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Cited by 175Neuroscience and Neuropharmacology ResearchMemory and Neural MechanismsNeurotransmitter Receptor Influence on Behavior

Long-Term Plasticity of Neurotransmitter Release: Emerging Mechanisms and Contributions to Brain Function and Disease

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Monday, Hannah R., Younts, Thomas J., Castillo, Pablo E.·2018·Annual Review of Neuroscience
DOI 10.1146/annurev-neuro-080317-062155PMC PMC6238218
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Abstract

Long-lasting changes of brain function in response to experience rely on diverse forms of activity-dependent synaptic plasticity. Chief among them are long-term potentiation and long-term depression of neurotransmitter release, which are widely expressed by excitatory and inhibitory synapses throughout the central nervous system and can dynamically regulate information flow in neural circuits. This review article explores recent advances in presynaptic long-term plasticity mechanisms and contributions to circuit function. Growing evidence indicates that presynaptic plasticity may involve structural changes, presynaptic protein synthesis, and transsynaptic signaling. Presynaptic long-term plasticity can alter the short-term dynamics of neurotransmitter release, thereby contributing to circuit computations such as novelty detection, modifications of the excitatory/inhibitory balance, and sensory adaptation. In addition, presynaptic long-term plasticity underlies forms of learning and its dysregulation participates in several neuropsychiatric conditions, including schizophrenia, autism, intellectual disabilities, neurodegenerative diseases, and drug abuse.

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  1. Abbott LF, Regehr WG. 2004 Synaptic computation. Nature 431: 796– 803 15483601
  2. Acuna C, Liu X, Gonzalez A, Südhof TC. 2015 RIM-BPs mediate tight coupling of action potentials to Ca2+-triggered neurotransmitter release. Neuron 87: 1234– 47 26402606
  3. Ahmed MS, Siegelbaum SA. 2009 Recruitment of N-type Ca2+ channels during LTP enhances low release efficacy of hippocampal CA1 perforant path synapses. Neuron 63: 372– 85 19679076 PMC2746441
  4. Akins MR, Berk-Rauch HE, Kwan KY, Mitchell ME, Shepard KA, 2017 Axonal ribosomes and mRNAs associate with fragile X granules in adult rodent and human brains. Hum. Mol. Genet 26: 192– 209 28082376 PMC5815656
  5. Alvarez J, Giuditta A, Koenig E. 2000 Protein synthesis in axons and terminals: significance for maintenance, plasticity and regulation of phenotype. With a critique of slow transport theory. Prog. Neurobiol 62: 1– 62 10821981
  6. Anderson GR, Aoto J, Tabuchi K, Foldy C, Covy J, 2015 β-neurexins control neural circuits by regulating synaptic endocannabinoid signaling. Cell 162: 593– 606 26213384 PMC4709013
  7. 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– 54 27282393 PMC4961031
  8. Atwood BK, Lovinger DM, Mathur BN. 2014 Presynaptic long-term depression mediated by Gi/o-coupled receptors. Trends Neurosci. 37: 663– 73 25160683 PMC4252515
  9. Atwood HL, Wojtowicz JM. 1999 Silent synapses in neural plasticity: current evidence. Learn. Mem 6: 542– 71 10641762
  10. Basu J, Srinivas KV, Cheung SK, Taniguchi H, Huang ZJ, Siegelbaum SA. 2013 A corticohippocampal learning rule shapes inhibitory microcircuit activity to enhance hippocampal information flow. Neuron 79: 1208– 21 24050406 PMC3836574
  11. Bauer EP, LeDoux JE. 2004 Heterosynaptic long-term potentiation of inhibitory interneurons in the lateral amygdala. J. Neurosci 24: 9507– 12 15509737 PMC6730154
  12. Becker N, Wierenga CJ, Fonseca R, Bonhoeffer T, Nagerl UV. 2008 LTD induction causes morphological changes of presynaptic boutons and reduces their contacts with spines. Neuron 60: 590– 97 19038217
  13. Blundell J, Kaeser PS, Südhof TC, Powell CM. 2010 RIM1α and interacting proteins involved in presynaptic plasticity mediate prepulse inhibition and additional behaviors linked to schizophrenia. J. Neurosci 30: 5326– 33 20392954 PMC2860606
