Human Lateral Frontal Pole Contributes to Control over Emotional Approach–Avoidance Actions

Abstract

Regulation of emotional behavior is essential for human social interactions. Recent work has exposed its cognitive complexity, as well as its unexpected reliance on portions of the anterior PFC (aPFC) also involved in exploration, relational reasoning, and counterfactual choice, rather than on dorsolateral and medial prefrontal areas involved in several forms of cognitive control. This study anatomically qualifies the contribution of aPFC territories to the regulation of prepotent approach-avoidance action tendencies elicited by emotional faces, and explores a possible structural pathway through which this emotional action regulation might be implemented. We provide converging evidence from task-based fMRI, diffusion-weighted imaging, and functional connectivity fingerprints for a novel neural element in emotional regulation. Task-based fMRI in human male participants (N ϭ 40) performing an emotional approach-avoidance task identified aPFC territories involved in the regulation of action tendencies elicited by emotional faces. Connectivity fingerprints, based on diffusion-weighted imaging and resting-state connectivity, localized those task-defined frontal regions to the lateral frontal pole (FPl), an anatomically defined portion of the aPFC that lacks a homologous counterpart in macaque brains. Probabilistic tractography indicated that 10%-20% of interindividual variation in emotional regulation abilities is accounted for by the strength of structural connectivity between FPl and amygdala. Evidence from an independent replication sample (N ϭ 50; 10 females) further substantiated this result. These findings provide novel neuroanatomical evidence for incorporating FPl in models of control over human action tendencies elicited by emotional faces.

Improving emotional-action control by targeting long-range phase-amplitude neuronal coupling

“…The study was approved by the local ethics committee (CMO2014/288). Only male participants were recruited to avoid having to control for potential variability that could be introduced by sex-related differences in hormone levels known to be associated with this task ( Volman et al, 2011b ) (for a full discussion see Bramson et al, 2020 ). Participants reported no history of mental illness or use of psychoactive medication.…”

“…Participants performed a social-emotional approach-avoidance task that has previously been shown to require control over prepotent habitual action-tendencies to approach happy- and avoid angry faces ( Phaf et al, 2014 ; Roelofs et al, 2009 ). Overriding these action-tendencies requires a complex form of cognitive control that operates on the interaction between emotional percepts and the emotional valence of the required actions ( Volman et al, 2011a ; Roelofs et al, 2009 ; Volman et al, 2013 ), and depends on aPFC control over downstream regions ( Koch et al, 2018 ; Volman et al, 2011a ; Bramson et al, 2020 ), implemented by theta-gamma phase-amplitude coupling ( Bramson et al, 2018 ). Participants responded through a joystick with one degree of freedom (along the participant’s midsagittal plane), holding the joystick with their right hand on top of their abdomen, while laying the MR-scanner and seeing a visual projection screen through a mirror system (see below).…”

“…Stimulation conditions were alternated between blocks in pseudo-random fashion with the constraint that stimulation condition could never be repeated for two consecutive blocks. The position of the electrodes on the skull was determined for each participant by using individual structural T1 scans to which we registered masks of the regions of interest (MNI [−28–32 64] for SMC [ Bramson et al, 2018 ]; and MNI [26 54 0] for lateral frontal pole (FPl) [ Bramson et al, 2020 ; Neubert et al, 2014 ]). Precise placement of the centre electrode was achieved using Localite TMS Navigator ( https://www.localite.de/en/products/tms-navigator/ ; RRID: SCR_016126 ).…”

“…in this case tACS present or absent). We preregistered the hypothesis that changes in connectivity between aPFC and SMC due to tACS might be mediated by the amygdala, a region linked to the regulation of social-emotional action tendencies ( Volman et al, 2011a ; Kaldewaij et al, 2019 ; Bramson et al, 2020 ). To test this hypothesis, we constructed a model space in which each model contained three regions; the left amygdala (see GLM results); the right aPFC; and the left SMC.…”

“…Model structure for all models under comparison was based on the minimal architecture needed to dissociate whether synchronization between aPFC and SMC was gated by the amygdala or via other region(s). All models consisted of a directed connection between the amygdala and SMC ( Grèzes et al, 2014 ) (indicated as amygdala→SMC, amygdala → aPFC, and aPFC → amygdala [ Bramson et al, 2020 ; Folloni et al, 2019 ]). A subset of models also included aPFC → SMC ( Figure 3 ), which captures the connectivity between aPFC and SMC gated via cerebral structures other than the amygdala given that the two structures do not share a monosynaptic connection ( Neubert et al, 2014 ).…”