Connectivity Strength of Dissociable Striatal Tracts Predict Individual Differences in Temporal Discounting

Bos, Wouter van den; Rodriguez, Christian A.; Schweitzer, Julie B.; McClure, Samuel M.

doi:10.1523/jneurosci.4105-13.2014

Cited by 170 publications

(140 citation statements)

References 71 publications

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“…Finally, whereas functional connectivity between medial prefrontal cortex, amygdala, and striatum has been shown to mediate avoidance learning (43), it did not mediate learning biases in our task, suggesting that such connectivity might be equally involved in learning from increases and decreases in aversive outcomes. Several reports have linked variations in the structure of the striatum to individual differences in healthy and pathological decision-making behavior (46,47) and to the expression of certain pain disorders (48,49). Of particular relevance to the present study is the observation that obsessive-compulsive disorder (OCD), which features compulsive harm-avoidance behavior, is associated with higher gray matter density in the putamen (50).…”

Section: Discussionmentioning

confidence: 71%

Striatal structure and function predict individual biases in learning to avoid pain

Eldar

Hauser

Dayan

et al. 2016

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

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Pain is an elemental inducer of avoidance. Here, we demonstrate that people differ in how they learn to avoid pain, with some individuals refraining from actions that resulted in painful outcomes, whereas others favor actions that helped prevent pain. These individual biases were best explained by differences in learning from outcome prediction errors and were associated with distinct forms of striatal responses to painful outcomes. Specifically, striatal responses to pain were modulated in a manner consistent with an aversive prediction error in individuals who learned predominantly from pain, whereas in individuals who learned predominantly from success in preventing pain, modulation was consistent with an appetitive prediction error. In contrast, striatal responses to success in preventing pain were consistent with an appetitive prediction error in both groups. Furthermore, variation in striatal structure, encompassing the region where pain prediction errors were expressed, predicted participants' predominant mode of learning, suggesting the observed learning biases may reflect stable individual traits. These results reveal functional and structural neural components underlying individual differences in avoidance learning, which may be important contributors to psychiatric disorders involving pathological harm avoidance behavior.avoidance learning | pain | individual differences | striatum | prediction errors P ain conveys vital feedback on our actions, informing us whether an action compromises our safety and should be avoided. However, learning what to avoid doing, rather than what to do, could lead to maladaptive passive risk-avoidant behavior. For instance, when learning to ski, an overreaction to a painful fall could render a person overly cautious and hinder progress in skill acquisition. Likewise, failed investments might lead to an overconservative passive financial strategy, whereas social rejection might engender reclusive behavior. In some individuals, such as those with avoidant personality disorders, refraining too much from potentially harmful actions can manifest as a stable personality trait (1).However, an opposite tendency, to learn predominantly from successful actions that helped avoid harm, might lead to maladaptive active behavior. Thus, in soccer, sporadic success in preventing goals by diving to the left or right before seeing where a penalty kick is heading is sufficient for goalkeepers to overwhelmingly prefer this suboptimal active strategy, when in fact the optimal strategy is to passively stay put (2). In the extreme, excessive repetitive activity so as to avoid harm may constitute compulsivity, a debilitating feature of obsessive-compulsive disorder (3).Complementing previous studies of learning about abstract outcomes (4, 5), we investigated individual biases in learning to avoid pain. To this end, we used a novel gambling task that probes how participants adjust their choices in response to painful electrical shocks and, additionally, how they adjust their choices in response t...

