Biophysical properties of presynaptic short-term plasticity in hippocampal neurons: Insights from electrophysiology, imaging and mechanistic models

Frontiers in Cellular Neuroscience

Volumn 8, Issue MAY, 2014, Pages

  Dutta Roy, Ranjita ^a,b   Stefan, Melanie I ^c   Rosenmund, Christian ^b  

^a KAROLINSKA INSTITUTE   (Sweden)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Biophysical models; Electrophysiology; Hippocampal neurons; Imaging; Short term plasticity; Vesicle dynamics

Indexed keywords

NEURONAL CALCIUM SENSOR; PLASMA MEMBRANE CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; SNARE PROTEIN; SODIUM CALCIUM EXCHANGE PROTEIN; SYNAPTOTAGMIN;

ACTION POTENTIAL; BIOPHYSICS; BRAIN ELECTROPHYSIOLOGY; CALCIUM BINDING; CELL FUSION; ENDOCYTOSIS; HIPPOCAMPAL NEURONAL CULTURE; MOLECULAR DOCKING; NERVE CELL PLASTICITY; NEUROTRANSMITTER RELEASE; REVIEW; SYNAPSE VESICLE; SYNAPTIC POTENTIAL;

EID: 84901390484     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2014.00141     Document Type: Review

References (78)

