Reward Contexts Extend Dopamine Signals to Unrewarded Stimuli

Summary

Basic tenets of sensory processing emphasize the importance of accurate identification and discrimination of environmental objects [ 1]. Although this principle holds also for reward, the crucial acquisition of reward for survival would be aided by the capacity to detect objects whose rewarding properties may not be immediately apparent. Animal learning theory conceptualizes how unrewarded stimuli induce behavioral reactions in rewarded contexts due to pseudoconditioning and higher-order context conditioning [ 2–6]. We hypothesized that the underlying mechanisms may involve context-sensitive reward neurons. We studied short-latency activations of dopamine neurons to unrewarded, physically salient stimuli while systematically changing reward context. Dopamine neurons showed substantial activations to unrewarded stimuli and their conditioned stimuli in highly rewarded contexts. The activations decreased and often disappeared entirely with stepwise separation from rewarded contexts. The influence of reward context suggests that dopamine neurons respond to real and potential reward. The influence of reward context is compatible with the reward nature of phasic dopamine responses. The responses may facilitate rapid, default initiation of behavioral reactions in environments usually containing reward. Agents would encounter more and miss less reward, resulting in survival advantage and enhanced evolutionary fitness.

Highlights

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  Dopamine neurons are activated by unrewarded events in rewarded contexts

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  More rewarded contexts are associated with stronger dopamine activations

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  The effective unrewarded events do not induce bidirectional prediction error signals

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  Reward context-dependent signaling conceivably leads to more reward

Abstract

When rewards are frequent and everywhere, any object could be a reward. Reacting to objects in such reward contexts would enhance the chance of getting a reward. Kobayashi and Schultz show that dopamine neurons respond in reward contexts even to unrewarded objects.