  14. Bocklisch C, Pascoli V, Wong JC, House DR, Yvon C, 2013 Cocaine disinhibits dopamine neurons by potentiation of GABA transmission in the ventral tegmental area. Science 341: 1521– 25 24072923
  15. Bolshakov VY, Golan H, Kandel ER, Siegelbaum SA. 1997 Recruitment of new sites of synaptic transmission during the cAMP-dependent late phase of LTP at CA3-CA1 synapses in the hippocampus. Neuron 19: 635– 51 9331354
  16. Bourne JN, Chirillo MA, Harris KM. 2013 Presynaptic ultrastructural plasticity along CA3→CA1 axons during long-term potentiation in mature hippocampus. J. Comp. Neurol 521: 3898– 912 23784793 PMC3838200
  17. Broek JAC, Lin Z, de Gruiter HM, van’t Spijker H, Haasdijk ED, 2016 Synaptic vesicle dynamic changes in a model of fragile X. Mol. Autism 7: 17 26933487 PMC4772588
  18. Buonanno A 2010 The neuregulin signaling pathway and schizophrenia: from genes to synapses and neural circuits. Brain Res. Bull 83: 122– 31 20688137 PMC2958213
  19. Buzsaki G 2010 Neural syntax: cell assemblies, synapsembles, and readers. Neuron 68: 362– 85 21040841 PMC3005627
  20. Castillo PE. 2012 Presynaptic LTP and LTD of excitatory and inhibitory synapses. Cold Spring Harb. Perspect. Biol 4: a005728 22147943 PMC3281573
  21. Castillo PE, Chiu CQ, Carroll RC. 2011 Long-term plasticity at inhibitory synapses. Curr. Opin. Neurobiol 21: 328– 38 21334194 PMC3092861
  22. Castillo PE, Younts TJ, Chávez AE, Hashimotodani Y. 2012 Endocannabinoid signaling and synaptic function. Neuron 76: 70– 81 23040807 PMC3517813
  23. Chaudhuri R, Fiete I. 2016 Computational principles of memory. Nat. Neurosci 19: 394– 403 26906506
  24. Cheng F, Vivacqua G, Yu S. 2011 The role of α-synuclein in neurotransmission and synaptic plasticity. J. Chem. Neuroanat 42: 242– 48 21167933
  25. Cho JH, Deisseroth K, Bolshakov VY. 2013 Synaptic encoding of fear extinction in mPFC-amygdala circuits. Neuron 80: 1491– 507 24290204 PMC3872173
  26. Cho RW, Buhl LK, Volfson D, Tran A, Li F, 2015 Phosphorylation of complexin by PKA regulates activity-dependent spontaneous neurotransmitter release and structural synaptic plasticity. Neuron 88: 749– 61 26590346 PMC4847943
  27. Christie SB, Akins MR, Schwob JE, Fallon JR. 2009 The FXG: a presynaptic fragile X granule expressed in a subset of developing brain circuits. J. Neurosci 29: 1514– 24 19193898 PMC2746438
  28. Cingolani LA, Goda Y. 2008 Actin in action: the interplay between the actin cytoskeleton and synaptic efficacy. Nat. Rev. Neurosci 9: 344– 56 18425089
  29. Contractor A, Rogers C, Maron C, Henkemeyer M, Swanson GT, Heinemann SF. 2002 Trans-synaptic Eph receptor-ephrin signaling in hippocampal mossy fiber LTP. Science 296: 1864– 69 12052960
  30. Costa RP, Mizusaki BE, Sjöström PJ, van Rossum MC. 2017 Functional consequences of pre- and postsynaptic expression of synaptic plasticity. Philos. Trans. R. Soc. B 372: 20160153 PMC5247585 28093547
  31. 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 25505409 PMC4243504
  32. Crawford DC, Chang CY, Hyrc KL, Mennerick S. 2011 Calcium-independent inhibitory G-protein signaling induces persistent presynaptic muting of hippocampal synapses. J. Neurosci 31: 979– 91 21248122 PMC3311872
  33. Crawford DC, Mennerick S. 2012 Presynaptically silent synapses: dormancy and awakening of presynaptic vesicle release. Neuroscientist 18: 216– 23 21908849 PMC3951726
  34. Dalva MB, McClelland AC, Kayser MS. 2007 Cell adhesion molecules: signalling functions at the synapse. Nat. Rev. Neurosci 8: 206– 20 17299456 PMC4756920
  35. Darnell JC, Klann E. 2013 The translation of translational control by FMRP: therapeutic targets for FXS. Nat. Neurosci 16: 1530– 36 23584741 PMC3999698
  36. Davis GW, Müller M. 2015 Homeostatic control of presynaptic neurotransmitter release. Annu. Rev. Physiol 77: 251– 70 25386989
