Striatal dopamine release codes uncertainty in pathological gambling

Linnet, Jakob; Mouridsen, Kim; Peterson, Ericka; Møller, Arne; Doudet, Doris J.; Gjedde, Albert

doi:10.1016/j.pscychresns.2012.04.012

Cited by 73 publications

(78 citation statements)

References 46 publications

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“…Several studies have highlighted the role of midbrain dopamine in coding reward uncertainty in primates [37,48], healthy humans [49,50], and pathological gamblers [27]. These studies suggest that more dopamine can be released when the event's probability of occurrence is more uncertain (is or is close to 50%) for a two-outcome event than when its probability is less uncertain.…”

Section: Discussionmentioning

confidence: 99%

“…At a neuronal level, there is evidence to suggest that reward uncertainty can enhance extracellular dopamine levels in nucleus accumbens [26], and sign-tracking also involves a greater dopaminergic response [5,6,9]. Human pathological gambling also has been related to striatal dopamine [27], and compulsive gambling severity is associated with larger dopamine responses [28]. …”

Section: Introductionmentioning

confidence: 99%

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Initial uncertainty in Pavlovian reward prediction persistently elevates incentive salience and extends sign-tracking to normally unattractive cues

Robinson¹,

Anselme²,

Fischer³

et al. 2014

Behavioural Brain Research

116

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Uncertainty is a component of many gambling games and may play a role in incentive motivation and cue attraction. Uncertainty can increase the attractiveness for predictors of reward in the Pavlovian procedure of autoshaping, visible as enhanced sign-tracking (or approach and nibbles) by rats of a metal lever whose sudden appearance acts as a conditioned stimulus (CS+) to predict sucrose pellets as an unconditioned stimulus (UCS). Here we examined how reward uncertainty might enhance incentive salience as sign-tracking both in intensity and by broadening the range of attractive CS+s. We also examined whether initially-induced uncertainty enhancements of CS+ attraction can endure beyond uncertainty itself, and persist even when Pavlovian prediction becomes 100% certain. Our results show that uncertainty can broaden incentive salience attribution to make CS cues attractive that would otherwise not be (either because they are too distal from reward or too risky to normally attract sign-tracking). In addition, uncertainty enhancement of CS+ incentive salience, once induced by initial exposure, persisted even when Pavlovian CS-UCS correlations later rose toward 100% certainty in prediction. Persistence suggests an enduring incentive motivation enhancement potentially relevant to gambling, which in some ways resembles incentive-sensitization. Higher motivation to uncertain CS+s leads to more potent attraction to these cues when they predict the delivery of uncertain rewards. In humans, those cues might possibly include the sights and sounds associated with gambling, which contribute a major component of the play immersion experienced by problematic gamblers.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Initial uncertainty in Pavlovian reward prediction persistently elevates incentive salience and extends sign-tracking to normally unattractive cues

Robinson¹,

Anselme²,

Fischer³

et al. 2014

Behavioural Brain Research

116

View full text Add to dashboard Cite

show abstract

“…Similarly, recent evidence suggests that uncertainty of reward delivery in CS-UCS relations, creating an approach toward a gambling-like scenario, can also raise dopamine levels and similarly contribute to the motivational attraction to cues for uncertain rewards, which could be potentially relevant to addiction-type pursuit of gambling by some individuals (Boileau et al, 2013; Hart, Clark, & Phillips, 2015; Linnet et al, 2012; M. J. F. Robinson, Anselme, Fischer, & Berridge, 2014a; Zack, Featherstone, Mathewson, & Fletcher, 2014).…”

Section: Introductionmentioning

confidence: 99%

“…Potential interaction between sensitization and uncertainty is suggested by findings that exposure to uncertainty in reward conditions can promote cross-sensitization to subsequent amphetamine (Berridge & Robinson, 1998; Boileau et al, 2013; Linnet et al, 2012; Singer, Scott-Railton, & Vezina, 2012; Zack et al, 2014). Also, the excitatory effects of reward uncertainty on behavior are relatively persistent in time, similar to sensitization (Bradberry et al, 2000; Giorgetti et al, 2001; Vezina, 2004; Wyvell & Berridge, 2001), even after the uncertainty conditions are reduced (M.…”

Section: Introductionmentioning

confidence: 99%

Amphetamine-induced sensitization and reward uncertainty similarly enhance incentive salience for conditioned cues.