1. Auger, C., and Marty, A. (2000). Quantal currents at single-site central synapses. J. Physiol. 526, 3-11. doi: 10.1111/j.1469-7793.2000.t01-3-00003.x
2. Basu, J., Betz, A., Brose, N., and Rosenmund, C. (2007). Munc13-1 C1 domain activation lowers the energy barrier for synaptic vesicle fusion. J. Neurosci. 27, 1200-1210. doi: 10.1523/JNEUR0SCI.4908-06.2007
3. Bekkers, J. M., Richerson, G. B., and Stevens, C. F. (1990). Origin of vari-ability in quantal size in cultured hippocampal neurons and hippocampal slices. Proc. Natl. Acad. Sci. U.S.A. 87, 5359-5362. doi: 10.1073/pnas.87. 14.5359
4. Berggard, T., Miron, S., Onnerfjord, P., Thulin, E., Akerfeldt, K. S., Enghild, J. J., et al. (2002). Calbindin D28k exhibits properties characteristic of a Ca2+ sensor. J. Biol. Chem. 277, 16662-16672. doi: 10.1074/jbc.M200415200
5. Bischofberger, J., Geiger, J. R. P., and Jonas, P. (2002). Timing and efficacy of Ca2+ channel activation in hippocampal mossy fiber boutons. J. Neurosci. 22, 10593-10602.
6. Blakely, R. D., and Edwards, R. H. (2012). Vesicular and plasma membrane trans-porters for neurotransmitters. Cold Spring Harb. Perspect. Biol. 4, 1-24. doi: 10.1101/cshperspect.a005595
7. Boyken, J., Grønborg, M., Riedel, D., Urlaub, H., Jahn, R., and Chua, J. J. (2013). Molecular profiling of synaptic vesicle docking sites reveals novel proteins but few differences between glutamatergic and GABAergic synapses. Neuron 78, 285-297. doi: 10.1016/j.neuron.2013.02.027
8. Brini, M. (2009) Plasmamembrane Ca(2+)-ATPase: from ahousekeepingfunction to aversatile signalingrole. PugersArch. 457, 657-664. doi: 10.1007/s00424-008-0505-6
9. Bruton, J. D., Katz, A., andWesterblad, H. (1999). Insulin increases near-membrane but not global Ca2+ in isolated skeletal muscle. Proc. Natl. Acad. Sci. U.S.A. 96, 3281-3286. doi: 10.1073/pnas.96.6.3281
10. Carter, A. G., Vogt, K. E., Foster, K. A., and Regehr, W. G. (2002). Assessing the role of calcium-induced calcium release in short-term presynaptic plasticity at excitatorycentral synapses. J. Neurosci. 22, 21-28.
11. Ceccarelli, B., Hurlbut, W. P., and Mauro, A. (1973). Turnover of transmitter and synaptic vesicles at the frog neuromuscular junction. J. Cell Biol. 57, 499-524. doi: 10.1083/jcb.57.2.499
12. Christie, J. M., and Jahr, C. E. (2006). Multivesicular release at schaf-fer collateral-CA1 hippocampal synapses. J. Neurosci. 26, 210-216. doi: 10.1523/JNEUR0SCI.4307-05.2006
13. Dodge, F. A., and Rahamimoff, R. (1967). On the relationship between calcium concentration and the amplitude of the end-plate potential. J. Physiol. 189, 90-92.
14. Eggermann, E., Bucurenciu, I., Goswami, S. P., and Jonas, P. (2012). Nanodomain coupling between Ca2+ channels and sensors of exocytosis at fast mammalian synapses. Nat. Rev. Neurosci. 13, 7-21. doi: 10.1038/nrn3125
15. Felmy, F., Neher, E., and Schneggenburger, R. (2003). Probing the intracellular cal-cium sensitivity of transmitter release during synaptic facilitation. Neuron 37, 801-811. doi: 10.1016/S0896-6273(03)00085-0
16. Froc, D. J., Eadie, B., Li, A. M., Wodtke, K., Tse, M., and Christie, B. R. (2003). Reduced synaptic plasticity in the lateral perforant path input to the dentate gyrus of aged C57BL/6 mice. J. Neurophysiol. 90, 32-38. doi: 10.1152/jn.00105.2003
17. Gandhi, S. P., and Stevens, C. F. (2003). Three modes of synaptic vesicu-lar recycling revealed by single-vesicle imaging. Nature 423, 607-613. doi: 10.1038/nature01677
18. Goda, Y., and Stevens, C. F. (1994). Two components of transmitter release at a central synapse. Proc. Natl. Acad. Sci. U.S.A. 91, 12942-12946. doi: 10.1073/pnas.91.26.12942
19. Granseth, B., and Lagnado, L. (2008). The role of endocytosis in regulat-ing the strength of hippocampal synapses. J. Physiol. 586, 5969-5982. doi: 10.1113/jphysiol.2008.159715
20. Granseth, B., Odermatt, B., Royle, S. J., and Lagnado, L. (2006). Clathrin-mediated endocytosis is the dominant mechanism of vesicle retrieval at hippocampal synapses. Neuron 51, 773-786. doi: 10.1016/j.neuron.2006.08.029
