Defective synaptic transmission and structure in the dentate gyrus and selective fear memory impairment in the Rsk2 mutant mouse model of Coffin-Lowry syndrome

Neurobiology of Disease

Volumn 58, Issue , 2013, Pages 156-168

  Morice, Elise ^a,b,d   Farley, Séverine ^a,b,d   Poirier, Roseline ^a,b   Dallerac, Glenn ^a,b,e   Chagneau, Carine ^a,b   Pannetier, Solange ^c   Hanauer, André ^c   Davis, Sabrina ^a,b   Vaillend, Cyrille ^a,b   Laroche, Serge ^a,b  

^a CNRS   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^d Université Pierre et Marie Curie   (France)

^e Centre de Recherche Interdisciplinaire en Biologie   (France)

Author keywords

Coffin Lowry; Hippocampus; Intellectual disability; Mental retardation; Reconsolidation; Synaptic morphology; Synaptic plasticity; Trace fear conditioning; Transcription factors

Indexed keywords

ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; EARLY GROWTH RESPONSE FACTOR 1; GLUTAMATE RECEPTOR; N METHYL DEXTRO ASPARTIC ACID; PROTEIN NRSK2; PROTEIN SERINE THREONINE KINASE; PROTEIN SHANK3; SCAFFOLD PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ZIF268; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOCHEMISTRY; BRAIN ELECTROPHYSIOLOGY; CELL FUNCTION; CELL STRUCTURE; COFFIN LOWRY SYNDROME; CONDUCTANCE; CONTROLLED STUDY; DENTATE GYRUS; ELECTRON MICROSCOPY; EMBRYO; FEAR; FEMALE; GENE; GENE CONTROL; HIPPOCAMPUS; IN VITRO STUDY; IN VIVO STUDY; KNOCKOUT MOUSE; LONG TERM POTENTIATION; MALE; MEMORY CONSOLIDATION; MEMORY DISORDER; MORPHOLOGY; MOUSE; MUTANT; NERVE CELL; NERVE CELL EXCITABILITY; NERVE CELL NETWORK; NERVOUS SYSTEM PARAMETERS; NEUROANATOMY; NEUROLOGIC DISEASE; NONHUMAN; PATHOPHYSIOLOGY; POSTSYNAPTIC DENSITY; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; RSK2 GENE; SHORT TERM POTENTIATION; SYNAPTIC TRANSMISSION; ULTRASTRUCTURE;

Α-AMINO-3-HYDROXY-5-METHYL-4-ISOXAZOLEPROPIONIC ACID RECEPTOR; 90-KDA RIBOSOMAL S6 KINASE; AMPAR; CAMP-RESPONSE ELEMENT BINDING PROTEIN; CLS; COFFIN-LOWRY; COFFIN-LOWRY SYNDROME; CONDITIONED STIMULUS; CREB; CS; ELECTRON MICROSCOPY; EM; EPSC; ERK; EXCITATORY POSTSYNAPTIC CURRENTS; EXTRACELLULAR SIGNAL-REGULATED KINASE; FEPSP; FIELD EXCITATORY POSTSYNAPTIC POTENTIAL; GLUR; GLUTAMATE RECEPTOR; HIPPOCAMPUS; IEG; IMMEDIATE EARLY GENE; INTELLECTUAL DISABILITY; INTER-STIMULUS INTERVAL; INTER-TRIAL INTERVAL; ISI; ITI; LONG-TERM POTENTIATION; LTP; MEDIAL PERFORANT PATH; MENTAL RETARDATION; METABOTROPIC GLUTAMATE RECEPTOR; MGLUR; MITOGEN STRESS-ACTIVATED KINASE 1 AND 2; MPP; MSB; MSK1/2; MULTIPLE SPINE BOUTON; N-METHYL-D-ASPARTATE RECEPTOR; NMDAR; PAIRED-PULSE FACILITATION; PAIRED-PULSE INHIBITION; POST-TETANIC POTENTIATION; POSTSYNAPTIC DENSITY; PPF; PPI; PSD; PTP; RECONSOLIDATION; RSK; SHORT-TERM POTENTIATION; STP; SYNAPTIC MORPHOLOGY; SYNAPTIC PLASTICITY; TRACE FEAR CONDITIONING; TRANSCRIPTION FACTORS; UNCONDITIONED STIMULUS; US; WILD-TYPE; WT;

