Neuronal Plasticity: Neuronal Organization is Associated with Neurological Disorders

Abstract

Stimuli from stressful events, attention in the classroom, and many other experiences affect the functionality of the brain by changing the structure or reorganizing the connections between neurons and their communication. Modification of the synaptic transmission is a vital mechanism for generating neural activity via internal or external stimuli. Neuronal plasticity is an important driving force in neuroscience research, as it is the basic process underlying learning and memory and is involved in many other functions including brain development and homeostasis, sensorial training, and recovery from brain injury. Indeed, neuronal plasticity has been explored in numerous studies, but it is still not clear how neuronal plasticity affects the physiology and morphology of the brain. Thus, unraveling the molecular mechanisms of neuronal plasticity is essential for understanding the operation of brain functions. In this timeline review, we discuss the molecular mechanisms underlying different forms of synaptic plasticity and their association with neurodegenerative/neurological disorders as a consequence of alterations in neuronal plasticity.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Abbreviations

PTP:

Post-tetanic potentiation

DSC:

Voltage-dependent sodium channel

VDCC:

Voltage-dependent calcium channel

LTP:

Long term potentiation

LTD:

Long-term depression

mGLUR:

Metabotropic glutamate receptor

PKC:

Protein kinase C

References

  1. Abbott LF, Regehr WG (2004) Synaptic computation. Nature 431(7010):796

    CAS  PubMed  Article  Google Scholar 

  2. Abraham WC, Bear MF (1996) Metaplasticity: the plasticity of synaptic plasticity. Trends Neurosci 19(4):126–130

    CAS  PubMed  Article  Google Scholar 

  3. Abraham WC, Williams JM (2003) Properties and mechanisms of LTP maintenance. Neuroscientist 9(6):463–474

    CAS  PubMed  Article  Google Scholar 

  4. Agarwal A, Zhang M, Trembak-Duff I, Unterbarnscheidt T, Radyushkin K, Dibaj P, Berning S (2014) Dysregulated expression of neuregulin-1 by cortical pyramidal neurons disrupts synaptic plasticity. Cell Rep 8(4):1130–1145

    CAS  PubMed  Article  Google Scholar 

  5. Aggen JB, Nairn AC, Chamberlin R (2000) Regulation of protein phosphatase-1. Chem Biol 7(1):R13–R23

    CAS  PubMed  Article  Google Scholar 

  6. Albert PR (2019) Adult neuroplasticity: a new “cure” for major depression? J Psych Neurosci: JPN 44(3):147

    Article  Google Scholar 

  7. Amici M, Doherty A, Jo J, Jane D, Cho K, Collingridge G, Dargan S (2009) Neuronal calcium sensors and synaptic plasticity

  8. Anggono V, Huganir RL (2012) Regulation of AMPA receptor trafficking and synaptic plasticity. Curr Opin Neurobiol 22(3):461–469

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  9. Babiec WE, Guglietta R, Jami SA, Morishita W, Malenka RC, O'Dell TJ (2014) Ionotropic NMDA receptor signaling is required for the induction of long-term depression in the mouse hippocampal CA1 region. J Neurosci 34(15):5285–5290

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  10. Baldessarini RJ, Tarazi FI (2006) Pharmacotherapy of Psychosis and Mania; The Pharmacological Basis of Therapeutics. 11e

  11. Bangasser DA, Valentino RJ (2014) Sex differences in stress-related psychiatric disorders: neurobiological perspectives. Front Neuroendocrinol 35(3):303–319

    PubMed  PubMed Central  Article  Google Scholar 

  12. Banke TG, Bowie DLHK, Lee HK, Huganir RL, Schousboe A, Traynelis SF (2000) Control of GluR1 AMPA receptor function by cAMP-dependent protein kinase. J Neurosci 20(1):89–102

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  13. Bannai H, Lévi S, Schweizer C, Inoue T, Launey T, Racine V, Triller A (2009) Activity-dependent tuning of inhibitory neurotransmission based on GABAAR diffusion dynamics. Neuron 62(5):670–682

    CAS  PubMed  Article  Google Scholar 

  14. Barrett AB, Billings GO, Morris RG, Van Rossum MC (2009) State based model of long-term potentiation and synaptic tagging and capture. PLoS Comput Biol 5(1):e1000259

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  15. Battaglia S, Renner M, Russeau M, Côme E, Tyagarajan SK, Lévi S (2018) Activity-dependent inhibitory synapse scaling is determined by gephyrin phosphorylation and subsequent regulation of GABAA receptor diffusion. Eneuro. 5(1)

  16. Beste C, Wascher E, Dinse HR, Saft C (2012) Faster perceptual learning through excitotoxic neurodegeneration. Curr Biol 22(20):1914–1917

    CAS  PubMed  Article  Google Scholar 

  17. Betz WJ (1970) Depression of transmitter release at the neuromuscular junction of the frog. J Physiol 206(3):629–644

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  18. Bissen D, Foss F, Acker-Palmer A (2019) AMPA receptors and their minions: auxiliary proteins in AMPA receptor trafficking. Cell Mol Life Sci 76(11):2133–2169

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  19. Blatow M, Caputi A, Burnashev N, Monyer H, Rozov A (2003) Ca2+ buffer saturation underlies paired pulse facilitation in calbindin-D28k-containing terminals. Neuron 38(1):79–88

    CAS  PubMed  Article  Google Scholar 

  20. Bliss TVP, Collingridge GL, Morris RGM (2014) Synaptic plasticity in health and disease: introduction and overview

  21. Blum BP, Mann JJ (2002) The GABAergic system in schizophrenia. Int J Neuropsychopharmacol 5(2):159–179

    CAS  PubMed  Article  Google Scholar 

  22. Bornschein G, Schmidt H (2018) Synaptotagmin Ca2+ sensors and their spatial coupling to presynaptic Cav channels in central cortical synapses. Front Mol Neurosci 11

  23. Bosch M, Castro J, Saneyoshi T, Matsuno H, Sur M, Hayashi Y (2014) Structural and molecular remodeling of dendritic spine substructures during long-term potentiation. Neuron 82(2):444–459

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  24. Bourgeron T (2015) From the genetic architecture to synaptic plasticity in autism spectrum disorder. Nat Rev Neurosci 16(9):551

    CAS  PubMed  Article  Google Scholar 

  25. Bredt DS, Nicoll RA (2003) AMPA receptor trafficking at excitatory synapses. Neuron 40(2):361–379

    CAS  PubMed  Article  Google Scholar 

  26. Buttelmann F, Karbach J (2017) Development and plasticity of cognitive flexibility in early and middle childhood. Front Psychol 8:1040

    PubMed  PubMed Central  Article  Google Scholar 

  27. Calakos N, Schoch S, Südhof TC, Malenka RC (2004) Multiple roles for the active zone protein RIM1α in late stages of neurotransmitter release. Neuron 42(6):889–896

    CAS  PubMed  Article  Google Scholar 

  28. Campa CC, Hirsch E (2017) Rab11 and phosphoinositides: a synergy of signal transducers in the control of vesicular trafficking. Adv Biol Reg 63:132–139

    CAS  Article  Google Scholar 

  29. Cardoso-Leite P, Ascher P, Bavelier D (2012) Brain plasticity: paradoxical case of a neurodegenerative disease? Curr Biol 22(20):R884–R886

    CAS  PubMed  Article  Google Scholar 

  30. Carroll RC, Beattie EC, von Zastrow M, Malenka RC (2001) Role of AMPA receptor endocytosis in synaptic plasticity. Nat Rev Neurosci 2(5):315

    CAS  PubMed  Article  Google Scholar 

  31. Castillo PE, Chiu CQ, Carroll RC (2011) Long-term plasticity at inhibitory synapses. Curr Opin Neurobiol 21(2):328–338

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  32. Catterall WA, Leal K, Nanou E (2013) Calcium channels and short-term synaptic plasticity. J Biol Chem 288(15):10742–10749

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  33. Chater TE, Goda Y (2014) The role of AMPA receptors in postsynaptic mechanisms of synaptic plasticity. Front Cell Neurosci 8:401

    PubMed  PubMed Central  Article  Google Scholar 

  34. Chen L, Chetkovich DM, Petralia RS, Sweeney NT, Kawasaki Y, Wenthold RJ, Nicoll RA (2000) Stargazin regulates synaptic targeting of AMPA receptors by two distinct mechanisms. Nature 408(6815):936

    CAS  PubMed  Article  Google Scholar 

  35. Chidambaram SB, Rathipriya AG, Bolla SR, Bhat A, Ray B, Mahalakshmi AM, Chandra R (2019) Dendritic spines: revisiting the physiological role. Prog Neuro-Psychopharmacol Biol Psychiatry

  36. Chiu CQ, Barberis A, Higley MJ (2019) Preserving the balance: diverse forms of long-term GABAergic synaptic plasticity. Nat Rev Neurosci 20(5):272–281

