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Cited by 506Neurotransmitter Receptor Influence on BehaviorNeural and Behavioral Psychology StudiesMemory and Neural Mechanisms

Is the short-latency dopamine response too short to signal reward error?

Redgrave, Peter, Prescott, Tony J., Gurney, Kevin·1999·Trends in Neurosciences
DOI 10.1016/s0166-2236(98)01373-3
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Abstract

Unexpected stimuli that are behaviourally significant have the capacity to elicit a short-latency, short-duration burst of firing in mesencephalic dopaminergic neurones. An influential interpretation of the experimental data that characterize this response proposes that dopaminergic neurones have a crucial role in reinforcement learning because they signal error in the prediction of future reward. In this article we propose a different functional role for this 'short-latency dopamine response' in the mechanisms that underlie associative learning. We suggest that the initial burst of dopaminergic-neurone firing could represent an essential component in the process of switching attentional and behavioural selections to unexpected, behaviourally important stimuli. This switching response could be a crucial prerequisite for associative learning and might be part of a general short-latency response that is mediated by catecholamines and prepares the organism for an appropriate reaction to biologically significant events. Any act which in a given situation produces satisfaction becomes associated with that situation so that when the situation recurs the act is more likely than before to recur also. E.L. Thorndike (1911) 1.

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  • Reward-related mesolimbic dopamine steers animal behavior, creating automatic approach toward reward-associated objects and avoidance of objects unlikely to be beneficial.

    “Reward-related mesolimbic dopamine steers animal behavior, creating automatic approach toward reward-associated objects and avoidance of objects unlikely to be beneficial.”

    From Reward Changes Salience in Human Vision via the Anterior Cingulate (2010) · cites this paper as Redgrave et al., 1999

    The Introduction (p. 3) says rewarding stimuli elicit approach, and the discussion (p. 6) links dopamine responses to switching behavior to locate and acquire reward. But the paper does not establish that mesolimbic dopamine automatically produces approach or avoidance of objects unlikely to be beneficial. In Response generalisation (p. 8), a never-baited box evokes a dopamine response and orienting, although the monkey does not reach for it. (LLM, conf=0.86)

    Experimental — accuracy not yet measured

  • Theories of the function of dopamine in reinforcement learning and animal approach behavior place reward firmly at the center of attentional control.

    “theories of the function of dopamine in reinforcement learning and animal approach behavior place reward firmly at the center of attentional control (Berridge and Robinson, 1998; Ikemoto and Panksepp, 1999; Redgrave et al., 1999; Wise, 2004; Alcaro et al., 2007).”

    From Reward Changes Salience in Human Vision via the Anterior Cingulate (2010) · cites this paper as Redgrave et al., 1999

    The introduction (p. 3) describes a popular theory in which dopamine signals reinforcement and influences action selection, and notes that rewarding stimuli elicit approach. But it does not say that these reward-centered theories put reward at the center of attentional control. Instead, the authors propose that dopamine reallocates attention toward unexpected biologically significant events, including non-rewarding ones (pp. 3, 6). (LLM, conf=0.83)

    Experimental — accuracy not yet measured

  • Recognition of the two-component structure of phasic dopamine responses may resolve earlier controversies that suggested an attentional rather than rewarding role of the dopamine prediction-error signal.

    “Recognition of the two-component structure of phasic dopamine responses may also resolve earlier controversies, which suggested an attentional rather than rewarding role of the dopamine prediction-error signal64,65 on the basis of activations following exposure to physically salient stimuli16,20 and punishers24.”

    From Dopamine reward prediction-error signalling: A two-component response (2016) · cites this paper as [64]

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Research works printed but not linked: 3

  1. 16 Redgrave, P., et al. (1998) Neuroscience in press
  2. 17 Prescott, T. J., et al. (1998) Adaptive Behavior (in press)
  3. 39 Weiner, I. (1990) Psychological Bulletin 108, 442-461

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Authors
Redgrave, P., Prescott, T. J., & Gurney, K.
Affiliations
University of Sheffield (GB)
ORCID
Venue
Trends in Neurosciences
Publisher
Elsevier BV
Published
1999-04
Volume
22
Issue
4
Pages
146-151
ISSN
0166-2236 (ISSN-L)
DOI
10.1016/s0166-2236(98)01373-3
OpenAlex
W2041589773
Cited by
506
References
38
Citations by year
2026: 2 · 2025: 4 · 2024: 2 · 2023: 9 · 2022: 8 · 2021: 9 · 2020: 3 · 2019: 9 · 2018: 2 · 2017: 13 · 2016: 17 · 2015: 17 · 2014: 16 · 2013: 23 · 2012: 26
FWCI
2.62
Type
journal article
Language
en
Open access
closed
Licence
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations
  • Trends in Neurosciences (publishedVersion)
  • PubMed (publishedVersion)
  • White Rose Research Online (University of Leeds, The University of Sheffield, University of York) (acceptedVersion)
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 prediction error, reinforcement learning, associative learning, attentional shift, behavioural selection, catecholamines, midbrain
MeSH terms
Action Potentials, Animals, Association, Attention, Avoidance Learning, Basal Ganglia, Behavior, Animal, Catecholamines, Conditioning, Operant, Dopamine, Exploratory Behavior, Humans, Learning, Mesencephalon, Models, Neurological, Models, Psychological, Reaction Time, Reinforcement, Psychology, Reward, Time Factors

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