21. Hallermann, S., Pawlu, C., Jonas, P., and Heckmann, M. (2003). A large pool of releasable vesicles in a cortical glutamatergic synapse. Proc. Natl. Acad. Sci. U.S.A. 100, 8975-8980. doi: 10.1073/pnas.1432836100
22. Hanse, E., and Gustafsson, B. (2001). Factors explaining heterogeneity in short-term synaptic dynamics of hippocampal glutamatergic synapses in the neonatal rat. J. Physiol. 537, 141-149. doi: 10.1111/j.1469-7793.2001. 0141k.x
23. Hefft, S., and Jonas, P. (2005). Asynchrounous GABA release generates long-lasting inhibition at a hippocampal interneuron-principal neuron synapse. Nat. Neurosci. 8, 1319-1328. doi: 10.1038/nn1542
24. Heuser, J. E., and Reese, T. S. (1973). Evidence for recycling ofsynapticvesicle mem-brane duringtransmitter release at the frogneuromuscularjunction. J. CellBiol. 57, 315-344. doi: 10.1083/jcb.57.2.315
25. Heuser, J. E., Reese, T. S., Dennis, M. J., Jan, Y., Jan, L., and Evans, L. (1979). Synaptic vesicle exocytosis captured by quick freezing and correlated with quantal transmitter release. J. CellBiol. 81, 275-300. doi: 10.1083/jcb.81.2.275
26. Holderith, N., Lorincz, A., Katona, G., Rozsa, B., Kulik, A., Watanabe, M., et al. (2012). Release probability of hippocampal glutamatergic terminals scales with the size of the active zone. Nat. Neurosci. 15, 988-997. doi: 10.1038/nn.3137
27. Hori, T., and Takahashi, T. (2012). Kinetics of synaptic vesicle refillingwith neuro-transmitter glutamate. Neuron 76, 511-517. doi: 10.1016/j.neuron.2012.08.013
28. Jouvenceau, A., Potier, B., Battini, R., Ferrari, S., Dutar, P., and Billard, J. M. (1999). Glutamatergic synaptic responses and long-term potentiation are impaired in the CA1 hippocampal area of calbindin D(28k)-deficient mice. Synapse 33, 172-180. doi: 10.1002/(SICI)1098-2396(19990901)33:3< 172::AID-SYN2>3.0.C0;2-S
29. Kaeser, P. S., and Regehr, W. G. (2014). Molecular mechanisms for synchronous, asynchronous, and spontaneous neurotransmitter release. Annu. Rev. Physiol. 76, 333-363. doi: 10.1146/annurev-physiol-021113-170338
30. Kamin, D., Lauterbach, M. A., Westphal, V., Keller, J., Schonle, A., Hell, S. W., et al. (2010). High-and low-mobility stages in the synaptic vesicle cycle. Biophys. J. 99, 675-684. doi: 10.1016/j.bpj.2010.04.054
31. Katz, B., and Miledi, R. (1968). The role of calcium in neuromuscular facilitation. J. Physiol. 195, 481-492.
32. Katz, B., and Miledi, R. (1963). A study of spontaneous miniature potentials in spinal motoneurones. J. Physiol. 168, 389-422.
33. Koester, H. J., and Sakmann, B. (2000). Calcium dynamics associated with action potentials in single nerve terminals of pyramidal cells in layer 2/3 of the young rat neocortex. J. Physiol. 529, 625-646. doi: 10.1111/j.1469-7793.2000.00625.x
34. Lee, J. S., Ho, W. K., and Lee, S. H. (2012). Actin-dependent rapid recruitment of reluctant synapticvesicles into afast-releasingvesicle pool. Proc. Natl. Acad. Sci. U.S.A. 109, E765-E774. doi: 10.1073/pnas.1114072109
35. Locke, J. C. W., Westermark, P. O., Kramer, A., and Herzel, H. (2008). Global parameter search reveals design principles of the mammalian circadian clock. BMCSyst. Biol. 2:22. doi: 10.1186/1752-0509-2-22
36. Martin, T. F. (2001). Pi(4, 5)p(2) regulation of surface membrane traffic. Curr. Opin. CellBiol. 13, 493-499. doi: 10.1016/S0955-0674(00)00241-6
37. Meinrenken, C. J., Borst, J. G. G., and Sakmann, B. (2003). Local routes revisited: the space and time dependence of the Ca2+ signal for phasic transmitter release at the rat calyx of Held. J. Physiol. 547, 665-689. doi: 10.1111/j.2003.t01-1-00665.x
38. Moulder, K. L., and Mennerick, S. (2005). Reluctant vesicles contribute to the total readily releasable pool in glutamatergic hippocampal neurons. J. Neurosci. 25, 3842-3850. doi: 10.1523/JNEUR0SCI.5231-04.2005
39. Murthy, VN., and Stevens, C. F. (1999). Reversal of synaptic vesicle docking at central synapses. Nat. Neurosci. 2, 503-507. doi: 10.1038/9149