  37. Deguchi Y, Harada M, Shinohara R, Lazarus M, Cherasse Y, 2016 mDia and ROCK mediate actin-dependent presynaptic remodeling regulating synaptic efficacy and anxiety. Cell Rep. 17: 2405– 17 27880913
  38. Deneve S, Alemi A, Bourdoukan R. 2017 The brain as an efficient and robust adaptive learner. Neuron 94: 969– 77 28595053
  39. Earls LR, Zakharenko SS. 2014 A synaptic function approach to investigating complex psychiatric diseases. Neuroscientist 20: 257– 71 23907185 PMC4057991
  40. Eggermann E, Bucurenciu I, Goswami SP, Jonas P. 2011 Nanodomain coupling between Ca2+ channels and sensors of exocytosis at fast mammalian synapses. Nat. Rev. Neurosci 13: 7– 21 22183436 PMC3617475
  41. Evstratova A, Tóth K. 2014 Information processing and synaptic plasticity at hippocampal mossy fiber terminals. Front. Cell Neurosci. 8: 28 24550783 PMC3912358
  42. Fernandes HB, Riordan S, Nomura T, Remmers CL, Kraniotis S, 2015 Epac2 mediates cAMP-dependent potentiation of neurotransmission in the hippocampus. J. Neurosci 35: 6544– 53 25904804 PMC4405561
  43. Fernandez-Busnadiego R, Asano S, Oprisoreanu AM, Sakata E, Doengi M, 2013 Cryo-electron tomography reveals a critical role of RIM1alpha in synaptic vesicle tethering. J Cell Biol 201: 725– 40 23712261 PMC3664715
  44. Ferron L, Nieto-Rostro M, Cassidy JS, Dolphin AC. 2014 Fragile X mental retardation protein controls synaptic vesicle exocytosis by modulating N-type calcium channel density. Nat. Commun 5: 3628 24709664 PMC3982139
  45. Forner S, Baglietto-Vargas D, Martini AC, Trujillo-Estrada L, LaFerla FM. 2017 Synaptic impairment in Alzheimer’s disease: a dysregulated symphony. Trends Neurosci. 40: 347– 57 28494972
  46. Fourcaudot E, Gambino F, Casassus G, Poulain B, Humeau Y, Luthi A. 2009 L-type voltage-dependent Ca2+ channels mediate expression of presynaptic LTP in amygdala. Nat. Neurosci 12: 1093– 95 19648911
  47. Fourgeaud L, Mato S, Bouchet D, Hemar A, Worley PF, Manzoni OJ. 2004 A single in vivo exposure to cocaine abolishes endocannabinoid-mediated long-term depression in the nucleus accumbens. J. Neurosci 24: 6939– 45 15295029 PMC6729592
  48. Frias CP, Wierenga CJ. 2013 Activity-dependent adaptations in inhibitory axons. Front. Cell Neurosci 7: 219 24312009 PMC3836028
  49. Froemke RC. 2015 Plasticity of cortical excitatory-inhibitory balance. Annu. Rev. Neurosci 38: 195– 219 25897875 PMC4652600
  50. Froemke RC, Carcea I, Barker AJ, Yuan K, Seybold BA, 2013 Long-term modification of cortical synapses improves sensory perception. Nat. Neurosci 16: 79– 88 23178974 PMC3711827
  51. Galimberti I, Gogolla N, Alberi S, Santos AF, Müller D, Caroni P. 2006 Long-term rearrangements of hippocampal mossy fiber terminal connectivity in the adult regulated by experience. Neuron 50: 749– 63 16731513
  52. García-Morales V, Montero F, Moreno-López B. 2015 Cannabinoid agonists rearrange synaptic vesicles at excitatory synapses and depress motoneuron activity in vivo. Neuropharmacology 92: 69– 79 25595101
  53. Gibson JR, Huber KM, Südhof TC. 2009 Neuroligin-2 deletion selectively decreases inhibitory synaptic transmission originating from fast-spiking but not from somatostatin-positive interneurons. J. Neurosci 29: 13883– 97 19889999 PMC2814361
  54. Glebov OO, Jackson RE, Winterflood CM, Owen DM, Barker EA, 2017 Nanoscale structural plasticity of the active zone matrix modulates presynaptic function. Cell Rep. 18: 2715– 28 28297674 PMC5368346
  55. Gogolla N, Galimberti I, Caroni P. 2007 Structural plasticity of axon terminals in the adult. Curr. Opin. Neurobiol 17: 516– 24 17950593
  56. Gogolla N, Galimberti I, Deguchi Y, Caroni P. 2009 Wnt signaling mediates experience-related regulation of synapse numbers and mossy fiber connectivities in the adult hippocampus. Neuron 62: 510– 25 19477153
  57. Gómez-Gonzalo M, Navarrete M, Perea G, Covelo A, Martín-Fernández M, 2015 Endocannabinoids induce lateral long-term potentiation of transmitter release by stimulation of gliotransmission. Cereb. Cortex 25: 3699– 712 25260706
