NMDA receptors in axons: there's no coincidence.
NMDA receptor
axon
long-term plasticity
metabotropic signalling
neuropathic pain
neurotransmitter release
presynaptic terminal
short-term plasticity
Journal
The Journal of physiology
ISSN: 1469-7793
Titre abrégé: J Physiol
Pays: England
ID NLM: 0266262
Informations de publication
Date de publication:
01 2021
01 2021
Historique:
received:
30
08
2020
accepted:
27
10
2020
pubmed:
4
11
2020
medline:
13
4
2021
entrez:
3
11
2020
Statut:
ppublish
Résumé
In the textbook view, N-methyl-d-aspartate (NMDA) receptors are postsynaptically located detectors of coincident activity in Hebbian learning. However, controversial presynaptically located NMDA receptors (preNMDARs) have for decades been repeatedly reported in the literature. These preNMDARs have typically been implicated in the regulation of short-term and long-term plasticity, but precisely how they signal and what their functional roles are have been poorly understood. The functional roles of preNMDARs across several brain regions and different forms of plasticity can differ vastly, with recent discoveries showing key involvement of unusual subunit composition. Increasing evidence shows preNMDAR can signal through both ionotropic action by fluxing calcium and in metabotropic mode even in the presence of magnesium blockade. We argue that these unusual properties may explain why controversy has surrounded this receptor type. In addition, the expression of preNMDARs at some synapse types but not others can underlie synapse-type-specific plasticity. Last but not least, preNMDARs are emerging therapeutic targets in disease states such as neuropathic pain. We conclude that axonally located preNMDARs are required for specific purposes and do not end up there by accident.
Substances chimiques
Receptors, N-Methyl-D-Aspartate
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
367-387Subventions
Organisme : CFI LOF
ID : 28331
Organisme : CIHR OG
ID : 126137
Organisme : CIHR NIA
ID : 288936
Informations de copyright
© 2020 The Authors. The Journal of Physiology © 2020 The Physiological Society.
Références
Abbott LF & Nelson SB (2000). Synaptic plasticity: taming the beast. Nat Neurosci 3, 1178-1183.
Abrahamsson T, Chou CYC, Li SY, Mancino A, Costa RP, Brock JA, Nuro E, Buchanan KA, Elgar D, Blackman AV, Tudor-Jones A, Oyrer J, Farmer WT, Murai KK & Sjöström PJ (2017). Differential regulation of evoked and spontaneous release by presynaptic NMDA receptors. Neuron 96, 839-855.e5.
Akazawa C, Shigemoto R, Bessho Y, Nakanishi S & Mizuno N (1994). Differential expression of five N-methyl-D-aspartate receptor subunit mRNAs in the cerebellum of developing and adult rats. J Comp Neurol 347, 150-160.
Alkondon M, Costa AC, Radhakrishnan V, Aronstam RS & Albuquerque EX (1990). Selective blockade of NMDA-activated channel currents may be implicated in learning deficits caused by lead. FEBS Lett 261, 124-130.
Allen Developing Mouse Brain Atlas (2008). http://developingmouse.brain-map.org/
Andrade-Talavera Y, Duque-Feria P, Paulsen O & Rodríguez-Moreno A (2016). Presynaptic spike timing-dependent long-term depression in the mouse hippocampus. Cereb Cortex 26, 3637-3654.
Angulo MC, Kozlov AS, Charpak S & Audinat E (2004). Glutamate released from glial cells synchronizes neuronal activity in the hippocampus. J Neurosci 24, 6920-6927.
Aoki C, Venkatesan C, Go CG, Mong JA & Dawson TM (1994). Cellular and subcellular localization of NMDA-R1 subunit immunoreactivity in the visual cortex of adult and neonatal rats. J Neurosci 14, 5202-5222.
Aow J, Dore K & Malinow R (2015). Conformational signaling required for synaptic plasticity by the NMDA receptor complex. Proc Natl Acad Sci U S A 112, 14711-14716.
Astorga G, Li D, Therreau L, Kassa M, Marty A & Llano I (2017). Concerted interneuron activity in the cerebellar molecular layer during rhythmic oromotor behaviors. J Neurosci 37, 11455-11468.
Atasoy D, Ertunc M, Moulder KL, Blackwell J, Chung C, Su J & Kavalali ET (2008). Spontaneous and evoked glutamate release activates two populations of NMDA receptors with limited overlap. J Neurosci 28, 10151-10166.
Banerjee A, González-Rueda A, Sampaio-Baptista C, Paulsen O & Rodríguez-Moreno A (2014). Distinct mechanisms of spike timing-dependent LTD at vertical and horizontal inputs onto L2/3 pyramidal neurons in mouse barrel cortex. Physiol Rep 2, e00271.
Banerjee A, Larsen RS, Philpot BD & Paulsen O (2016). Roles of presynaptic NMDA receptors in neurotransmission and plasticity. Trends Neurosci 39, 26-39.
