Human lateral Frontal Pole contributes to control over social-emotional action

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 prefrontal cortex (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 social-emotional actions, and explores a possible structural pathway through which emotional 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 = 40) performing a social-emotional approach-avoidance task identified aPFC territories involved in the regulation of social-emotional actions. 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 inter-individual variation in social-emotional regulation abilities is accounted for by the strength of structural connectivity between FPl and amygdala. Evidence from an independent replication sample (N = 50; 10 females) further substantiated this result. These findings provide novel neuroanatomical evidence for incorporating FPl in models of control over human social-emotional behavior.Significance statementSuccessful regulation of emotional behaviors is a prerequisite for successful participation in human society, as is evidenced by the social isolation and loss of occupational opportunities often encountered by people suffering from emotion-regulation disorders such as social-anxiety disorder and psychopathy. Knowledge about the precise cortical regions and connections supporting this control is crucial for understanding both the nature of computations needed to successfully traverse the space of possible actions in social situations, and the potential interventions that might result in efficient treatment of social-emotional disorders. This study provides evidence for a precise cortical region (FPl) and a structural pathway (the ventral amygdalofugal bundle) through which a cognitively complex form of emotional action regulation might be implemented in the human brain.

Enhanced Performance by Interpretable Low-Frequency Electroencephalogram Oscillations in the Machine Learning-Based Diagnosis of Post-traumatic Stress Disorder

“…The mean PSD values of each ROI of the mentioned fronto-temporal areas were significantly smaller in PTSD patients than those in HC. According to previous studies, the frontal regions, including the frontal pole and opercular part of the inferior frontal area, are involved in emotion regulation processing ( Grecucci et al, 2013 ; Bramson et al, 2019 ) and temporal areas are significantly related to rumination symptom of PTSD patients ( Ferdek et al, 2016 ); PTSD patients showed significantly reduced brain activation in both brain areas in resting-state ( Rabe et al, 2006 ), as shown in this study. Therefore, it is neurophysiologically plausible to obtain better classification performance for PTSD diagnosis when using PSD features extracted from fronto-temporal areas.…”

Dichotomous organization of amygdala/temporal-prefrontal bundles in both humans and monkeys

“…However, the tractography recipes developed as part of this study have already been shown to be applicable and successful in human diffusion MRI data of more conventional quality. In fact, the approach and results achieved here, including the division between these two amygdala-prefrontal tracts, are behaviorally relevant in the context of social-emotional actions, advancing our understanding of the neurobiology of emotion regulation (Bramson et al, 2019).…”

“…The importance of understanding a dissociation between AmF and UF may be further underlined by considering the directionality of influence of these two bundles as described by more invasive investigations: the UF is a bidirectional tract with many projections from prefrontal cortex terminating in medial and lateral basal nuclei of the amygdala, whereas the AmF predominantly carries efferent projections from the amygdala to subcortical and prefrontal targets (Bickart et al, 2012). Potentially, this dissociation can help us to understand whether abnormal neural processes that are central to certain psychiatric disorders are more related to efferent or afferent projections of the amygdala (Bramson et al, 2019; Murray and Rudebeck, 2018; Volman et al, 2013). Unfortunately, one of the limitations of probabilistic tractography is that it cannot infer the directionality of the reconstructed bundles and is unable to differentiate monosynaptic from polysynaptic connections.…”

“…By placing the bundle at the core of the analyses, our results become more reliable. This approach also allows us to create more easily tractography recipes for the fiber bundles of interest that can then be shared with other researchers (e.g., Bramson et al, 2019).…”

Improving emotion control in social anxiety by targeting rhythmic brain activity

“…In healthy individuals, prefrontal control emerged from lPFC (Bramson et al, 2020) rather than dlPFC (this study). lPFC is a region that can flexibly integrate valence signals with approach-avoid action selection, allowing lPFC to orchestrate goal-directed control over automatic emotional action tendencies (Bramson et al, 2019; Lapate et al, 2022). Unfortunately, the lPFC is overexcitable in high-anxious individuals (Bramson et al, 2023), likely reducing its ability to discriminate between afferent emotional valence signals.…”