Upregulation of transmitter release probability improves a conversion of synaptic analogue signals into neuronal digital spikes

Molecular Brain

Volumn 5, Issue 1, 2012, Pages

  Yu, Jiandong ^a,b   Qian, Hao ^a,b   Wang, Jin Hui ^a,b  

^a INSTITUTE OF BIOPHYSICS   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

Action potential and Neuronal encoding; Neuron; Release probability; Synapse

Indexed keywords

GLUTAMIC ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FACILITATION; GABAERGIC TRANSMISSION; MOUSE; NEUROTRANSMITTER RELEASE; NONHUMAN; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROBABILITY; SPIKE WAVE; SYNAPSE; UPREGULATION;

ACTION POTENTIALS; ANIMALS; CALCIUM; COMPUTER SIMULATION; EGTAZIC ACID; GABAERGIC NEURONS; GLUTAMIC ACID; MICE; NEURONS; NEUROTRANSMITTER AGENTS; PRESYNAPTIC TERMINALS; SIGNAL TRANSDUCTION; SYNAPSES; SYNAPTIC TRANSMISSION; UP-REGULATION;

EID: 84864399227     PISSN: None     EISSN: 17566606     Source Type: Journal    
DOI: 10.1186/1756-6606-5-26     Document Type: Article

References (89)