ALPHA-AMINO-3-HYDROXY-5-METHYL-4-ISOXAZOLEPROPIONIC ACID; ANIMALS; COFFIN-LOWRY SYNDROME; CONDITIONING (PSYCHOLOGY); CUES; DENTATE GYRUS; DISEASE MODELS, ANIMAL; ELECTRIC STIMULATION; EXCITATORY POSTSYNAPTIC POTENTIALS; FEAR; FREEZING REACTION, CATALEPTIC; MEMORY DISORDERS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROSCOPY, ELECTRON, TRANSMISSION; MUTATION; N-METHYLASPARTATE; NERVE TISSUE PROTEINS; RIBOSOMAL PROTEIN S6 KINASES, 90-KDA; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 84879442034     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2013.05.016     Document Type: Article

References (86)

1. Alberini C.M. Mechanisms of memory stabilization: are consolidation and reconsolidation similar or distinct processes?. Trends Neurosci. 2005, 28:51-56.
2. Alvarez V.A., Sabatini B.L. Anatomical and physiological plasticity of dendritic spines. Annu. Rev. Neurosci. 2007, 30:79-97.
3. Anagnostaras S.G., Gale G.D., Fanselow M.S. Hippocampus and contextual fear conditioning: recent controversies and advances. Hippocampus 2001, 11:8-17.
4. Anjum R., Blenis J. The RSK family of kinases: emerging roles in cellular signalling. Nat. Rev. Mol. Cell Biol. 2008, 9:747-758.
5. Arthur J.S., Fong A.L., Dwyer J.M., Davare M., Reese E., Obrietan K., Impey S. Mitogen- and stress-activated protein kinase 1 mediates cAMP response element-binding protein phosphorylation and activation by neurotrophins. J. Neurosci. 2004, 24:4324-4332.
6. Besnard A., Caboche J., Laroche S. Reconsolidation of memory: a decade of debate. Prog. Neurobiol. 2012, 99:61-80.
7. Bourne J., Harris K.M. Do thin spines learn to be mushroom spines that remember?. Curr. Opin. Neurobiol. 2007, 17:381-386.
8. Bourtchuladze R., Frenguelli B., Blendy J., Cioffi D., Schutz G., Silva A.J. Deficient long-term memory in mice with a targeted mutation of the cAMP-responsive element-binding protein. Cell 1994, 79:59-68.
9. Bozon B., Kelly A., Josselyn S.A., Silva A.J., Davis S., Laroche S. MAPK, CREB and zif268 are all required for the consolidation of recognition memory. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2003, 358:805-814.
10. Darcq E., Koebel P., Del Boca C., Pannetier S., Kirstetter A.S., Garnier J.M., et al. RSK2 signaling in brain habenula contributes to place aversion learning. Learn. Mem. 2011, 18:574-578.
11. Davis S., Laroche S. MAP kinase/ERK signalling and memory stabilisation: a review. Genes Brain Behav. 2006, 5:61-72.
12. Davis S., Bliss T.V.P., Dutrieux G., Laroche S., Errington M.L. Induction and duration of long-term potentiation in the hippocampus of the freely moving mouse. J. Neurosci. Methods 1997, 75:75-80.
13. Davis S., Vanhoutte P., Pages C., Caboche J., Laroche S. The MAPK/ERK cascade targets both elk-1 and cAMP response element-binding protein to control long-term potentiation-dependent gene expression in the dentate gyrus in vivo. J. Neurosci. 2000, 20:4563-4572.
14. Davis S., Renaudineau S., Poirier R., Poucet B., Save E., Laroche S. The formation and stability of recognition memory: what happens upon recall?. Front. Behav. Neurosci. 2010, 4(177):1-11. 10.3389/fnbeh.2010.00177.
15. De Cesare D., Jacquot S., Hanauer A., Sassone-Corsi P. Rsk-2 activity is necessary for epidermal growth factor-induced phosphorylation of CREB protein and transcription of c-Fos gene. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:12202-12207.