    CAS  PubMed  Article  Google Scholar 

  37. Citri A, Malenka RC (2008) Synaptic plasticity: multiple forms, functions, and mechanisms. Neuropsychopharmacology 33(1):18

    PubMed  PubMed Central  Article  Google Scholar 

  38. Collingridge GL, Isaac JT, Wang YT (2004) Receptor trafficking and synaptic plasticity. Nat Rev Neurosci 5(12):952

    CAS  PubMed  Article  Google Scholar 

  39. Costa JT, Mele M, Baptista MS, Gomes JR, Ruscher K, Nobre RJ, Duarte CB (2016) Gephyrin cleavage in in vitro brain ischemia decreases GABA a receptor clustering and contributes to neuronal death. Mol Neurobiol 53(6):3513–3527

    CAS  PubMed  Article  Google Scholar 

  40. Cottrell JR, Borok E, Horvath TL, Nedivi E (2004) CPG2: a brain-and synapse-specific protein that regulates the endocytosis of glutamate receptors. Neuron 44(4):677–690

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Crabtree GW, Gogos JA (2014) Synaptic plasticity, neural circuits, and the emerging role of altered short-term information processing in schizophrenia. Front Synaptic Neurosci 6:28

    PubMed  PubMed Central  Article  Google Scholar 

  42. Dan Y, Poo MM (2006) Spike timing-dependent plasticity: from synapse to perception. Physiol Rev 86(3):1033–1048

    PubMed  Article  Google Scholar 

  43. Daskalakis ZJ, Christensen BK, Fitzgerald PB, Chen R (2008) Dysfunctional neural plasticity in patients with schizophrenia. Arch Gen Psychiatry 65(4):378–385

    PubMed  Article  Google Scholar 

  44. Dedic N, Pöhlmann ML, Richter JS, Mehta D, Czamara D, Metzger MW, Jurik A (2018) Cross-disorder risk gene CACNA1C differentially modulates susceptibility to psychiatric disorders during development and adulthood. Mol Psychiatry 23(3):533

    CAS  PubMed  Article  Google Scholar 

  45. Dejanovic B, Schwarz G (2014) Neuronal nitric oxide synthase-dependent S-nitrosylation of gephyrin regulates gephyrin clustering at GABAergic synapses. J Neurosci 34(23):7763–7768

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  46. Dejanovic B, Semtner M, Ebert S, Lamkemeyer T, Neuser F, Lüscher B, Schwarz G (2014) Palmitoylation of gephyrin controls receptor clustering and plasticity of GABAergic synapses. PLoS Biol 12(7):e1001908

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  47. DeLong MR, Wichmann T (2007) Circuits and circuit disorders of the basal ganglia. Arch Neurol 64(1):20–24

    PubMed  Article  Google Scholar 

  48. Deng L, Kaeser PS, Xu W, Südhof TC (2011) RIM proteins activate vesicle priming by reversing autoinhibitory homodimerization of Munc13. Neuron 69(2):317–331

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  49. Deng PY, Klyachko VA (2011) The diverse functions of short-term plasticity components in synaptic computations. Commun Integ Biol 4(5):543–548

    Article  Google Scholar 

  50. Diering GH, Huganir RL (2018) The AMPA receptor code of synaptic plasticity. Neuron 100(2):314–329

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  51. Doyle M, Kiebler MA (2011) Mechanisms of dendritic mRNA transport and its role in synaptic tagging. EMBO J 30(17):3540–3552

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  52. Duclot F, Kabbaj M (2017) The role of early growth response 1 (EGR1) in brain plasticity and neuropsychiatric disorders. Front Behav Neurosci 11:35

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  53. Dudek SM, Bear MF (1992) Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-D-aspartate receptor blockade. Proc Natl Acad Sci 89(10):4363–4367

    CAS  PubMed  Article  Google Scholar 

  54. Duman RS, Aghajanian GK (2012) Synaptic dysfunction in depression: potential therapeutic targets. Science 338(6103):68–72

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  55. Duman RS, Aghajanian GK, Sanacora G, Krystal JH (2016) Synaptic plasticity and depression: new insights from stress and rapid-acting antidepressants. Nat Med 22(3):238

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  56. Eggermann E, Bucurenciu I, Goswami SP, Jonas P (2012) Nanodomain coupling between Ca 2+ channels and sensors of exocytosis at fast mammalian synapses. Nat Rev Neurosci 13(1):7

    CAS  Article  Google Scholar 

  57. Ehlers MD (2000) Reinsertion or degradation of AMPA receptors determined by activity-dependent endocytic sorting. Neuron 28(2):511

    CAS  PubMed  Article  Google Scholar 

  58. Ehrlich I, Malinow R (2004) Postsynaptic density 95 controls AMPA receptor incorporation during long-term potentiation and experiencedriven synaptic plasticity. J Neurosci 24(4):916–927

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  59. Evans RC, Blackwell KT (2015) Calcium: amplitude, duration, or location? Biol Bull 228(1):75–83

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  60. Fernandes D, Carvalho AL (2016) Mechanisms of homeostatic plasticity in the excitatory synapse. J Neurochem 139(6):973–996

    CAS  PubMed  Article  Google Scholar 

  61. Fioravante D, Regehr WG (2011) Short-term forms of presynaptic plasticity. Curr Opin Neurobiol 21(2):269–274

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  62. Fiuza M, Rostosky CM, Parkinson GT, Bygrave AM, Halemani N, Baptista M, Hanley JG (2017) PICK1 regulates AMPA receptor endocytosis via direct interactions with AP2 α-appendage and dynamin. J Cell Biol 216(10):3323–3338

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  63. Flachenecker P (2015) Clinical implications of neuroplasticity–the role of rehabilitation in multiple sclerosis. Front Neurol 6:36

    PubMed  PubMed Central  Article  Google Scholar 

  64. Flores CE, Nikonenko I, Mendez P, Fritschy JM, Tyagarajan SK, Muller D (2015) Activity-dependent inhibitory synapse remodeling through gephyrin phosphorylation. Proc Natl Acad Sci 112(1):E65–E72

    CAS  PubMed  Article  Google Scholar 

  65. Forrest MP, Parnell E, Penzes P (2018) Dendritic structural plasticity and neuropsychiatric disease. Nat Rev Neurosci 19(4):215

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  66. Forsythe ID, Tsujimoto T, Barnes-Davies M, Cuttle MF, Takahashi T (1998) Inactivation of presynaptic calcium current contributes to synaptic depression at a fast central synapse. Neuron 20(4):797–807

    CAS  PubMed  Article  Google Scholar 

  67. Freir DB, Herron CE (2003) Inhibition of L-type voltage dependent calcium channels causes impairment of long-term potentiation in the hippocampal CA1 region in vivo. Brain Res 967(1–2):27–36

    CAS  PubMed  Article  Google Scholar 

  68. Frey U, Morris RG (1997) Synaptic tagging and long-term potentiation. Nature 385(6616):533–536

    CAS  PubMed  Article  Google Scholar 

  69. Fritschy JM, Harvey RJ, Schwarz G (2008) Gephyrin: where do we stand, where do we go? Trends Neurosci 31(5):257–264

    CAS  PubMed  Article  Google Scholar 

  70. Fritschy JM, Panzanelli P, Tyagarajan SK (2012) Molecular and functional heterogeneity of GABAergic synapses. Cell Mol Life Sci 69(15):2485–2499

    CAS  PubMed  Article  Google Scholar 

  71. Gagnon D, Petryszyn S, Sanchez MG, Bories C, Beaulieu JM, De Koninck Y et al (2017) Striatal neurons expressing D 1 and D 2 receptors are morphologically distinct and differently affected by dopamine denervation in mice. Sci Rep 7(1):1–16

    Article  CAS  Google Scholar 

  72. Gallagher SM, Daly CA, Bear MF, Huber KM (2004) Extracellular signal-regulated protein kinase activation is required for metabotropic glutamate receptor-dependent long-term depression in hippocampal area CA1. J Neurosci 24(20):4859–4864

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  73. Gao PP, Goodman JH, Sacktor TC, Francis JT (2018) Persistent increases of PKMζ in sensorimotor cortex maintain procedural long-term memory storage. BioRxiv. 193508

  74. Garay PA, McAllister AK (2010) Novel roles for immune molecules in neural development: implications for neurodevelopmental disorders. Front Synaptic Neurosci 2:136

    PubMed  PubMed Central  Article  Google Scholar 

  75. Ghiglieri V, Calabrese V, Calabresi P (2018) Alpha-synuclein: from early synaptic dysfunction to neurodegeneration. Front Neurol 9

  76. Ghosh H, Auguadri L, Battaglia S, Thirouin ZS, Zemoura K, Messner S, Kawasaki H (2016) Several posttranslational modifications act in concert to regulate gephyrin scaffolding and GABAergic transmission. Nat Commun 7:13365

