Fear across the senses: brain responses to music, vocalizations and facial expressions

Abstract

Intrinsic emotional expressions such as those communicated by faces and vocalizations have been shown to engage specific brain regions, such as the amygdala. Although music constitutes another powerful means to express emotions, the neural substrates involved in its processing remain poorly understood. In particular, it is unknown whether brain regions typically associated with processing 'biologically relevant' emotional expressions are also recruited by emotional music. To address this question, we conducted an event-related functional magnetic resonance imaging study in 47 healthy volunteers in which we directly compared responses to basic emotions (fear, sadness and happiness, as well as neutral) expressed through faces, non-linguistic vocalizations and short novel musical excerpts. Our results confirmed the importance of fear in emotional communication, as revealed by significant blood oxygen level-dependent signal increased in a cluster within the posterior amygdala and anterior hippocampus, as well as in the posterior insula across all three domains. Moreover, subject-specific amygdala responses to fearful music and vocalizations were correlated, consistent with the proposal that the brain circuitry involved in the processing of musical emotions might be shared with the one that have evolved for vocalizations. Overall, our results show that processing of fear expressed through music, engages some of the same brain areas known to be crucial for detecting and evaluating threat-related information.

Keywords: amygdala; emotional expressions; fear; hippocampus; music; vocalizations.

Fig. 1

Statistical parametric map showing the significant clusters with the contrast of vocalizations > music (blue) and music > vocalizations (green).

Fig. 2

(A) Amygdala cluster associated with the main effect of fearful minus neutral expressions across domains ([−28, −8, −22] Z = 4.79). (B) Cluster-averaged parameter estimates for the conditions of interest. (C) Cluster-averaged evoked BOLD responses for fearful and neutral expressions corresponding to the three domains. a.u.: arbitrary units.

Fig. 3

(A)Significant clusters in the posterior insula for the main effect of fearful minus neutral expressions across domains, and (B) the corresponding cluster-averaged parameter estimates for the conditions of interest. Left [−38, −26, 2], right [42, −22, −6].

Fig. 4

Significant clusters in the temporal lobe for the contrasts (A) Fear minus neutral and (B) Happy minus neutral for musical expressions, and the corresponding cluster-averaged parameter estimates. (C) Significant clusters associated with the correlation between BOLD signal and intensity ratings, and the corresponding cluster-averaged scatter plots. The two points in red in each graph represents measures with high Cook’s Distance scores (Left: 0.37 and 0.11; Right: 0.93 and 0.1). Removing these outliers increased the correlation values of the clusters in the left and right hemispheres to 0.52 and 0.48 (P < 0.0001), respectively. (D) Cluster-averaged evoked BOLD responses for fearful and neutral music for the clusters depicted in C.