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Dopamine in Motivational Control: Rewarding, Aversive, and Alerting
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Midbrain dopamine neurons are well known for their strong responses to rewards and their critical role in positive motivation. It has become increasingly clear, however, that dopamine neurons also transmit signals related to salient but nonrewarding experiences such as aversive and alerting events. Here we review recent advances in understanding the reward and nonreward functions of dopamine. Based on this data, we propose that dopamine neurons come in multiple types that are connected with distinct brain networks and have distinct roles in motivational control. Some dopamine neurons encode motivational value, supporting brain networks for seeking, evaluation, and value learning. Others encode motivational salience, supporting brain networks for orienting, cognition, and general motivation. Both types of dopamine neurons are augmented by an alerting signal involved in rapid detection of potentially important sensory cues. We hypothesize that these dopaminergic pathways for value, salience, and alerting cooperate to support adaptive behavior.
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“The endogenous source for the majority of monoamines in the forebrain come from the midbrain, with serotonin, norepinephrine, and dopamine arising from the dorsal raphe (DR), locus coeruleus (LC), and ventral tegmental area (VTA) or substantia nigra pars compacta, respectively”
From Mechanisms of ketamine and its metabolites as antidepressants (2022) · cites this paper as Bromberg-Martin et al., 2010
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“Furthermore, midbrain DA neurons constitute the mesocorticolimbic pathway critical for creating rewards and signaling aversive outcomes (55, 56).”
From Emotional Blunting in Patients With Major Depressive Disorder: A Brief Non-systematic Review of Current Research (2021) · cites this paper as [55]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“DA neurotransmission is essential for diverse behavioral outputs, including motivation, cognition, reward learning, decision making, salience attribution, and voluntary motor control [121–127].”
From Adolescent nicotine exposure and persistent neurocircuitry changes: unveiling lifelong psychiatric risks (2025) · cites this paper as [123]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“In primates, even a very mild stress can activate the dopaminergic ‘salience’ neurons that respond to both aversive and rewarding events46 and can increase dopamine release in dlPFC47.”
From Stress weakens prefrontal networks: molecular insults to higher cognition (2015) · cites this paper as [46]
Experimental — accuracy not yet measuredThe cited source says what the claim attributes to it.
In the citing paper
“salience-signalling dopamine neurons do not differentiate the unpredicted absence of reward and aversion (right panel)”
From Aberrant Salience, Information Processing, and Dopaminergic Signaling in People at Clinical High Risk for Psychosis (2020) · cites this paper as Bromberg-Martin et al. (2010)
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“(B) dopamine neurons signalling salience activate to cues predicting reward (red) and aversion (blue) (left panel)”
From Aberrant Salience, Information Processing, and Dopaminergic Signaling in People at Clinical High Risk for Psychosis (2020) · cites this paper as Bromberg-Martin et al. (2010)
The cited source says what the claim attributes to it.
In the citing paper
“dopamine neurons activate to delivery of both salient rewarding (red) and aversive (blue) outcomes (middle panel)”
From Aberrant Salience, Information Processing, and Dopaminergic Signaling in People at Clinical High Risk for Psychosis (2020) · cites this paper as Bromberg-Martin et al. (2010)
The cited source says what the claim attributes to it.
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“Subsequent animal cell recordings have shown that other dopamine neurons are excited by outcomes other than rewards, and to the cues predicting these outcomes (5, 8-13).”
From Aberrant Salience, Information Processing, and Dopaminergic Signaling in People at Clinical High Risk for Psychosis (2020) · cites this paper as [11]
The cited source says what the claim attributes to it.
In the citing paper
“dopamine signals salient outcomes.”
From Aberrant Salience, Information Processing, and Dopaminergic Signaling in People at Clinical High Risk for Psychosis (2020) · cites this paper as Bromberg-Martin et al. (2010)
In the citing paper
“Such RPE signals are projected to a decision making network including striatal, prefrontal, and insular regions (e.g., Blakemore and Robbins, 2012; Bromberg-Martin et al., 2010; Gläscher et al., 2009).”
