Synaptic and Behavioral Profile of Multiple Glutamatergic Inputs to the Nucleus Accumbens

Britt, Jonathan P.; Benaliouad, Faiza; McDevitt, Ross A.; Stuber, Garret D.; Wise, Roy A.; Bonci, Antonello

doi:10.1016/j.neuron.2012.09.040

Cited by 716Neurotransmitter Receptor Influence on BehaviorNeuroscience and Neuropharmacology ResearchNeural and Behavioral Psychology Studies

Synaptic and Behavioral Profile of Multiple Glutamatergic Inputs to the Nucleus Accumbens

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Britt, Jonathan P., Benaliouad, Faiza, McDevitt, Ross A., Stuber, Garret D., Wise, Roy A., Bonci, Antonello·2012·Neuron

DOI 10.1016/j.neuron.2012.09.040PMC PMC3607383

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Abstract

Excitatory afferents to the nucleus accumbens (NAc) are thought to facilitate reward seeking by encoding reward-associated cues. Selective activation of different glutamatergic inputs to the NAc can produce divergent physiological and behavioral responses, but mechanistic explanations for these pathway-specific effects are lacking. Here, we compared the innervation patterns and synaptic properties of ventral hippocampus, basolateral amygdala, and prefrontal cortex input to the NAc. Ventral hippocampal input was found to be uniquely localized to the medial NAc shell, where it was predominant and selectively potentiated after cocaine exposure. In vivo, bidirectional optogenetic manipulations of this pathway attenuated and enhanced cocaine-induced locomotion. Challenging the idea that any of these inputs encode motivationally neutral information, activation of each discrete pathway reinforced instrumental behaviors. Finally, direct optical activation of medium spiny neurons proved to be capable of supporting self-stimulation, demonstrating that behavioral reinforcement is an explicit consequence of strong excitatory drive to the NAc.

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Activation of hippocampal and prefrontal inputs to the nucleus accumbens is rewarding and reinforces rewarding stimuli.
“Activation of inputs to the NAc from the hippocampus and PFC is rewarding and reinforcing of rewarding stimuli [227,228].”
From Plasticity of synapses and reward circuit function in the genesis and treatment of depression (2023) · cites this paper as [227]
Ventral hippocampal to nucleus accumbens projections are weighted differently by subregion, with larger ventral hippocampal excitatory currents in the nucleus accumbens shell.
“Interestingly, vHipp-NAc projections are weighted differently in a sub-region specific manner, where larger vHipp excitatory currents in the NAc shell are observed (49).”
From Emerging Role for Nucleus Accumbens Medium Spiny Neuron Subtypes in Depression (2017) · cites this paper as [49]
Stimulation of the mPFC-to-nucleus accumbens pathway is reinforcing.
“stimulation of this pathway is reinforcing120.”
From Resolving the neural circuits of anxiety (2015) · cites this paper as [120]

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Authors: Britt, J. P., Benaliouad, F., McDevitt, R. A., Stuber, G. D., Wise, R. A., & Bonci, A.
Affiliations: National Institutes of Health (US)
University of North Carolina at Chapel Hill (US)
Corresponding author: Bonci, Antonello
ORCID: Britt, Jonathan P.
McDevitt, Ross A.
Stuber, Garret D.
Wise, Roy A.
Bonci, Antonello
Venue: Neuron
Publisher: Elsevier BV
Published: 2012-11
Volume: 76
Issue: 4
Pages: 790-803
ISSN: 0896-6273 (ISSN-L)
DOI: 10.1016/j.neuron.2012.09.040
PMC: PMC3607383
OpenAlex: W2127114472
Cited by: 716
References: 70
Citations by year: 2026: 25 · 2025: 38 · 2024: 54 · 2023: 49 · 2022: 63 · 2021: 66 · 2020: 49 · 2019: 66 · 2018: 67 · 2017: 65 · 2016: 56 · 2015: 48 · 2014: 40 · 2013: 28 · 2012: 2
FWCI: 15.55
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 385 d)
Locations: Neuron (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Carolina Digital Repository (University of North Carolina at Chapel Hill) (submittedVersion)
UNC Libraries
Funders: National Institutes of Health
National Institute on Drug Abuse (DA029325, DA032750)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
Keywords: nucleus accumbens, glutamatergic afferents, ventral hippocampus, basolateral amygdala, prefrontal cortex, cocaine, synaptic potentiation, optogenetics, cocaine-induced locomotion, instrumental behavior, self-stimulation, medium spiny neurons, reward encoding
MeSH terms: Channelrhodopsins, Analysis of Variance, Animals, Bacterial Proteins, Biophysics, Cerebral Cortex, Cocaine, Electric Stimulation, Hippocampus, Light, Locomotion, Luminescent Proteins, Male, Membrane Potentials, Mice, Inbred C57BL, Microinjections, Neural Pathways, Neurons, Nucleus Accumbens, Stilbamidines, Synapses, Transduction, Genetic, Patch-Clamp Techniques, Glutamic Acid, Dopamine Uptake Inhibitors, Mice, Optogenetics

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Synaptic and Behavioral Profile of Multiple Glutamatergic Inputs to the Nucleus Accumbens

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