Banerjee A, Meredith RM, Rodríguez-Moreno A, Mierau SB, Auberson YP & Paulsen O (2009). Double dissociation of spike timing-dependent potentiation and depression by subunit-preferring NMDA receptor antagonists in mouse barrel cortex. Cereb Cortex 19, 2959-2969.
Bender VA, Bender KJ, Brasier DJ & Feldman DE (2006). Two coincidence detectors for spike timing-dependent plasticity in somatosensory cortex. J Neurosci 26, 4166-4177.
Berretta N & Jones RS (1996). Tonic facilitation of glutamate release by presynaptic N-methyl-D-aspartate autoreceptors in the entorhinal cortex. Neuroscience 75, 339-344.
Bi GQ & Poo MM (1998). Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type. J Neurosci 18, 10464-10472.
Bidoret C, Ayon A, Barbour B & Casado M (2009). Presynaptic NR2A-containing NMDA receptors implement a high-pass filter synaptic plasticity rule. Proc Natl Acad Sci U S A 106, 14126-14131.
Bidoret C, Bouvier G, Ayon A, Szapiro G & Casado M (2015). Properties and molecular identity of NMDA receptors at synaptic and non-synaptic inputs in cerebellar molecular layer interneurons. Front Synaptic Neurosci 7, 1.
Blackman AV, Abrahamsson T, Costa RP, Lalanne T & Sjöström PJ (2013). Target-cell-specific short-term plasticity in local circuits. Front Synaptic Neurosci 5, 11.
Blatt GJ, Fitzgerald CM, Guptill JT, Booker AB, Kemper TL & Bauman ML (2001). Density and distribution of hippocampal neurotransmitter receptors in autism: an autoradiographic study. J Autism Dev Disord 31, 537-543.
Bouvier G, Higgins D, Spolidoro M, Carrel D, Mathieu B, Léna C, Dieudonné S, Barbour B, Brunel N & Casado M (2016). Burst-dependent bidirectional plasticity in the cerebellum is driven by presynaptic NMDA receptors. Cell Rep 15, 104-116.
Bouvier G, Larsen RS, Rodríguez-Moreno A, Paulsen O & Sjöström PJ (2018). Towards resolving the presynaptic NMDA receptor debate. Curr Opin Neurobiol 51, 1-7.
Brasier DJ & Feldman DE (2008). Synapse-specific expression of functional presynaptic NMDA receptors in rat somatosensory cortex. J Neurosci 28, 2199-2211.
Brock JA, Thomazeau A, Watanabe A, Li SSY & Sjöström PJ (2020). A practical guide to using CV analysis for determining the locus of synaptic plasticity. Front Synaptic Neurosci 12, 11.
Brown AM, Arancillo M, Lin T, Catt DR, Zhou J, Lackey EP, Stay TL, Zuo Z, White JJ & Sillitoe RV (2019). Molecular layer interneurons shape the spike activity of cerebellar Purkinje cells. Sci Rep 9, 1742.
Buchanan KA, Blackman AV, Moreau AW, Elgar D, Costa RP, Lalanne T, Tudor Jones AA, Oyrer J & Sjöström PJ (2012). Target-specific expression of presynaptic NMDA receptors in neocortical microcircuits. Neuron 75, 451-466.
Buchanan KA & Sjöström PJ (2009). A piece of the neocortical puzzle: the pyramid-Martinotti cell reciprocating principle. J Physiol 587, 5301-5302.
Carter BC & Jahr CE (2016). Postsynaptic, not presynaptic NMDA receptors are required for spike-timing-dependent LTD induction. Nat Neurosci 19, 1218-1224.
Casado M, Dieudonné S & Ascher P (2000). Presynaptic N-methyl-D-aspartate receptors at the parallel fiber-Purkinje cell synapse. Proc Natl Acad Sci U S A 97, 11593-11597.
Casado M, Isope P & Ascher P (2002). Involvement of presynaptic N-methyl-D-aspartate receptors in cerebellar long-term depression. Neuron 33, 123-130.
Castillo MA, Ghose S, Tamminga CA & Ulery-Reynolds PG (2010). Deficits in syntaxin 1 phosphorylation in schizophrenia prefrontal cortex. Biol Psychiatry 67, 208-216.
Chanaday NL & Kavalali ET (2018). Presynaptic origins of distinct modes of neurotransmitter release. Curr Opin Neurobiol 51, 119-126.
Chatterton JE, Awobuluyi M, Premkumar LS, Takahashi H, Talantova M, Shin Y, Cui J, Tu S, Sevarino KA, Nakanishi N, Tong G, Lipton SA & Zhang D (2002). Excitatory glycine receptors containing the NR3 family of NMDA receptor subunits. Nature 415, 793-798.
Chen Y, Chen SR, Chen H, Zhang J & Pan HL (2019). Increased α2δ-1-NMDA receptor coupling potentiates glutamatergic input to spinal dorsal horn neurons in chemotherapy-induced neuropathic pain. J Neurochem 148, 252-274.
