Opponency Revisited: Competition and Cooperation Between Dopamine and Serotonin

Boureau, Y-Lan; Dayan, Peter

doi:10.1038/npp.2010.151

Cited by 428 publications

(480 citation statements)

References 376 publications

(501 reference statements)

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“…Treatment with an SSRI enhanced the negative coupling between the NAcc and the key structure of the serotonergic system, and integrates well with previous ideas on a link between SSRI intake and altered processing of primary rewards (Kranz et al, 2010;Boureau and Dayan, 2011).…”

Section: Discussionsupporting

confidence: 83%

“…Sexual dysfunction, including reduced drive and desire, is a common phenomenon accompanying SSRI intake (Clayton et al, 2002;Serretti and Chiesa, 2009), pointing toward impaired processing of primary rewards. Diminished responsiveness to motivational stimuli under SSRIs has been related to the inhibition of dopaminergic reward circuits by serotonin (Kranz et al, 2010) and is in line with a proposed opponency of dopaminergic and serotonergic effects (Boureau and Dayan, 2011). However, mechanisms remain unclear.…”

Section: Introductionmentioning

confidence: 93%

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Modulation of Frontostriatal Interaction Aligns with Reduced Primary Reward Processing under Serotonergic Drugs

Abler¹,

Grön²,

Hartmann³

et al. 2012

J. Neurosci.

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Recently, functional interactions between anteroventral prefrontal cortex and nucleus accumbens (NAcc) have been shown to relate to behavior counteracting reward-desiring (Diekhof and Gruber, 2010). Downregulation of the reward system by serotonin has also been suggested as the mode of action accounting for unsatisfactory effects of serotonin reuptake inhibitors (SSRIs) such as insufficient alleviation or even increase of anhedonia, and loss of interest. However, understanding of the in vivo mechanisms of SSRI-related alteration of the human reward system is still incomplete. Using functional magnetic resonance imaging (fMRI) within a double-blind cross-over within-subjects study design and administering the SSRI paroxetine, the dopamine/norepinephrine reuptake inhibitor bupropione, and placebo for 7 d each, we investigated a group of 18 healthy male subjects. Under paroxetine, subjects showed significantly decreased activation of the bilateral NAcc during processing of primary rewards (erotic videos), but not under bupropion. Similar to the previous study, analysis of psychophysiological interactions revealed that this downregulation relied on negative interactions between left and right NAcc fMRI signals and the bilateral anteroventral prefrontal cortex that now were significantly enhanced under paroxetine and reduced under bupropion. Individual drug-dependent modulations of interacting brain regions were significantly associated with individual expressions of impulsivity as a personality trait. Our results corroborate and extend previous insights on interregional crosstalk from secondary to primary rewards and demonstrate parallels between active inhibitory control of and serotonergic effects on the dopaminergic reward system's activity.

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Section: Discussionsupporting

confidence: 83%

Section: Introductionmentioning

confidence: 93%

Modulation of Frontostriatal Interaction Aligns with Reduced Primary Reward Processing under Serotonergic Drugs

Abler¹,

Grön²,

Hartmann³

et al. 2012

J. Neurosci.

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“…Future studies can build on this study work by comparing the effects of MPH with the effects of atomoxetine (a prefrontal specific catecholamine agonist) and observe interactions with specific dopamine and noradrenaline antagonists to isolate the neural structures and specific neurotransmitters involved. Given the distribution of cortical and striatal systems involved in social conformity (Berns et al, 2010;Campbell-Meiklejohn et al, 2010;Klucharev et al, 2009), we expect that, as for nonsocial learning (Kehagia et al, 2010), conformity involves a network of brain regions, multiple cognitions, and interactions between multiple neurotransmitter systems (Boureau and Dayan, 2011;Cools et al, 2011). …”

Section: Discussionmentioning

confidence: 99%

Modulation of Social Influence by Methylphenidate

Campbell-Meiklejohn

Simonsen

Jensen

et al. 2012

Neuropsychopharmacol

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The ability to infer value from the reactions of other people is a common and essential ability with a poorly understood neurobiology. Commonly, social learning matches one's values and behavior to what is perceived as normal for one's social group. This is known as conformity. Conformity of value correlates with neural activity shared by cognitions that depend on optimum catecholamine levels, but catecholamine involvement in conformity has not been tested empirically. Methylphenidate (MPH) is an indirect dopamine and noradrenalin agonist, commonly used for the treatment of attention-deficit hyperactivity disorder for which it reduces undesirable behavior as evaluated by peers and authority figures, indicative of increased conformity. We hypothesized that MPH might increase conformity of value. In all, 38 healthy adult females received either a single oral 20 mg dose of MPH or placebo (PL). Each subject rated 153 faces for trustworthiness followed immediately by the face's mean rating from a group of peers. After 30 min and a 2-back continuousperformance working-memory task, subjects were unexpectedly asked to rate all the faces again. Both the groups tended to change their ratings towards the social norm. The MPH group exhibited twice the conformity effect of the PL group following moderate social conflict, but this did not occur following large conflicts. This suggests that MPH might enhance signals that would otherwise be too weak to evoke conformity. MPH did not affect 2-back performance. We provide a new working hypothesis of a neurocognitive mechanism by which MPH reduces socially disruptive behavior and provides novel evidence of catecholamine mediation of social learning.

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“…That is, although the nature of any opponency between appetitive and aversive systems remains the subject of much debate (12)(13)(14), there are suggestions that serotonin acts as a mirror to dopamine and is associated with behavioral inhibition in aversive contexts (13)(14)(15)(16)(17). These joint roles would lead to conflict when punishment can be avoided only by acting (go).…”

mentioning

confidence: 99%

Action controls dopaminergic enhancement of reward representations

Guitart-Masip

Chowdhury

Sharot

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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109

144

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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...

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Opponency Revisited: Competition and Cooperation Between Dopamine and Serotonin

Cited by 428 publications

References 376 publications

Modulation of Frontostriatal Interaction Aligns with Reduced Primary Reward Processing under Serotonergic Drugs

Modulation of Frontostriatal Interaction Aligns with Reduced Primary Reward Processing under Serotonergic Drugs

Modulation of Social Influence by Methylphenidate

Action controls dopaminergic enhancement of reward representations

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