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Convergent Processing of Both Positive and Negative Motivational Signals by the VTA Dopamine Neuronal Populations
Open accessAbstract
Dopamine neurons in the ventral tegmental area (VTA) have been traditionally studied for their roles in reward-related motivation or drug addiction. Here we study how the VTA dopamine neuron population may process fearful and negative experiences as well as reward information in freely behaving mice. Using multi-tetrode recording, we find that up to 89% of the putative dopamine neurons in the VTA exhibit significant activation in response to the conditioned tone that predict food reward, while the same dopamine neuron population also respond to the fearful experiences such as free fall and shake events. The majority of these VTA putative dopamine neurons exhibit suppression and offset-rebound excitation, whereas ∼25% of the recorded putative dopamine neurons show excitation by the fearful events. Importantly, VTA putative dopamine neurons exhibit parametric encoding properties: their firing change durations are proportional to the fearful event durations. In addition, we demonstrate that the contextual information is crucial for these neurons to respectively elicit positive or negative motivational responses by the same conditioned tone. Taken together, our findings suggest that VTA dopamine neurons may employ the convergent encoding strategy for processing both positive and negative experiences, intimately integrating with cues and environmental context.
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“Recent experiments also show that acute stressors are encoded by DA-releasing neurons in the VTA, cause DA sensitization in the NAC, and facilitate drug taking; demonstrating that mesolimbic DA release also encodes negative motivational states and stress responses (Miczek et al 2011; Wang and Tsien 2011).”
From The behavioral, anatomical and pharmacological parallels between social attachment, love and addiction (2012) · cites this paper as Wang and Tsien 2011
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“Some of the stress-related effects of CRF in the NAC shell may be DA-dependent; recall that DA is also modulated by acute and chronic stressors (Miczek et al 2011; Wang and Tsien 2011; Chen et al 2012b).”
From The behavioral, anatomical and pharmacological parallels between social attachment, love and addiction (2012) · cites this paper as Wang and Tsien 2011
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“Thus, although 89% of VTA dopaminergic neurons respond with activation to a conditioned reward, they also respond to fearful events, with the majority of the neurons showing suppression. Interestingly, 25% respond with excitation to both positive and fearful events [101].”
From A neoHebbian framework for episodic memory; role of dopamine-dependent late LTP (2011) · cites this paper as [101]
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Self-citationDopamine and Opioid regulation of amygdala function
Patel, S. (2020) · The Sydney eScholarship Repository (The University of Sydney)
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Metadata
- Authors
- Wang, D. V., & Tsien, J. Z.
- Affiliations
- East China Normal University (CN)
- Corresponding author
- Tsien, Joe Z.
- ORCID
- Wang, Dong V.
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2011-02-15
- Volume
- 6
- Issue
- 2
- Pages
- e17047
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC3039659
- OpenAlex
- W2083000736
- Cited by
- 116
- References
- 53
- Citations by year
- 2026: 2 · 2025: 8 · 2024: 5 · 2023: 1 · 2022: 4 · 2021: 4 · 2020: 6 · 2019: 6 · 2018: 6 · 2017: 5 · 2016: 8 · 2015: 7 · 2014: 17 · 2013: 13 · 2012: 17
- FWCI
- 7.15
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Funders
- Georgia Research Alliance
- National Institute on Aging (AG025918, R01AG034663, AG024022, R01AG025918, AG034663, R01AG024022)
- National Institute of Mental Health (MH060236, R01MH060236)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Keywords
- ventral tegmental area, dopaminergic neurons, fear, reward, contextual modulation, free fall, mice
- MeSH terms
- Animals, Fear, Male, Mice, Inbred C57BL, Motivation, Time Factors, Ventral Tegmental Area, Mice, Dopaminergic Neurons
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