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  77. Giese KP, Mizuno K (2013) The roles of protein kinases in learning and memory. Learn Mem 20(10):540–552

    CAS  PubMed  Article  Google Scholar 

  78. Gisabella B, Bolshakov VY, Benes FM (2005) Regulation of synaptic plasticity in a schizophrenia model. Proc Natl Acad Sci 102(37):13301–13306

    CAS  PubMed  Article  Google Scholar 

  79. Gitler D, Cheng Q, Greengard P, Augustine GJ (2008) Synapsin IIa controls the reserve pool of glutamatergic synaptic vesicles. J Neurosci 28(43):10835–10843

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  80. Glebov OO, Tigaret CM, Mellor JR, Henley JM (2015) Clathrin-independent trafficking of AMPA receptors. J Neurosci 35(12):4830–4836

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  81. Gómez-Pineda VG, Torres-Cruz FM, Vivar-Cortés CI, Hernández-Echeagaray E (2018) Neurotrophin - 3 restores synaptic plasticity in the striatum of a mouse model of Huntington’s disease. CNS Neuroscience & Therapeutics 24(4):353–363

    Article  CAS  Google Scholar 

  82. Graber TE, Hébert-Seropian S, Khoutorsky A, David A, Yewdell JW, Lacaille JC, Sossin WS (2013) Reactivation of stalled polyribosomes in synaptic plasticity. Proceed Nat Acad Sci. 201307747

  83. Granger AJ, Nicoll RA (2014) Expression mechanisms underlying long-term potentiation: a postsynaptic view, 10 years on. Philos Trans R Soc B 369(1633):20130136

    Article  CAS  Google Scholar 

  84. Gross M, Sheinin A, Nesher E, Tikhonov T, Baranes D, Pinhasov A, Michaelevski I (2015) Early onset of cognitive impairment is associated with altered synaptic plasticity and enhanced hippocampal GluA1 expression in a mouse model of depression. Neurobiol Aging 36(5):1938–1952

    CAS  PubMed  Article  Google Scholar 

  85. Guerrier C, Holcman D (2018) The first 100 nm inside the pre-synaptic terminal where calcium diffusion triggers vesicular release. Front Synaptic Neurosci. 10

  86. Gundelfinger ED, Reissner C, Garner CC (2016) Role of bassoon and piccolo in assembly and molecular organization of the active zone. Front Synaptic Neurosci 7:19

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  87. Guo H, Camargo LM, Yeboah F, Digan ME, Niu H, Pan Y, Shanker YG (2017) A NMDA-receptor calcium influx assay sensitive to stimulation by glutamate and glycine/D-serine. Sci Rep 7(1):11608

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  88. Hahn CG, Wang HY, Cho DS, Talbot K, Gur RE, Berrettini WH et al (2006) Altered neuregulin 1–erbB4 signaling contributes to NMDA> receptor hypofunction in schizophrenia. Nat Med 12(7):824–828

    CAS  PubMed  Article  Google Scholar 

  89. Hallermann S, Fejtova A, Schmidt H, Weyhersmüller A, Silver RA, Gundelfinger ED, Eilers J (2010) Bassoon speeds vesicle reloading at a central excitatory synapse. Neuron 68(4):710–723

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  90. Hamshere ML, Walters JT, Smith R, Richards AL, Green E, Grozeva D, Riley B (2013) Genome-wide significant associations in schizophrenia to ITIH3/4, CACNA1C and SDCCAG8, and extensive replication of associations reported by the schizophrenia PGC. Mol Psychiatry 18(6):708

    CAS  PubMed  Article  Google Scholar 

  91. Hanley JG (2014) Subunit-specific trafficking mechanisms regulating the synaptic expression of Ca2+−permeable AMPA receptors. In Seminars in cell & developmental biology (Vol. 27, pp. 14–22). Academic Press

  92. Hanley JG, Henley JM (2005) PICK1 is a calcium-sensor for NMDA-induced AMPA receptor trafficking. EMBO J 24(18):3266–3278

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  93. Hansel C (2018) Deregulation of synaptic plasticity in autism. Neurosci Lett

  94. Hardt O, Nader K, Wang YT (2014) GluA2-dependent AMPA receptor endocytosis and the decay of early and late long-term potentiation: possible mechanisms for forgetting of short-and long-term memories. Philos Trans R Soc B 369(1633):20130141

    Article  CAS  Google Scholar 

  95. Hausser A, Schlett K (2017) Coordination of AMPA receptor trafficking by Rab GTPases. Small GTPases 1–14

  96. Hebb DO (1949) The organization of behavior; a neuropsycholocigal theory. Wiley Book Clin Psychol 62–78

  97. Helassa N, Antonyuk SV, Lian LY, Haynes LP, Burgoyne RD (2017) Biophysical and functional characterization of hippocalcin mutants responsible for human dystonia. Hum Mol Genet 26(13):2426–2435

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  98. Henley JM, Wilkinson KA (2013) AMPA receptor trafficking and the mechanisms underlying synaptic plasticity and cognitive aging. Dialogues Clin Neurosci 15(1):11

    PubMed  PubMed Central  Google Scholar 

  99. Hou L, Klann E (2004) Activation of the phosphoinositide 3-kinase-Akt-mammalian target of rapamycin signaling pathway is required for metabotropic glutamate receptor-dependent long-term depression. J Neurosci 24(28):6352–6361

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  100. Huang YH, Schlüter OM, Dong Y (2015) Silent synapses speak up: updates of the neural rejuvenation hypothesis of drug addiction. Neuroscientist 21(5):451–459

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  101. Huang YY, Kandel ER, Varshavsky L, Brandont EP, Qi M, Idzerda RL, Bourtchouladz R (1995) A genetic test of the effects of mutations in PKA on mossy fiber LTP and its relation to spatial and contextual learning. Cell 83(7):1211–1222

    CAS  PubMed  Article  Google Scholar 

  102. Huganir R, Nicoll R (2013) AMPARs and synaptic plasticity: the last 25 years. Neuron 80(3):704–717

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  103. Inchauspe CG, Martini FJ, Forsythe ID, Uchitel OD (2004) Functional compensation of P/Q by N-type channels blocks short-term plasticity at the calyx of held presynaptic terminal. J Neurosci 24(46):10379–10383

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  104. Inchauspe CG, Forsythe ID, Uchitel OD (2007) Changes in synaptic transmission properties due to the expression of N-type calcium channels at the calyx of held synapse of mice lacking P/Q-type calcium channels. J Physiol 584(3):835–851

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  105. Irvine EE, Danhiez A, Radwanska K, Nassim C, Lucchesi W, Godaux E, Giese KP (2011) Properties of contextual memory formed in the absence of αCaMKII autophosphorylation. Mole Brain 4(1):8

    CAS  Article  Google Scholar 

  106. Irving AJ, Harvey J (2014) Leptin regulation of hippocampal synaptic function in health and disease. Philos Trans R Soc B 369(1633):20130155

    Article  CAS  Google Scholar 

  107. Jackman SL, Regehr WG (2017) The mechanisms and functions of synaptic facilitation. Neuron 94(3):447–464

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  108. Jackman SL, Turecek J, Belinsky JE, Regehr WG (2016) The calcium sensor synaptotagmin 7 is required for synaptic facilitation. Nature 529(7584):88

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  109. Jin XT, Smith Y (2007) Activation of presynaptic kainate receptors suppresses GABAergic synaptic transmission in the rat globus pallidus. Neuroscience 149(2):338–349

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  110. Ju W, Morishita W, Tsui J, Gaietta G, Deerinck TJ, Adams SR, Malenka RC (2004) Activity-dependent regulation of dendritic synthesis and trafficking of AMPA receptors. Nat Neurosci 7(3):244

    CAS  PubMed  Article  Google Scholar 

  111. Jurado-Coronel JC, Cabezas R, Rodríguez MFÁ, Echeverria V, García-Segura LM, Barreto GE (2018) Sex differences in Parkinson’s disease: features on clinical symptoms, treatment outcome, sexual hormones and genetics. Front Neuroendocrinol 50:18–30

    CAS  PubMed  Article  Google Scholar 

  112. Kabir ZD, Martínez-Rivera A, Rajadhyaksha AM (2017) From gene to behavior: L-type calcium channel mechanisms underlying neuropsychiatric symptoms. Neurotherapeutics 14(3):588–613

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  113. Kandel ER, Tauc L (1965) Mechanism of heterosynaptic facilitation in the giant cell of the abdominal ganglion of Aplysia depilans. J Physiol 181:28–47

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  114. Karolewicz B, Szebeni K, Gilmore T, Maciag D, Stockmeier CA, Ordway GA (2009) Elevated levels of NR2A and PSD-95 in the lateral amygdala in depression. Int J Neuropsychopharmacol 12(2):143–153

    CAS  PubMed  Article  Google Scholar 

  115. Katz B, Miledi R (1968) The role of calcium in neuromuscular facilitation. J Physiol 195:481–492

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  116. Kawaguchi SY (2019) Dynamic factors for transmitter release at small presynaptic Boutons revealed by direct patch-clamp recordings. Front Cell Neurosci 13:269

