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Linking Context with Reward: A Functional Circuit from Hippocampal CA3 to Ventral Tegmental Area
Open accessAbstract
Reward-motivated behavior is strongly influenced by the learned significance of contextual stimuli in the environment. However, the neural pathways that mediate context-reward relations are not well understood. We have identified a circuit from area CA3 of dorsal hippocampus to ventral tegmental area (VTA) that uses lateral septum (LS) as a relay. Theta frequency stimulation of CA3 excited VTA dopamine (DA) neurons and inhibited non-DA neurons. DA neuron excitation was likely mediated by disinhibition because local antagonism of γ-aminobutyric acid receptors blocked responses to CA3 stimulation. Inactivating components of the CA3-LS-VTA pathway blocked evoked responses in VTA and also reinstatement of cocaine-seeking by contextual stimuli. This transsynaptic link between hippocampus and VTA appears to be an important substrate by which environmental context regulates goal-directed behavior.
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“this area serves as a hub in the brain by integrating social, emotional, and contextual information from different brain systems and contributing to the coordination of adaptive context-specific behavioral responses (Sheehan et al., 2004; Luo et al., 2011)”
From Sex-specific modulation of juvenile social play behavior by vasopressin and oxytocin depends on social context (2014) · cites this paper as Luo et al., 2011
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“is necessary for the formation of cocaine conditioned place preference in rats [36,37].”
From Involvement of dopamine, but not norepinephrine, in the sex-specific regulation of juvenile socially rewarding behavior by vasopressin (2018) · cites this paper as [36]
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“and the lateral septum plays a key role in modulating context-specific motivational states (Sheehan et al., 2004; Luo et al., 2011; Sartor and Aston-Jones, 2012).”
From Sex-specific modulation of juvenile social play behavior by vasopressin and oxytocin depends on social context (2014) · cites this paper as Luo et al., 2011
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“other studies indicating that the LS is part of the brain reward system.”
From Involvement of dopamine, but not norepinephrine, in the sex-specific regulation of juvenile socially rewarding behavior by vasopressin (2018) · cites this paper as [36]
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“Our results thus provide novel insights into the relationship between midbrain dopaminergic neurons, encoding salient information about an environment9,10,16,19,20, and hippocampal assemblies, providing representations of space1-3, in modulating memory according to the value of the information to be remembered.”
From Dopaminergic neurons promote hippocampal reactivation and spatial memory persistence (2014) · cites this paper as [16]
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“This VTA firing response to spatial novelty, which might be partially informed by hippocampal spatio-contextual inputs10,16, resulted in a higher fraction of action potentials discharged in bursts (interspike interval<50ms; novelty-induced burst ratio change=0.31±0.07, t156=4.31, P=2.9×10−5, paired t-test), a potentially suitable signal to in turn modulate hippocampal dynamics.”
From Dopaminergic neurons promote hippocampal reactivation and spatial memory persistence (2014) · cites this paper as [16]
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Metadata
- Authors
- Luo, A. H., Tahsili-Fahadan, P., Wise, R. A., Lupica, C. R., & Aston-Jones, G.
- Affiliations
- National Institutes of Health (US)
- Department of Neurosciences, Medical University of South Carolina, Charleston, SC 29425, USA.
- Corresponding author
- Luo, Alice H.
- Venue
- Science
- Published
- 2011-07-15
- Volume
- 333
- Issue
- 6040
- Pages
- 353-357
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- PMC
- PMC3150711
- OpenAlex
- W2013438045
- Cited by
- 425
- References
- 17
- Citations by year
- 2026: 15 · 2025: 21 · 2024: 30 · 2023: 18 · 2022: 29 · 2021: 29 · 2020: 28 · 2019: 22 · 2018: 30 · 2017: 32 · 2016: 32 · 2015: 37 · 2014: 39 · 2013: 31 · 2012: 23
- FWCI
- 13.24
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Rutgers University Community Repository (Rutgers University) (submittedVersion)
- Funders
- National Institutes of Health
- National Institute of Mental Health (F31MH071093)
- National Institute on Drug Abuse (R37DA006214, ZIADA000471)
- National Center for Research Resources (UL1RR029882)
- 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 › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- hippocampal CA3, ventral tegmental area, lateral septum, dopaminergic neurons, disinhibition, GABA receptors, cocaine seeking, reinstatement, goal-directed behavior, contextual cues, neural circuits
- MeSH terms
- Action Potentials, Animals, Behavior, Animal, Brain Mapping, Cocaine, Dopamine, Electric Stimulation, gamma-Aminobutyric Acid, Hippocampus, Male, Models, Neurological, Neural Inhibition, Neural Pathways, Neurons, Reward, Self Administration, Septal Nuclei, Theta Rhythm, Rats, Sprague-Dawley, Ventral Tegmental Area, GABA Agonists, GABA Antagonists, Rats, CA3 Region, Hippocampal, Drug-Seeking Behavior
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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