Chez MG, Burton Q, Dowling T, Chang M, Khanna P & Kramer C (2007). Memantine as adjunctive therapy in children diagnosed with autistic spectrum disorders: an observation of initial clinical response and maintenance tolerability. J Child Neurol 22, 574-579.
Choi YB & Lipton SA (1999). Identification and mechanism of action of two histidine residues underlying high-affinity Zn2+ inhibition of the NMDA receptor. Neuron 23, 171-180.
Chou TH, Tajima N, Romero-Hernandez A & Furukawa H (2020). Structural basis of functional transitions in mammalian NMDA receptors. Cell 182, 357-371.e13.
Christie JM & Jahr CE (2008). Dendritic NMDA receptors activate axonal calcium channels. Neuron 60, 298-307.
Christie JM & Jahr CE (2009). Selective expression of ligand-gated ion channels in L5 pyramidal cell axons. J Neurosci 29, 11441-11450.
Cohen LD, Zuchman R, Sorokina O, Müller A, Dieterich DC, Armstrong JD, Ziv T & Ziv NE (2013). Metabolic turnover of synaptic proteins: kinetics, interdependencies and implications for synaptic maintenance. PLoS One 8, e63191.
Corlew R, Brasier DJ, Feldman DE & Philpot BD (2008). Presynaptic NMDA receptors: newly appreciated roles in cortical synaptic function and plasticity. Neuroscientist 14, 609-625.
Corlew R, Wang Y, Ghermazien H, Erisir A & Philpot BD (2007). Developmental switch in the contribution of presynaptic and postsynaptic NMDA receptors to long-term depression. J Neurosci 27, 9835-9845.
Costa RP, Mizusaki BE, Sjöström PJ & van Rossum MC (2017). Functional consequences of pre- and postsynaptic expression of synaptic plasticity. Philos Trans R Soc Lond B Biol Sci 372, 20160153.
Crabtree JW, Lodge D, Bashir ZI & Isaac JT (2013). GABAA, NMDA and mGlu2 receptors tonically regulate inhibition and excitation in the thalamic reticular nucleus. Eur J Neurosci 37, 850-859.
Debanne D, Gähwiler BH & Thompson SM (1998). Long-term synaptic plasticity between pairs of individual CA3 pyramidal cells in rat hippocampal slice cultures. J Physiol 507 237-247.
DeBiasi S, Minelli A, Melone M & Conti F (1996). Presynaptic NMDA receptors in the neocortex are both auto- and heteroreceptors. Neuroreport 7, 2773-2776.
Deng M, Chen SR & Pan HL (2019). Presynaptic NMDA receptors control nociceptive transmission at the spinal cord level in neuropathic pain. Cell Mol Life Sci 76, 1889-1899.
Di Prisco S, Olivero G, Merega E, Bonfiglio T, Marchi M & Pittaluga A (2016). CXCR4 and NMDA receptors are functionally coupled in rat hippocampal noradrenergic and glutamatergic nerve endings. J Neuroimmune Pharmacol 11, 645-656.
Dore K, Aow J & Malinow R (2015). Agonist binding to the NMDA receptor drives movement of its cytoplasmic domain without ion flow. Proc Natl Acad Sci U S A 112, 14705-14710.
Dore K, Stein IS, Brock JA, Castillo PE, Zito K & Sjöström PJ (2017). Unconventional NMDA receptor signaling. J Neurosci 37, 10800-10807.
Dörrbaum AR, Kochen L, Langer JD & Schuman EM (2018). Local and global influences on protein turnover in neurons and glia. Elife 7, e34202.
Dubois CJ, Lachamp PM, Sun L, Mishina M & Liu SJ (2016). Presynaptic GluN2D receptors detect glutamate spillover and regulate cerebellar GABA release. J Neurophysiol 115, 271-285.
Duguid I & Sjöström PJ (2006). Novel presynaptic mechanisms for coincidence detection in synaptic plasticity. Curr Opin Neurobiol 16, 312-322.
Duguid IC & Smart TG (2004). Retrograde activation of presynaptic NMDA receptors enhances GABA release at cerebellar interneuron-Purkinje cell synapses. Nat Neurosci 7, 525-533.
Eadie BD, Cushman J, Kannangara TS, Fanselow MS & Christie BR (2012). NMDA receptor hypofunction in the dentate gyrus and impaired context discrimination in adult Fmr1 knockout mice. Hippocampus 22, 241-254.
Endele S, Rosenberger G, Geider K, Popp B, Tamer C, Stefanova I, Milh M, Kortüm F, Fritsch A, Pientka FK, Hellenbroich Y, Kalscheuer VM, Kohlhase J, Moog U, Rappold G, Rauch A, Ropers HH, von Spiczak S, Tönnies H, Villeneuve N, Villard L, Zabel B, Zenker M, Laube B, Reis A, Wieczorek D, Van Maldergem L & Kutsche K (2010). Mutations in GRIN2A and GRIN2B encoding regulatory subunits of NMDA receptors cause variable neurodevelopmental phenotypes. Nat Genet 42, 1021-1026.
