Overriding Phasic Dopamine Signals Redirects Action Selection during Risk/Reward Decision Making

Abstract

Phasic increases and decreases in dopamine (DA) transmission encode reward prediction errors thought to facilitate reward-related learning, yet how these signals guide action selection in more complex situations requiring evaluation of different reward remains unclear. We manipulated phasic DA signals while rats performed a risk/reward decision-making task, using temporally discrete stimulation of either the lateral habenula (LHb) or rostromedial tegmental nucleus (RMTg) to suppress DA bursts (confirmed with neurophysiological studies) or the ventral tegmental area (VTA) to override phasic dips. When rats chose between small/certain and larger/risky rewards, LHb or RMTg stimulation, time-locked to delivery of one of these rewards, redirected bias toward the alternative option, whereas VTA stimulation after non rewarded choices increased risky choice. LHb stimulation prior to choices shifted bias away from more preferred options. Thus, phasic DA signals provide feedback on whether recent actions were rewarded to update decision policies and direct actions toward more desirable reward.

Functional Genetic Variation in Dopamine Signaling Moderates Prefrontal Cortical Activity During Risky Decision Making

“…The prefrontal cortex and striatum interact during the process of decision making, with dopamine signaling mediating-behavior in the context of relative risk and reward (Stopper et al, 2014). This study supports the view that Negative relationship between dopamine gene scores and the parametric modulation of activation by pump number during risky decision making.…”

Dopamine-associated cached values are not sufficient as the basis for action selection

“…A preponderance of evidence supports the notion that phasic dopamine transmission functions as a neural instantiation of the temporal-difference prediction errors that drive reinforcement learning (13)(14)(15)(16)(17)(18)(19)(20)(21)(22)(23)(24). Accordingly, changes in dopamine transmission are evoked whenever there is an unexpected reward-related event, both when reward delivery differs from expectations and when reward-predictive cues drive changes in expectation of available reward.…”

“…It is believed that these cached values are represented as synaptic weights within corticostriatal circuitry, reflected in the activity of subpopulations of striatal projection neurons (6)(7)(8)(9), and are updated by dopaminedependent synaptic plasticity (10)(11)(12). Indeed, a wealth of evidence suggests that the phasic activity of dopamine neurons reports instances in which current reward or expectation of future reward differs from current expectations (13)(14)(15)(16)(17)(18)(19)(20)(21)(22)(23)(24). This pattern of activity resembles the prediction-error term from temporal-difference reinforcement-learning algorithms, which is considered the critical teaching signal for updating cached values.…”

Neuronal Reward and Decision Signals: From Theories to Data

“…The dispreference might be due to monosynaptic excitation of aversive coding dopamine neurons, as suggested by FOS gene expression and excitatory currents (EPSCs) in dopamine neurons and by blunting of the dispreference with prefrontal D1 antagonists (303). However, dopamine neurons are not activated by aversive stimulus components (157,160), FOS activation is slow and may derive from rebound activation following dopamine depression (158,566), EPSCs do not necessarily induce action potentials required for dopamine release in target areas, and the optogenetic stimulation of presumed dopamine neurons might have included non-dopamine GABA neurons in used TH:Cre mice (304). Alternatively, dispreference might reflect disynaptic inhibition of dopamine neurons via the inhibitory rostromedial reticular nucleus (613).…”

“…Alternatively, dispreference might reflect disynaptic inhibition of dopamine neurons via the inhibitory rostromedial reticular nucleus (613). The monosynaptic habenula-dopamine projection is weak (625), and electrophysiology reports depression-activation sequence of VTA and nigral dopamine impulse activity following habenula stimulation (95,250,344,566) that likely involves the inhibitory rostromedial reticular nucleus (226,249). Furthermore, habenula glutamate receptor blockade increases striatal and prefrontal dopamine concentrations, probably reflecting blockade of the inhibitory habenuladopamine projection (310).…”