16. Deak M., Clifton A.D., Lucocq L.M., Alessi D.R. Mitogen- and stress-activated protein kinase-1 (MSK1) is directly activated by MAPK and SAPK2/p38, and may mediate activation of CREB. EMBO J. 1998, 17:4426-4441.
17. DeFelipe J., Marco P., Busturia I., Merchan-Perez A. Estimation of the number of synapses in the cerebral cortex: methodological considerations. Cereb. Cortex 1999, 9:722-732.
18. Delaunoy J., Abidi F., Zeniou M., Jacquot S., Merienne K., Pannetier S., et al. Mutations in the X-linked RSK2 gene (RPS6KA3) in patients with Coffin-Lowry syndrome. Hum. Mutat. 2001, 17:103-116.
19. Desmond N.L., Levy W.B. Changes in the postsynaptic density with long term potentiation in the dentate gyrus. J. Comp. Neurol. 1986, 253:476-482.
20. Errington M.L., Bliss T.V.P., Morris R.J., Laroche S., Davis S. Long-term potentiation in awake mutant mice. Nature 1997, 387:666-667.
21. Fanselow M.S. Contextual fear, gestalt memories, and the hippocampus. Behav. Brain Res. 2000, 110:73-81.
22. Fiala J.C., Harris K.M. Dendrite structure. Dendrites 1999, 1-34. Oxford University Press, Oxford. G. Stuart, N. Spruston, M. Häusser (Eds.).
23. French P.J., O'Connor V., Jones M.W., Davis S., Errington M.L., Voss K., et al. Subfield-specific immediate early gene expression associated with hippocampal long-term potentiation in vivo. Eur. J. Neurosci. 2001, 13:968-976.
24. Fritschy J.M. Epilepsy, E/I balance and GABA(A) receptor plasticity. Front. Mol. Neurosci. 2008, 1:5. 10.3389/neuro.02.005.2008.
25. Frodin M., Gammeltoft S. Role and regulation of 90kDa ribosomal S6 kinase (RSK) in signal transduction. Mol. Cell. Endocrinol. 1999, 151:65-77.
26. Gilmartin M.R., McEchron M.D. Single neurons in the dentate gyrus and CA1 of the hippocampus exhibit inverse patterns of encoding during trace fear conditioning. Behav. Neurosci. 2005, 119:164-179.
27. Gong Y., Lippa C.F., Zhu J., Lin Q., Rosso A.L. Disruption of glutamate receptors at Shank-postsynaptic platform in Alzheimer's disease. Brain Res. 2009, 19:191-198.
28. Grabrucker A.M., Schmeisser M.J., Schoen M., Boeckers T.M. Postsynaptic ProSAP/Shank scaffolds in the cross-hair of synaptopathies. Trends Cell Biol. 2011, 21:594-603.
29. Grunditz A., Holbro N., Tian L., Zuo Y., Oertner T.G. Spine neck plasticity controls postsynaptic calcium signals through electrical compartmentalization. J. Neurosci. 2008, 28:13457-13466.
30. Hanauer A., Young I.D. Coffin-Lowry syndrome: clinical and molecular features. J. Med. Genet. 2002, 39:705-713.
31. Hung A.Y., Futai K., Sala C., Valtschanoff J.G., Ryu J., Woodworth M.A., et al. Smaller dendritic spines, weaker synaptic transmission, but enhanced spatial learning in mice lacking Shank1. J. Neurosci. 2008, 28:1697-1708.
32. Isaac J.T., Ashby M., McBain C.J. The role of the GluR2 subunit in AMPA receptor function and synaptic plasticity. Neuron 2007, 54:859-871.
33. Jacquot S., Merienne K., De Cesare D., Pannetier S., Mandel J.L., Sassone-Corsi P., Hanauer A. Mutation analysis of the RSK2 gene in Coffin-Lowry patients: extensive allelic heterogeneity and a high rate of de novo mutations. Am. J. Hum. Genet. 1998, 63:1631-1640.
34. Jones M.W., Errington M.L., French P.J., Fine A., Bliss T.V.P., Garel S., et al. A requirement for the immediate early gene Zif268 in the expression of late LTP and the consolidation of long-term memories. Nat. Neurosci. 2001, 4:289-296.