40. Nadkarni, S., Bartol, T. M., Sejnowski, T. J., and Levine, H. (2010). Modelling vesicular release at hippocampal synapses. PLoS Comput. Biol. 6:e1000983. doi: 10.1371/journal.pcbi.1000983
41. Nadkarni, S., Bartol, T. M., Stevens, C. F., Sejnowski, T. J., Levine, H. (2012). Short-term plasticity constrains spatial organization of a hippocam-pal presynaptic terminal. Proc. Natl. Acad. Sci. U.S.A. 109, 14657-14662. doi: 10.1073/pnas.1211971109
42. Neher, E. (2010). What is rate-limiting during sustained synaptic activity: vesicle supply or the availability Of release sites. Front. Synaptic Neurosci. 2:144. doi: 10.3389/fnsyn.2010.00144
43. Neher, E., and Sakaba, T. (2008). Multiple roles of calcium ions in the regulation of neurotransmitter release. Neuron 59, 861-872. doi: 10.1016/j.neuron.2008. 08.019
44. Neves, G., Cooke, S. F., and Bliss, T. V. P. (2008). Synaptic plasticity, memory and the hippocampus: a neural network approach to causality. Nat. Rev. Neurosci. 9, 65-75. doi: 10.1038/nrn2303
45. Omote, H., Miyaji, T., Juge, N., and Moriyama, Y. (2011). Vesicular neuro-transmitter transporter: bioenergetics and regulation of glutamate transport. Biochemistry 50, 5558-5565. doi: 10.1021/bi200567k
46. Pan, B., and Zucker, R. S. (2009). A general model of synaptic transmission and short-term plasticity. Neuron 62, 539-554. doi: 10.1016/j.neuron.2009.03.025
47. Pyott, S. J., and Rosenmund, C. (2002). The effects of temperature on vesicular supply and release in autaptic cultures of rat and mouse hippocampal neurons. J. Physiol. 539, 523-535. doi: 10.1113/jphysiol.2001.013277
48. Rizo, J., and Rosenmund, C. (2008). Synaptic vesicle fusion. Nat. Struct. Mol. Biol. 15, 665-674. doi: 10.1038/nsmb.1450
49. Rodrigue, N., and Philippe, H. (2010). Mechanistic revisions of phenomenologi-cal modeling strategies in molecular evolution. Trends Genet. 26, 248-252. doi: 10.1016/j.tig.2010.04.001
50. Rohrbough, J., and Broadie, K. (2005). Lipid regulation of the synaptic vesicle cycle. Nat. Rev. Neurosci. 6, 139-150. doi: 10.1038/nrn1608
51. Rose, T., Schoenenberger, P., Jezek, K., and Oertner, T. G. (2013). Developmental refinement of vesicle cycling at Schaffer collateral synapses. Neuron 77, 1109-1121. doi: 10.1016/j.neuron.2013.01.021
52. Rosenmund, C., Rettig, J., and Brose, N. (2003). Molecular mechanisms of active zone function. Curr. Opin. Neurobiol. 13, 509-519. doi: 10.1016/j.conb.2003. 09.011
53. Rosenmund, C., and Stevens, C. F. (1996). Definition of the readily releasable pool ofvesicles at hippocampal synapses. Neuron 16, 1197-1207. doi: 10.1016/S0896-6273(00)80146-4
54. Ryan, T. A., Reuter, H., Wendland, B., Schweizer, F. E., Tsien, R. W., and Smith, S. J. (1993). The kinetics of synaptic vesicle recycling measured at single presynaptic boutons. Neuron 11, 713-724. doi: 10.1016/0896-6273(93)90081-2
55. Scheuss, V., Taschenberger, H., and Neher, E. (2007). Kinetics ofboth synchronous and asynchronous quantal release during trains of action potential-evoked EPSCs at the rat calyx of Held. J. Physiol. 585, 361-381. doi: 10.1113/jphys-iol.2007.140988
56. Schneggenburger, R., Meyer, A. C., andNeher, E. (1999). Releasedfraction andtotal size of a pool of immediately available transmitter quanta at a calyx synapse. Neuron 23, 399-409. doi: 10.1016/S0896-6273(00)80789-8
57. Schneggenburger, R., Sakaba, T., and Neher, E. (2002).Vesicle pools and short-term synaptic depression: lessons from alarge synapse. Trends Neurosci. 25, 206-212. doi: 10.1016/S0166-2236(02)02139-2
58. Shin, O. H., Lu, J., Rhee, J. S., Tomchick, D. R., Pang, Z. P., Wojcik, S. M., et al. (2010). Munc13 C2B domain is an activitydependent Ca2+ regulator ofsynaptic exocytosis. Nat. Struct. Mol. Biol. 17, 280-288. doi: 10.1038/nsmb.1758
59. Sorensen, J. B., Fernandez-Chacon, R., Sudhof, T. C., and Neher, E. (2003). Examining synaptotagmin 1 function in dense core vesicle exocyto-sis under direct control of Ca2+. J. Gen. Physiol. 122, 265-276. doi: 10.1085/jgp.200308855