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Section: Discussionmentioning

confidence: 71%

Striatal structure and function predict individual biases in learning to avoid pain

Eldar

Hauser

Dayan

et al. 2016

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

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“…Recent studies have shown that discount rates are not only associated with regional changes within the valuation and control networks, but also depend on the strength of connections within and between these networks (31). For instance, we recently showed that frontostriatal tracts predicted decreased delay discounting, whereas subcorticostriatal tracts predicted increased delay discounting in adults (21).…”

Section: Significancementioning

confidence: 80%

“…Research suggests that multiple cognitive and neural processes underlie delay discounting (18)(19)(20). On the one hand, more impatient behavior can result from oversensitivity to immediate rewards (21). For example, there are several studies that show that people are more impatient when an immediate option is present compared with when both options are in the future (22).…”

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confidence: 99%

“…On the other hand, more patient behavior may result from control processes that bias attention away from immediate rewards and/or emphasize the importance of future goals (24,25). There are several studies that show that individual differences in future orientation are associated with more patient choices (1,21,26). Explicitly instructed future orientation leads to (i) withinsubject reduction in discount rates (27)(28)(29) and (ii) increased activity in the brain's executive control network (30).…”

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confidence: 99%

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Adolescent impatience decreases with increased frontostriatal connectivity

Bos

Rodriguez

Schweitzer

et al. 2015

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

237

141

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Adolescence is a developmental period associated with an increase in impulsivity. Impulsivity is a multidimensional construct, and in this study we focus on one of the underlying components: impatience. Impatience can result from (i) disregard of future outcomes and/or (ii) oversensitivity to immediate rewards, but it is not known which of these evaluative processes underlie developmental changes. To distinguish between these two causes, we investigated developmental changes in the structural and functional connectivity of different frontostriatal tracts. We report that adolescents were more impatient on an intertemporal choice task and reported less future orientation, but not more present hedonism, than young adults. Developmental increases in structural connectivity strength in the right dorsolateral prefrontal tract were related to increased negative functional coupling with the striatum and an age-related decrease in discount rates. Our results suggest that mainly increased control, and the integration of future-oriented thought, drives the reduction in impatience across adolescence.adolescence | connectivity | impatience | delay discounting | DTI

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“…Stronger structural and functional connectivity between striatum and lateral pFC has been linked to greater patience across individuals ( Van den Bos, Rodriguez, Schweitzer, & McClure, 2014), and functional connectivity is influenced by dopamine: Pharmacologically increasing dopamine in pFC affects connectivity with the striatum in intertemporal choice (Kayser et al, 2012), and functional connectivity between striatum and lateral pFC during rest is enhanced by L-dopa relative to placebo (Kelly et al, 2009). Thus, enhanced connectivity through dopaminergic medication could also contribute to the results we report here.…”

Section: Locus Of Dopamine Effectsmentioning

confidence: 99%

Dopamine Modulation of Intertemporal Decision-making: Evidence from Parkinson Disease

Foerde

Figner

Doll

et al. 2016

Journal of Cognitive Neuroscience

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Abstract■ Choosing between sooner smaller rewards and larger later rewards is a common choice problem, and studies widely agree that frontostriatal circuits heavily innervated by dopamine are centrally involved. Understanding how dopamine modulates intertemporal choice has important implications for neurobiological models and for understanding the mechanisms underlying maladaptive decision-making. However, the specific role of dopamine in intertemporal decisions is not well understood. Dopamine may play a role in multiple aspects of intertemporal choices-the valuation of choice outcomes and sensitivity to reward delays. To assess the role of dopamine in intertemporal decisions, we tested Parkinson's disease patients who suffer from dopamine depletion in the striatum, in either high (on medication, PD ON ) or low (off medication, PD OFF ) dopaminergic states. Compared with both PD OFF and healthy controls, PD ON made more farsighted choices and reduced their valuations less as a function of increasing time to reward. Furthermore, reduced discounting in the high dopaminergic state was robust across multiple measures, providing new evidence for dopamine's role in making decisions about the future. ■

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Connectivity Strength of Dissociable Striatal Tracts Predict Individual Differences in Temporal Discounting

Cited by 170 publications

References 71 publications

Striatal structure and function predict individual biases in learning to avoid pain

Striatal structure and function predict individual biases in learning to avoid pain

Adolescent impatience decreases with increased frontostriatal connectivity

Dopamine Modulation of Intertemporal Decision-making: Evidence from Parkinson Disease

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