Engelman HS & MacDermott AB (2004). Presynaptic ionotropic receptors and control of transmitter release. Nat Rev Neurosci 5, 135-145.
Etherton M, Földy C, Sharma M, Tabuchi K, Liu X, Shamloo M, Malenka RC & Südhof TC (2011). Autism-linked neuroligin-3 R451C mutation differentially alters hippocampal and cortical synaptic function. Proc Natl Acad Sci U S A 108, 13764-13769.
Fiszman ML, Barberis A, Lu C, Fu Z, Erdélyi F, Szabó G & Vicini S (2005). NMDA receptors increase the size of GABAergic terminals and enhance GABA release. J Neurosci 25, 2024-2031.
Gaffield MA & Christie JM (2017). Movement rate is encoded and influenced by widespread, coherent activity of cerebellar molecular layer interneurons. J Neurosci 37, 4751-4765.
Glitsch M & Marty A (1999). Presynaptic effects of NMDA in cerebellar Purkinje cells and interneurons. J Neurosci 19, 511-519.
Glitsch MD (2008). Calcium influx through N-methyl-D-aspartate receptors triggers GABA release at interneuron-Purkinje cell synapse in rat cerebellum. Neuroscience 151, 403-409.
González-Rueda A, Pedrosa V, Feord RC, Clopath C & Paulsen O (2018). Activity-dependent downscaling of subthreshold synaptic inputs during slow-wave-sleep-like activity in vivo. Neuron 97, 1244-1252.e5.
Hafner AS, Donlin-Asp PG, Leitch B, Herzog E & Schuman EM (2019). Local protein synthesis is a ubiquitous feature of neuronal pre- and postsynaptic compartments. Science 364, eaau3644.
Hamdan FF, Gauthier J, Araki Y, Lin DT, Yoshizawa Y, Higashi K, Park AR, Spiegelman D, Dobrzeniecka S, Piton A, Tomitori H, Daoud H, Massicotte C, Henrion E, Diallo O, Shekarabi M, Marineau C, Shevell M, Maranda B, Mitchell G, Nadeau A, D'Anjou G, Vanasse M, Srour M, Lafrenière RG, Drapeau P, Lacaille JC, Kim E, Lee JR, Igarashi K, Huganir RL, Rouleau GA & Michaud JL (2011). Excess of de novo deleterious mutations in genes associated with glutamatergic systems in nonsyndromic intellectual disability. Am J Hum Genet 88, 306-316.
Häusser M & Clark BA (1997). Tonic synaptic inhibition modulates neuronal output pattern and spatiotemporal synaptic integration. Neuron 19, 665-678.
Hebb DO (1949). The Organization of Behavior: A Neuropsychological Theory. Wiley, New York.
Humeau Y, Shaban H, Bissière S & Lüthi A (2003). Presynaptic induction of heterosynaptic associative plasticity in the mammalian brain. Nature 426, 841-845.
Ikonomidou C & Turski L (2002). Why did NMDA receptor antagonists fail clinical trials for stroke and traumatic brain injury? Lancet Neurol 1, 383-386.
Isaacson JS & Scanziani M (2011). How inhibition shapes cortical activity. Neuron 72, 231-243.
Ishii T, Moriyoshi K, Sugihara H, Sakurada K, Kadotani H, Yokoi M, Akazawa C, Shigemoto R, Mizuno N, & Masu M (1993). Molecular characterization of the family of the N-methyl-D-aspartate receptor subunits. J Biol Chem 268, 2836-2843.
Jespersen A, Tajima N, Fernandez-Cuervo G, Garnier-Amblard EC & Furukawa H (2014). Structural insights into competitive antagonism in NMDA receptors. Neuron 81, 366-378.
Karakas E & Furukawa H (2014). Crystal structure of a heterotetrameric NMDA receptor ion channel. Science 344, 992-997.
Karakas E, Simorowski N & Furukawa H (2011). Subunit arrangement and phenylethanolamine binding in GluN1/GluN2B NMDA receptors. Nature 475, 249-253.
Kemp JA, Foster AC, Leeson PD, Priestley T, Tridgett R, Iversen LL & Woodruff GN (1988). 7-Chlorokynurenic acid is a selective antagonist at the glycine modulatory site of the N-methyl-D-aspartate receptor complex. Proc Natl Acad Sci U S A 85, 6547-6550.
Kesner P, Schohl A, Warren EC, Ma F & Ruthazer ES (2020). Postsynaptic and presynaptic NMDARs have distinct roles in visual circuit development. Cell Rep 32, 107955.
Kessels HW, Nabavi S & Malinow R (2013). Metabotropic NMDA receptor function is required for β-amyloid-induced synaptic depression. Proc Natl Acad Sci U S A 110, 4033-4038.
Kron M, Howell CJ, Adams IT, Ransbottom M, Christian D, Ogier M & Katz DM (2012). Brain activity mapping in Mecp2 mutant mice reveals functional deficits in forebrain circuits, including key nodes in the default mode network, that are reversed with ketamine treatment. J Neurosci 32, 13860-13872.
