Abstract
The neurobiological study of reward was launched by the discovery of intracranial self-stimulation (ICSS). Subsequent investigation of this phenomenon provided the initial link between reward-seeking behavior and dopaminergic neurotransmission. We re-evaluated this relationship by psychophysical, pharmacological, optogenetic, and computational means. In rats working for direct, optical activation of midbrain dopamine neurons, we varied the strength and opportunity cost of the stimulation and measured time allocation, the proportion of trial time devoted to reward pursuit. We found that the dependence of time allocation on the strength and cost of stimulation was similar formally to that observed when electrical stimulation of the medial forebrain bundle served as the reward. When the stimulation is strong and cheap, the rats devote almost all their time to reward pursuit; time allocation falls off as stimulation strength is decreased and/or its opportunity cost is increased. A 3D plot of time allocation versus stimulation strength and cost produces a surface resembling the corner of a plateau (the "reward mountain"). We show that dopamine-transporter blockade shifts the mountain along both the strength and cost axes in rats working for optical activation of midbrain dopamine neurons. In contrast, the same drug shifted the mountain uniquely along the opportunity-cost axis when rats worked for electrical MFB stimulation in a prior study. Dopamine neurons are an obligatory stage in the dominant model of ICSS, which positions them at a key nexus in the final common path for reward seeking. This model fails to provide a cogent account for the differential effect of dopamine transporter blockade on the reward mountain. Instead, we propose that midbrain dopamine neurons and neurons with non-dopaminergic, MFB axons constitute parallel limbs of brain-reward circuitry that ultimately converge on the final-common path for the evaluation and pursuit of rewards.
Highlights
We and our cohabitants are fortunate winners
We show that dopamine-transporter blockade shifts the mountain along both the strength and cost axes in rats working for optical activation of midbrain dopamine neurons
The reward-mountain model was developed to account for data from eICSS experiments in which rats worked for rewarding electrical stimulation of the medial forebrain bundle (MFB)
Summary
We and our cohabitants are fortunate winners. We have enjoyed reproductive success due to a combination of luck and an array of skills among which acumen in cost/benefit decision making is of paramount importance. Despite the artificial spatiotemporal distribution of the evoked neural activity, the rats behaved as if procuring a highly valuable, natural goal object, such as energy-rich food This striking phenomenon, dubbed “intracranial selfstimulation” (ICSS), has been investigated subsequently by means of perturbational, pharmacological, correlational, computational, and behavioral methods that have seen dramatic recent improvements in precision, specificity, and power. We combine, for the first time, direct, specific optical activation of midbrain dopamine neurons, modulation of dopaminergic neurotransmission by a highly selective dopamine-reuptake blocker, psychophysical inference of the values of variables underlying cost-benefit decision making, computational modeling of the processes that intervene between the optical activation of the dopamine neurons and the consequent behavioral output, and simulation of model output.
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