Stimulus arousal drives amygdalar responses to emotional expressions across sensory modalities

Abstract

The factors that drive amygdalar responses to emotionally significant stimuli are still a matter of debate - particularly the proneness of the amygdala to respond to negatively-valenced stimuli has been discussed controversially. Furthermore, it is uncertain whether the amygdala responds in a modality-general fashion or whether modality-specific idiosyncrasies exist. Therefore, the present functional magnetic resonance imaging (fMRI) study systematically investigated amygdalar responding to stimulus valence and arousal of emotional expressions across visual and auditory modalities. During scanning, participants performed a gender judgment task while prosodic and facial emotional expressions were presented. The stimuli varied in stimulus valence and arousal by including neutral, happy and angry expressions of high and low emotional intensity. Results demonstrate amygdalar activation as a function of stimulus arousal and accordingly associated emotional intensity regardless of stimulus valence. Furthermore, arousal-driven amygdalar responding did not depend on the visual and auditory modalities of emotional expressions. Thus, the current results are consistent with the notion that the amygdala codes general stimulus relevance across visual and auditory modalities irrespective of valence. In addition, whole brain analyses revealed that effects in visual and auditory areas were driven mainly by high intense emotional facial and vocal stimuli, respectively, suggesting modality-specific representations of emotional expressions in auditory and visual cortices.

Figure 1

Each condition was presented in one block, consisting of ten trials. Visual stimuli were presented for 658 ms, while acoustic stimuli were in average presented for 658 ms with a stimulus onset asynchrony of 2000 ms. When presenting auditory stimuli, a blank screen was presented simultaneously. Each block was presented twice resulting in 20 blocks per run. Sequence of blocks were counterbalanced between runs and across participants. Participants were instructed to perform a gender judgment task in order to ensure that participants paid attention to the presented voices and faces.

Figure 2

Enhanced activation in the right amygdala (x = 25, y = −4, z = −10) as a function of stimulus arousal for visual and auditory stimuli (CBP-corrected statistical map, initial voxel-level threshold p = 0.005). Bar plots show parameter estimates for visual (left side), and auditory (right side) stimuli. Parameter estimates refer to the mean cluster value, error bars indicate standard errors.

Figure 3

Significant activation cluster in posterior superior temporal sulcus (x = 48, y = −53, z = 18) as revealed by arousal contrast weights and significant activation clusters in medial superior temporal sulcus (x = 54, y = −16, z = 6) and fusiform gyrus (x = −39, y = −40, z = −8) as revealed by arousal × modality interaction contrast. Bar plots represent parameter estimates for arousal-driven effects in SMG, mSTS, and FG. Parameter estimates refer to peak voxels, error bars indicate standard errors.