60. Stevens, C. F., and Wang, Y. (1995). Facilitation and depression at single central synapses. Neuron 14, 795-802. doi: 10.1016/0896-6273(95)90223-6
61. Sun, J., Pang, Z. P., Qin, D., Fahim, A. T., Adachi, R., and Sudhof, T. C. (2007). A dual-Ca2+-sensor model for neurotransmitter release in a central synapse. Nature 450, 676-682. doi: 10.1038/nature06308
62. Takamori, S., Holt, M., Stenius, K., Lemke, E. A., Grønborg, M., Riedel, D., et al. (2006). Molecular anatomy of a trafficking organelle. Cell 127, 831-846. doi: 10.1016/j.cell.2006.10.030
63. Toonen, R. F., Kochubey, O., de Wit, H., Gulyas-Kovacs, A., Konijnenburg, B., Sorensen, J. B., et al. (2006). Dissecting docking and tethering of secretory vesicles at the target membrane. EMBO J. 25, 3725-3737. doi: 10.1038/sj.emboj.7601256
64. Trommershauser, J., Schneggenburger, R., Zippelius, A., and Neher, E. (2003). Heterogeneous presynaptic release probabilities: functional relevance for short-term plasticity. Biophys.J. 84, 1563-1579.doi: 10.1016/S0006-3495(03)74967-4
65. Verhage, M., and Sorensen, J. B. (2008). Vesicle docking in regulated exocytosis. Traffic 9, 1414-1424. doi: 10.1111/j.1600-0854.2008.00759.x
66. Vyleta, N. P., and Smith, S. M. (2011). Spontaneous glutamate release is indepen-dent of calcium influx and tonically activated by the calcium-sensing receptor. J. Neurosci. 31, 4593-4606. doi: 10.1523/JNEUR0SCI.6398-10.2011
67. Walter, A. M., Groffen, A. J., Sorensen, J. B., andVerhage, M. (2011). Multiple Ca2+ sensors in secretion:teammates, competitors or autocrats? Trends Neurosci. 34, 487-497. doi: 10.1016/j.tins.2011.07.003
68. Wan, Q. F., Nixon, E., and Heidelberger, R. (2012). Regulation of presynaptic calcium in a mammalian synaptic terminal. J. Neurophysiol. 108, 3059-3067. doi: 10.1152/jn.00213.2012
69. Wang, R., Hosaka, M., Han, L., Yokota-Hashimoto, H., Suda, M., Mitsushima, D., et al. (2006). Molecular probes for sensing the cholesterol composition of subcellular organelle membranes. Biochim. Biophys. Acta 1761, 1169-1181. doi: 10.1016/j.bbalip.2006.06.016
70. Wasser, C. R., and Kavalali, E. T. (2009). Leaky synapses: regulation of sponta-neous neurotransmission in central synapses. Neuroscience 158, 177-188. doi: 10.1016/j.neuroscience.2008.03.028
71. Watanabe, S., Rost, B. R., Camacho-Perez, M., Davis, M. W., Sohl-Kielczynski, B., Rosenmund, C., et al. (2013). Ultrafast endocytosis at mouse hippocampal synapses. Nature 504, 242-247. doi: 10.1038/nature12809
72. Witton, J., Brown, J. T., Jones, M. W., and Randall, A. D. (2010). Altered synaptic plasticity in the mossy fibre pathway of transgenic mice expressing mutant amyloid precursor protein. Mol. Brain 3, 32. doi: 10.1186/1756-6606-3-32
73. Wood, E. R., Dudchenko, P. A., Robitsek, R. J., and Eichenbaum, H. (2000). Hippocampal neurons encode information about different types of mem-ory episodes occurring in the same location. Neuron 27, 623-633. doi: 10.1016/S0896-6273(00)00071-4
74. Wu, L. G. (2004). Kinetic regulation of vesicle endocytosis at synapses. Trends Neurosci. 27, 548-554. doi: 10.1016/j.tins.2004.07.001
75. Wu, L. G., Hamid, E., Shin, W., and Chiang, H. C. (2014). Exocytosis and endo-cytosis: modes, functions, and coupling mechanisms. Annu. Rev. Physiol. 76, 301-331. doi: 10.1146/annurev-physiol-021113-170305
76. Xue, M., Stradomska, A., Chen, H., Brose, N., Zhang, W., Rosenmund, C., et al. (2008). Complexins facilitate neurotransmitter release at excitatory and inhibitory synapses in mammalian central nervous system. Proc. Natl. Acad. Sci. U.S.A. 105, 7875-7880. doi: 10.1073/pnas.0803012105
77. Zhang, Q., Li, Y., and Tsien, R. W. (2009). The dynamic control of kiss-and-run and vesicular reuse probed with single nanoparticles. Science 323, 1448-1453. doi: 10.1126/science.1167373
78. Zucker, R. S., and Regehr, W. G. (2002). Short-term synaptic plasticity. Annu. Rev. Physiol. 64, 355-405. doi: 10.1146/annurev.physiol.64.092501.114547