1. Elementary interactions between neurons: Synaptic transmission. Kandel ER, Siegelbaum SA, Schwartz JH, Principles of Neural Science New York: McGraw-Hill, Kandel ER, Schwartz JH, Jessell TM, 2000 175 308
2. Synaptic transmission. Shepherd GM, Neurobiology New York: Oxford University Press, Shepherd GM, 1998
3. Synaptic computation. Abbott LF, Regehr WG, Nature 2004 431 796 802 10.1038/nature03010 15483601 (Pubitemid 39434069)
4. Dynamic spike threshold reveals a mechanism for synaptic coincidence detection in cortical neurons in vivo. Azous R, Gray CM, Proc Natl Acad Sci U S A 2000 97 8110 8115 10.1073/pnas.130200797 10859358 (Pubitemid 30460781)
5. Byrne JH, Learning and Memory: Basic Mechanisms Amsterdam: Academic Press 2003
6. Axons amplify somatic incomplete spikes into uniform amplitudes in mouse cortical pyramidal neurons. Chen N, Yu J, Qian H, Ge R, Wang JH, PLoS One 2010 5 7 11868 10.1371/journal.pone.0011868 20686619
7. Interneuron, spike timing, and perception. Fricker D, Miles R, Neuron 2001 32 771 774 10.1016/S0896-6273(01)00528-1 11738024 (Pubitemid 34024839)
8. Excitatory and feed-forward inhibitory hippocampal synapses work synergistically as adaptive filter of neural spike trains. Klyachko VA, Stevens CF, PLoS Biol 2006 4 207 10.1371/journal.pbio.0040207 16774451 (Pubitemid 44049616)
9. Rieke F, Warland D, De Ruyter van Steveninck R, Bialek W, Spikes: Exploring the neural codes Cambridge, MA: MIT 1998
10. The Possible Role of Spike Patterns in Cortical Information Processing. Tiesinga PHE, Toups JV, J Comput Neurosci 2005 18 275 286 10.1007/s10827-005- 0330-2 15830164 (Pubitemid 40626656)
11. Action potential evoked transmitter release in central synapses: insights from the developing calyx of Held. Wang LY, Fedchyshyn MJ, Yang YM, Mol Brain 2009 2 36 10.1186/1756-6606-2-36 19939269
12. The gain and fidelity of transmission patterns at cortical excitatory unitary synapses improve spike encoding. Wang JH, Wei J, Chen X, Yu J, Chen N, Shi J, J Cell Sci 2008 121 2951 2960 10.1242/jcs.025684 18697836
13. Action potential bursts enhance transmitter release at a giant central synapse. Zhang B, et al. J Physiol 2011 589 2213 2227 10.1113/jphysiol.2010. 200154 21486773
14. Origin of variability in quantal size in cultured hippocampal neuron and hippocampal slice. Bekkers JM, Richerson GB, Stevens CF, Proc Natl Acad Sci U S A 1990 87 5359 5362 10.1073/pnas.87.14.5359 2371276 (Pubitemid 20260179)
15. Quantal size is independent of the release probability at hippocampal excitatory synapses. Biro AA, Holderith NB, Nusser Z, J Neurosci 2005 25 223 232 10.1523/JNEUROSCI.3688-04.2005 15634785 (Pubitemid 40110784)
16. The low synaptic release probability in vivo. Borst JG, Trends Neurosci 2010 33 259 266 10.1016/j.tins.2010.03.003 20371122
17. The probability of neurotransmitter release: variability and feedback control at single synapses. Branco T, Staras K, Nat Rev Neurosci 2009 10 373 383 19377502
18. Heterogeneity of release probability, facilitation, and depletion at central synapses. Dobrunz LE, Stevens CF, Neuron 1997 18 995 1008 10.1016/S0896-6273(00)80338-4 9208866 (Pubitemid 27274617)
19. Regehr WG, Stevens CF, Physiology of synaptic transmission and short-term plasticity Boltimore and London: The Johns Hopkins University Press 2001
20. High-probability uniquantal transmission at excitatory synapses in barrel cortex. Silver RA, Lubke J, Sakmann B, Feldmeyer D, Science 2003 302 1981 1984 10.1126/science.1087160 14671309 (Pubitemid 37523509)
21. Facilitation and depression at single central synapses. Stevens CF, Wang Y-Y, Neuron 1995 14 795 802 10.1016/0896-6273(95)90223-6 7718241
22. Changes in presynaptic function during long-term potentiation. Tsien RW, Malinow R, Ann N Y Acad Sci 1991 635 208 220 10.1111/j.1749-6632.1991.tb36493.x 1741585
23. The dynamic range for gain control of NMDA receptor-mediated synaptic transmission at a single synapse. Wang LY, J Neurosci 2000 20 C115 11125014
24. Short-term synaptic plasticity. Zucker RS, Regehr WG, Ann Rev Physiol 2002 25 355 405 (Pubitemid 34259234)
25. Functional comparison of neurotransmitter receptor subtypes in mammalian central nervous system. Nicoll RA, Malenka RC, Kauer JA, Physiol Rev 1990 70 513 565 1690904 (Pubitemid 20140189)