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  117. Keil MF, Briassoulis G, Stratakis CA (2016) The role of protein kinase a in anxiety behaviors. Neuroendocrinology 103(6):625–639

    CAS  PubMed  Article  Google Scholar 

  118. Kelly MT, Crary JF, Sacktor TC (2007) Regulation of protein kinase Mζ synthesis by multiple kinases in long-term potentiation. J Neurosci 27(13):3439–3444

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  119. Kemp M, Roberts P, Pook P, Jane D, Jones A, Jones P, Watkins J (1994) Antagonism of presynaptically mediated depressant responses and cyclic AMP-coupled metabotropic glutamate receptors. Eur J Pharmacol: Mole Pharm 266(2):187–192

    CAS  Article  Google Scholar 

  120. Kerrigan TL, Whitcomb D, Regan P, Cho K (2012) The role of neuronal calcium sensors in balancing synaptic plasticity and synaptic dysfunction. Front Mol Neurosci 5:57

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  121. Kerschensteiner M (2017) Neuroplasticity and its relevance for multiple sclerosis. Neurodegener Dis Manag 7(6s):31–33

    PubMed  Article  Google Scholar 

  122. Khelfaoui M, Gambino F, Houbaert X, Ragazzon B, Müller C, Carta M, Zhang CL (2014) Lack of the presynaptic RhoGAP protein oligophrenin1 leads to cognitive disabilities through dysregulation of the cAMP/PKA signalling pathway. Philosoph Trans Royal Soc London B: Biol Sci 369(1633):20130160

    Article  CAS  Google Scholar 

  123. Kimura T, Whitcomb DJ, Jo J, Regan P, Piers T, Heo S, Sotiropoulos I (2014) Microtubule-associated protein tau is essential for long-term depression in the hippocampus. Philos Trans R Soc B 369(1633):20130144

    Article  CAS  Google Scholar 

  124. Klyubin I, Ondrejcak T, Hayes J, Cullen WK, Mably AJ, Walsh DM, Rowan MJ (2014) Neurotransmitter receptor and time dependence of the synaptic plasticity disrupting actions of Alzheimer's disease Aβ in vivo. Philos Trans R Soc B 369(1633):20130147

    Article  CAS  Google Scholar 

  125. Kneussel M, Brandstätter JH, Laube B, Stahl S, Müller U, Betz H (1999) Loss of postsynaptic GABAA receptor clustering in gephyrin-deficient mice. J Neurosci 19(21):9289–9297

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  126. Ko MC, Hung YH, Ho PY, Yang YL, Lu KT (2014) Neonatal glucocorticoid treatment increased depression-like behaviour in adult rats. Int J Neuropsychopharmacol 17(12):1995–2004

    CAS  PubMed  Article  Google Scholar 

  127. Koller D, Bynum JP (2014) Dementia in the USA: state variation in prevalence. J Public Health 37(4):597–604

    Google Scholar 

  128. Kolodziejczyk K, Parsons MP, Southwell AL, Hayden MR, Raymond LA (2014) Striatal synaptic dysfunction and hippocampal plasticity deficits in the Hu97/18 mouse model of Huntington disease. PLoS One 9(4):e94562

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  129. Krystal JH, Anticevic A, Yang GJ, Dragoi G, Driesen NR, Wang XJ, Murray JD (2017) Impaired tuning of neural ensembles and the pathophysiology of schizophrenia: a translational and computational neuroscience perspective. Biol Psychiatry 81(10):874–885

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  130. Ksiazek-Winiarek DJ, Szpakowski P, Glabinski A (2015) Neural plasticity in multiple sclerosis: the functional and molecular background. Neural Plasticity

  131. La Via L, Bonini D, Russo I, Orlandi C, Barlati S, Barbon A (2012) Modulation of dendritic AMPA receptor mRNA trafficking by RNA splicing and editing. Nucleic Acids Res 41(1):617–631

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  132. Leal K, Mochida S, Scheuer T, Catterall WA (2012) Fine-tuning synaptic plasticity by modulation of CaV2. 1 channels with Ca2+ sensor proteins. Proc Natl Acad Sci 109(42):17069–17074

    CAS  PubMed  Article  Google Scholar 

  133. Lee H, Lee EJ, Song YS, Kim E (2014) Long-term depression-inducing stimuli promote cleavage of the synaptic adhesion molecule NGL-3 through NMDA receptors, matrix metalloproteinases and presenilin/γ-secretase. Philos Trans R Soc B 369(1633):20130158

    Article  CAS  Google Scholar 

  134. Lee HK, Barbarosie M, Kameyama K, Bear MF, Huganir RL (2000) Regulation of distinct AMPA receptor phosphorylation sites during bidirectional synaptic plasticity. Nature 405(6789):955–959

    CAS  PubMed  Article  Google Scholar 

  135. Lee HK, Takamiya K, Han JS, Man H, Kim CH, Rumbaugh G, Wenthold RJ (2003) Phosphorylation of the AMPA receptor GluR1 subunit is required for synaptic plasticity and retention of spatial memory. Cell 112(5):631–643

    CAS  PubMed  Article  Google Scholar 

  136. Lee HK, Takamiya K, He K, Song L, Huganir RL (2009) Specific roles of AMPA receptor subunit GluR1 (GluA1) phosphorylation sites in regulating synaptic plasticity in the CA1 region of hippocampus. J Neurophysiol 103(1):479–489

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  137. Lee Y, Zhang Y, Kim S, Han K (2018) Excitatory and inhibitory synaptic dysfunction in mania: an emerging hypothesis from animal model studies. Exp Mol Med 50(4):1–11

    PubMed  PubMed Central  Google Scholar 

  138. Lepeta K, Lourenco MV, Schweitzer BC, Martino Adami PV, Banerjee P, Catuara-Solarz S, Nadorp B (2016) Synaptopathies: synaptic dysfunction in neurological disorders–a review from students to students. J Neurochem 138(6):785–805

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  139. Lévi S, Logan SM, Tovar KR, Craig AM (2004) Gephyrin is critical for glycine receptor clustering but not for the formation of functional GABAergic synapses in hippocampal neurons. J Neurosci 24(1):207–217

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  140. Levinstein MR, Samuels BA (2014) Mechanisms underlying the antidepressant response and treatment resistance. Front Behav Neurosci 8:208

    PubMed  PubMed Central  Article  Google Scholar 

  141. Lewis DA, Gonzalez-Burgos G (2006) Pathophysiologically based treatment interventions in schizophrenia. Nat Med 12(9):1016–1022

    CAS  PubMed  Article  Google Scholar 

  142. Li B, Tadross MR, Tsien RW (2016a) Sequential ionic and conformational signaling by calcium channels drives neuronal gene expression. Science 351(6275):863–867

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  143. Li YH, Zhang N, Wang YN, Shen Y, Wang Y (2016b) Multiple faces of protein interacting with C kinase 1 (PICK1): structure, function, and diseases. Neurochem Int 98:115–121

    CAS  PubMed  Article  Google Scholar 

  144. Liao D, Hessler NA, Malinow R (1995) Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice. Nature 375(6530):400

    CAS  PubMed  Article  Google Scholar 

  145. Lisman J (1989) A mechanism for the Hebb and the anti-Hebb processes underlying learning and memory. Proc Natl Acad Sci 86(23):9574–9578

    CAS  PubMed  Article  Google Scholar 

  146. Liu W, Ge T, Leng Y, Pan Z, Fan J, Yang W, Cui R (2017) The role of neural plasticity in depression: from hippocampus to prefrontal cortex. Neural Plasticity

  147. Lledo PM, Hjelmstad GO, Mukherji S, Soderling TR, Malenka RC, Nicoll RA (1995) Calcium/calmodulin-dependent kinase II and long-term potentiation enhance synaptic transmission by the same mechanism. Proc Natl Acad Sci 92(24):11175–11179

    CAS  PubMed  Article  Google Scholar 

  148. Loebrich S, Djukic B, Tong ZJ, Cottrell JR, Turrigiano GG, Nedivi E (2013) Regulation of glutamate receptor internalization by the spine cytoskeleton is mediated by its PKA-dependent association with CPG2. Proc Natl Acad Sci 110(47):E4548–E4556

    CAS  PubMed  Article  Google Scholar 

  149. López-Bendito G, Shigemoto R, Kulik A, Vida I, Fairén A, Luján R (2004) Distribution of metabotropic GABA receptor subunits GABAB1a/b and GABAB2 in the rat hippocampus during prenatal and postnatal development. Hippocampus 14(7):836–848

    PubMed  Article  CAS  Google Scholar 

  150. Lorenzetti V, Allen NB, Fornito A, Yücel M (2009) Structural brain abnormalities in major depressive disorder: a selective review of recent MRI studies. J Affect Disord 117(1–2):1–17

