AMPARs and Synaptic Plasticity: The Last 25 Years
Open accessAbstract
The study of synaptic plasticity and specifically LTP and LTD is one of the most active areas of research in neuroscience. In the last 25 years we have come a long way in our understanding of the mechanisms underlying synaptic plasticity. In 1988, AMPA and NMDA receptors were not even molecularly identified and we only had a simple model of the minimal requirements for the induction of plasticity. It is now clear that the modulation of the AMPA receptor function and membrane trafficking is critical for many forms of synaptic plasticity and a large number of proteins have been identified that regulate this complex process. Here we review the progress over the last two and a half decades and discuss the future challenges in the field.
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The prevailing model posits that LTP-mediated covalent modification of the intracellular CTD of GluA1 results in capture of modified GluA1-containing receptors by preexisting slots in the PSD.
“The prevailing model posits that LTP-mediated covalent modification of the intracellular CTD of GluA1 results in the capture of these modified GluA1-containing receptors by preexisting “slots” in the postsynaptic density (PSD) (17, 18, 212).”
From Synaptic memory and CaMKII (2023) · cites this paper as [17]
In “Proposed Working Models for LTP” (page unavailable), the paper describes capture by preexisting PSD slots as one of three possible models, not the prevailing model. It explicitly says that C-terminal domains would be modulatory but not essential to that capture; modification of other receptor domains or auxiliary subunits would play the essential role. (LLM, conf=0.85)
Checked by a reasoning model — may be wrong.
Experimental — accuracy not yet measuredLTP requires an enhancement of synaptic AMPARs.
“To summarize, LTP requires an enhancement of synaptic AMPARs (Huganir and Nicoll, 2013).”
From The AMPA Receptor Code of Synaptic Plasticity (2018) · cites this paper as Huganir and Nicoll, 2013
The Long-Term Potentiation section describes LTP-associated increases in AMPAR responses, supporting AMPAR enhancement as a common expression mechanism. But the Subunit Dependence section says LTP can be expressed with exogenously supplied kainate receptors, and the Conclusions say LTP mechanisms can act on either receptor type. Thus, the source does not support an absolute requirement for enhanced synaptic AMPARs. Page numbers were not provided in our copy. (LLM, conf=0.87)
Experimental — accuracy not yet measuredCerebellar LTD, NMDAR-dependent LTD, and mGluR-dependent LTD are expressed by a decrease in synaptic AMPAR content.
“Several major forms of LTD described in the brain including, cerebellar LTD and NMDAR-dependent and mGluR-dependent LTD, are expressed by a decrease in synaptic AMPAR content (Huganir and Nicoll, 2013).”
From The AMPA Receptor Code of Synaptic Plasticity (2018) · cites this paper as Huganir and Nicoll, 2013
The NMDAR-Dependent LTD section says there is general consensus that LTD-related depression reflects a loss of synaptic AMPARs. The Cerebellar LTD section describes AMPAR endocytosis and retention of GluA2 inside the cell. Although it says mGluR1 activation induces cerebellar LTD, the passages do not establish the claim for mGluR-dependent LTD as a separately named form. (LLM, conf=0.83)
Experimental — accuracy not yet measuredThe induction of LTD requires PKA phosphorylation of GluA1 even though receptors are eventually dephosphorylated.
“indicating that the induction of LTD requires PKA phosphorylation of GluA1 even though receptors are eventually dephosphorylated (Huganir and Nicoll, 2013).”
From The AMPA Receptor Code of Synaptic Plasticity (2018) · cites this paper as Huganir and Nicoll, 2013
The “AMPAR Phosphorylation and LTP” section reports significant deficits in LTD induction when GluA1 CaMKII and PKA phosphorylation sites cannot be phosphorylated, and reports that LTD decreases phosphorylation. But it does not establish that PKA phosphorylation of GluA1 is strictly required: the “NMDAR-Dependent LTD” section also notes normal LTD in mice lacking GluA1. (LLM, conf=0.86)
Experimental — accuracy not yet measuredForms of LTP, LTD and homeostatic scaling have been shown to be intact in knock-out mice of different AMPAR subunits as well as in molecular replacement experiments.
“Forms of LTP, LTD and homeostatic scaling have been shown to be intact in knock-out mice of different AMPAR subunits as well as in using molecular replacement experiments (Huganir and Nicoll, 2013, Granger et al., 2013, Ancona Esselmann et al., 2017).”
