Relationship between impulsivity, prefrontal anticipatory activation, and striatal dopamine release during rewarded task performance

Abstract

Impulsivity, and in particular the negative urgency aspect of this trait, is associated with poor inhibitory control when experiencing negative emotion. Individual differences in aspects of impulsivity have been correlated with striatal dopamine D2/D3 receptor availability and function. This multi-modal pilot study used both positron emission tomography (PET) and functional magnetic resonance imaging (fMRI) to evaluate dopaminergic and neural activity, respectively, using modified versions of the monetary incentive delay task. Twelve healthy female subjects underwent both scans and completed the NEO Personality Inventory Revised to assess Impulsiveness (IMP). We examined the relationship between nucleus accumbens (NAcc) dopaminergic incentive/reward release, measured as a change in D2/D3 binding potential between neutral and incentive/reward conditions with [(11)C]raclopride PET, and blood oxygen level-dependent (BOLD) activation elicited during the anticipation of rewards, measured with fMRI. Left NAcc incentive/reward dopaminergic release correlated with anticipatory reward activation within the medial prefrontal cortex (mPFC), left angular gyrus, mammillary bodies, and left superior frontal cortex. Activation in the mPFC negatively correlated with IMP and mediated the relationship between IMP and incentive/reward dopaminergic release in left NAcc. The mPFC, with a regulatory role in learning and valuation, may influence dopamine incentive/reward release.

Keywords: Dopamine; NAcc; PET; Reward; fMRI; mPFC.

Conflict of interest statement

The authors have no conflicts of interest to declare.

Copyright © 2014 Elsevier Ireland Ltd. All rights reserved.

Figures

Fig. 1

(A) Schematic of fMRI paradigm: A single trial of 6 s consisted of 2000 ms each for cue; anticipation; and target plus feedback. Subjects complete 2 runs of 5 min each. Reward, loss, and neutral cues were counterbalanced and presented pseudorandomly throughout each run. (B) Schematic of reward condition of PET paradigm: Trials followed the same timing as in the fMRI paradigm, presented in a single run of 30 min with reward and loss cues. Novel changes to cues and feedback were added over time including color and sound to maintain subject interest. A neutral condition presenting a neutral cue and target with no feedback was presented during a separate single 30-min run.

Fig. 2

(A) Statistical parametric maps of medial prefrontal cortex (mPFC) BOLD reward anticipation activity positively correlated with left NAcc incentive/reward dopamine release. Color bars represent t-values. (B) Plot of mPFC BOLD activation during reward anticipation versus NEO Impulsiveness.

Fig. 3

Mediation model illustrating the influence of mPFC BOLD activation during reward on the relationship between IMP and left NAcc incentive/reward dopamine release.