Kuner T & Schoepfer R (1996). Multiple structural elements determine subunit specificity of Mg2+ block in NMDA receptor channels. J Neurosci 16, 3549-3558.
Lachamp PM, Liu Y & Liu SJ (2009). Glutamatergic modulation of cerebellar interneuron activity is mediated by an enhancement of GABA release and requires protein kinase A/RIM1α signaling. J Neurosci 29, 381-392.
Laing MD & Bashir ZI (2015). Presynaptic NR2A-containing NMDARs are required for LTD between the amygdala and the perirhinal cortex: a potential mechanism for the emotional modulation of memory? eNeuro 2, ENEURO.0046-14.2015.
Larsen RS, Corlew RJ, Henson MA, Roberts AC, Mishina M, Watanabe M, Lipton SA, Nakanishi N, Pérez-Otaño I, Weinberg RJ & Philpot BD (2011). NR3A-containing NMDARs promote neurotransmitter release and spike timing-dependent plasticity. Nat Neurosci 14, 338-344.
Larsen RS & Sjöström PJ (2015). Synapse-type-specific plasticity in local circuits. Curr Opin Neurobiol 35, 127-135.
Larsen RS, Smith IT, Miriyala J, Han JE, Corlew RJ, Smith SL & Philpot BD (2014). Synapse-specific control of experience-dependent plasticity by presynaptic NMDA receptors. Neuron 83, 879-893.
Lau A & Tymianski M (2010). Glutamate receptors, neurotoxicity and neurodegeneration. Pflugers Arch 460, 525-542.
Lien CC, Mu Y, Vargas-Caballero M & Poo MM (2006). Visual stimuli-induced LTD of GABAergic synapses mediated by presynaptic NMDA receptors. Nat Neurosci 9, 372-380.
Liu H, Mantyh PW & Basbaum AI (1997). NMDA-receptor regulation of substance P release from primary afferent nociceptors. Nature 386, 721-724.
Liu H, Wang H, Sheng M, Jan LY, Jan YN & Basbaum AI (1994). Evidence for presynaptic N-methyl-D-aspartate autoreceptors in the spinal cord dorsal horn. Proc Natl Acad Sci U S A 91, 8383-8387.
Liu SJ & Lachamp P (2006). The activation of excitatory glutamate receptors evokes a long-lasting increase in the release of GABA from cerebellar stellate cells. J Neurosci 26, 9332-9339.
LoGrasso P & McKelvy J (2003). Advances in pain therapeutics. Curr Opin Chem Biol 7, 452-456.
Lourenço J, Cannich A, Carta M, Coussen F, Mulle C & Marsicano G (2010). Synaptic activation of kainate receptors gates presynaptic CB1 signaling at GABAergic synapses. Nat Neurosci 13, 197-204.
Maccaferri G, Tóth K & McBain CJ (1998). Target-specific expression of presynaptic mossy fiber plasticity. Science 279, 1368-1371.
Maheux J, Froemke R & Sjöström PJ (2016). Functional plasticity at dendritic synapses. In Dendrites, 3rd edn, eds. Stuart G, Spruston N & Häusser M. Oxford University Press, Oxford, UK, 465-498.
Marcelli S, Iannuzzi F, Ficulle E, Mango D, Pieraccini S, Pellegrino S, Corbo M, Sironi M, Pittaluga A, Nisticò R & Feligioni M (2019). The selective disruption of presynaptic JNK2/STX1a interaction reduces NMDA receptor-dependent glutamate release. Sci Rep 9, 7146.
Markram H, Lübke J, Frotscher M & Sakmann B (1997). Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 275, 213-215.
McKinney RA, Capogna M, Dürr R, Gähwiler BH & Thompson SM (1999). Miniature synaptic events maintain dendritic spines via AMPA receptor activation. Nat Neurosci 2, 44-49.
Meguro H, Mori H, Araki K, Kushiya E, Kutsuwada T, Yamazaki M, Kumanishi T, Arakawa M, Sakimura K & Mishina M (1992). Functional characterization of a heteromeric NMDA receptor channel expressed from cloned cDNAs. Nature 357, 70-74.
Min R & Nevian T (2012). Astrocyte signaling controls spike timing-dependent depression at neocortical synapses. Nat Neurosci 15, 746-753.
Mony L, Zhu S, Carvalho S & Paoletti P (2011). Molecular basis of positive allosteric modulation of GluN2B NMDA receptors by polyamines. EMBO J 30, 3134-3146.
Monyer H, Burnashev N, Laurie DJ, Sakmann B & Seeburg PH (1994). Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12, 529-540.
Monyer H, Sprengel R, Schoepfer R, Herb A, Higuchi M, Lomeli H, Burnashev N, Sakmann B & Seeburg PH (1992). Heteromeric NMDA receptors: molecular and functional distinction of subtypes. Science 256, 1217-1221.
Nabavi S, Fox R, Alfonso S, Aow J & Malinow R (2014a). GluA1 trafficking and metabotropic NMDA: addressing results from other laboratories inconsistent with ours. Philos Trans R Soc Lond B Biol Sci 369, 20130145.