35. Katz B., Miledi R. The role of calcium in neuromuscular facilitation. J. Physiol. Lond. 1968, 195:481-492.
36. Kelly A., Laroche S., Davis S. Activation of mitogen-activated protein kinase/extracellular signal-regulated kinase in hippocampal circuitry is required for consolidation and reconsolidation of recognition memory. J. Neurosci. 2003, 12:5354-5360.
37. Kesler S.R., Simensen R.J., Voeller K., Abidi F., Stevenson R.E., Schwartz C.E., Reiss A.L. Altered neurodevelopment associated with mutations of RSK2: a morphometric MRI study of Coffin-Lowry. Neurogenetics 2007, 8:143-147.
38. Liu X., Ramirez S., Pang P.T., Puryear C.B., Govindarajan A., Deisseroth K., Tonegawa S. Optogenetic stimulation of a hippocampal engram activates fear memory recall. Nature 2012, 484:381-385.
39. Lu J., Helton T.D., Blanpied T.A., Rácz B., Newpher T.M., Weinberg R.J., Ehlers M.D. Postsynaptic positioning of endocytic zones and AMPA receptor cycling by physical coupling of dynamin-3 to Homer. Neuron 2007, 55:874-889.
40. Mahanty N.K., Sah P. Excitatory synaptic inputs to pyramidal neurons of the lateral amygdala. Eur. J. Neurosci. 1999, 11:1217-1222.
41. Marques Pereira P., Gruss M., Braun K., Foos N., Pannetier S., Hanauer A. Dopaminergic system dysregulation in the mrsk2_KO mouse, an animal model of the Coffin-Lowry syndrome. J. Neurochem. 2008, 107:1325-1334.
42. Marrone D.F., Petit T.L. The role of synaptic morphology in neural plasticity: structural interactions underlying synaptic power. Brain Res. Rev. 2002, 38:291-308.
43. Matsuzaki M. Factors critical for the plasticity of dendritic spines and memory storage. Neurosci. Res. 2007, 57:1-9.
44. Mayhew T.M. How to count synapses unbiasedly and efficiently at the ultrastructural level: proposal for a standard sampling and counting protocol. J. Neurocytol. 1996, 25:793-804.
45. McEchron M.D., Bouwmeester H., Tseng W., Weiss C., Disterhoft J.F. Hippocampectomy disrupts auditory trace fear conditioning and contextual fear conditioning in the rat. Hippocampus 1998, 8:638-646.
46. Mehmood T., Schneider A., Sibille J., Marques Pereira P., Pannetier S., Ammar M.R., et al. Transcriptome profile reveals AMPA receptor dysfunction in the hippocampus of the Rsk2-knockout mice, an animal model of Coffin-Lowry syndrome. Hum. Genet. 2011, 129:255-269.
47. Miranda R., Sébrié C., Degrouard J., Gillet B., Jaillard D., Laroche S., Vaillend C. Reorganization of inhibitory synapses and increased PSD length of perforated-excitatory synapses in hippocampal area CA1 of dystrophin-deficient mdx mice. Cereb. Cortex 2009, 19:876-888.
48. Moore M.D., Cushman J., Chandra D., Homanics G.E., Olsen R.W., Fanselow M.S. Trace and contextual fear conditioning is enhanced in mice lacking the alpha4 subunit of the GABA(A) receptor. Neurobiol. Learn. Mem. 2010, 93:383-387.
49. Peça J., Feliciano C., Ting J.T., Wang W., Wells M.F., Venkatraman T.N., et al. Shank3 mutant mice display autistic-like behaviours and striatal dysfunction. Nature 2011, 472:437-442.
50. Pereira P.M., Schneider A., Pannetier S., Heron D., Hanauer A. Coffin-Lowry syndrome. Eur. J. Hum. Genet. 2010, 18:627-633.
51. Phillips R.G., LeDoux J.E. Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav. Neurosci. 1992, 106:274-285.
