Inhibition of Lateral Prefrontal Cortex Produces Emotionally Biased First Impressions: A Transcranial Magnetic Stimulation and Electroencephalography Study

Regina C Lapate, Jason Samaha, Bas Rokers, Hamdi Hamzah, Bradley R Postle, Richard J Davidson, Regina C Lapate, Jason Samaha, Bas Rokers, Hamdi Hamzah, Bradley R Postle, Richard J Davidson

Abstract

Optimal functioning in everyday life requires the ability to override reflexive emotional responses and prevent affective spillover to situations or people unrelated to the source of emotion. In the current study, we investigated whether the lateral prefrontal cortex (lPFC) causally regulates the influence of emotional information on subsequent judgments. We disrupted left lPFC function using transcranial magnetic stimulation (TMS) and recorded electroencephalography (EEG) before and after. Subjects evaluated the likeability of novel neutral faces after a brief exposure to a happy or fearful face. We found that lPFC inhibition biased evaluations of novel faces according to the previously processed emotional expression. Greater frontal EEG alpha power, reflecting increased inhibition by TMS, predicted increased behavioral bias. TMS-induced affective misattribution was long-lasting: Emotionally biased first impressions formed during lPFC inhibition were still detectable outside of the laboratory 3 days later. These findings indicate that lPFC serves an important emotion-regulation function by preventing incidental emotional encoding from automatically biasing subsequent appraisals.

Keywords: causality; emotional control; facial expressions; frontal lobe; open materials; priming.

Conflict of interest statement

Declaration of Conflicting Interests: R. J. Davidson serves on the board of directors for two nonprofit organizations: The Mind and Life Institute and Healthy Minds Innovations. The authors declared that they had no other conflicts of interest with respect to their authorship or the publication of this article.<?release-delay 12|0>

Figures

Fig. 1.
Fig. 1.
Experimental design of the transcranial magnetic stimulation (TMS) and electroencephalography (EEG) session. The brain images (a) show the lateral prefrontal cortex (lPFC) and control (primary somatosensory cortex, or S1) regions targeted during the administration of continuous theta-burst stimulation (cTBS). The target regions are overlaid on a representative subject’s T1-weighted image in native space. Each subject received TMS at both sites during the session. The timeline for each cTBS administration is shown in (b). After cTBS was administered to either left lPFC or to left S1 for 20 s, subjects completed the affective-coloring task. EEG recordings, which provided a neurophysiological index of cortical excitability, were conducted twice for each cTBS administration, before and after completion of the affective-coloring task. The trial structure for the affective-coloring task is shown in the bracketed area above the timeline. Subjects were informed that the task measured the formation of first impressions in the presence of emotional distractors. After the brief presentation of a happy or fearful face, subjects evaluated novel individuals for their likeability.
Fig. 2.
Fig. 2.
Impact of inhibition of lateral prefrontal cortex (lPFC) by continuous theta-burst stimulation (cTBS) on evaluative behavior after emotional processing. The bar graph (a) shows neutral-face likeability separately for faces presented after cTBS to the lPFC and S1, following the presentation of positively and negatively valenced emotional expressions. The error bars represent ±1SEM of the within-subjects difference between valence conditions. The asterisks indicate significant differences (p < .05). The scatterplot (with best-fitting regression line; b) shows the relationship between change in neutral-face likeability after cTBS administration to lPFC and power in the alpha band (controlling for alpha and behavioral responses in the control condition). Power was measured over the electrode (F7) closest to the location of the transcranial magnetic stimulation coil on lPFC. Plotted on both axes are the residuals saved from linear regressions in which responses recorded in the control condition were regressed out of responses in the lPFC condition. Each data point denotes results for a single subject. (For the scalp topography of this correlation, see Fig. S2 in the Supplemental Material.)
Fig. 3.
Fig. 3.
Setup for online ratings task and longevity of first impressions formed during the transcranial magnetic stimulation (TMS) session. Three days after the TMS session in the lab, subjects were asked to complete an online rating task (a) in which they evaluated the likeability of the 144 neutral faces (first encountered during the TMS session). These faces were intermixed with 36 foils. Subjects used a continuous scale unanchored by numbers and were given unlimited time to respond. The bar graph (b) shows the neutral-face likeability ratings outside of the lab, separately for faces that had been presented in the TMS session after continuous theta-burst stimulation (cTBS) to the lateral prefrontal cortex (lPFC) or to S1, following the presentation of positively or negatively valenced emotional expressions. The error bars represent ±1SEM of the within-subjects difference between valence conditions. The asterisk indicates a significant difference (p < .05).

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