Nabavi S, Fox R, Proulx CD, Lin JY, Tsien RY & Malinow R (2014b). Engineering a memory with LTD and LTP. Nature 511, 348-352.
Nabavi S, Kessels HW, Alfonso S, Aow J, Fox R & Malinow R (2013). Metabotropic NMDA receptor function is required for NMDA receptor-dependent long-term depression. Proc Natl Acad Sci U S A 110, 4027-4032.
Neal AP, Worley PF & Guilarte TR (2011). Lead exposure during synaptogenesis alters NMDA receptor targeting via NMDA receptor inhibition. Neurotoxicology 32, 281-289.
Nevian T & Sakmann B (2006). Spine Ca2+ signaling in spike-timing-dependent plasticity. J Neurosci 26, 11001-11013.
Nisticò R, Florenzano F, Mango D, Ferraina C, Grilli M, Di Prisco S, Nobili A, Saccucci S, D'Amelio M, Morbin M, Marchi M, Mercuri NB, Davis RJ, Pittaluga A & Feligioni M (2015). Presynaptic c-Jun N-terminal Kinase 2 regulates NMDA receptor-dependent glutamate release. Sci Rep 5, 9035.
Olivero G, Cisani F, Vergassola M & Pittaluga A (2019). Prolonged activation of CXCR4 hampers the release-regulating activity of presynaptic NMDA receptors in rat hippocampal synaptosomes. Neurochem Int 126, 59-63.
Olverman HJ, Jones AW & Watkins JC (1984). L-glutamate has higher affinity than other amino acids for [3H]-D-AP5 binding sites in rat brain membranes. Nature 307, 460-462.
O'Roak BJ, Vives L, Fu W, Egertson JD, Stanaway IB, Phelps IG, Carvill G, Kumar A, Lee C, Ankenman K, Munson J, Hiatt JB, Turner EH, Levy R, O'Day DR, Krumm N, Coe BP, Martin BK, Borenstein E, Nickerson DA, Mefford HC, Doherty D, Akey JM, Bernier R, Eichler EE & Shendure J (2012). Multiplex targeted sequencing identifies recurrently mutated genes in autism spectrum disorders. Science 338, 1619-1622.
Pachernegg S, Strutz-Seebohm N & Hollmann M (2012). GluN3 subunit-containing NMDA receptors: not just one-trick ponies. Trends Neurosci 35, 240-249.
Padamsey Z, Tong R & Emptage N (2017). Glutamate is required for depression but not potentiation of long-term presynaptic function. Elife 6, e29688.
Pafundo DE, Miyamae T, Lewis DA & Gonzalez-Burgos G (2018). Presynaptic effects of N-methyl-D-aspartate receptors enhance parvalbumin cell-mediated inhibition of pyramidal cells in mouse prefrontal cortex. Biol Psychiatry 84, 460-470.
Paoletti P, Bellone C & Zhou Q (2013). NMDA receptor subunit diversity: impact on receptor properties, synaptic plasticity and disease. Nat Rev Neurosci 14, 383-400.
Paquet M & Smith Y (2000). Presynaptic NMDA receptor subunit immunoreactivity in GABAergic terminals in rat brain. J Comp Neurol 423, 330-347.
Park H, Popescu A & Poo MM (2014). Essential role of presynaptic NMDA receptors in activity-dependent BDNF secretion and corticostriatal LTP. Neuron 84, 1009-1022.
Parpura V, Basarsky TA, Liu F, Jeftinija K, Jeftinija S & Haydon PG (1994). Glutamate-mediated astrocyte-neuron signalling. Nature 369, 744-747.
Parsons MP & Raymond LA (2014). Extrasynaptic NMDA receptor involvement in central nervous system disorders. Neuron 82, 279-293.
Pérez-Rodríguez M, Arroyo-García LE, Prius-Mengual J, Andrade-Talavera Y, Armengol JA, Pérez-Villegas EM, Duque-Feria P, Flores G & Rodríguez-Moreno A (2019). Adenosine receptor-mediated developmental loss of spike timing-dependent depression in the hippocampus. Cereb Cortex 29, 3266-3281.
Pressey JC & Woodin MA (2021). Kainate receptor regulation of synaptic inhibition in the hippocampus. J Physiol 599, 485-492.
Prius-Mengual J, Pérez-Rodríguez M, Andrade-Talavera Y & Rodríguez-Moreno A (2019). NMDA receptors containing GluN2B/2C/2D subunits mediate an increase in glutamate release at hippocampal CA3-CA1 synapses. Mol Neurobiol 56, 1694-1706.
Pugh JR & Jahr CE (2011). NMDA receptor agonists fail to alter release from cerebellar basket cells. J Neurosci 31, 16550-16555.
Purcell AE, Jeon OH, Zimmerman AW, Blue ME & Pevsner J (2001). Postmortem brain abnormalities of the glutamate neurotransmitter system in autism. Neurology 57, 1618-1628.
