Multiple value signals in dopaminergic midbrain and their role in avoidance contexts

Francesco Rigoli,Benjamin Chew,Peter Dayan,Raymond J Dolan

doi:10.1016/j.neuroimage.2016.04.062

Abstract

The role of dopaminergic brain regions in avoidance behaviour is unclear. Active avoidance requires motivation, and the latter is linked to increased activity in dopaminergic regions. However, avoidance is also often tethered to the prospect of punishment, a state typically characterized by below baseline levels of dopaminergic function. Avoidance has been considered from the perspective of two-factor theories where the prospect of safety is considered to act as a surrogate for reward, leading to dopamine release and enhanced motivational drive. Using fMRI we investigated predictions from two-factor theory by separating the neural representation of a conventional net expected value, which is negative in the case of avoidance, from an adjusted expected value which factors in a possibility of punishment and is larger for both big rewards and big (predictably avoidable) punishments. We show that neural responses in ventral striatum and ventral tegmental area/substantial nigra (VTA/SN) covaried with net expected value. Activity in VTA/SN also covaried with an adjusted expected value, as did activity in anterior insula. Consistent with two-factor theory models, the findings indicate that VTA/SN and insula process an adjusted expected value during avoidance behaviour.

Highlights

Dopaminergic rich brain regions, including ventral striatum and midbrain ventral tegmental area/substantia nigra (VTA/SN), are implicated in evaluation and motivation (D'Ardenne et al, 2008; Kable and Glimcher, 2007; O'Doherty et al, 2004; Seymour et al, 2007; Tobler et al, 2005; Tom et al, 2007)
We focus our analysis on regions of interest (ROIs) within a priori dopaminergic rich regions, namely VTA/SN and ventral striatum, plus anterior insula, a region implicated in processing stimulus salience and motivation (Bartra et al, 2013; Critchley et al, 2001)
Enhanced performance for large compared to small monetary amount can be interpreted as a motivational effect dependent on EVADJ, while the absence of a difference in performance between reward and punishment conditions provides no support for a motivational effect of EVRAW

Summary

Introduction

Dopaminergic rich brain regions, including ventral striatum and midbrain ventral tegmental area/substantia nigra (VTA/SN), are implicated in evaluation and motivation (D'Ardenne et al, 2008; Kable and Glimcher, 2007; O'Doherty et al, 2004; Seymour et al, 2007; Tobler et al, 2005; Tom et al, 2007). In appetitive contexts, these regions show enhanced responses to larger rewards, consistent with representing expected value (EV) and reinforcement prediction error (RPE). Given an association between dopamine activity and motivation (Berridge and Robinson, 1998; Niv et al, 2007; Salamone and Correa, 2002), these findings hint at an increased dopaminergic response with larger punishment

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Conclusion