Self-regulatory depletion increases emotional reactivity in the amygdala

Abstract

The ability to self-regulate can become impaired when people are required to engage in successive acts of effortful self-control, even when self-control occurs in different domains. Here, we used functional neuroimaging to test whether engaging in effortful inhibition in the cognitive domain would lead to putative dysfunction in the emotional domain. Forty-eight participants viewed images of emotional scenes during functional magnetic resonance imaging in two sessions that were separated by a challenging attention control task that required effortful inhibition (depletion group) or not (control group). Compared to the control group, depleted participants showed increased activity in the left amygdala to negative but not to positive or neutral scenes. Moreover, whereas the control group showed reduced amygdala activity to all scene types (i.e. habituation), the depletion group showed increased amygdala activity relative to their pre-depletion baseline; however this was only significant for negative scenes. Finally, depleted participants showed reduced functional connectivity between the left amygdala and ventromedial prefrontal cortex during negative scene processing. These findings demonstrate that consuming self-regulatory resources leads to an exaggerated neural response to emotional material that appears specific to negatively valenced stimuli and further suggests a failure to recruit top-down prefrontal regions involved in emotion regulation.

Fig. 1

Schematic of the study design. Participants were randomly assigned to either a depletion (n = 24) or control (n = 24) group. Both groups completed a single functional run of the emotional scenes task followed by either the attention control task (depletion group) or passive viewing (control group) which were identical in instruction save for the requirement that the depletion group inhibit reading a series of words that appeared on screen (see ‘Methods’ section). Finally, participants completed another functional run of the emotional scenes task, in this way the first functional run served as a pre-depletion measure of baseline emotional reactivity.

Fig. 2

(A) Brain regions showing a main effect of emotional scene valence (negative, neutral or positive) across both depletion and control groups (P < 0.05 corrected). (B) ROI analysis of parameter estimates in the left amygdala (−21, −6, −21) and (C) left LPFC (inferior frontal gyrus; −48,24,6) (B) demonstrate that these regions responded primarily to negatively valenced emotional scenes. Error bars indicate SEM based on the mean squared error term for within subjects comparisons. Coordinates (x, y, z) are in Montreal Neurological Institute stereotaxic space. IFG = Inferior Frontal Gyrus.

Fig. 3

Compared to control participants, depleted participants exhibited greater left amygdala (−21, −6, −21) reactivity to negative emotional material following depletion [t(46) = 2.38, P = 0.021]. Within groups, depleted participants exhibited increased amygdala activity to negative emotional material compared to their pre-depletion baseline [t(23) = 2.1, P = 0.047] whereas control participants did not [t(23) = 1.2, P = 0.242]. This was also true of an anatomically defined left amygdala ROI (see text). Error bars indicate SEM.

Fig. 4

ROI Analysis demonstrated that the functional coupling between the VMPFC and the left amygdala seed differed between depleted and control participants during negative scene processing [t(46) = 2.27, P = 0.028]. This difference was driven primarily by an increase in the functional coupling between amygdala and VMPFC in control subjects during the second session (positive change scores) whereas depleted participants showed reduced coupling between these regions after depletion (negative change scores). Error bars indicate SEM.