  58. Hagena H, Manahan-Vaughan D. 2011 Learning-facilitated synaptic plasticity at CA3 mossy fiber and commissural-associational synapses reveals different roles in information processing. Cereb. Cortex 21: 2442– 49 21493717 PMC3183418
  59. Han Y, Kaeser PS, Südhof TC, Schneggenburger R. 2011 RIM determines Ca2+ channel density and vesicle docking at the presynaptic active zone. Neuron 69: 304– 16 21262468 PMC3259453
  60. Harris JJ, Jolivet R, Attwell D. 2012 Synaptic energy use and supply. Neuron 75: 762– 77 22958818
  61. Hayashi-Takagi A, Yagishita S, Nakamura M, Shirai F, Wu YI, 2015 Labelling and optical erasure of synaptic memory traces in the motor cortex. Nature 525: 333– 38 26352471 PMC4634641
  62. Hegde AN. 2017 Proteolysis, synaptic plasticity and memory. Neurobiol. Learn. Mem 138: 98– 110 27614141 PMC5336522
  63. Hennequin G, Agnes EJ, Vogels TP. 2017 Inhibitory plasticity: balance, control, and codependence. Annu. Rev. Neurosci 40: 557– 79 28598717
  64. Hoffman AF, Oz M, Caulder T, Lupica CR. 2003 Functional tolerance and blockade of long-term depression at synapses in the nucleus accumbens after chronic cannabinoid exposure. J. Neurosci 23: 4815– 20 12832502 PMC6741179
  65. Holtmaat A, Caroni P. 2016 Functional and structural underpinnings of neuronal assembly formation in learning. Nat. Neurosci 19: 1553– 62 27749830
  66. Hsiao K, Harony-Nicolas H, Buxbaum JD, Bozdagi-Gunal O, Benson DL. 2016 Cyfip1 regulates presynaptic activity during development. J. Neurosci 36: 1564– 76 26843638 PMC4737770
  67. Huang YY, Kandel ER. 1998 Postsynaptic induction and PKA-dependent expression of LTP in the lateral amygdala. Neuron 21: 169– 78 9697861
  68. Humeau Y, Shaban H, Bissiere S, Luthi A. 2003 Presynaptic induction of heterosynaptic associative plasticity in the mammalian brain. Nature 426: 841– 45 14685239
  69. Jackman SL, Regehr WG. 2017 The mechanisms and functions of synaptic facilitation. Neuron 94: 447– 64 28472650 PMC5865607
  70. Jang S, Lee H, Kim E. 2017 Synaptic adhesion molecules and excitatory synaptic transmission. Curr. Opin. Neurobiol 45: 45– 50 28390263
  71. Jedlicka P, Hoon M, Papadopoulos T, Vlachos A, Winkels R, 2011 Increased dentate gyrus excitability in neuroligin-2-deficient mice in vivo. Cereb. Cortex 21: 357– 67 20530218
  72. Jiang X, Litkowski PE, Taylor AA, Lin Y, Snider BJ, Moulder KL. 2010 A role for the ubiquitin-proteasome system in activity-dependent presynaptic silencing. J. Neurosci 30: 1798– 809 20130189 PMC2824895
  73. Jones BW, Deem J, Younts TJ, Weisenhaus M, Sanford CA, 2016 Targeted deletion of AKAP7 in dentate granule cells impairs spatial discrimination. eLife 5: e20695 27911261 PMC5135391
  74. Jourdain P, Bergersen LH, Bhaukaurally K, Bezzi P, Santello M, 2007 Glutamate exocytosis from astrocytes controls synaptic strength. Nat. Neurosci 10: 331– 39 17310248
  75. Jung KM, Sepers M, Henstridge CM, Lassalle O, Neuhofer D, 2012 Uncoupling of the endocannabinoid signalling complex in a mouse model of fragile X syndrome. Nat. Commun 3: 1080 23011134 PMC3657999
  76. Kaeser-Woo YJ, Younts TJ, Yang X, Zhou P, Wu D, 2013 Synaptotagmin-12 phosphorylation by cAMP-dependent protein kinase is essential for hippocampal mossy fiber LTP. J. Neurosci 33: 9769– 80 23739973 PMC3703303
  77. Katayama N, Yamamori S, Fukaya M, Kobayashi S, Watanabe M, 2017 SNAP-25 phosphorylation at Ser187 regulates synaptic facilitation and short-term plasticity in an age-dependent manner. Sci. Rep 7: 7996 28801590 PMC5554206
  78. Koga K, Liu MG, Qiu S, Song Q, O’Den G, 2015 Impaired presynaptic long-term potentiation in the anterior cingulate cortex of Fmr1 knock-out mice. J. Neurosci 35: 2033– 43 25653361 PMC6705363
  79. Kreitzer AC, Malenka RC. 2008 Striatal plasticity and basal ganglia circuit function. Neuron 60: 543– 54 19038213 PMC2724179
  80. Krueger DD, Tuffy LP, Papadopoulos T, Brose N. 2012 The role of neurexins and neuroligins in the formation, maturation, and function of vertebrate synapses. Curr. Opin. Neurobiol 22: 412– 22 22424845
