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Preferential activation of midbrain dopamine neurons by appetitive rather than aversive stimuli
Abstract
Midbrain dopamine systems are crucially involved in motivational processes underlying the learning and execution of goal-directed behaviour. Dopamine neurons in monkeys are uniformly activated by unpredicted appetitive stimuli such as food and liquid rewards and conditioned, reward-predicting stimuli. By contrast, fully predicted stimuli are ineffective, and the omission of predicted reward depresses their activity. These characteristics follow associative-learning rules, suggesting that dopamine responses report an error in reward prediction. Accordingly, neural network models are efficiently trained using a dopamine-like reinforcement signal. However, it is unknown whether the responses to environmental stimuli concern specific motivational attributes or reflect more general stimulus salience. To resolve this, we have compared dopamine impulse responses to motivationally opposing appetitive and aversive stimuli. In contrast to appetitive events, primary and conditioned non-noxious aversive stimuli either failed to activate dopamine neurons or, in cases of close resemblance with appetitive stimuli, induced weaker responses than appetitive stimuli. Thus, dopamine neurons preferentially report environmental stimuli with appetitive rather than aversive motivational value.
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“In responding to infant social cues, whether positive or negative, mothers need to integrate both affective and cognitive information about their baby, and evaluate competing demands, before choosing the most appropriate behavioral response (52;53).”
From What’s in a smile? Maternal brain responses to infant facial cues (2008) · cites this paper as [53]
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“Thus, it is possible that the previously reported activations of dopamine neurons by punishers15,17,19,21–24,134 may have been due to physical impact of the tested stimuli, rather than true aversiveness.”
From Dopamine reward prediction-error signalling: A two-component response (2016) · cites this paper as [19]
In the citing paper
“The phasic dopamine activations by aversive stimuli seem to constitute the initial, unselective dopamine response component driven by physical impact25, and possibly boosted by reward context and reward generalization19, rather than reflecting a straightforward aversive response”
From Dopamine reward prediction-error signalling: A two-component response (2016) · cites this paper as [19]
In the citing paper
“whereas some studies have reported that aversive stimuli inhibit the DA activity of midbrain neurons (e.g., [67]), others have found that they elicit phasic DA release in the VS (e.g., [68]).”
From Contributions of the striatum to learning, motivation, and performance: an associative account (2012) · cites this paper as [67]
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Metadata
- Authors
- Mirenowicz, J., & Schultz, W.
- Affiliations
- University of Fribourg (CH)
- Venue
- Nature
- Published
- 1996-02
- Volume
- 379
- Issue
- 6564
- Pages
- 449-451
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W1979640215
- Cited by
- 829
- References
- 33
- Citations by year
- 2026: 8 · 2025: 16 · 2024: 23 · 2023: 14 · 2022: 22 · 2021: 15 · 2020: 17 · 2019: 19 · 2018: 33 · 2017: 23 · 2016: 34 · 2015: 39 · 2014: 40 · 2013: 46 · 2012: 45
- FWCI
- 11.74
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- 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
- midbrain dopaminergic neurons, appetitive stimuli, aversive stimuli, reward prediction error, motivational value, stimulus salience, reinforcement learning, goal-directed behavior
- MeSH terms
- Animals, Haplorhini, Appetitive Behavior, Avoidance Learning, Dopamine, Mesencephalon, Neurons
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