26. Homeostasis established by coordination of subcellular compartment plasticity improves spike encoding. Chen N, Chen X, Wang J-H, J Cell Sci 2008 121 2961 2971 10.1242/jcs.022368 18697837
27. New calcium indicators and buffers with high selectivity against magnesium and protons: design, synthesis, and properties of prototype structures. Tsien RY, Biochemistry 1980 19 2396 2404 10.1021/bi00552a018 6770893
28. Contributions of residual calcium to fast synaptic transmission. Chen C, Regehr WG, J Neurosci 1999 19 6257 6266 10414955 (Pubitemid 29347426)
29. Asynchronous GABA release generates long-lasting inhibition at a hippocampal interneuron-pyramidal neuron synapse. Hefft S, Jonas P, Nat Neurosci 2005 8 1319 1328 10.1038/nn1542 16158066 (Pubitemid 41630419)
30. Quantal glutamate release is essential for reliable neuronal encodings in cerebral networks. Yu J, Qian H, Chen N, Wang JH, PLoS One 2011 6 25219 10.1371/journal.pone.0025219 21949885
31. Presynaptic release probability influences the locus of long-term potentiation. Larkman A, Hannay T, Stratford K, Jack J, Nature 1992 360 70 73 10.1038/360070a0 1331808
32. Long-term potentiation: evidence against an increase in transmitter release probability in the CA1 region of the hippocampus. Manabe T, Nicoll RA, Science 1994 265 1888 1892 10.1126/science.7916483 7916483 (Pubitemid 24324249)
33. Facilitation at single synapses probed with optical quantal analysis. Oertner TG, Sabatini BL, Nimchinsky EA, Svoboda K, Nat Neurosci 2002 5 657 664 12055631 (Pubitemid 34742981)
34. Presynaptic Ca2+ dynamics, Ca2+ buffers and synaptic efficacy. Burnashev N, Rozov A, Cell Calcium 2005 37 489 495 10.1016/j.ceca.2005.01.003 15820398 (Pubitemid 40458447)
35. Synaptotagmin I functions as a calcium regulator of release probability. Fernandez-Chacon R, et al. Nature 2001 410 41 49 10.1038/35065004 11242035 (Pubitemid 32225830)
36. The role of calcium in neuromuscular facilitation. Katz B, Miledi R, J Physiol (Lond) 1968 195 481 492
37. Katz B, The release of neural transmitter substances Liverpool: Liverpool University Press 1969
38. Ca2+dependent mechanisms of presynaptic control at central synapses. Rusakov DA, Neuroscientist 2006 12 317 326 10.1177/1073858405284672 16840708 (Pubitemid 44050860)
39. Amyloid-beta as a positive endogenous regulator of release probability at hippocampal synapses. Abramov E, Dolev I, Fogel H, Ciccotosto GD, Ruff E, Slutsky I, Nat Neurosci 2009 12 1567 1576 10.1038/nn.2433 19935655
40. Astrocytes impose postburst depression of release probability at hippocampal glutamate synapses. Andersson M, Hanse E, J Neurosci 2010 30 5776 5780 10.1523/JNEUROSCI.3957-09.2010 20410129
41. beta-Arrestin2, interacting with phosphodiesterase 4, regulates synaptic release probability and presynaptic inhibition by opioids. Bradaia A, Berton F, Ferrari S, Luscher C, Proc Natl Acad Sci U S A 2005 102 3034 3039 10.1073/pnas.0406632102 15718284 (Pubitemid 40299911)
42. Presynaptic release probability is increased in hippocampal neurons from ASIC1 knockout mice. Cho JH, Askwith CC, J Neurophysiol 2008 99 426 441 10.1152/jn.00940.2007 18094106 (Pubitemid 351253207)
43. Synaptic vesicle protein 2 enhances release probability at quiescent synapses. Custer KL, Austin NS, Sullivan JM, Bajjalieh SM, J Neurosci 2006 26 1303 1313 10.1523/JNEUROSCI.2699-05.2006 16436618 (Pubitemid 43237062)
44. Cholecystokinin facilitates glutamate release by increasing the number of readily releasable vesicles and releasing probability. Deng PY, et al. J Neurosci 2010 30 5136 5148 10.1523/JNEUROSCI.5711-09.2010 20392936
45. Dynasore, an inhibitor of dynamin, increases the probability of transmitter release. Douthitt HL, Luo F, McCann SD, Meriney SD, Neuroscience 2010 172 187 195 21056636
46. MicroRNA132 modulates short-term synaptic plasticity but not basal release probability in hippocampal neurons. Lambert TJ, Storm DR, Sullivan JM, PLoS One 2011 5 15182
47. Presynaptic release probability and readily releasable pool size are regulated by two independent mechanisms during posttetanic potentiation at the calyx of Held synapse. Lee JS, Kim MH, Ho WK, Lee SH, J Neurosci 2008 28 7945 7953 10.1523/JNEUROSCI.2165-08.2008 18685020
