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Cited by 63Neurotransmitter Receptor Influence on BehaviorNeural and Behavioral Psychology StudiesMemory and Neural Mechanisms

Reward Contexts Extend Dopamine Signals to Unrewarded Stimuli

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Kobayashi, Shunsuke, Schultz, Wolfram·2014·Current Biology
DOI 10.1016/j.cub.2013.10.061PMC PMC3898276
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Abstract

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.

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  • The magnitude of dopaminergic responses to unrewarded visual stimuli in primates is significantly more robust in rewarded environments.

    “However, the magnitude of these responses is significantly more robust in rewarded environments, suggesting that dopaminergic responses to sensory stimuli primarily serve to promote interaction with potentially rewarding objects (Kobayashi and Schultz, 2014) or enable novel action discovery that could lead to reward (Redgrave and Gurney, 2006).”

    From Ventral striatum dopamine release encodes unique properties of visual stimuli in mice (2023) · cites this paper as Kobayashi and Schultz, 2014

  • Increasing the probability that the animal will receive a reward in a given experiment increases the incidence of dopamine activations to unrewarded stimuli.

    “Similarly, increasing the probability that the animal will receive a reward in a given experiment constitutes a more rewarded context and increases the incidence of dopamine activations to unrewarded stimuli5,6,34.”

    From Dopamine reward prediction-error signalling: A two-component response (2016) · cites this paper as [34]

  • Unrewarded stimuli elicit little dopamine activation when well separated from reward, but the same unrewarded stimuli effectively elicit dopamine activations when presented in the same context in which the animal receives a reward.

    “Unrewarded stimuli elicit little dopamine activation when they are well separated from reward; however, the same unrewarded stimuli effectively elicit dopamine activations when presented in the same context in which the animal receives a reward34 (FIG. 3b).”

    From Dopamine reward prediction-error signalling: A two-component response (2016) · cites this paper as [34]

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Research works printed but not linked: 1

  1. [7]Pavlov P.I. Conditioned Reflexes 1927 Oxford University Press New York

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Authors
Kobayashi, S., & Schultz, W.
Affiliations
University of Cambridge (GB)
Corresponding author
Kobayashi, Shunsuke
ORCID
Venue
Current Biology
Publisher
Elsevier BV
Published
2014-01
Volume
24
Issue
1
Pages
56-62
ISSN
0960-9822 (ISSN-L)
DOI
10.1016/j.cub.2013.10.061
PMC
PMC3898276
OpenAlex
W2079540635
Cited by
63
References
32
Citations by year
2026: 1 · 2025: 10 · 2024: 6 · 2023: 5 · 2022: 7 · 2021: 2 · 2020: 4 · 2019: 3 · 2018: 5 · 2017: 5 · 2016: 7 · 2015: 6 · 2014: 2
FWCI
2.45
Type
journal article
Language
en
Update notices
erratum (2014-02-17)
Open access
Licence
Locations
  • Current Biology (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Institutional Repositories DataBase (IRDB) (submittedVersion)
Funders
  • Wellcome Trust (095495, 093875)
  • Japan Society for the Promotion of Science (23500393)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Keywords
dopaminergic neurons, reward context, pseudoconditioning
MeSH terms
Animals, Behavior, Animal, Choice Behavior, Dopamine, Macaca mulatta, Male, Neurons, Reward, Signal Transduction

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