Rachline J, Perin-Dureau F, Le Goff A, Neyton J & Paoletti P (2005). The micromolar zinc-binding domain on the NMDA receptor subunit NR2B. J Neurosci 25, 308-317.
Rieubland S, Roth A & Häusser M (2014). Structured connectivity in cerebellar inhibitory networks. Neuron 81, 913-929.
Rodríguez-Moreno A, Herreras O & Lerma J (1997). Kainate receptors presynaptically downregulate GABAergic inhibition in the rat hippocampus. Neuron 19, 893-901.
Rodríguez-Moreno A, González-Rueda A, Banerjee A, Upton AL, Craig MT & Paulsen O (2013). Presynaptic self-depression at developing neocortical synapses. Neuron 77, 35-42.
Rodríguez-Moreno A, Kohl MM, Reeve JE, Eaton TR, Collins HA, Anderson HL & Paulsen O (2011). Presynaptic induction and expression of timing-dependent long-term depression demonstrated by compartment-specific photorelease of a use-dependent NMDA receptor antagonist. J Neurosci 31, 8564-8569.
Rodríguez-Moreno A, López-García JC & Lerma J (2000). Two populations of kainate receptors with separate signaling mechanisms in hippocampal interneurons. Proc Natl Acad Sci U S A 97, 1293-1298.
Rodríguez-Moreno A & Paulsen O (2008). Spike timing-dependent long-term depression requires presynaptic NMDA receptors. Nat Neurosci 11, 744-745.
Roggenhofer E, Fidzinski P, Bartsch J, Kurz F, Shor O & Behr J (2010). Activation of dopamine D1/D5 receptors facilitates the induction of presynaptic long-term potentiation at hippocampal output synapses. Eur J Neurosci 32, 598-605.
Rossi B, Ogden D, Llano I, Tan YP, Marty A & Collin T (2012). Current and calcium responses to local activation of axonal NMDA receptors in developing cerebellar molecular layer interneurons. PLoS One 7, e39983.
Samson RD & Paré D (2005). Activity-dependent synaptic plasticity in the central nucleus of the amygdala. J Neurosci 25, 1847-1855.
Savtchouk I, Di Castro MA, Ali R, Stubbe H, Luján R & Volterra A (2019). Circuit-specific control of the medial entorhinal inputs to the dentate gyrus by atypical presynaptic NMDARs activated by astrocytes. Proc Natl Acad Sci U S A 116, 13602-13610.
Sceniak MP, Lang M, Enomoto AC, James Howell C, Hermes DJ & Katz DM (2016). Mechanisms of functional hypoconnectivity in the medial prefrontal cortex of Mecp2 null mice. Cereb Cortex 26, 1938-1956.
Sheng M, Cummings J, Roldan LA, Jan YN & Jan LY (1994). Changing subunit composition of heteromeric NMDA receptors during development of rat cortex. Nature 368, 144-147.
Shin JH & Linden DJ (2005). An NMDA receptor/nitric oxide cascade is involved in cerebellar LTD but is not localized to the parallel fiber terminal. J Neurophysiol 94, 4281-4289.
Sjöström PJ & Nelson SB (2002). Spike timing, calcium signals and synaptic plasticity. Curr Opin Neurobiol 12, 305-314.
Sjöström PJ, Rancz EA, Roth A & Häusser M (2008). Dendritic excitability and synaptic plasticity. Physiol Rev 88, 769-840.
Sjöström PJ, Turrigiano GG & Nelson SB (2003). Neocortical LTD via coincident activation of presynaptic NMDA and cannabinoid receptors. Neuron 39, 641-654.
Sjöström PJ, Turrigiano GG & Nelson SB (2007). Multiple forms of long-term plasticity at unitary neocortical layer 5 synapses. Neuropharmacology 52, 176-184.
Sohal VS & Rubenstein JLR (2019). Excitation-inhibition balance as a framework for investigating mechanisms in neuropsychiatric disorders. Mol Psychiatry 24, 1248-1257.
Song X, Jensen MO, Jogini V, Stein RA, Lee CH, McHaourab HS, Shaw DE & Gouaux E (2018). Mechanism of NMDA receptor channel block by MK-801 and memantine. Nature 556, 515-519.
Stein IS, Gray JA & Zito K (2015). Non-ionotropic NMDA receptor signaling drives activity-induced dendritic spine shrinkage. J Neurosci 35, 12303-12308.
Stein IS, Park DK, Flores JC, Jahncke JN & Zito K (2020). Molecular mechanisms of non-ionotropic NMDA receptor signaling in dendritic spine shrinkage. J Neurosci 40, 3741-3750.
Stern P, Béhé P, Schoepfer R & Colquhoun D (1992). Single-channel conductances of NMDA receptors expressed from cloned cDNAs: comparison with native receptors. Proc Biol Sci 250, 271-277.
Stroebel D, Casado M & Paoletti P (2018). Triheteromeric NMDA receptors: from structure to synaptic physiology. Curr Opin Physiol 2, 1-12.