From The AMPA Receptor Code of Synaptic Plasticity (2018) · cites this paper as Huganir and Nicoll, 2013
In “Subunit Dependence of AMPAR Trafficking and LTP and LTD” (page unavailable), the review reports that molecular replacement found no specific AMPAR-subunit requirement for LTP. “NMDAR-Dependent LTD” reports normal LTD in mice lacking GluA2/GluA3 or GluA1. The review describes homeostatic synaptic scaling in “Dynamic Regulation of AMPAR Membrane Trafficking,” but does not say it remains intact in AMPAR-subunit knockout mice or molecular replacement experiments. (LLM, conf=0.88)
Experimental — accuracy not yet measured
The 'slot hypothesis' offers some explanation for the prominent role of GluA1 in LTP and of GluA2 in LTD, via the rapid activity-dependent mobilization of GluA1-containing receptors onto the cell surface during LTP, and the removal of GluA2 containing receptors from the cell-surface during LTD through interactions with AP2 and/or through interactions involving the GluA2 Y-rich motif.
“Thus the “slot hypothesis” offers some explanation for the prominent role of GluA1 in LTP and of GluA2 in LTD, via the rapid activity-dependent mobilization of GluA1-containing receptors onto the cell surface during LTP, and the removal of GluA2 containing receptors from the cell-surface during LTD through interactions with AP2 and/or through interactions involving the GluA2 Y-rich motif (Ahmadian”
From The AMPA Receptor Code of Synaptic Plasticity (2018) · cites this paper as Huganir and Nicoll, 2013
Split into 2 atoms — 0 confirmed, 2 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.
Experimental — accuracy not yet measuredAMPARs play an essential role in the functioning of the brain, and changes in the abundance of post-synaptic AMPARs are a fundamental mechanism for most forms of synaptic plasticity.
“AMPARs play an essential role in the functioning of the brain, and changes in the abundance of post-synaptic AMPARs are a fundamental mechanism for most forms of synaptic plasticity (Huganir and Nicoll, 2013).”
From The AMPA Receptor Code of Synaptic Plasticity (2018) · cites this paper as Huganir and Nicoll, 2013
The Conclusions and Future Directions section says changes in AMPAR number at synaptic spines mediate changes in strength during LTP and LTD. The Proposed Working Models for LTP section calls AMPAR regulation key to many forms of synaptic plasticity and important for learning and memory, but it does not establish the claim’s stronger scope of “most forms.” Page numbers are unavailable in our copy. (LLM, conf=0.84)
Experimental — accuracy not yet measuredThe expression of NMDAR-dependent LTP is primarily postsynaptic, although a minor presynaptic component is difficult to entirely exclude.
“Although it is difficult to entirely exclude the possibility of a minor presynaptic component of NMDAR-dependent LTP, the evidence is overwhelming that its expression is primarily postsynaptic.”
From Synaptic memory and CaMKII (2023) · cites this paper as [17]
Long-term potentiation (LTP) is brief repetitive synaptic stimulation that results in long-lasting increases in synaptic strength.
“long-term potentiation (LTP), in which brief repetitive synaptic stimulation results in long-lasting increases in synaptic strength, was gaining popularity as a cellular model for learning and memory (16–22).”
From Synaptic memory and CaMKII (2023) · cites this paper as [17]
LTP expression is due to rapid postsynaptic accumulation of AMPARs.
“Thus, it is now generally accepted that LTP expression is due to the rapid postsynaptic accumulation of AMPARs.”
From Synaptic memory and CaMKII (2023) · cites this paper as [17]
Alteration in the number, composition and biophysical properties of AMPARs in the post-synaptic membrane is a primary mechanism in the control of synaptic strength during plasticity.
“A primary mechanism in the control of synaptic strength during plasticity is an alteration in the number, composition and biophysical properties of AMPA-type glutamate receptors (AMPARs) in the post-synaptic membrane (Huganir and Nicoll, 2013, Malinow and Malenka, 2002).”
From The AMPA Receptor Code of Synaptic Plasticity (2018) · cites this paper as Huganir and Nicoll, 2013
AMPARs are highly dynamic, undergoing continuous endocytosis, exocytosis, lateral diffusion, reversible trapping at PSD, and modifications in channel properties.
“AMPARs are highly dynamic, undergoing continuous endocytosis, exocytosis, lateral diffusion in the plane of the membrane, reversible trapping at synapses at the post-synaptic density (PSD), and modifications in channel properties (Opazo et al., 2012, Huganir and Nicoll, 2013, Malinow and Malenka, 2002).”
