Striatal Dopamine and the Interface between Motivation and Cognition

Abstract

Brain dopamine has long been known to be implicated in the domains of appetitive motivation and cognition. Recent work indicates that dopamine also plays a role in the interaction between appetitive motivation and cognition. Here we review this work. Animal work has revealed an arrangement of spiraling connections between the midbrain and the striatum that subserves a mechanism by which dopamine can direct information flow from ventromedial to more dorsal regions in the striatum. In line with current knowledge about dopamine's effects on cognition, we hypothesize that these striato-nigro-striatal connections provide the basis for functionally specific effects of appetitive motivation on cognition. One implication of this hypothesis is that appetitive motivation can induce cognitive improvement or impairment depending on task demands.

Keywords: Parkinson's disease; cognition; dopamine; flexibility; motivation; prefrontal cortex; reward; striatum.

Figure 1

Ventromedial to dorsolateral direction of information flow through frontostriatal-nigral circuitry. Interactions between the different frontostriatal loops involved in motivational control (red), cognitive control (yellow), and motor control (blue) can take place at the level of the SNS connections (bend arrows) or at the level of the frontostriatal connections (straight arrows). The direction of information flow is always from ventromedial to dorsolateral regions in the frontostriatal circuitry. SNS, striato-nigral-striatal; N. Acc, nucleus accumbens (ventromedial striatum); Caud, caudate nucleus (dorsomedial striatum); Put, putamen (dorsolateral striatum); OFC, orbitofrontal cortex; ACC, anterior cingulate cortex; DLPFC, dorsolateral prefrontal cortex; PMC, premotor cortex.

Figure 2

Experimental evidence for the beneficial effect of motivation on cognitive flexibility in humans. (A) The rewarded set-shifting paradigm used in our studies to investigate the motivation–cognition interface. (B) In our genetic imaging study (Aarts et al., 2010), participants with genetically determined high striatal dopamine levels benefited more from reward anticipation in terms of set-shifting than participants with low dopamine levels. (C) In our genetic imaging study (Aarts et al., 2010), reward cues elicited activity in VMS (in red), whereas the dopamine-dependent effect of reward prediction on set shifting was observed in DMS (in yellow). (D) Activity in these striatal sub-regions [see (C)] was positively correlated, with high striatal dopamine subjects showing high activity in both VMS and DMS during reward anticipation and rewarded set-shifting respectively. (E) In our SPECT study in Parkinson's disease (Aarts et al., under review), patients showed the most marked dopamine depletion in dorsolateral striatum (posterior putamen), whereas ventromedial striatum (n. accumbens) was least affected. (F) Patients with the greatest dopamine depletion (i.e., least dopamine cell integrity) showed the greatest effects of anticipated reward in reducing the switch cost in the dominant arrow task [(switch-repeat)low − (switch-repeat)high]; presumably by increased reward-induced dopamine release in the relatively intact neurons in ventromedial striatum.

Figure 3

Incentive motivation might have detrimental effects on cognitive focusing. (A) The rewarded Stroop paradigm, including a reward cue (1 or 15 cent), an information cue about the upcoming target congruency [informative: incongruent (this example) or congruent (green circle); or uninformative (gray question mark)], and an arrow-word Stroop target. The task was to respond to the direction indicated by the word. (B) Reward anticipation had opposite effects on widening and focusing of attention as measured with the information benefit (uninformed–informed) on congruent and incongruent targets respectively; with high anticipated reward particularly impairing proactive focusing on the incongruent trials (M. van Holstein, E. Aarts, R. Cools, unpublished observations).