Interactions between emotion and action in the brain

Abstract

A growing literature supports the existence of interactions between emotion and action in the brain, and the central participation of the anterior midcingulate cortex (aMCC) in this regard. In the present functional magnetic resonance imaging study, we sought to investigate the role of self-relevance during such interactions by varying the context in which threating pictures were presented (with guns pointed towards or away from the observer). Participants performed a simple visual detection task following exposure to such stimuli. Except for voxelwise tests, we adopted a Bayesian analysis framework which evaluated evidence for the hypotheses of interest, given the data, in a continuous fashion. Behaviorally, our results demonstrated a valence by context interaction such that there was a tendency of speeding up responses to targets after viewing threat pictures directed towards the participant. In the brain, interaction patterns that paralleled those observed behaviorally were observed most notably in the middle temporal gyrus, supplementary motor area, precentral gyrus, and anterior insula. In these regions, activity was overall greater during threat conditions relative to neutral ones, and this effect was enhanced in the directed towards context. A valence by context interaction was observed in the aMCC too, where we also observed a correlation (across participants) of evoked responses and reaction time data. Taken together, our study revealed the context-sensitive engagement of motor-related areas during emotional perception, thus supporting the idea that emotion and action interact in important ways in the brain.

Keywords: Action; Anterior midcingulate cortex; Emotion; Self-relevance; fMRI.

Fig. 1.. Experimental design.

Each block contained three trials, each of which began with the presentation of a picture together with a central fixation cross. Three seconds after picture onset, a square (cue) appeared around the fixation cross, indicating that the target would appear at any moment. The target, a small central circle, appeared 700–1, 200 ms after the square, and both remained on until the end of the trial. The fixation cross, the cue, and target were shown over the picture. Example of threat stimuli directed towards and directed away from the participant, and neutral stimuli directed towards and directed away from the participant are presented in a clockwise fashion.

Fig. 2.. Different probability definitions and goals of conventional and Bayesian frameworks.

Left: Statistical inferences under null hypothesis significance testing are based on how extreme the data are in the context of the null hypothesis. Green/yellow tails symbolize a two-sided significance level of 0.05/0.1. In the example, the data produces a t-value of 2.85 (small gray square). Right: Inferences under the Bayesian framework directly address the question of research interest: what is the probability of the effect magnitude being greater than 0 with the data at hand? The “output” in a Bayesian inference comprises the entire posterior density function, which summarizes the uncertainty in estimating the effect magnitude.

Fig. 3.. Behavioral data and Bayesian posterior density plots.

(A) The circles show reaction time (RT, ms) differences (threat minus neutral), and a behavioral interaction index (RT difference during directed towards minus RT difference during directed away). Thicker lines mark the mean and thinner lines the deciles for each experimental condition. The thin purple line marks the shift between means. Data illustrations used some of the graphical tools proposed by Rousselet et al. (Rousselet et al., 2017). (B) Bayesian posterior density plots of the valence by context interaction effect, the main effect of valence, and the main effect of context for RT data. Inferences under the Bayesian framework directly address the probability of the effect magnitude being greater than 0, which we call P+. The color bar represents P+. Note that the reddish to dark purple color associated with small values of P+ convey support that the effect is negative; in this case, P+ = 0.04 indicates that the probability of theeffect being positive is only 0.04, so that the probability of it being negative is 0.96.

Fig. 4.. Voxelwise analysis:

Main effect of valence. See Table 1 for the Tailarach coordinates. The color bar represents the value of the F-statistic. Abbreviations: A: Anterior; AI: Anterior insula; Amy: Amygdala; IFG: Inferior frontal gyrus; L: Left; LG: Lingual gyrus; MCC: Middle cingulated cortex; MTG: Middle temporal gyrus; P: Posterior; PG: Precentral gyrus; Put: Putamen; R: Right; SFG: Superior frontal gyrus; SMA: Supplementary motor area; SPL: Superior parietal lobule.

Fig. 5.. Voxelwise analysis:

Valence by context interaction effect. See Table 3 for the Tailarach coordinates. The color bar represents the value of the F-statistic. Abbreviations: IFGop/AI: Inferior frontal gyrus pars opercularis/anterior insula; IOG: Inferior occipital gyrus; L: Left; LG: Lingual gyrus; R: Right; SFG: Superior frontal gyrus; SMA: Supplementary motor area.

Fig. 6.. Bayesian posterior density plots of the valence by context interaction for ROIs reported in Table 1.

The color bar indicates P+, the probability of the effect being greater than zero. Larger values of P+ convey support that the activity was greater for (Threat - Neutral)_Towards relative to (Threat - Neutral)_Away; small values of P+ convey support of the reverse pattern. The color bar represents P+. See the caption of Fig. 3 for discussion of interpretation.

Fig. 7.. Regions of interest and valence by context interaction.

(A) Supplementary Motor Area (11, 8, 56) (B) Precentral Gyrus (38, 7, 38) (C) Left Anterior Insula (34, 26, 8) (D) Right Middle temporal Gyrus (MTG, Right: 44, −67, −7) (E) Left Middle temporal Gyrus (MTG, −46, −64, −1). Circles represent the mean parameter estimate for each subject per condition: ThreatTowards, Neutral_Towards, Threat_Away, Neutral_Away. The interaction index was calculated as follows: ((Threat - Neutral)_Towards - (Threat - Neutral)_Away). Thicker lines mark the mean and thinner lines the deciles for each experimental condition. The thin purple line marks the shift between means. Data illustrations used some of the graphical tools proposed by Rousselet et al. (Rousselet et al., 2017).

Fig. 8.. Anterior middle cingulate cortex (aMCC).

(A) The anatomical ROI (green) is shown together with the midcingulate cluster that exhibited a main effect of valence (orange); the overlap between the two is shown in red. (B) Bayesian posterior density plots of interaction ((Threat - Neutral)_Towards − (Threat-Neutral)_Away), valence ((Towards + Away)_Threat − (Towards + Away)_Neutral) and context ((Threat + Neutral)_Towards − (Threat + Neutral)_Away) effect for anterior right and left middle cingulate ROI based on atlas-based anatomical ROIs. The color bar indicates P+, the probability of the effect being greater than zero. The color bar represents P+. See the caption of Fig. 3 for discussion of interpretation. (C) Parameter estimates for the anatomical aMCC ROI. (see Fig. 7 for additional definitions). (D-E) Brain-behavior correlations in the directed towards (top) and in the directed away context (bottom) for the left (D) and right (E) aMCC.

Fig. 9.. Brain-behavior relationship in regions showing evidence of an interaction between valence and context.

(A) Bayesian posterior density plots of the brain-behavior correlation for the towards context, the away context, and the difference between them. The color bar indicates P+, the probability of the effect being greater than zero. See the caption of Fig. 3 for discussion of interpretation. (B) Brain-behavior correlation in the directed towards (left plots) and in the directed away contexts (right plots) for the right anterior middle cingulate cortex (R aMCC, functionally defined), right supplementary motor area (rSMA), left anterior insula and right precentral gyrus.