  81. Kvajo M, McKellar H, Drew LJ, Lepagnol-Bestel AM, Xiao L, 2011 Altered axonal targeting and short-term plasticity in the hippocampus of Disc1 mutant mice. PNAS 108: E1349– 58 22049344 PMC3241761
  82. Larsen RS, Sjöström PJ. 2015 Synapse-type-specific plasticity in local circuits. Curr. Opin. Neurobiol 35: 127– 35 26310110 PMC5280068
  83. Lisman JE. 1997 Bursts as a unit of neural information: making unreliable synapses reliable. Trends Neurosci. 20: 38– 43 9004418
  84. Liu QS, Pu L, Poo MM. 2005 Repeated cocaine exposure in vivo facilitates LTP induction in midbrain dopamine neurons. Nature 437: 1027– 31 16222299 PMC1457101
  85. Liu S, Ninan I, Antonova I, Battaglia F, Trinchese F, 2004 α-Synuclein produces a long-lasting increase in neurotransmitter release. EMBO J. 23: 4506– 16 15510220 PMC526467
  86. Losonczy A, Biro AA, Nusser Z. 2004 Persistently active cannabinoid receptors mute a subpopulation of hippocampal interneurons. PNAS 101: 1362– 67 14734812 PMC337058
  87. Lu Y, Sun XD, Hou FQ, Bi LL, Yin DM, 2014 Maintenance of GABAergic activity by neuregulin 1-ErbB4 in amygdala for fear memory. Neuron 84: 835– 46 25451196
  88. Lüscher C, Malenka RC. 2011 Drug-evoked synaptic plasticity in addiction: from molecular changes to circuit remodeling. Neuron 69: 650– 63 21338877 PMC4046255
  89. Lutz B 2007 The endocannabinoid system and extinction learning. Mol. Neurobiol 36: 92– 101 17952654
  90. Ma L, Zablow L, Kandel ER, Siegelbaum SA. 1999 Cyclic AMP induces functional presynaptic boutons in hippocampal CA3-CA1 neuronal cultures. Nat. Neurosci 2: 24– 30 10195176
  91. Markram H, Tsodyks M. 1996 Redistribution of synaptic efficacy between neocortical pyramidal neurons. Nature 382: 807– 10 8752273
  92. Maruo T, Mandai K, Takai Y, Mori M. 2016 Activity-dependent alteration of the morphology of a hippocampal giant synapse. Mol. Cell Neurosci 71: 25– 33 26687760
  93. Mato S, Chevaleyre V, Robbe D, Pazos A, Castillo PE, Manzoni OJ. 2004 A single in-vivo exposure to Δ9THC blocks endocannabinoid-mediated synaptic plasticity. Nat. Neurosci 7: 585– 86 15146190
  94. Mato S, Robbe D, Puente N, Grandes P, Manzoni OJ. 2005 Presynaptic homeostatic plasticity rescues long-term depression after chronic Δ9-tetrahydrocannabinol exposure. J. Neurosci 25: 11619– 27 16354920 PMC6726043
  95. McKernan MG, Shinnick-Gallagher P. 1997 Fear conditioning induces a lasting potentiation of synaptic currents in vitro. Nature 390: 607– 11 9403689
  96. Meyer D, Bonhoeffer T, Scheuss V. 2014 Balance and stability of synaptic structures during synaptic plasticity. Neuron 82: 430– 43 24742464
  97. Michel K, Müller JA, Oprisoreanu AM, Schoch S. 2015 The presynaptic active zone: a dynamic scaffold that regulates synaptic efficacy. Exp. Cell Res 335: 157– 64 25720549
  98. Min R, Santello M, Nevian T. 2012 The computational power of astrocyte mediated synaptic plasticity. Front. Comput. Neurosci 6: 93 23125832 PMC3485583
  99. Missler M, Zhang W, Rohlmann A, Kattenstroth G, Hammer RE, 2003 α-Neurexins couple Ca2+ channels to synaptic vesicle exocytosis. Nature 423: 939– 48 12827191
  100. Monday HR, Castillo PE. 2017 Closing the gap: long-term presynaptic plasticity in brain function and disease. Curr. Opin. Neurobiol 45: 106– 12 28570863 PMC5554717
  101. Moulder KL, Jiang X, Chang C, Taylor AA, Benz AM, 2008 A specific role for Ca2+-dependent adenylyl cyclases in recovery from adaptive presynaptic silencing. J. Neurosci 28: 5159– 68 18480272 PMC2684782
  102. Moulder KL, Meeks JP, Shute AA, Hamilton CK, de Erausquin G, Mennerick S. 2004 Plastic elimination of functional glutamate release sites by depolarization. Neuron 42: 423– 35 15134639
  103. Mukai J, Tamura M, Fenelon K, Rosen AM, Spellman TJ, 2015 Molecular substrates of altered axonal growth and brain connectivity in a mouse model of schizophrenia. Neuron 86: 680– 95 25913858 PMC4603834