Stroebel D & Paoletti P (2020). Architecture and function of NMDA receptors: an evolutionary perspective. J Physiol, https://doi.org/10.1113/JP279028.
Tarabeux J, Kebir O, Gauthier J, Hamdan FF, Xiong L, Piton A, Spiegelman D, Henrion É, Millet B, Fathalli F, Joober R, Rapoport JL, DeLisi LE, Fombonne É, Mottron L, Forget-Dubois N, Boivin M, Michaud JL, Drapeau P, Lafrenière RG, Rouleau GA & Krebs MO (2011). Rare mutations in N-methyl-D-aspartate glutamate receptors in autism spectrum disorders and schizophrenia. Transl Psychiatry 1, e55.
The UniProt Consortium (2018). UniProt: the universal protein knowledgebase. Nucleic Acids Res 46, 2699.
Thomazeau A, Bosch M, Essayan-Perez S, Barnes SA, De Jesus-Cortes H & Bear MF (2020). Dissociation of functional and structural plasticity of dendritic spines during NMDAR and mGluR-dependent long-term synaptic depression in wild-type and fragile X model mice. Mol Psychiatry, https://doi.org/10.1038/s41380-020-0821-6.
Tóth K & McBain CJ (2000). Target-specific expression of pre- and postsynaptic mechanisms. J Physiol 525, 41-51.
Traynelis SF, Wollmuth LP, McBain CJ, Menniti FS, Vance KM, Ogden KK, Hansen KB, Yuan H, Myers SJ & Dingledine R (2010). Glutamate receptor ion channels: structure, regulation, and function. Pharmacol Rev 62, 405-496.
Ujihara H & Albuquerque EX (1992). Developmental change of the inhibition by lead of NMDA-activated currents in cultured hippocampal neurons. J Pharmacol Exp Ther 263, 868-875.
Wong HH, Lin JQ, Ströhl F, Roque CG, Cioni JM, Cagnetta R, Turner-Bridger B, Laine RF, Harris WA, Kaminski CF & Holt CE (2017). RNA docking and local translation regulate site-specific axon remodeling in vivo. Neuron 95, 852-868.e858.
Wong HK, Liu XB, Matos MF, Chan SF, Pérez-Otaño I, Boysen M, Cui J, Nakanishi N, Trimmer JS, Jones EG, Lipton SA & Sucher NJ (2002). Temporal and regional expression of NMDA receptor subunit NR3A in the mammalian brain. J Comp Neurol 450, 303-317.
Wozny C, Maier N, Schmitz D & Behr J (2008). Two different forms of long-term potentiation at CA1-subiculum synapses. J Physiol 586, 2725-2734.
Wyllie DJ, Béhé P, Nassar M, Schoepfer R & Colquhoun D (1996). Single-channel currents from recombinant NMDA NR1a/NR2D receptors expressed in Xenopus oocytes. Proc Biol Sci 263, 1079-1086.
Xie JD, Chen SR & Pan HL (2017). Presynaptic mGluR5 receptor controls glutamatergic input through protein kinase C-NMDA receptors in paclitaxel-induced neuropathic pain. J Biol Chem 292, 20644-20654.
Yamamoto T & Yaksh TL (1992). Spinal pharmacology of thermal hyperesthesia induced by constriction injury of sciatic nerve. Excitatory amino acid antagonists. Pain 49, 121-128.
Yan X, Jiang E, Gao M & Weng HR (2013). Endogenous activation of presynaptic NMDA receptors enhances glutamate release from the primary afferents in the spinal dorsal horn in a rat model of neuropathic pain. J Physiol 591, 2001-2019.
Yizhar O, Fenno LE, Prigge M, Schneider F, Davidson TJ, O'Shea DJ, Sohal VS, Goshen I, Finkelstein J, Paz JT, Stehfest K, Fudim R, Ramakrishnan C, Huguenard JR, Hegemann P & Deisseroth K (2011). Neocortical excitation/inhibition balance in information processing and social dysfunction. Nature 477, 171-178.
Zeng J, Thomson LM, Aicher SA & Terman GW (2006). Primary afferent NMDA receptors increase dorsal horn excitation and mediate opiate tolerance in neonatal rats. J Neurosci 26, 12033-12042.
Zhou JJ, Li DP, Chen SR, Luo Y & Pan HL (2018). The α2δ-1-NMDA receptor coupling is essential for corticostriatal long-term potentiation and is involved in learning and memory. J Biol Chem 293, 19354-19364.
Zhu Z, Yi F, Epplin MP, Liu D, Summer SL, Mizu R, Shaulsky G, XiangWei W, Tang W, Burger PB, Menaldino DS, Myers SJ, Liotta DC, Hansen KB, Yuan H & Traynelis SF (2020). Negative allosteric modulation of GluN1/GluN3 NMDA receptors. Neuropharmacology 176, 108117.
Zukin RS & Bennett MV (1995). Alternatively spliced isoforms of the NMDARI receptor subunit. Trends Neurosci 18, 306-313.