Multivariate fMRI pattern analysis of fear perception across modalities

Abstract

The emotional expression of fear can be processed through a number of modalities, and of varying forms, however, much of the functional imaging literature has centered on investigating fear as expressed through faces. Findings point to an active involvement of the amygdala, and remain fairly consistent in other studies of unimodal fear perception; however, few studies have looked at within‐subject cross‐modal responses to fear. Thus, we approached this inquiry by testing 30 healthy young adults with fast, high‐resolution fMRI, recording the neural responses of fear perception, as expressed through faces, bodies, prosody, and vocalizations. The study was analyzed using a multivariate approach (multi‐voxel pattern analysis) and yielded a significant distinction in the responses associated with the perception of fearful vs. neutral emotions. Calculated weights highlighted areas in the amygdala and surrounding subcortical structures as contributing the greatest to the discrimination; however, a whole‐brain analysis was necessary to obtain above‐chance classification accuracy, suggesting that processing fear across modalities likely involves a broad, distributed network. Thus, our findings support a multivariate approach to studying a highly complex construct such as emotion, as it accounts for multiple voxels simultaneously and can accommodate the high subject‐level variability that oftentimes comes with studying emotion perception.

Negative content enhances stimulus‐specific cerebral activity during free viewing of pictures, faces, and words

“…This has not only been shown for pictures of negative compared to neutral complex scenes (Aldhafeeri, Mackenzie, Kay, Alghamdi, & Sluming, 2012;Lang et al, 1998;Sabatinelli, Bradley, Fitzsimmons, & Lang, 2005;Sambuco, Bradley, Herring, Hillbrandt, & Lang, 2020a) and fearful versus neutral faces (Vuilleumier, Armony, Driver, & Dolan, 2001), but also for emotional words (Herbert et al, 2009;Hoffmann, Mothes-Lasch, Miltner, & Straube, 2015). In line with studies showing converging emotional modulation of brain activation even across different modalities (Hayes & Northoff, 2011;Kim, Shinkareva, & Wedell, 2017;Whitehead & Armony, 2019), for example, visual and auditory, these results suggest a common network of brain structures underlying emotion processing (Lindquist, Wager, Kober, Bliss-Moreau, & Barrett, 2012), independent from the induction context.…”

Decoding of emotion expression in the face, body and voice reveals sensory modality specific representations

“…Note that no amygdala activity was reported in that study. The second study using passive listening or viewing of still bodies and comparing fear and neutral expressions also concludes about a distributed network of cortical and subcortical regions responsive to fear in the two stimulus types they used (Whitehead JC and JL Armony 2019). Of interest is their finding concerning the amygdalae and fear processing.…”

Effects of transcranial direct current stimulation on neural activity and functional connectivity during fear extinction

“…However, in Ganho-Ávila et al., 2022 , our early vs. late extinction analysis might have hindered the variability across the extinction session, that a trial-by-trial approach can offer. Additionally, recent studies have employed multivariate fMRI pattern analysis to clarify the neural mechanics associated with fear conditioning and expression while accounting for inter-subject variability and complex multi-voxel patterns ( Graner et al., 2020 ; Sjouwerman et al., 2020 ; Whitehead & Armony, 2019 ; Zhou et al., 2021 ).…”