  104. Nugent FS, Penick EC, Kauer JA. 2007 Opioids block long-term potentiation of inhibitory synapses. Nature 446: 1086– 90 17460674
  105. Orr AL, Hanson JE, Li D, Klotz A, Wright S, 2014 β-Amyloid inhibits E-S potentiation through suppression of cannabinoid receptor 1-dependent synaptic disinhibition. Neuron 82: 1334– 45 24945775 PMC4114400
  106. Pan B, Hillard CJ, Liu QS. 2008 Endocannabinoid signaling mediates cocaine-induced inhibitory synaptic plasticity in midbrain dopamine neurons. J. Neurosci 28: 1385– 97 18256258 PMC6671588
  107. Patel AB, Hays SA, Bureau I, Huber KM, Gibson JR. 2013 A target cell-specific role for presynaptic Fmr1 in regulating glutamate release onto neocortical fast-spiking inhibitory neurons. J. Neurosci 33: 2593– 604 23392687 PMC3711607
  108. Pathak D, Shields LY, Mendelsohn BA, Haddad D, Lin W, 2015 The role of mitochondrially derived ATP in synaptic vesicle recycling. J. Biol. Chem 290: 22325– 36 26126824 PMC4566209
  109. Perea G, Araque A. 2007 Astrocytes potentiate transmitter release at single hippocampal synapses. Science 317: 1083– 86 17717185
  110. Perea G, Navarrete M, Araque A. 2009 Tripartite synapses: astrocytes process and control synaptic information. Trends Neurosci. 32: 421– 31 19615761
  111. Petzoldt AG, Lutzkendorf J, Sigrist SJ. 2016 Mechanisms controlling assembly and plasticity of presynaptic active zone scaffolds. Curr. Opin. Neurobiol 39: 69– 76 27131423
  112. Picconi B, Centonze D, Hakansson K, Bernardi G, Greengard P, 2003 Loss of bidirectional striatal synaptic plasticity in L-DOPA-induced dyskinesia. Nat. Neurosci 6: 501– 6 12665799
  113. Pilo Boyl P, Di Nardo A, Mulle C, Sassoè-Pognetto M, Panzanelli P, 2007 Profilin2 contributes to synaptic vesicle exocytosis, neuronal excitability, and novelty-seeking behavior. EMBO J. 26: 2991– 3002 17541406 PMC1894775
  114. Polter AM, Bishop RA, Briand LA, Graziane NM, Pierce RC, Kauer JA. 2014 Poststress block of κ opioid receptors rescues long-term potentiation of inhibitory synapses and prevents reinstatement of cocaine seeking. Biol. Psychiatry 76: 785– 93 24957331 PMC4240751
  115. Poo MM, Pignatelli M, Ryan TJ, Tonegawa S, Bonhoeffer T, 2016 What is memory? The present state of the engram. BMC Biol. 14: 40 27197636 PMC4874022
  116. Powell CM, Schoch S, Monteggia L, Barrot M, Matos MF, 2004 The presynaptic active zone protein RIM1α is critical for normal learning and memory. Neuron 42: 143– 53 15066271 PMC3910111
  117. Ramírez-Franco J, Bartolomé-Martin D, Alonso B, Torres M, Sánchez-Prieto J. 2014 Cannabinoid type 1 receptors transiently silence glutamatergic nerve terminals of cultured cerebellar granule cells. PLOS ONE 9: e88594 24533119 PMC3922925
  118. Rangaraju V, Calloway N, Ryan TA. 2014 Activity-driven local ATP synthesis is required for synaptic function. Cell 156: 825– 35 24529383 PMC3955179
  119. Rebola N, Carta M, Mulle C. 2017 Operation and plasticity of hippocampal CA3 circuits: implications for memory encoding. Nat. Rev. Neurosci 18: 208– 20 28251990
  120. Robbe D, Kopf M, Remaury A, Bockaert J, Manzoni OJ. 2002 Endogenous cannabinoids mediate long-term synaptic depression in the nucleus accumbens. PNAS 99: 8384– 88 12060781 PMC123076
  121. Rost BR, Schneider F, Grauel MK, Wozny C, Bentz C, 2015 Optogenetic acidification of synaptic vesicles and lysosomes. Nat. Neurosci 18: 1845– 52 26551543 PMC4869830
  122. Ruediger S, Vittori C, Bednarek E, Genoud C, Strata P, 2011 Learning-related feedforward inhibitory connectivity growth required for memory precision. Nature 473: 514– 18 21532590
  123. Sankaranarayanan S, Atluri PP, Ryan TA. 2003 Actin has a molecular scaffolding, not propulsive, role in presynaptic function. Nat. Neurosci 6: 127– 35 12536209
  124. Schmitz SK, King C, Kortleven C, Huson V, Kroon T, 2016 Presynaptic inhibition upon CB1 or mGlu2/3 receptor activation requires ERK/MAPK phosphorylation of Munc18–1. EMBO J. 35: 1236– 50 27056679 PMC4888233