    PubMed  Article  Google Scholar 

  151. Lüscher C, Malenka RC (2012) NMDA receptor-dependent long-term potentiation and long-term depression (LTP/LTD). Cold Spring Harb Perspect Biol 4(6):a005710

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  152. MacDougall MJ, Fine A (2014) The expression of long-term potentiation: reconciling the preists and the postivists. Philos Trans R Soc B 369(1633):20130135

    Article  CAS  Google Scholar 

  153. Makhinson M, Chotiner JK, Watson JB, O’Dell TJ (1999) Adenylyl cyclase activation modulates activity-dependent changes in synaptic strength and Ca2+/calmodulin-dependent kinase II autophosphorylation. J Neurosci 19(7):2500–2510

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  154. Maki BA, Popescu GK (2014) Extracellular Ca2+ ions reduce NMDA receptor conductance and gating. J Gen Physiol 144(5):379–392

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  155. Malhi GS, Mann JJ (2018) Depression. Lancet 392:2299–2312

    PubMed  Article  Google Scholar 

  156. Malinow R, Malenka RC (2002) AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 25(1):103–126

    CAS  PubMed  Article  Google Scholar 

  157. Maraschi A, Ciammola A, Folci A, Sassone F, Ronzitti G, Cappelletti G, Chieregatti E (2014) Parkin regulates kainate receptors by interacting with the GluK2 subunit. Nat Commun 5:5182

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  158. Matthews EA, Dietrich D (2015) Buffer mobility and the regulation of neuronal calcium domains. Front Cell Neurosci 9:48

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  159. Matveev V (2013) Ca 2+ buffering as a mechanism of short-term synaptic plasticity. BMC Neurosci 14(1):P269

    PubMed Central  Article  Google Scholar 

  160. Matveev V, Zucker RS, Sherman A (2004) Facilitation through buffer saturation: constraints on endogenous buffering properties. Biophys J 86(5):2691–2709

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  161. Mayford M, Siegelbaum SA, Kandel ER (2012) Synapses and memory storage. Cold Spring Harb Perspect Biol 4(6):a005751

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  162. McEwen BS, Eiland L, Hunter RG, Miller MM (2012) Stress and anxiety: structural plasticity and epigenetic regulation as a consequence of stress. Neuropharmacology 62(1):3–12

    CAS  PubMed  Article  Google Scholar 

  163. Mellone M, Stanic J, Hernandez LF, Iglesias E, Zianni E, Longhi A, Obeso JA (2015) NMDA receptor GluN2A/GluN2B subunit ratio as synaptic trait of levodopa-induced dyskinesias: from experimental models to patients. Front Cell Neurosci 9:245

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  164. Mendoza E, Miranda-Barrientos JA, Vázquez-Roque RA, Morales-Herrera E, Ruelas A, De la Rosa G, Hernández-Echeagaray E (2014) In vivo mitochondrial inhibition alters corticostriatal synaptic function and the modulatory effects of neurotrophins. Neuroscience 280:156–170

    CAS  PubMed  Article  Google Scholar 

  165. Milnerwood AJ, Cummings DM, Dallérac GM, Brown JY, Vatsavayai SC, Hirst MC, Murphy KP (2006) Early development of aberrant synaptic plasticity in a mouse model of Huntington's disease. Hum Mol Genet 15(10):1690–1703

    CAS  PubMed  Article  Google Scholar 

  166. Missler M, Südhof TC, Biederer T (2012) Synaptic cell adhesion. Cold Spring Harbor perspectives in Biology. a005694

  167. Mochida S (2019) Presynaptic calcium channels. Int J Mol Sci 20(9):2217

    CAS  PubMed Central  Article  Google Scholar 

  168. Mohn AR, Gainetdinov RR, Caron MG, Koller BH (1999) Mice with reduced NMDA receptor expression display behaviors related to schizophrenia. Cell 98(4):427–436

    CAS  PubMed  Article  Google Scholar 

  169. Moncada D, Ballarini F, Viola H (2015) Behavioral tagging: a translation of the synaptic tagging and capture hypothesis. Neural Plasticity

  170. Moosmang S, Haider N, Klugbauer N, Adelsberger H, Langwieser N, Müller J, Goebbels S (2005) Role of hippocampal Cav1. 2 Ca2+ channels in NMDA receptor-independent synaptic plasticity and spatial memory. J Neurosci 25(43):9883–9892

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  171. Morishita W, Connor JH, Xia H, Quinlan EM, Shenolikar S, Malenka RC (2001) Regulation of synaptic strength by protein phosphatase 1. Neuron 32(6):1133–1148

    CAS  PubMed  Article  Google Scholar 

  172. Moskvina V, Craddock N, Holmans P, Nikolov I, Pahwa JS, Green E, O'Donovan MC (2009) Gene-wide analyses of genome-wide association data sets: evidence for multiple common risk alleles for schizophrenia and bipolar disorder and for overlap in genetic risk. Mol Psychiatry 14(3):252

    CAS  PubMed  Article  Google Scholar 

  173. Moult PR, Gladding CM, Sanderson TM, Fitzjohn SM, Bashir ZI, Molnar E, Collingridge GL (2006) Tyrosine phosphatases regulate AMPA receptor trafficking during metabotropic glutamate receptor-mediated long-term depression. J Neurosci 26(9):2544–2554

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  174. Mulkey RM, Endo S, Shenolikar S, Malenka RC (1994) Involvement of a calcineurin/inhibitor-1 phosphatase cascade in hippocampal long-term depression. Nature 369(6480):486

    CAS  PubMed  Article  Google Scholar 

  175. Muñoz B, Fritz BM, Yin F, Atwood BK (2018) Alcohol exposure disrupts mu opioid receptor-mediated long-term depression at insular cortex inputs to dorsolateral striatum. Nat Commun 9(1):1318

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  176. Muñoz, Pablo, Carolina Estay, Paula Díaz, Claudio Elgueta, Álvaro O. Ardiles, and Pablo A. Lizana (2016) "Inhibition of DNA methylation impairs synaptic plasticity during an early time window in rats." Neural Plasticity

  177. Nanou E, Catterall WA (2018) Calcium channels, synaptic plasticity, and neuropsychiatric disease. Neuron 98(3):466–481

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  178. Nanou E, Sullivan JM, Scheuer T, Catterall WA (2016) Calcium sensor regulation of the CaV2. 1 Ca2+ channel contributes to short-term synaptic plasticity in hippocampal neurons. Proc Natl Acad Sci 113(4):1062–1067

    CAS  PubMed  Article  Google Scholar 

  179. Nanou E, Lee A, Catterall WA (2018) Control of excitation/inhibition balance in a hippocampal circuit by calcium sensor protein regulation of presynaptic calcium channels. J Neurosci 38(18):4430–4440

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  180. Neher E (1995) The use of fura-2 for estimating Ca buffers and Ca fluxes. Neuropharmacology 34(11):1423–1442

    CAS  PubMed  Article  Google Scholar 

  181. Neher E (2015) Merits and limitations of vesicle pool models in view of heterogeneous populations of synaptic vesicles. Neuron 87(6):1131–1142

    CAS  PubMed  Article  Google Scholar 

  182. Nicoll RA (2017) A brief history of long-term potentiation. Neuron 93(2):281–290

    CAS  PubMed  Article  Google Scholar 

  183. Nistico R, Mori F, Feligioni M, Nicoletti F, Centonze D (2014) Synaptic plasticity in multiple sclerosis and in experimental autoimmune encephalomyelitisPhil. Trans R Soc B 369(1633):20130162

    Article  CAS  Google Scholar 

  184. Niwa F, Bannai H, Arizono M, Fukatsu K, Triller A, Mikoshiba K (2012) Gephyrin-independent GABAAR mobility and clustering during plasticity. PLoS One 7(4):e36148

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  185. Nyegaard M, Demontis D, Thestrup BB, Hedemand A, Sørensen KM, Hansen T, Mors O (2012) No association of polymorphisms in human endogenous retrovirus K18 and CD48 with schizophrenia. Psychiatr Genet 22(3):146–148

    PubMed  Article  Google Scholar 

  186. Ostroff LE, Watson DJ, Cao G, Parker PH, Smith H, Harris KM (2018) Shifting patterns of polyribosome accumulation at synapses over the course of hippocampal long-term potentiation. Hippocampus 28(6):416–430

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  187. O'Sullivan GA, Jedlicka P, Chen HX, Kalbouneh H, Ippolito A, Deller T, Schwarzacher SW (2016) Forebrain-specific loss of synaptic GABAA receptors results in altered neuronal excitability and synaptic plasticity in mice. Mol Cell Neurosci 72:101–113

    CAS  PubMed  Article  Google Scholar 

  188. Ouattara B, Hoyer D, Grégoire L, Morissette M, Gasparini F, Gomez-Mancilla B, Di Paolo T (2010) Changes of AMPA receptors in MPTP monkeys with levodopa-induced dyskinesias. Neuroscience 167(4):1160–1167

