Abstract
Author SummaryThe rewards one receives during decision-making has a profound impact on learning. Much recent interest has focused on the role of the neurotransmitter dopamine in the basal ganglia for influencing learning and behaviour. Here, we ask whether reward can influence low-level sensory processing, for instance in primary sensory cortex, and how dopamine mediates this process. We show in humans that dopamine level, as manipulated with a dopamine agonist and antagonist in a double-blind placebo-controlled design, is involved in reward modulation of primary somatosensory cortex. Higher anticipated reward improved tactile decisions, and receipt of visual reward signals reactivated primary somatosensory cortex for the judged hand as measured using functional neuroimaging. After receiving a higher reward on one trial, somatosensory activations and decisions were enhanced on the next trial, suggesting that reward outcome provides a form of teaching signal that may be fed back to task-relevant sensory cortex. All these behavioural and neural effects of reward on somatosensory decision-making were strongly modulated by the availability of dopamine as the mediating neurotransmitter. These findings raise the tantalising new possibility that reward manipulations in conjunction with dopaminergic drugs might be used to enhance pathologically deficient or lapsed sensory processes, analogous to how rewards can be used to shape or correct behaviour.
Highlights
A role for dopamine in Pavlovian and instrumental learning, as well as in consolidating plastic changes in corticostriatal pathways, is well established [1,2]
We found a clear impact of dopaminergic modulation on somatosensory decisions
We ask whether reward can influence low-level sensory processing, for instance in primary sensory cortex, and how dopamine mediates this process
Summary
A role for dopamine in Pavlovian and instrumental learning, as well as in consolidating plastic changes in corticostriatal pathways, is well established [1,2]. Research on reward has focused on learning, there is growing interest in a possible rewardmediated modulation of perception and sensory decision-making [3,4,5]. It remains unclear whether effects of reward on human sensory processing are influenced by dopamine. We examined possible dopaminergic modulatory influences on neural activity in human primary somatosensory cortex (PSC) and on sensory decisions. To examine any contribution of dopamine to reward modulation of somatosensation, we combine the sensory decision-making paradigm with concurrent functional magnetic resonance imaging (fMRI) (see Materials and Methods, and Figure 1) in the context of both agonist and antagonist dopaminergic pharmacological manipulations
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