Neurotransmitter roles in synaptic modulation, plasticity and learning in the dorsal striatum

Lovinger, David M.

doi:10.1016/j.neuropharm.2010.01.008

Cited by 489Neuroscience and Neuropharmacology ResearchNeurotransmitter Receptor Influence on BehaviorMemory and Neural Mechanisms

Neurotransmitter roles in synaptic modulation, plasticity and learning in the dorsal striatum

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Lovinger, David M.·2010·Neuropharmacology

DOI 10.1016/j.neuropharm.2010.01.008PMC PMC2849868

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Abstract

The dorsal striatum is a large forebrain region involved in action initiation, timing, control, learning and memory. Learning and remembering skilled movement sequences requires the dorsal striatum, and striatal subregions participate in both goal-directed (action-outcome) and habitual (stimulus-response) learning. Modulation of synaptic transmission plays a large part in controlling input to as well as the output from striatal medium spiny projection neurons (MSNs). Synapses in this brain region are subject to short-term modulation, including allosteric alterations in ion channel function and prominent presynaptic inhibition. Two forms of long-term synaptic plasticity have also been observed in striatum, long-term potentiation (LTP) and long-term depression (LTD). LTP at glutamatergic synapses onto MSNs involves activation of NMDA-type glutamate receptors and D1 dopamine or A2A adenosine receptors. Expression of LTP appears to involve postsynaptic mechanisms. LTD at glutamatergic synapses involves retrograde endocannabinoid signaling stimulated by activation of metabotropic glutamate receptors (mGluRs) and D2 dopamine receptors. While postsynaptic mechanisms participate in LTD induction, maintained expression involves presynaptic mechanisms. A similar form of LTD has also been observed at GABAergic synapses onto MSNs. Studies have just begun to examine the roles of synaptic plasticity in striatal-based learning. Findings to date indicate that molecules implicated in induction of plasticity participate in these forms of learning. Neurotransmitter receptors involved in LTP induction are necessary for proper skill and goal-directed instrumental learning. Interestingly, receptors involved in LTP and LTD at glutamatergic synapses onto MSNs of the "indirect pathway" appear to have important roles in habit learning. More work is needed to reveal if and when synaptic plasticity occurs during learning and if so what molecules and cellular processes, both short- and long-term, contribute to this plasticity.

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The interaction between glutamate and striatal activity serves as an important modulator of synaptic plasticity and neural excitability.
“It is believed that the interaction between glutamate and striatal activity serves as an important modulator of synaptic plasticity and neural excitability (Surmeier et al., 2007; Kreitzer et al., 2009; Lovinger et al., 2010; Gleich et al., 2015).”
From Circuit Mechanisms of Reward, Anhedonia, and Depression (2019) · cites this paper as Lovinger et al., 2010

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Dopamine Prediction Errors in Reward Learning and Addiction: From Theory to Neural Circuitry
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Circuit Mechanisms of Reward, Anhedonia, and Depression
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M4 Muscarinic Receptor Signaling Ameliorates Striatal Plasticity Deficits in Models of L-DOPA-Induced Dyskinesia
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The Challenges and Promise of Neuroimaging in Psychiatry
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Parallel, but Dissociable, Processing in Discrete Corticostriatal Inputs Encodes Skill Learning
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Adenosine hypothesis of schizophrenia – Opportunities for pharmacotherapy
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Striatopallidal dysfunction underlies repetitive behavior in Shank3-deficient model of autism
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Rapid Target-Specific Remodeling of Fast-Spiking Inhibitory Circuits after Loss of Dopamine
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Acute and chronic effects of ethanol on learning-related synaptic plasticity
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A trans-diagnostic perspective on obsessive-compulsive disorder
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Authors: Lovinger, D. M.
Affiliations: National Institutes of Health (US)
Corresponding author: Lovinger, David M.
ORCID: Lovinger, David M.
Venue: Neuropharmacology
Publisher: Elsevier BV
Published: 2010-06
Volume: 58
Issue: 7
Pages: 951-961
ISSN: 0028-3908 (ISSN-L)
DOI: 10.1016/j.neuropharm.2010.01.008
PMC: PMC2849868
OpenAlex: W2086614467
Cited by: 488
References: 150
Citations by year: 2026: 10 · 2025: 19 · 2024: 28 · 2023: 21 · 2022: 37 · 2021: 32 · 2020: 27 · 2019: 32 · 2018: 30 · 2017: 39 · 2016: 25 · 2015: 38 · 2014: 30 · 2013: 39 · 2012: 29
FWCI: 3.43
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Neuropharmacology (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health
National Institute on Alcohol Abuse and Alcoholism (Z01AA000407)
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: dorsal striatum, synaptic plasticity, long-term potentiation, long-term depression, medium spiny neurons, glutamatergic synapses, GABAergic synapses, NMDA receptor, dopamine D1 receptor, adenosine A2A receptor, dopamine D2 receptor, metabotropic glutamate receptors, retrograde endocannabinoid signaling, presynaptic inhibition, allosteric modulation, operant conditioning, habit learning, goal-directed learning, indirect pathway, neurotransmitter receptors
MeSH terms: Animals, Corpus Striatum, Learning, Neuronal Plasticity, Synapses, Neurotransmitter Agents

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Neurotransmitter roles in synaptic modulation, plasticity and learning in the dorsal striatum

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