    CAS  PubMed  Article  Google Scholar 

  189. Panzanelli P (2011) Distinct mechanisms regulate GABAA receptor and gephyrin clustering at perisomatic and axo-axonic synapses on CA1 pyramidal cells. J Physiol 589:4959–4980

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  190. Parisi L, Di Filippo T, Roccella M (2015) Autism spectrum disorder in kabuki syndrome: clinical, diagnostic and rehabilitative aspects assessed through the presentation of three cases. Minerva Pediatr 67(4):369–375

    CAS  PubMed  Google Scholar 

  191. Park J, Chávez AE, Mineur YS, Morimoto-Tomita M, Lutzu S, Kim KS, Tomita S (2016) CaMKII phosphorylation of TARPγ-8 is a mediator of LTP and learning and memory. Neuron 92(1):75–83

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  192. Park, J. W. (2014). Investigation of the molecular mechanisms of synaptic tagging and capture

    Google Scholar 

  193. Park M, Penick EC, Edwards JG, Kauer JA, Ehlers MD (2004) Recycling endosomes supply AMPA receptors for LTP. Science 305(5692):1972–1975

    CAS  PubMed  Article  Google Scholar 

  194. Park S, Park JM, Kim S, Kim JA, Shepherd JD, Smith-Hicks CL, Huganir RL (2008) Elongation factor 2 and fragile X mental retardation protein control the dynamic translation of arc/Arg3. 1 essential for mGluR-LTD. Neuron 59(1):70–83

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  195. Parkinson GT, Chamberlain SE, Jaafari N, Turvey M, Mellor JR, Hanley JG (2018) Cortactin regulates endo-lysosomal sorting of AMPARs via direct interaction with GluA2 subunit. Sci Rep 8(1):4155

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  196. Patel V, Abas M, Broadhead J, Todd C, Reeler A (2001) Depression in developing countries: lessons from Zimbabwe. Bmj 322(7284):482–484

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  197. Patrizi A, Scelfo B, Viltono L, Briatore F, Fukaya M, Watanabe M, Sassoè-Pognetto M (2008) Synapse formation and clustering of neuroligin-2 in the absence of GABAA receptors. Proc Natl Acad Sci 105(35):13151–13156

    CAS  PubMed  Article  Google Scholar 

  198. Peineau S, Taghibiglou C, Bradley C, Wong TP, Liu L, Lu J, Matthews P (2007) LTP inhibits LTD in the hippocampus via regulation of GSK3β. Neuron 53(5):703–717

    CAS  PubMed  Article  Google Scholar 

  199. Peng S, Zhang Y, Zhang J, Wang H, Ren B (2010) ERK in learning and memory: a review of recent research. Int J Mol Sci 11(1):222–232

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  200. Penke Z, Morice E, Veyrac A, Gros A, Chagneau C, LeBlanc P, Laroche S (2014) Zif268/Egr1 gain of function facilitates hippocampal synaptic plasticity and long-term spatial recognition memory. Philos Trans R Soc B 369(1633):20130159

    Article  CAS  Google Scholar 

  201. Petrini EM, Ravasenga T, Hausrat TJ, Iurilli G, Olcese U, Racine V, Medini P (2014) Synaptic recruitment of gephyrin regulates surface GABA a receptor dynamics for the expression of inhibitory LTP. Nat Commun 5:3921

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  202. Pi HJ, Otmakhov N, Lemelin D, De Koninck P, Lisman J (2010) Autonomous CaMKII can promote either long-term potentiation or long-term depression, depending on the state of T305/T306 phosphorylation. J Neurosci 30(26):8704–8709

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  203. Picconi B, Piccoli G, Calabresi P (2012) Synaptic dysfunction in Parkinson’s disease. In Synaptic Plasticity (pp. 553–572). Springer, Vienna

  204. Pignatelli M, Feligioni M, Piccinin S, Molinaro G, Nicoletti F, Nisticò R (2013) Synaptic plasticity as a therapeutic target in the treatment of autism-related single-gene disorders. Curr Pharm Des 19(36):6480–6490

    CAS  PubMed  Article  Google Scholar 

  205. Pilato F, Profice P, Ranieri F, Capone F, Di Iorio R, Florio L, Di Lazzaro V (2012) Synaptic plasticity in neurodegenerative diseases evaluated and modulated by in vivo neurophysiological techniques. Mol Neurobiol 46(3):563–571

    CAS  PubMed  Article  Google Scholar 

  206. Pin JP, Duvoisin R (1995) The metabotropic glutamate receptors: structure and functions. Neuropharmacology 34(1):1–26

    CAS  PubMed  Article  Google Scholar 

  207. Pizzarelli R, Griguoli M, Zacchi P, Petrini EM, Barberis A, Cattaneo A, Cherubini E (2019) Tuning GABAergic Inhibition: Gephyrin Molecular Organization and Functions. Neuroscience

  208. Popoli M, Yan Z, McEwen BS, Sanacora G (2012) The stressed synapse: the impact of stress and glucocorticoids on glutamate transmission. Nat Rev Neurosci 13(1):22

    CAS  Article  Google Scholar 

  209. Poulopoulos A, Aramuni G, Meyer G, Soykan T, Hoon M, Papadopoulos T, Jedlicka P (2009) Neuroligin 2 drives postsynaptic assembly at perisomatic inhibitory synapses through gephyrin and collybistin. Neuron 63(5):628–642

    CAS  PubMed  Article  Google Scholar 

  210. Qian H, Patriarchi T, Price JL, Matt L, Lee B, Nieves-Cintrón M, Catterall WA (2017) Phosphorylation of Ser1928 mediates the enhanced activity of the L-type Ca2+ channel Cav1. 2 by the β2-adrenergic receptor in neurons. Sci Signal 10(463):eaaf9659

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  211. Radley JJ, Morrison JH (2005) Repeated stress and structural plasticity in the brain. Ageing Res Rev 4(2):271–287

    PubMed  Article  Google Scholar 

  212. Rebola N, Srikumar BN, Mulle C (2010) Activity-dependent synaptic plasticity of NMDA receptors. J Physiol 588(1):93–99

    CAS  PubMed  Article  Google Scholar 

  213. Regehr WG (2012) Short-term presynaptic plasticity. Cold Spring Harb Perspect Biol 4(7):a005702

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  214. Reymann KG, Frey JU (2007) The late maintenance of hippocampal LTP: requirements, phases,‘synaptic tagging’,‘late-associativity’and implications. Neuropharmacology 52(1):24–40

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  215. Ripke S, O'Dushlaine C, Chambert K, Moran JL, Kähler AK, Akterin S, Kim Y (2013) Genome-wide association analysis identifies 13 new risk loci for schizophrenia. Nat Genet 45(10):1150

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  216. Rocher AB, Gubellini P, Merienne N, Boussicault L, Petit F, Gipchtein P, Bonvento G (2016) Synaptic scaling up in medium spiny neurons of aged BACHD mice: a slow-progression model of Huntington's disease. Neurobiol Dis 86:131–139

    CAS  PubMed  Article  Google Scholar 

  217. Rosahl TW, Geppert M, Spillane D, Herz J, Hammer RE, Malenka RC (1993) Short-term synaptic plasticity is altered in mice lacking synapsin I. Cell 75:661–670

    CAS  PubMed  Article  Google Scholar 

  218. Rosahl TW, Spillane D, Missler M, Herz J, Selig DK, Wolff JR (1995) Essential functions of synapsins I and II in synaptic vesicle regulation. Nature 375:488–493

    CAS  PubMed  Article  Google Scholar 

  219. Rosendale M, Jullié D, Choquet D, Perrais D (2017) Spatial and temporal regulation of receptor endocytosis in neuronal dendrites revealed by imaging of single vesicle formation. Cell Rep 18(8):1840–1847

    CAS  PubMed  Article  Google Scholar 

  220. Rozov A, Burnashev N, Sakmann B, Neher E (2001) Transmitter release modulation by intracellular Ca2+ buffers in facilitating and depressing nerve terminals of pyramidal cells in layer 2/3 of the rat neocortex indicates a target cell-specific difference in presynaptic calcium dynamics. J Physiol 531(3):807–826

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  221. Sabaliauskas N, Shen H, Homanics GE, Smith SS, Aoki C (2012) Knockout of the γ-aminobutyric acid receptor subunit α4 reduces functional δ-containing extrasynaptic receptors in hippocampal pyramidal cells at the onset of puberty. Brain Res 1450:11–23

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  222. Sajikumar S, Navakkode S, Frey JU (2007) Identification of compartment-and process-specific molecules required for “synaptic tagging” during long-term potentiation and long-term depression in hippocampal CA1. J Neurosci 27(19):5068–5080

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  223. Salter MW, Kalia LV (2004) Src kinases: a hub for NMDA receptor regulation. Nat Rev Neurosci 5(4):317

