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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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In the citing paper
“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
About these checks
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.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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