  125. Schuemann A, Klawiter A, Bonhoeffer T, Wierenga CJ. 2013 Structural plasticity of GABAergic axons is regulated by network activity and GABAA receptor activation. Front. Neural Circuits 7: 113 23805077 PMC3693093
  126. Seshadri S, Faust T, Ishizuka K, Delevich K, Chung Y, 2015 Interneuronal DISC1 regulates NRG1-ErbB4 signalling and excitatory-inhibitory synapse formation in the mature cortex. Nat. Commun 6: 10118 26656849 PMC4682104
  127. Shaban H, Humeau Y, Herry C, Cassasus G, Shigemoto R, 2006 Generalization of amygdala LTP and conditioned fear in the absence of presynaptic inhibition. Nat. Neurosci 9: 1028– 35 16819521
  128. Shamir A, Kwon OB, Karavanova I, Vullhorst D, Leiva-Salcedo E, 2012 The importance of the NRG-1/ErbB4 pathway for synaptic plasticity and behaviors associated with psychiatric disorders. J. Neurosci 32: 2988– 97 22378872 PMC3302154
  129. Sheffler-Collins SI, Dalva MB. 2012 EphBs: an integral link between synaptic function and synaptopathies. Trends Neurosci. 35: 293– 304 22516618 PMC3631563
  130. Shigeoka T, Jung H, Jung J, Turner-Bridger B, Ohk J, 2016 Dynamic axonal translation in developing and mature visual circuits. Cell 166: 181– 92 27321671 PMC4930487
  131. Shin RM, Tully K, Li Y, Cho JH, Higuchi M, 2010 Hierarchical order of coexisting pre- and postsynaptic forms of long-term potentiation at synapses in amygdala. PNAS 107: 19073– 78 20956319 PMC2973868
  132. Siegert S, Seo J, Kwon EJ, Rudenko A, Cho S, 2015 The schizophrenia risk gene product miR-137 alters presynaptic plasticity. Nat. Neurosci 18: 1008– 16 26005852 PMC4506960
  133. Sigrist SJ, Schmitz D. 2011 Structural and functional plasticity of the cytoplasmic active zone. Curr. Opin. Neurobiol 21: 144– 50 20832284
  134. Sigurdsson T, Stark KL, Karayiorgou M, Gogos JA, Gordon JA. 2010 Impaired hippocampalprefrontal synchrony in a genetic mouse model of schizophrenia. Nature 464: 763– 67 20360742 PMC2864584
  135. Sinnen BL, Bowen AB, Forte JS, Hiester BG, Crosby KC, 2017 Optogenetic control of synaptic composition and function. Neuron 93: 646– 60.e5 28132827 PMC5300939
  136. Sjöström PJ, Turrigiano GG, Nelson SB. 2003 Neocortical LTD via coincident activation of presynaptic NMDA and cannabinoid receptors. Neuron 39: 641– 54 12925278
  137. Smith HL, Bourne JN, Cao G, Chirillo MA, Ostroff LE, 2016 Mitochondrial support of persistent presynaptic vesicle mobilization with age-dependent synaptic growth after LTP. eLife 5: e15275 27991850 PMC5235352
  138. Su B, Ji YS, Sun XL, Liu XH, Chen ZY. 2014 Brain-derived neurotrophic factor (BDNF)-induced mitochondrial motility arrest and presynaptic docking contribute to BDNF-enhanced synaptic transmission. J. Biol. Chem 289: 1213– 26 24302729 PMC3894308
  139. Südhof TC. 2017 Synaptic Neurexin Complexes: A Molecular Code for the Logic of Neural Circuits. Cell. 171(4), pp. 745– 769. 29100073 PMC5694349
  140. Varoqueaux F, Jamain S, Brose N. 2004 Neuroligin 2 is exclusively localized to inhibitory synapses. Eur. J. Cell Biol 83: 449– 56 15540461
  141. Villa KL, Berry KP, Subramanian J, Cha JW, Oh WC, 2016 Inhibitory synapses are repeatedly assembled and removed at persistent sites in vivo. Neuron 89: 756– 69 26853302 PMC4760889
  142. Volk L, Chiu SL, Sharma K, Huganir RL. 2015 Glutamate synapses in human cognitive disorders. Annu. Rev. Neurosci 38: 127– 49 25897873
  143. Voronin LL, Cherubini E. 2004 ‘Deaf, mute and whispering’ silent synapses: their role in synaptic plasticity. J. Physiol 557: 3– 12 15034124 PMC1665055
  144. Waites CL, Garner CC. 2011 Presynaptic function in health and disease. Trends Neurosci. 34: 326– 37 21596448
  145. Wang H, Song L, Laird F, Wong PC, Lee HK. 2008 BACE1 knock-outs display deficits in activity-dependent potentiation of synaptic transmission at mossy fiber to CA3 synapses in the hippocampus. J. Neurosci 28: 8677– 81 18753368 PMC2728626
  146. Wang W, Jia Y, Pham DT, Palmer LC, Jung KM, 2017 Atypical endocannabinoid signaling initiates a new form of memory-related plasticity at a cortical input to hippocampus. Cereb. Cortex 17: 1– 14 PMC5998949 28520937