    CAS  PubMed  Article  Google Scholar 

  224. Sanacora G, Zarate CA, Krystal JH, Manji HK (2008) Targeting the glutamatergic system to develop novel, improved therapeutics for mood disorders. Nat Rev Drug Discov 7(5):426

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  225. Sattar Y, Wilson J, Khan AM, Adnan M, Larios DA, Shrestha S, Tariq N (2018) A review of the mechanism of antagonism of N-methyl-D-aspartate receptor by ketamine in treatment-resistant depression. Cureus 10(5)

  226. Sawa A, Snyder SH (2002) Schizophrenia: diverse approaches to a complex disease. Science 296(5568):692–695

    CAS  PubMed  Article  Google Scholar 

  227. Sawyer K, Corsentino E, Sachs-Ericsson N, Steffens DC (2012) Depression, hippocampal volume changes, and cognitive decline in a clinical sample of older depressed outpatients and non-depressed controls. Aging Ment Health 16(6):753–762

    PubMed  PubMed Central  Article  Google Scholar 

  228. Schnell E, Sizemore M, Karimzadegan S, Chen L, Bredt DS, Nicoll RA (2002) Direct interactions between PSD-95 and stargazin control synaptic AMPA receptor number. Proc Natl Acad Sci 99(21):13902–13907

    CAS  PubMed  Article  Google Scholar 

  229. Sengpiel F (2018) Overview: neuroplasticity and synaptic function in neuropsychiatric disorders. J Physiol 596(14):2745–2746

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  230. Serrano-Pozo A, Frosch MP, Masliah E, Hyman BT (2011) Neuropathological alterations in Alzheimer disease. Cold Spring Harbor Perspectives Med 1(1):a006189

    Article  CAS  Google Scholar 

  231. Serwanski DR, Miralles CP, Christie SB, Mehta AK, Li X, De Blas AL (2006) Synaptic and nonsynaptic localization of GABAA receptors containing the α5 subunit in the rat brain. J Comp Neurol 499(3):458–470

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  232. Shankar GM, Li S, Mehta TH, Garcia-Munoz A, Shepardson NE, Smith I, Regan CM (2008) Amyloid-β protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat Med 14(8):837

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  233. Shioda N, Fukunaga K (2017) Physiological and pathological roles of CaMKII-PP1 Signaling in the brain. Int J Mol Sci 19(1):20

    PubMed Central  Article  CAS  Google Scholar 

  234. Sippy T, Cruz-Martín A, Jeromin A, Schweizer FE (2003) Acute changes in short-term plasticity at synapses with elevated levels of neuronal calcium sensor-1. Nat Neurosci 6(10):1031

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  235. Slutsky I, Abumaria N, Wu LJ, Huang C, Zhang L, Li B, Tonegawa S (2010) Enhancement of learning and memory by elevating brain magnesium. Neuron 65(2):165–177

    CAS  PubMed  Article  Google Scholar 

  236. Smolen P (2015) Modeling maintenance of long-term potentiation in clustered synapses: long-term memory without bistability. Neural Plasticity:2015

  237. Smolen P, Baxter DA, Byrne JH (2012) Molecular constraints on synaptic tagging and maintenance of long-term potentiation: a predictive model. PLoS Comput Biol 8(8):e1002620

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  238. Snyder EM, Colledge M, Crozier RA, Chen WS, Scott JD, Bear MF (2005) Role for a kinase anchoring proteins (AKAPs) in glutamate receptor trafficking and long-term synaptic depression. J Biol Chem

  239. Somogyi P, Tamas G, Lujan R, Buhl EH (1998) Salient features of synaptic organisation in the cerebral cortex. Brain Res Rev 26(2–3):113–135

    CAS  PubMed  Article  Google Scholar 

  240. Song Q, Zheng HW, Li XH, Huganir RL, Kuner T, Zhuo M, Chen T (2017) Selective phosphorylation of AMPA receptor contributes to the network of long-term potentiation in the anterior cingulate cortex. J Neurosci 0925–17

  241. Spires TL, Meyer-Luehmann M, Stern EA, McLean PJ, Skoch J, Nguyen PT, Hyman BT (2005) Dendritic spine abnormalities in amyloid precursor protein transgenic mice demonstrated by gene transfer and intravital multiphoton microscopy. J Neurosci 25(31):7278–7287

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  242. Stefansson H, Petursson H, Sigurdsson E, Steinthorsdottir V, Bjornsdottir S, Sigmundsson T, Chou TT (2002) Neuregulin 1 and susceptibility to schizophrenia. Am J Hum Genet 71(4):877–892

    PubMed  PubMed Central  Article  Google Scholar 

  243. Stein V, House DR, Bredt DS, Nicoll RA (2003) Postsynaptic density-95 mimics and occludes hippocampal long-term potentiation and enhances long-term depression. J Neurosci 23(13):5503–5506

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  244. Steinberg JP, Huganir RL, Linden DJ (2004) N-ethylmaleimide-sensitive factor is required for the synaptic incorporation and removal of AMPA receptors during cerebellar long-term depression. Proc Natl Acad Sci 101(52):18212–18216

    CAS  PubMed  Article  Google Scholar 

  245. Suarez LM, Solis O, Aguado C, Lujan R, Moratalla R (2016) L-DOPA oppositely regulates synaptic strength and spine morphology in D1 and D2 striatal projection neurons in dyskinesia. Cereb Cortex 26(11):4253–4264

    PubMed  PubMed Central  Article  Google Scholar 

  246. Südhof TC, Malenka RC (2008) Understanding synapses: past, present, and future. Neuron 60(3):469–476

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  247. Surmeier DJ, Graves SM, Shen W (2014) Dopaminergic modulation of striatal networks in health and Parkinson's disease. Curr Opin Neurobiol 29:109–117

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  248. Sweatt JD (2004) Mitogen-activated protein kinases in synaptic plasticity and memory. Curr Opin Neurobiol 14(3):311–317

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  249. Sweatt JD (1999) Toward a molecular explanation for long-term potentiation. Learn Mem 6(5):399–416

    CAS  PubMed  Article  Google Scholar 

  250. Tamano H, Morioka H, Nishio R, Takeuchi A, Takeda A (2018) AMPA-induced extracellular Zn2+ influx into nigral dopaminergic neurons causes movement disorder in rats. Neurotoxicology 69:23–28

    CAS  PubMed  Article  Google Scholar 

  251. Tamas G, Buhl EH, Somogyi P (1997) Fast IPSPs elicited via multiple synaptic release sites by different types of GABAergic neurone in the cat visual cortex. J Physiol 500(3):715–738

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  252. Thomas GM, Huganir RL (2004) MAPK cascade signalling and synaptic plasticity. Nat Rev Neurosci 5(3):173

    CAS  PubMed  Article  Google Scholar 

  253. Thompson SM, Kallarackal AJ, Kvarta MD, Van Dyke AM, LeGates TA, Cai X (2015) An excitatory synapse hypothesis of depression. Trends Neurosci 38(5):279–294

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  254. Tomita S, Stein V, Stocker TJ, Nicoll RA, Bredt DS (2005) Bidirectional synaptic plasticity regulated by phosphorylation of stargazin-like TARPs. Neuron 45(2):269–277

    CAS  PubMed  Article  Google Scholar 

  255. Tretter V et al (2012) Gephyrin, the enigmatic organizer at GABAergic synapses. Front Cell Neurosci 6:23

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  256. Tsui J, Malenka RC (2006) Substrate localization creates specificity in calcium/calmodulin-dependent protein kinase II signaling at synapses. J Biol Chem 281(19):13794–13804

    CAS  PubMed  Article  Google Scholar 

  257. Tsujimoto T, Jeromin A, Saitoh N, Roder JC, Takahashi T (2002) Neuronal calcium sensor 1 and activity-dependent facilitation of P/Q-type calcium currents at presynaptic nerve terminals. Science 295(5563):2276–2279

    CAS  PubMed  Article  Google Scholar 

  258. Turecek J, Regehr WG (2018) Synaptotagmin 7 mediates both facilitation and asynchronous release at granule cell synapses. J Neurosci 38(13):3240–3251

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  259. Turrigiano G (2012) Homeostatic synaptic plasticity: local and global mechanisms for stabilizing neuronal function. Cold Spring Harb Perspect Biol 4(1):a005736

    PubMed  PubMed Central  Article  Google Scholar 

  260. Turrigiano GG, Nelson SB (2004) Homeostatic plasticity in the developing nervous system. Nat Rev Neurosci 5(2):97

    CAS  PubMed  Article  Google Scholar 

  261. Tyagarajan SK, Fritschy JM (2014) Gephyrin: a master regulator of neuronal function? Nat Rev Neurosci 15:141–156

    CAS  PubMed  Article  Google Scholar 

  262. Tyagarajan SK, Ghosh H, Yévenes GE, Nikonenko I, Ebeling C, Schwerdel C, Fritschy JM (2011) Regulation of GABAergic synapse formation and plasticity by GSK3β-dependent phosphorylation of gephyrin. Proc Natl Acad Sci 108(1):379–384

