Reward behaviour is regulated by the strength of hippocampus–nucleus accumbens synapses

LeGates, Tara A.; Kvarta, Mark D.; Tooley, Jessica R.; Francis, T. Chase; Lobo, Mary Kay; Creed, Meaghan C.; Thompson, Scott M.

doi:10.1038/s41586-018-0740-8

Cited by 290Neuroscience and Neuropharmacology ResearchNeurotransmitter Receptor Influence on BehaviorMemory and Neural Mechanisms

Reward behaviour is regulated by the strength of hippocampus–nucleus accumbens synapses

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LeGates, Tara A., Kvarta, Mark D., Tooley, Jessica R., Francis, T. Chase, Lobo, Mary Kay, Creed, Meaghan C., Thompson, Scott M.·2018·Nature

DOI 10.1038/s41586-018-0740-8PMC PMC6292781

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Abstract

Reward drives motivated behaviours and is essential for survival, and therefore there is strong evolutionary pressure to retain contextual information about rewarding stimuli. This drive may be abnormally strong, such as in addiction, or weak, such as in depression, in which anhedonia (loss of pleasure in response to rewarding stimuli) is a prominent symptom. Hippocampal input to the shell of the nucleus accumbens (NAc) is important for driving NAc activity 1,2 and activity-dependent modulation of the strength of this input may contribute to the proper regulation of goal-directed behaviours. However, there have been few robust descriptions of the mechanisms that underlie the induction or expression of long-term potentiation (LTP) at these synapses, and there is, to our knowledge, no evidence about whether such plasticity contributes to reward-related behaviour. Here we show that high-frequency activity induces LTP at hippocampus-NAc synapses in mice via canonical, but dopamine-independent, mechanisms. The induction of LTP at this synapse in vivo drives conditioned place preference, and activity at this synapse is required for conditioned place preference in response to a natural reward. Conversely, chronic stress, which induces anhedonia, decreases the strength of this synapse and impairs LTP, whereas antidepressant treatment is accompanied by a reversal of these stress-induced changes. We conclude that hippocampus-NAc synapses show activity-dependent plasticity and suggest that their strength may be critical for contextual reward behaviour.

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In the prefrontal cortex, chronic stress affects AMPAR and NMDAR components of EPSPs equally, unlike in the nucleus accumbens and hippocampus.
“Both AMPAR-and NMDAR-components of the EPSP were equally affected, unlike in the NAc [192,193] and hippocampus [110].”
From Plasticity of synapses and reward circuit function in the genesis and treatment of depression (2023) · cites this paper as [193]
Activity-dependent LTP in vivo was necessary and sufficient to induce a conditioned place preference lasting at least 24 hours.
“Activity-dependent LTP in vivo was both necessary and sufficient to induce a conditioned place preference lasting for at least 24hrs [193].”
From Plasticity of synapses and reward circuit function in the genesis and treatment of depression (2023) · cites this paper as [193]
High-frequency stimulation of hippocampal afferents to the nucleus accumbens produces a rapid and persistent NMDAR-triggered, Ca2+- and CaMK-dependent increase in postsynaptic AMPAR responses in D1 and D2 medium spiny neurons.
“Much like canonical hippocampal LTP, high frequency stimulation of hippocampal afferents to the NAc elicits a rapid and persistent NMDAR-triggered, Ca 2+ -and CaMKdependent increase in postsynaptic AMPAR responses in D1 and D2 MSNs [193].”
From Plasticity of synapses and reward circuit function in the genesis and treatment of depression (2023) · cites this paper as [193]
Chronic stress reduces evoked AMPA receptor-mediated excitatory synaptic currents in D1, but not D2, medium spiny neurons, including responses to hippocampal afferents.
“Similarly, evoked AMPA receptor-mediated excitatory synaptic currents are reduced by chronic stress in D1, but not D2, MSNs [236], including in response to afferents from the hippocampus [193].”
From Plasticity of synapses and reward circuit function in the genesis and treatment of depression (2023) · cites this paper as [193]
Chronic, but not acute, fluoxetine in stressed mice restores hippocampal excitatory synapse strength in D1 medium spiny neurons and their ability to undergo LTP, alongside restored sucrose preference.
“Chronic, but not acute, administration of fluoxetine to stressed mice restores the strength of hippocampal excitatory synapses in D1 MSNs and their ability to undergo LTP, concomitant with restoration of sucrose preference [193].”
From Plasticity of synapses and reward circuit function in the genesis and treatment of depression (2023) · cites this paper as [193]

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Dorsal Hippocampus To Nucleus Accumbens Projections Drive Reinforcement Via Activation of Accumbal Dynorphin NeuronsPreprint
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Sex-specific mechanisms underlie long-term potentiation at hippocampus-nucleus accumbens synapsesPreprint
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EXCITATORY AND INHIBITORY INPUTS CONTRIBUTE TO LONG-LASTING PLASTICITY IN A REWARD LEARNING CIRCUIT.
Copenhaver, A. E. (2025) · Maryland Shared Open Access Repository (USMAI Consortium) · doi:10.13016/m2hrgz-aldb

Authors: LeGates, T. A., Kvarta, M. D., Tooley, J. R., Francis, T. C., Lobo, M. K., Creed, M. C., & Thompson, S. M.
Affiliations: University of Maryland, Baltimore (US)
Corresponding author: Thompson, Scott M.
ORCID: LeGates, Tara A.
Kvarta, Mark D.
Tooley, Jessica R.
Francis, T. Chase
Lobo, Mary Kay
Creed, Meaghan C.
Thompson, Scott M.
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2018-11-26
Volume: 564
Issue: 7735
Pages: 258-262
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/s41586-018-0740-8
PMC: PMC6292781
OpenAlex: W2900803145
Cited by: 290
References: 23
Citations by year: 2026: 36 · 2025: 33 · 2024: 41 · 2023: 36 · 2022: 41 · 2021: 45 · 2020: 25 · 2019: 30 · 2018: 1 · 2017: 1
FWCI: 11.49
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
RePEc: Research Papers in Economics (submittedVersion)
Funders: National Institute of Mental Health (R01MH106500, R01MH086828)
National Institute on Drug Abuse (R01DA038613)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Keywords: hippocampus, nucleus accumbens, long-term potentiation, synaptic plasticity, conditioned place preference, anhedonia, chronic stress, antidepressant treatment, goal-directed behavior
MeSH terms: Animals, Chronic Disease, Conditioning, Psychological, Dopamine, Female, Goals, Hippocampus, Male, Neuronal Plasticity, Nucleus Accumbens, Reward, Stress, Psychological, Synapses, Long-Term Potentiation, Mice, Anhedonia

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Reward behaviour is regulated by the strength of hippocampus–nucleus accumbens synapses

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