52. Poirier R., Jacquot S., Vaillend C., Soutthiphong A.A., Libbey M., Davis S., et al. Deletion of the Coffin-Lowry syndrome gene Rsk2 in mice is associated with impaired spatial learning and reduced control of exploratory behavior. Behav. Genet. 2007, 37:31-50.
53. Poteet-Smith C.E., Smith J.A., Lannigan D.A., Freed T.A., Sturgill T.W. Generation of constitutively active p90 ribosomal S6 kinase in vivo: implications for the mitogen-activated protein kinase-activated protein kinase family. J. Biol. Chem. 1999, 274:22135-22138.
54. Quinn J.J., Oommen S.S., Morrison G.E., Fanselow M.S. Post-training excitotoxic lesions of the dorsal hippocampus attenuate forward trace, backward trace, and delay fear conditioning in a temporally specific manner. Hippocampus 2002, 12:495-504.
55. Raybuck J.D., Lattal K.M. Double dissociation of amygdala and hippocampal contributions to trace and delay fear conditioning. PLoS One 2011, 6(1):e15982.
56. Raymond C.R., Redman S.J. Spatial segregation of neuronal calcium signals encodes different forms of LTP in rat hippocampus. J. Physiol. 2006, 570:97-111.
57. Romeo Y., Zhang X., Roux P.P. Regulation and function of the RSK family of protein kinases. Biochem. J. 2012, 441:553-569.
58. Roussignol G., Ango F., Romorini S., Tu J.C., Sala C., Worley P.F., et al. Shank expression is sufficient to induce functional dendritic spine synapses in aspiny neurons. J. Neurosci. 2005, 25:3560-3570.
59. Sala C., Piëch V., Wilson N.R., Passafaro M., Liu G., Sheng M. Regulation of dendritic spine morphology and synaptic function by Shank and Homer. Neuron 2001, 31:115-130.
60. Santamaria F., Wils S., De Schutter E., Augustine G.J. Anomalous diffusion in Purkinje cell dendrites caused by spines. Neuron 2006, 52:635-648.
61. Sassone-Corsi P., Mizzen C.A., Cheung P., Crosio C., Monaco L., Jacquot S., et al. Requirement of Rsk-2 for epidermal growth factor-activated phosphorylation of histone H3. Science 1999, 285:886-891.
62. Savtchouk I., Liu S.J. Remodeling of synaptic AMPA receptor subtype alters the probability and pattern of action potential firing. J. Neurosci. 2011, 31:501-511.
63. Schneider A., Mehmood T., Pannetier S., Hanauer A. Altered ERK/MAPK signaling in the hippocampus of the mrsk2_KO mouse model of Coffin-Lowry syndrome. J. Neurochem. 2011, 119:447-459.
64. Schulz S., Siemer H., Krug M., Höllt V. Direct evidence for biphasic cAMP responsive element-binding protein phosphorylation during long-term potentiation in the rat dentate gyrus in vivo. J. Neurosci. 1999, 19:5683-5692.
65. Sheng M., Kim E. The Shank family of scaffold proteins. J. Cell Sci. 2000, 113:1851-1856.
66. Shi L., Linville M.C., Tucker E.W., Sonntag W.E., Brunso-Bechtold J.K. Differential effects of aging and insulin-like growth factor-1 on synapses in CA1 of rat hippocampus. Cereb. Cortex 2005, 15:571-577.
67. Shors T.J., Miesegaes G., Beylin A., Zhao M., Rydel T., Gould E. Neurogenesis in the adult is involved in the formation of trace memories. Nature 2001, 410:372-376.
68. Sutherland R.J., Whishaw I.Q., Kolb B. A behavioural analysis of spatial localization following electrolytic, kainate- or colchicine-induced damage to the hippocampal formation in the rat. Behav. Brain Res. 1983, 7:133-153.
