How music alters a kiss: superior temporal gyrus controls fusiform-amygdalar effective connectivity

Abstract

While watching movies, the brain integrates the visual information and the musical soundtrack into a coherent percept. Multisensory integration can lead to emotion elicitation on which soundtrack valences may have a modulatory impact. Here, dynamic kissing scenes from romantic comedies were presented to 22 participants (13 females) during functional magnetic resonance imaging scanning. The kissing scenes were either accompanied by happy music, sad music or no music. Evidence from cross-modal studies motivated a predefined three-region network for multisensory integration of emotion, consisting of fusiform gyrus (FG), amygdala (AMY) and anterior superior temporal gyrus (aSTG). The interactions in this network were investigated using dynamic causal models of effective connectivity. This revealed bilinear modulations by happy and sad music with suppression effects on the connectivity from FG and AMY to aSTG. Non-linear dynamic causal modeling showed a suppressive gating effect of aSTG on fusiform-amygdalar connectivity. In conclusion, fusiform to amygdala coupling strength is modulated via feedback through aSTG as region for multisensory integration of emotional material. This mechanism was emotion-specific and more pronounced for sad music. Therefore, soundtrack valences may modulate emotion elicitation in movies by differentially changing preprocessed visual information to the amygdala.

Keywords: emotion; fMRI; multisensory integration; non-linear DCM; superior temporal gyrus.

Fig. 1

Experimental design and brain activations. In the upper panel, the mute kissing scenes are illustrated with behavioral ratings and brain activations (A, green). The lower panel depicts both audiovisual conditions (B, red). The additive overlay is indicated by yellow colored activations (B, yellow). All activations depicted P < 0.05 FWE whole-brain corrected, cluster extent threshold k > 5 voxels.

Fig. 2

Model space. Models 1–16 present all possible forward and backward connection and bidirectional modulations of happy and sad music as red arrows. (A1) Initial model family of connectivity without non-linear modulation of aSTG. (A2) Includes the non-linear modulation on the connection between AMY and FG. (A3) Winning family with a non-linear modulation on the connection from FG to AMY. All models were tested within the two non-linear families, except for model 1 in the bilinear family (A1), resulting in a model space of 47 models total. To note, the same model space was tested in the two hemispheres separately. For clarity the red arrow shows the modulatory input of music, but in fact happy and sad music were modeled separately.

Fig. 3

Regional brain activations. The emotion effect of music (happy > sad) is located in the aSTG. The plot shows parameter estimates including betas at the individual peak within a 12 mm sphere around the group peak in the right aSTG with error bars indicating standard errors. All activations depicted P < 0.05 FWE whole-brain corrected, cluster extent threshold k > 5 voxels. Maximum t values in the left hemisphere t = 10.11 and in the right hemisphere t = 10.43. Coordinates are listed in Table 2.

Fig. 4

Bayesian model selection. Results of Bayesian model selection for the left Hemisphere (LH, A1) and the right hemisphere (RH, A2). EP are reported as a measure of relative model fit. From left to right: Family selection of bilinear (BL) and non-linear (NL) model families, family selection of the two non-linear families: aSTG on AMY to FG connectivity (AMY ⇒ FG) and aSTG on FG to AMY connectivity (FG ⇒ AMY) and model selection for the model-subspace containing 16 models with all possible combinations of happy and sad music modulation. The winning models are number 3 (B2—model 3) and 4 (B1—model 4) for the left hemisphere and model 4 (B1—model 4) for the right hemisphere with backward projections from AMY and FG to aSTG.

Fig. 5

Bilinear Modulation on the connection from FG to aSTG. In both hemispheres, suppressing influence of sad music on the connection from FG to aSTG was significantly stronger for sad than for happy music resulting in enhanced neural propagation of the FG to AMY. Error bars indicate standard error. **P < 0.001.