48. BDNF increases release probability and the size of a rapidly recycling vesicle pool within rat hippocampal excitatory synapses. Tyler WJ, Zhang XL, Hartman K, Winterer J, Muller W, Stanton PK, Pozzo-Miller L, J Physiol 2006 574 787 803 10.1113/jphysiol.2006.111310 16709633 (Pubitemid 44089071)
49. Involvement of pre- and postsynaptic mechanisms in posttetanic potentiation in Aplysia synapses. Bao J-X, Kandel ER, Hawkins RD, Science 1997 275 969 973 10.1126/science.275.5302.969 9020078 (Pubitemid 27087711)
50. Role of presynaptic calcium ions and channels in synaptic facilitation and depression at the squid giant synapse. Charlton MP, Smith SJ, Zucker RS, J Physiol (Lond) 1982 323 173 193 (Pubitemid 12180903)
51. Adenosine increases synaptic facilitation in the in vitro rat hippocampus: evidence for a presynaptic site of action. Dunwiddie TV, Haas HL, J Physiol (London) 1985 369 365 377 (Pubitemid 16176884)
52. Residual Ca2+ and short-term synaptic plasticity. Kamlya H, Zucker RS, Nature 1994 371 603 606 10.1038/371603a0 7935792
53. Mitochondrial involvement in post-tetanic potentiation of synaptic transmission. Tang Y-G, Zucker RS, Neuron 1997 18 483 491 10.1016/S0896-6273(00) 81248-9 9115741 (Pubitemid 27138795)
54. Homosynaptic facilitation of transmitter release in Crayfish is not affected by mobile calcium chelators: implications for the residual ionized calcium hypothsis from electrophysiological and computational analyses. Winslow JL, Duffy SN, Charlton MP, J Neurophsiol 1994 72 1769 1793 (Pubitemid 24325102)
55. Short-term synaptic plasticity. Zucker RS, Ann Rev Neurosci 1989 12 13 31 10.1146/annurev.ne.12.030189.000305 2648947 (Pubitemid 19085445)
56. Local dendritic activity sets release probability at hippocampal synapses. Branco T, Staras K, Darcy KJ, Goda Y, Neuron 2008 59 475 485 10.1016/j.neuron.2008.07.006 18701072
57. Regulation of synaptic facilitation by postsynaptic Ca2+/CaM pathways in hippocampal CA1 neurons. Wang J-H, Kelly PT, J Neurophysiol 1996 76 276 286 8836224 (Pubitemid 26251168)
58. Attenuation of paired-pulse facilitation associated with synaptic potentiation mediated by postsynaptic mechanisms. Wang J-H, Kelly PT, J Neurophysiol 1997 78 2707 2716 9356420 (Pubitemid 27495496)
59. Synaptic plasticity in the hippocampal formation. Bliss T, Gardner-Medwin A, Lomo T, Macromolecules and behaviour London, England: MacMillan, Ansell G, Bradley P, 1973 193 203
60. Long-term plasticity of intrinsic excitability: learning rules and mechanisms. Daoudal D, Debanne D, Learn Mem 2003 10 456 465 10.1101/lm.64103 14657257 (Pubitemid 37499775)
61. A study of long-term potentiation in transgenic mice over-expressing mutant forms of both amyloid precursor protein and presenilin-1. Fitzjohn SM, Kuenzi F, Morton RA, Rosahl TW, Lewis H, Smith D, Seabrook GR, Collingridge GL, Mol Brain 2010 3 21 10.1186/1756-6606-3-21 20630068
62. The current excitement in long-term potentiation. Nicoll RA, Kauer JA, Malenka RC, Neuron 1988 1 93 103
63. Imaging synaptic plasticity. Padamsey Z, Emptage NJ, Mol Brain 2011 4 36 10.1186/1756-6606-4-36 21958593
64. Plasticity between neuronal pairs in layer 4 of visual cortex varies with synapse state. Saez I, Friedlander MJ, J Neurosci 2009 29 15286 15298 10.1523/JNEUROSCI.2980-09.2009 19955381
65. Calcium/calmodulin-dependent kinase IV contributes to translation-dependent early synaptic potentiation in the anterior cingulate cortex of adult mice. Toyoda H, Zhao MG, Mercaldo V, Chen T, Descalzi G, Kida S, Zhuo M, Mol Brain 2010 3 27 10.1186/1756-6606-3-27 20846411
66. Altered synaptic plasticity in the mossy fibre pathway of transgenic mice expressing mutant amyloid precursor protein. Witton J, Brown JT, Jones MW, Randall AD, Mol Brain 2010 3 32 10.1186/1756-6606-3-32 21040543
67. Calcium signal-dependent plasticity of neuronal excitability developed postnatally. Zhang M, Hung F, Zhu Y, Xie Z, Wang J, J Neurobiol 2004 61 277 287 10.1002/neu.20045 15382030 (Pubitemid 39426152)
68. Evidence for silent synapses: implications for the expression of LTP. Isaac JTR, Nicoll RA, Malenka RC, Neuron 1995 15 427 434 10.1016/0896-6273(95) 90046-2 7646894