From Cognitive flexibility in adolescence: Neural and behavioral mechanisms of reward prediction error processing in adaptive decision making during development (2015) · cites this paper as Bromberg-Martin et al., 2010
In the citing paper
“distinct populations of dopamine neurons encode: 1) motivational value, whereby certain dopamine neurons are excited by appetitive stimuli, which promote approach, and inhibited by aversive stimuli, which promote withdrawal”
From Oxytocin, motivation and the role of dopamine (2014) · cites this paper as Bromberg-Martin et al., 2010
In the citing paper
“2) motivational salience, as other dopamine neurons show weak responses to neutral events but are excited by salient events (i.e. regardless of whether the event was appetitive or aversive in nature (Bromberg-Martin et al., 2010).”
From Oxytocin, motivation and the role of dopamine (2014) · cites this paper as Bromberg-Martin et al., 2010
In the citing paper
“Hence, dopaminergic manipulations appear to influence assignment of motivational value or salience, impacting the drive toward such rewards, rather than the pleasure derived from the reward itself (Berridge and Robinson, 1998, Bromberg-Martin et al., 2010, Salamone, 2007).”
From Oxytocin, motivation and the role of dopamine (2014) · cites this paper as Bromberg-Martin et al., 2010
In the citing paper
“As discussed above, signals within certain subpopulations of dopamine neurons are hypothesized to encode motivational salience while others carry signal relating to the motivational value (appetitive versus aversive; Bromberg-Martin et al., 2010).”
From Oxytocin, motivation and the role of dopamine (2014) · cites this paper as Bromberg-Martin et al., 2010
In the citing paper
“The OFC projects reward-related information to the ventral striatum (Williams et al., 1993), and this provides a route, in part via the habenula, for reward-related information to reach the dopamine neurons (Rolls, 2017), which respond inter alia to positive reward prediction error (Bromberg-Martin et al., 2010; Schultz, 2016a, 2017).”
From The orbitofrontal cortex: reward, emotion and depression (2020) · cites this paper as Bromberg-Martin et al., 2010
In the citing paper
“It is now well-established that dopamine neurons can also fire in response to unexpected aversive outcomes and cues predicting punishments [45].”
From A neoHebbian framework for episodic memory; role of dopamine-dependent late LTP (2011) · cites this paper as [45]
In the citing paper
“More recent work has demonstrated conditions under which dopamine cells can be driven by aversive stimuli (reviewed in [45]; see also Box 2).”
From A neoHebbian framework for episodic memory; role of dopamine-dependent late LTP (2011) · cites this paper as [45]
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Metadata
- Authors
- Bromberg-Martin, E. S., Matsumoto, M., & Hikosaka, O.
- Affiliations
- National Institutes of Health (US)
- Corresponding author
- Hikosaka, Okihide
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2010-12
- Volume
- 68
- Issue
- 5
- Pages
- 815-834
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC3032992
- OpenAlex
- W2076457657
- Cited by
- 2,396
- References
- 274
- Citations by year
- 2026: 131 · 2025: 208 · 2024: 189 · 2023: 137 · 2022: 158 · 2021: 185 · 2020: 208 · 2019: 161 · 2018: 159 · 2017: 142 · 2016: 135 · 2015: 136 · 2014: 143 · 2013: 123 · 2012: 113
- FWCI
- 8.73
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health (Z99 EY999999)
- 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 › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- dopaminergic neurons, motivational control, reward, aversive stimuli, alerting, motivational salience, motivational value, value learning, orienting, midbrain dopamine, dopaminergic pathways
- MeSH terms
- Animals, Arousal, Avoidance Learning, Dopamine, Humans, Mesencephalon, Motivation, Neural Pathways, Neurons, Reward
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