Action controls dopaminergic enhancement of reward representations

Abstract

Dopamine is widely observed to signal anticipation of future rewards and thus thought to be a key contributor to affectively charged decision making. However, the experiments supporting this view have not dissociated rewards from the actions that lead to, or are occasioned by, them. Here, we manipulated dopamine pharmacologically and examined the effect on a task that explicitly dissociates action and reward value. We show that dopamine enhanced the neural representation of rewarding actions, without significantly affecting the representation of reward value as such. Thus, increasing dopamine levels with levodopa selectively boosted striatal and substantia nigra/ventral tegmental representations associated with actions leading to reward, but not with actions leading to the avoidance of punishment. These findings highlight a key role for dopamine in the generation of appetitively motivated actions.functional MRI | striatum | decision-making S ubstantial evidence indicates that the neuromodulator dopamine plays at least two roles in behavioral guidance. One is to signal prediction errors regarding expected reward value (1-3), prediction errors that are also used by the striatum to guide selection of appropriate actions (4-6). A second, less emphasized, role for dopamine is to invigorate actions associated with reward (7,8). Thus, dopamine depletion results in decreased motor activity and decreased motivated behavior (9, 10) along with decreased vigor or motivation to work for rewards in demanding reinforcement schedules (7,11). These joint roles in reward prediction and motivational control can create situations that result in conflict, such as what happens when reward is attainable solely by not acting (no-go).It has been suggest that the exact opposite may be true of serotonin. That is, although the nature of any opponency between appetitive and aversive systems remains the subject of much debate (12-14), there are suggestions that serotonin acts as a mirror to dopamine and is associated with behavioral inhibition in aversive contexts (13-17). These joint roles would lead to conflict when punishment can be avoided only by acting (go).Such conflicting cases have been a focal point of recent studies where the critical manipulation involved an orthogonalization of action requirements and outcome valence (15,18). In the latter study we highlighted anticipatory representations in the striatum and substantia nigra/ventral tegmental area (SN/VTA) that reflected a dominance of action representation over an expected dominance of reward value representations, thereby hinting at a specific role for dopamine in motivation for action (18).Here, we tested the contributions of dopamine and serotonin to action and valence representations, with a specific focus on the areas we had previously highlighted, namely the striatum and SN/ VTA. First, we trained participants on a balanced 2 (reward/ punishment) × 2 (go/no-go) task that orthogonalized action and valence (18). When performance reached 95% correct choices in all conditions...

Emotional Eating Phenotype is Associated with Central Dopamine D2 Receptor Binding Independent of Body Mass Index

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Dissociating Motivation from Reward in Human Striatal Activity

“…Our results also suggest a reinterpretation of the recent claims that the requirement for action strongly impacts activation in the CPu whereas the valence of the potential outcome (i.e., gaining vs. losing money) has a weaker relationship (Kurniawan et al, 2013; Guitart-Masip et al, 2011, 2012). In these studies, the difference in value between a successful versus unsuccessful response was the same regardless of whether participants attempted to obtain a reward or avoid a punishment.…”

“…Activation in the ventral and dorsal striatum is greatest when reward receipt requires direct action, suggesting that reward-related activity may be contingent on motivation (O'Doherty et al, 2004; Zink, Pagnoni, Martin-Skurski, Chappelow, & Berns, 2004). Furthermore, independent manipulation of outcome reward value and motor response requirements (i.e., go vs. no-go) suggests that striatal activity is more dependent on motor demands than anticipated reward (Kurniawan, Guitart-Masip, & Dayan, 2013; Guitart-Masip et al, 2011, 2012). …”

Dopamine modulates processing speed in the human mesolimbic system

“…Both substances were chosen because they are licensed for the treatment of Alzheimer's (galantamine) and Parkinson's disease (levodopa), provoke little to no side effects if taken in low dosages and because they have been used in previous studies (e.g. Guitart-Masip et al, 2012;Riemann et al, 1994). Both substances are rapidly absorbed and reach significant plasma concentration at around 30-60 min (Huang and Fu, 2010;Nyholm et al, 2012); therefore, MEG recordings started at 60 min after drug intake for both groups.…”