Ventromedial Prefrontal Cortex Activity and Sympathetic Allostasis During Value-Based Ambivalence.

Neil M Dundon,Scott T Grafton,Viktoriya Babenko,Allison D Shapiro,Gold N Okafor

doi:10.3389/fnbeh.2021.615796

Abstract

Anxiety is characterized by low confidence in daily decisions, coupled with high levels of phenomenological stress. Ventromedial prefrontal cortex (vmPFC) plays an integral role in maladaptive anxious behaviors via decreased sensitivity to threatening vs. non-threatening stimuli (fear generalization). vmPFC is also a key node in approach-avoidance decision making requiring two-dimensional integration of rewards and costs. More recently, vmPFC has been implicated as a key cortical input to the sympathetic branch of the autonomic nervous system. However, little is known about the role of this brain region in mediating rapid stress responses elicited by changes in confidence during decision making. We used an approach-avoidance task to examine the relationship between sympathetically mediated cardiac stress responses, vmPFC activity and choice behavior over long and short time-scales. To do this, we collected concurrent fMRI, EKG and impedance cardiography recordings of sympathetic drive while participants made approach-avoidance decisions about monetary rewards paired with painful electric shock stimuli. We observe first that increased sympathetic drive (shorter pre-ejection period) in states lasting minutes are associated with choices involving reduced decision ambivalence. Thus, on this slow time scale, sympathetic drive serves as a proxy for “mobilization” whereby participants are more likely to show consistent value-action mapping. In parallel, imaging analyses reveal that on shorter time scales (estimated with a trial-to-trial GLM), increased vmPFC activity, particularly during low-ambivalence decisions, is associated with decreased sympathetic state. Our findings support a role of sympathetic drive in resolving decision ambivalence across long time horizons and suggest a potential role of vmPFC in modulating this response on a moment-to-moment basis.

Highlights

Decisions can be so easy; approaching a large reward with minimal associated costs or avoiding a small reward with excessive associated costs requires precious little deliberation and minimal supportive decisional architecture
Recent human neuropsychological evidence, using feargeneralization paradigms with Generalized Anxiety Disorder patients (GAD), shows decreased ventromedial prefrontal cortex (vmPFC) activations while patients evaluated “safe” stimuli, i.e., those that had not been conditioned with an aversive outcome (Greenberg et al, 2013; Via et al, 2018). These findings suggest pervasive anxiety may stem from a continuous anticipation of harm, a response which is otherwise attenuated by vmPFC in healthy controls
The results show that we can extend a role of vmPFC to sympathetic regulation of ambivalence that is parsimonious with a resource model

Summary

Introduction

Decisions can be so easy; approaching a large reward with minimal associated costs or avoiding a small reward with excessive associated costs requires precious little deliberation and minimal supportive decisional architecture. Ventromedial prefrontal cortex (vmPFC) is linked to at least two valuebased decision parameters: coding for subjective value (high or low likelihood of approach) and ambivalence (proximity to the approach/avoid threshold; Rolls et al, 2010; De Martino et al, 2013; Lebreton et al, 2015). Resolution of value-based ambivalence is highly likely to interact with anticipatory allostatic control (Sterling and Eyer, 1988), a process observed across mammals where the brain makes predictive adjustments to physiological systems, such as metabolism, blood pressure, heart-rate and core temperature, preemptively increasing the likelihood of equilibrium between external demands and the internal milieu (Schulkin and Sterling, 2019). Separate branches of non-human and human research have implicated vmPFC in allostatic control, given first its top-down influence on the adrenal medulla (Dum et al, 2016, 2019), and its neural projections to other sites within an integrated visceromotor-interoceptive system, including cingulate, dorsal amygdala and various sites along the insula (Kleckner et al, 2017)

Methods

Results

Conclusion