69. Activation of postsynaptic silent synapses during pairing-induced LTP in CA1 region of hippocampal slice. Liao D-Z, Hessler NA, Malinow R, Nature 1995 375 400 404 10.1038/375400a0 7760933
70. Selective acquisition of AMPA receptors over postnatal development suggests a molecular basis for silent synapses. Petralia RS, Esteban JA, Wang Y-X, Partridge JG, Zhao H-M, Wenthold RJ, Malinow R, Nat Neurosci 1999 2 31 36 10.1038/4532 10195177 (Pubitemid 30488937)
71. Silent synapses in the developing rat visual cortex: Evidence for postsynaptic expression of synaptic plasticity. Rumpel S, Hatt H, Gottmann K, J Neurosci 1998 18 8863 8874 9786992 (Pubitemid 28491751)
72. Ca2+/CaM signalling pathway up-regulates glutamatergic synaptic function in non-pyramidal fast-spiking neurons of hippocampal CA1. Wang J-H, Kelly PT, J Physiol (Lond) 2001 533 407 422 10.1111/j.1469-7793.2001.0407a.x (Pubitemid 32519997)
73. Differential modulation of glutamatergic and cholinergic synapses by calcineurin in hippocampal CA1 fast-spiking interneurons. Wang J, Zhang M, Brain Res 2004 1004 125 135 10.1016/j.brainres.2004.01.025 15033427 (Pubitemid 38368068)
74. Silent synapses in the developing hippocampus: lack of functional AMPA receptors or low probability of glutamate release? Gasparini S, Saviane C, Voronin LL, Cherubini E, Proc Natl Acad Sci U S A 2000 97 9741 9746 10.1073/pnas.170032297 10931951 (Pubitemid 30650846)
75. Paired-pulse depression of unitary quantal amplitude at single hippocampal synapses. Chen G, Harata NC, Tsien RW, Proc Natl Acad Sci U S A 2003 101 1063 1068 (Pubitemid 38160584)
76. Presynaptic external calcium signaling involves the calcium-sensing receptor in neocortical nerve terminals. Chen W, et al. PLoS One 2010 5 8563 10.1371/journal.pone.0008563 20052292
77. Synapse geometry and receptor dynamics modulate synaptic strength. Freche D, Pannasch U, Rouach N, Holcman D, PLoS One 2011 6 25122 10.1371/journal.pone. 0025122 21984900
78. Quantal analysis reveals a functional correlation between presynaptic and postsynaptic efficacy in excitatory connections from rat neocortex. Hardingham NR, Read JC, Trevelyan AJ, Nelson JC, Jack JJ, Bannister NJ, J Neurosci 2010 30 1441 1451 10.1523/JNEUROSCI.3244-09.2010 20107071
79. The origin of quantal size variation: vesicular glutamate concentration plays a significant role. Wu X, Xue L, Mohan R, Paradiso K, Gillis KD, Wu L-G, J Neurosci 2007 27 3046 3056 10.1523/JNEUROSCI.4415-06.2007 17360928 (Pubitemid 46438971)
80. mGluR1,5 activation improves network asynchrony and GABAergic synapse attenuation in the amygdala: implication for anxiety-like behavior in DBA/2 mice. Zhang F, Liu B, Lei Z, Wang J, Mol Brain 2012 5 20 10.1186/1756-6606-5-20 22681774
81. Exocytosis: a molecular and physiological perspective. Zucker RS, Neuron 1996 17 1049 1055 10.1016/S0896-6273(00)80238-X 8982154 (Pubitemid 27021092)
82. Physiological synaptic signals initiate sequential spikes at soma of cortical pyramidal neurons. Ge R, Qian H, Wang JH, Mol Brain 2011 4 19 10.1186/1756-6606-4-19 21549002
83. Upregulation of barrel GABAergic neurons is associated with cross-modal plasticity in olfactory deficit. Ni H, et al. PLoS One 2010 5 13736 10.1371/journal.pone.0013736 21060832
84. Short-term cerebral ischemia causes the dysfunction of interneurons and more excitation of pyramidal neurons. Wang J-H, Brain Res Bull 2003 60 53 58 10.1016/S0361-9230(03)00026-1 12725892 (Pubitemid 36506452)
85. Interneurons of the hippocampus. Freund TF, Buzsaki G, Hippocampus 1996 6 347 470 8915675 (Pubitemid 126682925)
86. Dendritic integration of excitatory synaptic input. Magee JC, Nat Rev Neurosci 2000 1 181 190 10.1038/35044552 11257906
87. Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Klausberger T, Somogyi P, Science 2008 321 53 57 10.1126/science.1149381 18599766 (Pubitemid 351956237)
88. Neuronal integration of synaptic input in the fluctuation-driven regime. Kuhn A, Aertsen A, Roter S, J Neurosci 2004 24 2345 2356 10.1523/JNEUROSCI.3349- 03.2004 15014109 (Pubitemid 38327947)
89. Distinquishing theoretical synaptic potentials computed for different soma-dendritic distribution of synaptic inputs. Rall W, J Neurophysiol 1967 30 1138 1168 6055351