69. Sweatt J.D. The neuronal MAP kinase cascade: a biochemical signal integration system subserving synaptic plasticity and memory. J. Neurochem. 2001, 76:1-10.
70. Sweatt J.D. Mitogen-activated protein kinases in synaptic plasticity and memory. Curr. Opin. Neurobiol. 2004, 14:311-317.
71. Thomas G.M., Rumbaugh G.R., Harrar D.B., Huganir R.L. Ribosomal S6 kinase 2 interacts with and phosphorylates PDZ domain-containing proteins and regulates AMPA receptor transmission. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:15006-15011.
72. Toni N., Buchs P.A., Nikonenko I., Povilaitite P., Parisi L., Muller D. Remodeling of synaptic membranes after induction of long-term potentiation. J. Neurosci. 2001, 21:6245-6251.
73. Touraine R.L., Zeniou M., Hanauer A. A syndromic form of X-linked mental retardation: the Coffin-Lowry syndrome. Eur. J. Pediatr. 2002, 161:179-187.
74. Trivier E., De Cesare D., Jacquot S., Pannetier S., Zackai E., Young I., et al. Mutations in the kinase Rsk-2 associated with Coffin-Lowry syndrome. Nature 1996, 384:567-570.
75. Tronson N.C., Taylor J.R. Molecular mechanisms of memory reconsolidation. Nat. Rev. Neurosci. 2007, 8:262-275.
76. Tu J.C., Xiao B., Naisbitt S., Yuan J.P., Petralia R.S., Brakeman P., et al. Coupling of mGluR/Homer and PSD-95 complexes by the Shank family of postsynaptic density proteins. Neuron 1999, 23:583-592.
77. Vaillend C., Poirier R., Laroche S. Genes, plasticity and mental retardation. Behav. Brain Res. 2008, 192:88-105.
78. Verpelli C., Dvoretskova E., Vicidomini C., Rossi F., Chiappalone M., Schoen M., et al. Importance of Shank3 protein in regulating metabotropic glutamate receptor 5 (mGluR5) expression and signaling at synapses. J. Biol. Chem. 2011, 286:34839-34850.
79. Vialou V., Robison A.J., Laplant Q.C., Covington H.E., Dietz D.M., Ohnishi Y.N., et al. DeltaFosB in brain reward circuits mediates resilience to stress and antidepressant responses. Nat. Neurosci. 2010, 13:745-752.
80. Wang X., McCoy P.A., Rodriguiz R.M., Pan Y., Je H.S., Roberts A.C., et al. Synaptic dysfunction and abnormal behaviors in mice lacking major isoforms of Shank3. Hum. Mol. Genet. 2011, 20:3093-3108.
81. Xing J., Ginty D.D., Greenberg M.E. Coupling of the RAS-MAPK pathway to gene activation by RSK2, a growth factor-regulated CREB kinase. Science 1996, 273:959-963.
82. Yang X., Matsuda K., Bialek P., Jacquot S., Masuoka H.C., Schinke T., et al. ATF4 is a substrate of RSK2 and an essential regulator of osteoblast biology; implication for Coffin-Lowry Syndrome. Cell 2004, 117:387-398.
83. Zeniou M., Ding T., Trivier E., Hanauer A. Expression analysis of RSK gene family members: the RSK2 gene, mutated in Coffin-Lowry syndrome, is prominently expressed in brain structures essential for cognitive function and learning. Hum. Mol. Genet. 2002, 11:2929-2940.
84. Zeniou-Meyer M., Liu Y., Béglé A., Olanich M.E., Hanauer A., Becherer U., et al. The Coffin-Lowry syndrome-associated protein RSK2 is implicated in calcium-regulated exocytosis through the regulation of PLD1. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:8434-8439.
85. Zeniou-Meyer M., Gambino F., Ammar M.R., Humeau Y., Vitale N. The Coffin-Lowry syndrome-associated protein RSK2 and neurosecretion. Cell. Mol. Neurobiol. 2010, 30:1401-1406.
86. Zucker R.S. Changes in the statistics of transmitter release during facilitation. J. Physiol. Lond. 1973, 229:787-810.