  147. Wang XS, Peng CZ, Cai WJ, Xia J, Jin D, 2014 Activity-dependent regulation of release probability at excitatory hippocampal synapses: a crucial role of fragile X mental retardation protein in neurotransmission. Eur. J. Neurosci 39: 1602– 12 24646437 PMC4028396
  148. Wang YC, Lauwers E, Verstreken P. 2017 Presynaptic protein homeostasis and neuronal function. Curr. Opin. Genet. Dev 44: 38– 46 28213157
  149. Wierenga CJ, Becker N, Bonhoeffer T. 2008 GABAergic synapses are formed without the involvement of dendritic protrusions. Nat Neurosci 11: 1044– 52 19160502
  150. Wilhelm BG, Mandad S, Truckenbrodt S, Krohnert K, Schäfer C 2014 Composition of isolated synaptic boutons reveals the amounts of vesicle trafficking proteins. Science 344: 1023– 8 24876496
  151. Witton J, Brown JT, Jones MW, Randall AD. 2010 Altered synaptic plasticity in the mossy fibre pathway of transgenic mice expressing mutant amyloid precursor protein. Mol. Brain 3: 32 21040543 PMC2988062
  152. Woo RS, Li XM, Tao Y, Carpenter-Hyland E, Huang YZ, 2007 Neuregulin-1 enhances depolarization-induced GABA release. Neuron 54: 599– 610 17521572
  153. Woodin MA, Maffei AE. 2010 Inhibitory Synaptic Plasticity. New York: Springer
  154. Yang Y, Calakos N. 2013 Presynaptic long-term plasticity. Front Synaptic Neurosci 5: 8 24146648 PMC3797957
  155. Yao J, Qi J, Chen G. 2006 Actin-dependent activation of presynaptic silent synapses contributes to long-term synaptic plasticity in developing hippocampal neurons. J. Neurosci 26: 8137– 47 16885227 PMC6673772
  156. Younts TJ, Chevaleyre V, Castillo PE. 2013 CA1 pyramidal cell theta-burst firing triggers endocannabinoid-mediated long-term depression at both somatic and dendritic inhibitory synapses. J. Neurosci 33: 13743– 57 23966696 PMC3755719
  157. Younts TJ, Monday HR, Dudok B, Klein ME, Jordan BA, 2016 Presynaptic protein synthesis is required for long-term plasticity of GABA release. Neuron 92: 479– 92 27764673 PMC5119541
  158. Zhang C, Wu B, Beglopoulos V, Wines-Samuelson M, Zhang D, 2009 Presenilins are essential for regulating neurotransmitter release. Nature 460: 632– 36 19641596 PMC2744588
  159. Zhang L, Alger BE. 2010 Enhanced endocannabinoid signaling elevates neuronal excitability in fragile X syndrome. J. Neurosci 30: 5724– 29 20410124 PMC2906112

Cited by

Sorted by citations

Authors
Monday, H. R., Younts, T. J., & Castillo, P. E.
Affiliations
  • Albert Einstein College of Medicine (US)
  • University College London (GB)
Corresponding author
  • Monday, Hannah R.
  • Younts, Thomas J.
  • Castillo, Pablo E.
ORCID
Venue
Annual Review of Neuroscience
Publisher
Annual Reviews
Published
2018-07-08
Volume
41
Issue
1
Pages
299-322
ISSN
  • 0147-006X (ISSN-L)
  • 1545-4126
DOI
10.1146/annurev-neuro-080317-062155
PMC
PMC6238218
OpenAlex
W2800557840
Cited by
175
References
20
Citations by year
2026: 15 · 2025: 20 · 2024: 33 · 2023: 28 · 2022: 22 · 2021: 20 · 2020: 23 · 2019: 10 · 2018: 3
FWCI
1.81
Type
journal article
Language
en
Open access
Locations
  • Annual Review of Neuroscience (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • National Institute of Mental Health (F31MH114431, R01MH081935)
  • National Institute on Drug Abuse (R01DA017392)
  • Eunice Kennedy Shriver National Institute of Child Health and Human Development (U54HD090260)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Keywords
presynaptic plasticity, long-term potentiation, long-term depression, neurotransmitter release, synaptic plasticity, trans-synaptic signaling, excitation-inhibition balance, novelty detection, sensory adaptation, learning, neuropsychiatric disorders, schizophrenia, autism spectrum disorder, intellectual disability, neurodegenerative diseases, drug abuse
MeSH terms
Animals, Brain, Brain Diseases, Humans, Learning, Neuronal Plasticity, Synapses, Neurotransmitter Agents

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