    CAS  PubMed  Article  Google Scholar 

  263. Tyagarajan SK, Ghosh H, Yévenes GE, Imanishi SY, Zeilhofer HU, Gerrits B, Fritschy JM (2013) Extracellular signal-regulated kinase and glycogen synthase kinase 3β regulate gephyrin postsynaptic aggregation and GABAergic synaptic function in a calpain-dependent mechanism. J Biol Chem 288(14):9634–9647

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  264. Usdin MT, Shelbourne PF, Myers RM, Madison DV (1999) Impaired synaptic plasticity in mice carrying the Huntington's disease mutation. Hum Mol Genet 8(5):839–846

    CAS  PubMed  Article  Google Scholar 

  265. Vickers CA, Dickson KS, Wyllie DJA (2005) Induction and maintenance of late-phase long-term potentiation in isolated dendrites of rat hippocampal CA1 pyramidal neurones. J Physiol 568(3):803–813

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  266. Villalba RM, Smith Y (2018) Loss and remodeling of striatal dendritic spines in Parkinson’s disease: from homeostasis to maladaptive plasticity? J Neural Transm 125(3):431–447

    PubMed  Article  Google Scholar 

  267. Volianskis A, France G, Jensen MS, Bortolotto ZA, Jane DE, Collingridge GL (2015) Long-term potentiation and the role of N-methyl-D-aspartate receptors. Brain Res 1621:5–16

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  268. Vyleta NP, Jonas P (2014) Loose coupling between Ca2+ channels and release sensors at a plastic hippocampal synapse. Science 343(6171):665–670

    CAS  PubMed  Article  Google Scholar 

  269. Wang JK, Langfelder P, Horvath S, Palazzolo MJ (2017) Exosomes and homeostatic synaptic plasticity are linked to each other and to Huntington's, Parkinson's, and other neurodegenerative diseases by database-enabled analyses of comprehensively curated datasets. Front Neurosci 11:149

    PubMed  PubMed Central  Google Scholar 

  270. Wang YT (2008) Probing the role of AMPAR endocytosis and long-term depression in behavioural sensitization: relevance to treatment of brain disorders, including drug addiction. Br J Pharmacol 153(S1)

  271. Washbourne P, Dityatev A, Scheiffele P, Biederer T, Weiner JA, Christopherson KS, El-Husseini A (2004) Cell adhesion molecules in synapse formation. J Neurosci 24(42):9244–9249

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  272. Waung MW, Pfeiffer BE, Nosyreva ED, Ronesi JA, Huber KM (2008) Rapid translation of arc/Arg3. 1 selectively mediates mGluR-dependent LTD through persistent increases in AMPAR endocytosis rate. Neuron 59(1):84–97

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  273. Weyrer C, Turecek J, Niday Z, Liu PW, Nanou E, Catterall WA, Regehr WG (2019) The role of cav2. 1 channel facilitation in synaptic facilitation. Cell Rep 26(9):2289–2297

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  274. Wiera G, Nowak D, Van Hove I, Dziegiel P, Moons L, Mozrzymas JW (2017) Mechanisms of NMDA receptor-and voltage-gated L-type calcium channel-dependent hippocampal LTP critically rely on proteolysis that is mediated by distinct metalloproteinases. J Neurosci 37(5):1240–1256

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  275. Xie M, Li X, Han J, Vogt DL, Wittemann S, Mark MD, Herlitze S (2007) Facilitation versus depression in cultured hippocampal neurons determined by targeting of Ca2+ channel Cavβ4 versus Cavβ2 subunits to synaptic terminals. J Cell Biol 178(3):489–502

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  276. Xu J, Wu LG (2005) The decrease in the presynaptic calcium current is a major cause of short-term depression at a calyx-type synapse. Neuron 46(4):633–645

    CAS  PubMed  Article  Google Scholar 

  277. Xu J, He L, Wu LG (2007) Role of Ca2+ channels in short-term synaptic plasticity. Curr Opin Neurobiol 17(3):352–359

    CAS  PubMed  Article  Google Scholar 

  278. Yan J, Leal K, Magupalli VG, Nanou E, Martinez GQ, Scheuer T, Catterall WA (2014) Modulation of CaV2.1 channels by neuronal calcium sensor-1 induces short-term synaptic facilitation. Mol Cell Neurosci 63:124–131

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  279. Yizhar O, Fenno LE, Prigge M, Schneider F, Davidson TJ, O’shea DJ et al (2011) Neocortical excitation/inhibition balance in information processing and social dysfunction. Nature 477(7363):171–178

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  280. Yoo J, Bakes J, Bradley C, Collingridge GL, Kaang BK (2014) Shank mutant mice as an animal model of autism. Philos Trans R Soc Lond Ser B Biol Sci 369(1633):20130143

    Article  CAS  Google Scholar 

  281. Yoshioka M, Yamazaki Y, Fujii S, Kaneko K, Kato H, Mikoshiba K (2010) Intracellular calcium ion dynamics involved in long-term potentiation in hippocampal CA1 neurons in mice lacking the IP 3 type 1 receptor. Neurosci Res 67(2):149–155

    CAS  PubMed  Article  Google Scholar 

  282. Yu W, Lu B (2012) Synapses and dendritic spines as pathogenic targets in Alzheimer’s disease. Neural Plasticity 2012

  283. Zengel JE, Magleby KL (1982) Augmentation and facilitation of transmitter release. A quantitative description at the frog neuromuscular junction. J Gen Physiol 80:583–611

    CAS  PubMed  Article  Google Scholar 

  284. Zhai S, Shen W, Graves SM, Surmeier DJ (2019) Dopaminergic modulation of striatal function and Parkinson’s disease. J Neural Transm 126(4):411–422

    CAS  PubMed  Article  Google Scholar 

  285. Zhang H, Gong B, Liu S, Fa M, Ninan I, Staniszewski A, Arancio O (2005) Synaptic fatigue is more pronounced in the APP/PS1 transgenic mouse model of Alzheimer's disease. Curr Alzheimer Res 2(2):137–140

    CAS  PubMed  Article  Google Scholar 

  286. Zhang Y, Venkitaramani DV, Gladding CM, Zhang Y, Kurup P, Molnar E, Lombroso PJ (2008) The tyrosine phosphatase STEP mediates AMPA receptor endocytosis after metabotropic glutamate receptor stimulation. J Neurosci 28(42):10561–10566

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  287. Zhang Z, Zhang S, Fu P, Zhang Z, Lin K, Ko JKS, Yung KKL (2019) Roles of glutamate receptors in Parkinson’s disease. Int J Mol Sci 20(18):4391

    CAS  PubMed Central  Article  Google Scholar 

  288. Zhao JP, Murata Y, Constantine-Paton M (2013) Eye opening and PSD95 are required for long-term potentiation in developing superior colliculus. Proc Natl Acad Sci 110(2):707–712

    CAS  PubMed  Article  Google Scholar 

  289. Zhu JJ, Qin Y, Zhao M, Van Aelst L, Malinow R (2002) Ras and rap control AMPA receptor trafficking during synaptic plasticity. Cell 110(4):443–455

    CAS  PubMed  Article  Google Scholar 

  290. Zhu Y, Pak D, Qin Y, McCormack SG, Kim MJ, Baumgart JP, Sheng M (2005) Rap2-JNK removes synaptic AMPA receptors during depotentiation. Neuron 46(6):905–916

    CAS  PubMed  Article  Google Scholar 

  291. Zhu PJ, Chen CJ, Mays J, Stoica L, Costa-Mattioli M (2018a) mTORC2, but not mTORC1, is required for hippocampal mGluR-LTD and associated behaviors. Nat Neurosci

  292. Zhu M, Cortese G, Waites C (2018b) Parkinson's disease-linked Parkin mutations impair glutamatergic synaptic transmission and plasticity. bioRxiv, 373597

  293. Ziff EB (2007) TARPs and the AMPA receptor trafficking paradox. Neuronl 53(5):627–633

    CAS  Article  Google Scholar 

  294. Zucker RS, Regehr WG (2002) Short-term synaptic plasticity. Annu Rev Physiol 64:355–405

    CAS  PubMed  Article  Google Scholar 

Download references

Author information

Affiliations

Authors

Contributions

YKD and DS designed the study, wrote the manuscript, and finalized it. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Divakar Sharma.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Dhuriya, Y.K., Sharma, D. Neuronal Plasticity: Neuronal Organization is Associated with Neurological Disorders. J Mol Neurosci (2020). https://doi.org/10.1007/s12031-020-01555-2

Download citation

Keywords

  • Neuronal plasticity
  • Short-term plasticity
  • Long-term potentiation
  • Neurodegenerative diseases
  • AMPAR
  • NMDAR