granot

Abstract

How can music-merely a stream of sounds-be enjoyable for so many people? Recent accounts of this phenomenon are inspired by predictive coding models, hypothesizing that both confirmation and violations of musical expectations associate with the hedonic response to music via recruitment of the mesolimbic system and its connections with the auditory cortex. Here we provide support for this model, by revealing associations of music-induced pleasantness with musical surprises in the activity and connectivity patterns of the nucleus accumbens (NAcc)-a central component of the mesolimbic system. We examined neurobehavioral responses to surprises in three naturalistic musical pieces using fMRI and subjective ratings of valence and arousal. Surprises were associated with changes in reported valence and arousal, as well as with enhanced activations in the auditory cortex, insula and ventral striatum, relative to unsurprising events. Importantly, we found that surprise-related activation in the NAcc was more pronounced among individuals who experienced greater music-induced pleasantness. These participants also exhibited stronger surprise-related NAcc-auditory cortex connectivity during the most pleasant piece, relative to participants who found the music less pleasant. These findings provide a novel demonstration of a direct link between musical surprises, NAcc activation and music-induced pleasantness.

Keywords: fMRI; music; nucleus accumbens; surprise; valence.

© The Author(s) 2019. Published by Oxford University Press.

Figures

Fig. 1
Fig. 1
Transient changes in subjective valence and arousal reports are modulated as a function of surprise level. Relative to US events, surprising musical events associated with an increased arousal and valence across all musical pieces (Glass, top; Mussorgsky, center; Ligeti, bottom). In Mussorgsky and Ligeti surprises also related to greater valence decrease. Level of surprise is denoted by grayscale (highest is equal to dark). Stars above the graph bars denote significant main effects in Glass and Mussorgsky and significant pairwise comparisons in Ligeti; asterisks below the graph bars indicate significance of pairwise comparisons in Glass and Mussorgsky; significance of results is indicated: *P <0.05; **P < 0.01; ***P ≤ 0.001; qFDR < 0.05. Error bars represent 1 deviation from the mean (SEM).
Fig. 2
Fig. 2
Modulation of brain activation as a function of surprise level. Across three distinct musical pieces [Glass, left (L); Mussorgsky, center; Ligeti, R], surprising events consistently elicited stronger activations relative to US events in the (1) auditory cortex, (2) VS and (3) anterior insula (P < 0.05, FDR-corrected). The high surprise vs US contrast is depicted for Glass and Mussorgsky. Images are presented in Talairach space and radiological convention.
Fig. 3
Fig. 3
Surprise-related activation and experienced pleasantness interact within the NAcc but not within the STG. (A) Subgroups’ clustering based on continuous valence reports. The continuous mean ratings on the scales of valence (L panel) and arousal (R panel) are denoted per group and musical piece (Glass, top; Mussorgsky, center; Ligeti, bottom). Note that while valence ratings clearly differentiate the two groups, arousal ratings do not. Thickness of shading represents 1 SEM. (B) ROI analysis in the NAcc and STG. Consistently across musical pieces, the high- but not low-pleasantness groups exhibited stronger activation in response to surprising events in the NAcc, relative to less surprising events (L panel). In contrast, groups showed similar surprise-related activation in the STG (R panel). Level of surprise is denoted by grayscale (highest is equal to dark). The high- and low-pleasantness groups are marked by blue and red contours, respectively. Stars above the graph bars denote interaction effects’ significance: *P < 0.05; **P = 0.01. Asterisks below the graph bars indicate the significance of pairwise comparisons: (*)P < 0.05, uncorrected; **P < 0.01; qFDR < 0.05. Error bars represent 1 SEM.
Fig. 4
Fig. 4
Surprise-related NAcc–STG functional connectivity varies as function of music-induced pleasantness. (A) The NAcc (L) and STG (R) ROIs used for a PPI analysis comparing the surprise-related functional connectivity between the high- and low-pleasantness groups. (B) Surprise-related connectivity is represented per group and musical piece (Glass, L; Mussorgsky, center; Ligeti, R) as the difference between PPI parameter estimates (beta) of surprising relative to US conditions. High- and low-pleasantness groups are marked by blue and red contours, respectively. The asterisk above the graph bars indicates the significance of group comparisons: *P < 0.005; qFDR < 0.05. Error bars represent 1 SEM.

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