The Role of Dopamine in Value-Based Attentional Orienting

Abstract

Reward learning gives rise to strong attentional biases. Stimuli previously associated with reward automatically capture visual attention regardless of intention. Dopamine signaling within the ventral striatum plays an important role in reward learning, representing the expected reward initiated by a cue. How dopamine and the striatum may be involved in maintaining behaviors that have been shaped by reward learning, even after reward expectancies have changed, is less well understood. Nonspecific measures of brain activity have implicated the striatum in value-based attention. However, the neurochemical mechanisms underlying the attentional priority of learned reward cues remain unexplored. Here, we investigated the contribution of dopamine to value-based attention using positron emission tomography (PET) with [(11)C]raclopride. We show that, in the explicit absence of reward, the magnitude of attentional capture by previously reward-associated but currently task-irrelevant distractors is correlated across individuals with changes in available D2/D3 dopamine receptors (presumably due to intrasynaptic dopamine) linked to distractor processing within the right caudate and posterior putamen. Our findings provide direct evidence linking dopamine signaling within the striatum to the involuntary orienting of attention, and specifically to the attention-grabbing quality of learned reward cues. These findings also shed light on the neurochemical basis of individual susceptibility to value-driven attentional capture, which is known to play a role in addiction. More broadly, the present study highlights the value and feasibility of using PET to relate changes in the release of a neurotransmitter to learning-dependent changes in healthy adults.

Figure 1

Time course and trial events for the training phase (A) and test phase (B) of the experimental task.

Figure 2

Response time by value condition during the training phase (A) and test phase (B) of the experiment. Error bars reflect the within-subjects SEM. *p < .05. See also Table S1 (for panel A) and S2 (for panel B).

Figure 3

Visual depiction of VOIs and observed correlations between value-based distraction and distractor-evoked dopamine release (see Methods for calculations) across participants. vS = ventral striatum, CN = caudate nucleus, PU = putamen. See also Table S3.