Robinson¹,

Anselme²,

Suchomel³

et al. 2015

Behavioral Neuroscience

105

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Amphetamine and stress can sensitize mesolimbic dopamine-related systems. In Pavlovian autoshaping, repeated exposure to uncertainty of reward prediction can enhance motivated sign-tracking or attraction to a discrete reward-predicting cue (lever CS+), as well as produce cross-sensitization to amphetamine. However, it remains unknown how amphetamine-sensitization or repeated restraint stress interact with uncertainty in controlling CS+ incentive salience attribution reflected in sign-tracking. Here rats were tested in three successive phases. First, different groups underwent either induction of amphetamine sensitization or repeated restraint stress, or else were not sensitized or stressed as control groups (either saline injections only, or no stress or injection at all). All next received Pavlovian autoshaping training under either certainty conditions (100% CS-UCS association) or uncertainty conditions (50% CS-UCS association and uncertain reward magnitude). During training, rats were assessed for sign-tracking to the lever CS+ versus goal-tracking to the sucrose dish. Finally, all groups were tested for psychomotor sensitization of locomotion revealed by an amphetamine challenge. Our results confirm that reward uncertainty enhanced sign-tracking attraction toward the predictive CS+ lever, at the expense of goal-tracking. We also report that amphetamine sensitization promoted sign-tracking even in rats trained under CS-UCS certainty conditions, raising them to sign-tracking levels equivalent to the uncertainty group. Combining amphetamine sensitization and uncertainty conditions together did not add together to elevate sign-tracking further above the relatively high levels induced by either manipulation alone. In contrast, repeated restraint stress enhanced subsequent amphetamine-elicited locomotion, but did not enhance CS+ attraction.

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“…As such, it is observed in a variety of mental disorders, such as mania 1,2 , substance addiction [3][4][5][6] , and as a side effect of dopamine (DA) replacement therapy in Parkinson's disease 7,8 . Importantly, these disorders are associated with aberrations in DAergic neurotransmission 9,10 , and DA has been implicated in decision-making processes [11][12][13] . However, ascending DAergic projections from the ventral mesencephalon are anatomically and functionally heterogeneous [14][15][16] and the contribution of these distinct DA pathways to decision-making processes remains elusive.…”

mentioning

confidence: 99%

A neuronal mechanism underlying decision-making deficits during hyperdopaminergic states

Verharen

Jong

Roelofs

et al. 2017

Preprint

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Hyperdopaminergic states in mental disorders are associated with disruptive deficits in decision-making. However, the precise contribution of topographically distinct mesencephalic dopamine pathways to decision-making processes remains elusive. Here we show, using a multidisciplinary approach, how hyperactivity of ascending projections from the ventral tegmental area (VTA) contributes to faulty decision-making in rats. Activation of the VTA-nucleus accumbens pathway leads to insensitivity to loss and punishment due to impaired processing of negative reward prediction errors. In contrast, activation of the VTAprefrontal cortex pathway promotes risky decision-making without affecting the ability to choose the economically most beneficial option. Together, these findings show how malfunction of ascending VTA projections affects value-based decision-making, providing a mechanistic understanding of the reckless behaviors seen in substance abuse, mania, and after dopamine replacement therapy in Parkinson's disease.Impaired decision-making can have profound negative consequences, both in the short and in the long term. As such, it is observed in a variety of mental disorders, such as mania 1,2 , substance addiction [3][4][5][6] , and as a side effect of dopamine (DA) replacement therapy in Parkinson's disease 7,8 . Importantly, these disorders are associated with aberrations in DAergic neurotransmission 9,10 , and DA has been implicated in decision-making processes [11][12][13] . However, ascending DAergic projections from the ventral mesencephalon are anatomically and functionally heterogeneous [14][15][16] and the contribution of these distinct DA pathways to decision-making processes remains elusive.The mesocorticolimbic system, comprising DA cells within the ventral tegmental area (VTA) that mainly project to the nucleus accumbens (NAc; mesoaccumbens pathway) and medial prefrontal cortex (mPFC; mesocortical pathway), has an important role in value-based learning and decision-making [14][15][16] . When an experienced reward is better than expected, the firing of VTA DA neurons increases, thereby signaling a discrepancy between anticipated and experienced reward to downstream regions. Conversely, when a reward does not fulfill expectations, DA neuronal activity decreases. This pattern of DA cell activity is the basis of reward prediction error (RPE) theory [17][18][19][20] , which describes an essential mechanism through which organisms learn to flexibly alter their behavior when the costs and benefits associated with different courses of action shift. Although the relevance of RPEs in value-based learning is widely acknowledged, little is known about how different VTA target regions process these DA-mediated error signals, and how this ultimately leads to adaptations in behavior.Here, we used projection-specific chemogenetics combined with behavioral tasks, pharmacological interventions, computational modelling, in vivo microdialysis and in vivo neuronal population recordings to investigate how different ascending V...

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Striatal dopamine release codes uncertainty in pathological gambling

Cited by 73 publications

References 46 publications

Initial uncertainty in Pavlovian reward prediction persistently elevates incentive salience and extends sign-tracking to normally unattractive cues

Initial uncertainty in Pavlovian reward prediction persistently elevates incentive salience and extends sign-tracking to normally unattractive cues

Amphetamine-induced sensitization and reward uncertainty similarly enhance incentive salience for conditioned cues.

A neuronal mechanism underlying decision-making deficits during hyperdopaminergic states

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