scholarly journals Dopaminergic modulation of the exploration/exploitation trade-off in human decision-making

2019 ◽  
Author(s):  
Karima Chakroun ◽  
David Mathar ◽  
Antonius Wiehler ◽  
Florian Ganzer ◽  
Jan Peters

SummaryA central issue in reinforcement learning and decision-making is whether to exploit knowledge of reward values, or to explore novel options. Although it is widely hypothesized that dopamine neurotransmission plays a key role in regulating this balance, causal evidence for a role of dopamine in human exploration is still lacking. Here, we use a combination of computational modeling, pharmacological intervention and functional magnetic resonance imaging (fMRI) to test for a causal effect of dopamine transmission on the exploration-exploitation trade-off in humans. 31 healthy male subjects performed a restless four-armed bandit task in a within-subjects design under three drug conditions: 150mg of the dopamine precursor L-dopa, 2mg of the D2 receptor antagonist haloperidol, and placebo. In all conditions, choice behavior was best explained by an extension of an established Bayesian learning model accounting for perseveration, uncertainty-based exploration and random exploration. Uncertainty-based exploration was attenuated under L-dopa compared to placebo and haloperidol. There was no evidence for a modulation of prediction error signaling or categorical effects of exploration/exploitation under L-dopa, whereas model-based fMRI revealed that L-dopa attenuated neural representations of overall uncertainty in insula and dorsal anterior cingulate cortex. Our results highlight the computational role of these regions in exploration and suggest that dopamine modulates exploration by modulating how this circuit tracks accumulating uncertainty during decision-making.


eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Karima Chakroun ◽  
David Mathar ◽  
Antonius Wiehler ◽  
Florian Ganzer ◽  
Jan Peters

Involvement of dopamine in regulating exploration during decision-making has long been hypothesized, but direct causal evidence in humans is still lacking. Here, we use a combination of computational modeling, pharmacological intervention and functional magnetic resonance imaging to address this issue. Thirty-one healthy male participants performed a restless four-armed bandit task in a within-subjects design under three drug conditions: 150 mg of the dopamine precursor L-dopa, 2 mg of the D2 receptor antagonist haloperidol, and placebo. Choices were best explained by an extension of an established Bayesian learning model accounting for perseveration, directed exploration and random exploration. Modeling revealed attenuated directed exploration under L-dopa, while neural signatures of exploration, exploitation and prediction error were unaffected. Instead, L-dopa attenuated neural representations of overall uncertainty in insula and dorsal anterior cingulate cortex. Our results highlight the computational role of these regions in exploration and suggest that dopamine modulates how this circuit tracks accumulating uncertainty during decision-making.



2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Luca F. Kaiser ◽  
Theo O. J. Gruendler ◽  
Oliver Speck ◽  
Lennart Luettgau ◽  
Gerhard Jocham

AbstractIn a dynamic world, it is essential to decide when to leave an exploited resource. Such patch-leaving decisions involve balancing the cost of moving against the gain expected from the alternative patch. This contrasts with value-guided decisions that typically involve maximizing reward by selecting the current best option. Patterns of neuronal activity pertaining to patch-leaving decisions have been reported in dorsal anterior cingulate cortex (dACC), whereas competition via mutual inhibition in ventromedial prefrontal cortex (vmPFC) is thought to underlie value-guided choice. Here, we show that the balance between cortical excitation and inhibition (E/I balance), measured by the ratio of GABA and glutamate concentrations, plays a dissociable role for the two kinds of decisions. Patch-leaving decision behaviour relates to E/I balance in dACC. In contrast, value-guided decision-making relates to E/I balance in vmPFC. These results support mechanistic accounts of value-guided choice and provide evidence for a role of dACC E/I balance in patch-leaving decisions.



2021 ◽  
Author(s):  
Malou Dongelmans ◽  
Romain Durand-de Cuttoli ◽  
Claire Nguyen ◽  
Maxime Come ◽  
Etienne K. Duranté ◽  
...  

SummaryLong-term exposure to nicotine alters brain circuits and induces profound changes in decision-making strategies, affecting behaviors both related and unrelated to drug seeking and consumption. Using an intracranial self-stimulation reward-based foraging task, we investigated the impact of chronic nicotine on the trade-off between exploitation and exploration, and the role of ventral tegmental area (VTA) dopamine (DA) neuron activity in decision-making unrelated to nicotine-seeking. Model-based and archetypal analysis revealed a substantial inter-individual variability in decision-making strategies, with mice passively exposed to chronic nicotine visiting more frequently options associated with higher reward probability and therefore shifting toward a more exploitative profile compared to non-exposed animals. We then mimicked the effect of chronic nicotine on the tonic activity of VTA DA neurons using optogenetics, and found that photo-stimulated mice had a behavioral phenotype very close to that of mice exposed to nicotine, suggesting that the dopaminergic control of the exploration/exploitation balance is altered under nicotine exposure. Our results thus reveal a key role of tonic midbrain DA in the exploration/exploitation trade-off and highlight a potential mechanism by which nicotine affects decision-making.