From The AMPA Receptor Code of Synaptic Plasticity (2018) · cites this paper as Huganir and Nicoll, 2013
NMDAR-dependent LTP is the result of increased AMPAR density in the post-synaptic membrane and/or single channel conductance of the AMPAR.
“The major form of LTP identified in the brain, NMDAR-dependent LTP, is the result of increased AMPAR density in the post-synaptic membrane and/or single channel conductance of the AMPAR (Huganir and Nicoll, 2013, Herring and Nicoll, 2016, Poncer et al., 2002, Benke et al., 1998).”
From The AMPA Receptor Code of Synaptic Plasticity (2018) · cites this paper as Huganir and Nicoll, 2013
LTD requires a net removal of AMPARs from the post synaptic membrane.
“To summarize, LTD requires a net removal of AMPARs from the post synaptic membrane.”
From The AMPA Receptor Code of Synaptic Plasticity (2018) · cites this paper as Huganir and Nicoll, 2013
The post-synaptic density contains 'slots' that might be occupied by AMPARs supplied by lateral diffusion from the peri-synaptic region.
“A prominent model of synaptic strength posits that the post-synaptic density (PSD), a dense network of synaptic scaffolding, adhesion and cytoskeletal proteins, contains ‘slots’ that might be occupied by AMPARs supplied by lateral diffusion from the peri-synaptic region (Opazo et al., 2012, Huganir and Nicoll, 2013, Kessels and Malinow, 2009).”
From The AMPA Receptor Code of Synaptic Plasticity (2018) · cites this paper as Huganir and Nicoll, 2013
Long-term potentiation and long-term depression are two mechanisms that impact cognitive and affective functions impaired in major depressive disorder.
“Long-term potentiation (LTP) and long-term depression (LTD) are two mechanisms that impact cognitive and affective functions impaired in MDD133-135.”
From Dysregulation of adult hippocampal neuroplasticity in major depression: Pathogenesis and therapeutic implications (2022) · cites this paper as [135]
NMDAR-dependent mechanisms could work through αCaMKII accumulation to drive AMPAR incorporation and LTP.
“Furthermore, NMDAR-dependent mechanisms could work through αCaMKII accumulation to drive AMPAR incorporation and LTP (Huganir and Nicoll, 2013; Lisman et al., 1997).”
From Unifying Views of Autism Spectrum Disorders: A Consideration of Autoregulatory Feedback Loops (2016) · cites this paper as Huganir and Nicoll, 2013
The vast majority of plastic changes at synapses onto principal cells rely on activation of the NMDAR, which acts as a coincidence detector, and the primary route of Ca2+ entry that triggers downstream second messenger cascades to ultimately influence AMPAR trafficking.
“Although a number of potentially distinct, but overlapping mechanisms have been identified at synapses onto principal cells, the vast majority of these plastic changes rely on activation of the NMDAR, which acts as a coincidence detector, and the primary route of Ca2+ entry that triggers downstream second messenger cascades to ultimately influence AMPAR trafficking (509).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [509]
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“LTD, on the other hand, is an activity-dependent reduction in the efficacy and connection of neuronal synapses [135].”
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- Authors
- Huganir, R. L., & Nicoll, R. A.
- Affiliations
- Johns Hopkins University (US)
- University of California, San Francisco (US)
- Corresponding author
- Huganir, Richard L.
- Nicoll, Roger A.
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2013-10
- Volume
- 80
- Issue
- 3
- Pages
- 704-717
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC4195488
- OpenAlex
- W2080640632
- Cited by
- 968
- References
- 182
- Citations by year
- 2026: 54 · 2025: 62 · 2024: 75 · 2023: 58 · 2022: 65 · 2021: 94 · 2020: 87 · 2019: 72 · 2018: 99 · 2017: 89 · 2016: 79 · 2015: 73 · 2014: 58 · 2013: 2
- FWCI
- 34.68
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- National Institute of Mental Health (R01MH070957)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Health Sciences › Medicine › Pharmacology › Treatment of Major Depression
- Keywords
- AMPA receptors, NMDA receptor, synaptic plasticity, long-term potentiation, long-term depression, receptor trafficking, receptor modulation
- MeSH terms
- Animals, Neuronal Plasticity, Neurosciences, Synapses, Receptors, AMPA, History, 20th Century, History, 21st Century
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