2019 ◽  
Author(s):  
Luca F. Kaiser ◽  
Theo O.J. Gruendler ◽  
Oliver Speck ◽  
Lennart Luettgau ◽  
Gerhard Jocham

AbstractIn a dynamic world, it is essential to decide when to leave an exploited resource. Such patch-leaving decisions involve balancing the cost of moving against the gain expected from the alternative patch. This is in contrast with value-guided decisions that typically involve maximizing reward by selecting the current best option. Patterns of neuronal activity pertaining to patch-leaving decisions have been reported in the dorsal anterior cingulate cortex (dACC), whereas competition via mutual inhibition in the ventromedial prefrontal cortex (vmPFC) is thought to underlie value-guided choice. Here, we show that the balance between cortical excitation and inhibition (E/I balance), measured by the ratio of GABA and glutamate concentrations, plays a dissociable role for the two kinds of decisions. Patch-leaving decision behaviour was related to E/I balance in dACC. In contrast, value-guided decision making was related to E/I balance in vmPFC. These results support previous mechanistic accounts of value-guided choice and provide novel evidence for a role of dACC E/I balance in patch-leaving decisions.



2009 ◽  
Vol 29 (8) ◽  
pp. 1678-1691 ◽  
Author(s):  
Mark E. Walton ◽  
James Groves ◽  
Katie A. Jennings ◽  
Paula L. Croxson ◽  
Trevor Sharp ◽  
...  


2016 ◽  
Author(s):  
Miriam C Klein-Flügge ◽  
Steven W Kennerley ◽  
Karl Friston ◽  
Sven Bestmann

AbstractIntegrating costs and benefits is crucial for optimal decision-making. While much is known about decisions that involve outcome-related costs (e.g., delay, risk), many of our choices are attached to actions and require an evaluation of the associated motor costs. Yet how the brain incorporates motor costs into choices remains largely unclear. We used human functional magnetic resonance imaging during choices involving monetary reward and physical effort to identify brain regions that serve as a choice comparator for effort-reward trade-offs. By independently varying both options' effort and reward levels, we were able to identify the neural signature of a comparator mechanism. A network involving supplementary motor area (SMA) and the caudal portion of dorsal anterior cingulate cortex (dACC) encoded the difference in reward (positively) and effort levels (negatively) between chosen and unchosen choice options. We next modelled effort-discounted subjective values using a novel behavioural model. This revealed that the same network of regions involving dACC and SMA encoded the difference between the chosen and unchosen options' subjective values, and that activity was best described using a concave model of effort-discounting. In addition, this signal reflected how precisely value determined participants' choices. By contrast, separate signals in SMA and ventro-medial PFC (vmPFC) correlated with participants' tendency to avoid effort and seek reward, respectively. This suggests that the critical neural signature of decision-making for choices involving motor costs is found in human cingulate cortex and not vmPFC as typically reported for outcome-based choice. Furthermore, distinct frontal circuits ‘drive’ behaviour towards reward-maximization and effort-minimization.Significance StatementThe neural processes that govern the trade-off between expected benefits and motor costs remain largely unknown. This is striking because energetic requirements play an integral role in our day-to-day choices and instrumental behaviour, and a diminished willingness to exert effort is a characteristic feature of a range of neurological disorders. We use a new behavioural characterization of how humans trade-off reward-maximization with effort-minimization to examine the neural signatures that underpin such choices, using BOLD MRI neuroimaging data. We find the critical neural signature of decision-making, a signal that reflects the comparison of value between choice options, in human cingulate cortex, whereas two distinct brain circuits ‘drive’ behaviour towards reward-maximization or effort-minimization.



2018 ◽  
Vol 235 (5) ◽  
pp. 1427-1437 ◽  
Author(s):  
Aaron P. Smith ◽  
Rebecca S. Hofford ◽  
Thomas R. Zentall ◽  
Joshua S. Beckmann




2021 ◽  
Vol 118 (35) ◽  
pp. e2014781118
Author(s):  
Atsushi Fujimoto ◽  
Elisabeth A. Murray ◽  
Peter H. Rudebeck

Decision-making and representations of arousal are intimately linked. Behavioral investigations have classically shown that either too little or too much bodily arousal is detrimental to decision-making, indicating that there is an inverted “U” relationship between bodily arousal and performance. How these processes interact at the level of single neurons as well as the neural circuits involved are unclear. Here we recorded neural activity from orbitofrontal cortex (OFC) and dorsal anterior cingulate cortex (dACC) of macaque monkeys while they made reward-guided decisions. Heart rate (HR) was also recorded and used as a proxy for bodily arousal. Recordings were made both before and after subjects received excitotoxic lesions of the bilateral amygdala. In intact monkeys, higher HR facilitated reaction times (RTs). Concurrently, a set of neurons in OFC and dACC selectively encoded trial-by-trial variations in HR independent of reward value. After amygdala lesions, HR increased, and the relationship between HR and RTs was altered. Concurrent with this change, there was an increase in the proportion of dACC neurons encoding HR. Applying a population-coding analysis, we show that after bilateral amygdala lesions, the balance of encoding in dACC is skewed away from signaling either reward value or choice direction toward HR coding around the time that choices are made. Taken together, the present results provide insight into how bodily arousal and decision-making are signaled in frontal cortex.





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