Probing synaptic function in dendrites with calcium imaging

Experimental Neurology

Volumn 242, Issue , 2013, Pages 27-32

  Siegel, Friederike ^a   Lohmann, Christian ^a  

^a NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

Author keywords

Spine; Synapse development; Synaptic plasticity; Two photon microscopy

Indexed keywords

CALCIUM; CHANNELRHODOPSIN 2; METABOTROPIC RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; RHODOPSIN; UNCLASSIFIED DRUG;

BRAIN ELECTROPHYSIOLOGY; BRAIN REGION; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL ACTIVATION; CELL POPULATION; CELL STIMULATION; CELLULAR DISTRIBUTION; DENDRITE; HIPPOCAMPUS; HUMAN; IN VIVO STUDY; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MOLECULAR DYNAMICS; MOLECULAR IMAGING; MOLECULAR PROBE; NEOCORTEX; NERVE CELL PLASTICITY; NEUROIMAGING; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; CALCIUM; DENDRITES; NEURONS; OPTICAL IMAGING; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 84875056012     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2012.02.007     Document Type: Review

References (103)

1. Albantakis L., Lohmann C. A simple method for quantitative calcium imaging in unperturbed developing neurons. J. Neurosci. Methods 2009, 184:206-212.
2. Allene C., Cossart R. Early NMDA receptor-driven waves of activity in the developing neocortex: physiological or pathological network oscillations?. J. Physiol. 2010, 588:83-91.
3. Araya R., Jiang J., Eisenthal K.B., Yuste R. The spine neck filters membrane potentials. Proc. Natl. Acad. Sci. 2006, 103:17961-17966.
4. Augustine G.J., Santamaria F., Tanaka K. Local calcium signaling in neurons. Neuron 2003, 40:331-346.
5. Berridge M.J., Lipp P., Bootman M.D. The versatility and universality of calcium signalling. Nat. Rev. Mol. Cell Biol. 2000, 1:11-21.
6. Bloodgood B.L., Sabatini B.L. Neuronal activity regulates diffusion across the neck of dendritic spines. Science 2005, 310:866-869.
7. Bloodgood B.L., Sabatini B.L. Nonlinear regulation of unitary synaptic signals by CaV(2.3) voltage-sensitive calcium channels located in dendritic spines. Neuron 2007, 53:249-260.
8. Bloodgood B.L., Giessel A.J., Sabatini B.L. Biphasic synaptic Ca influx arising from compartmentalized electrical signals in dendritic spines. PLoS Biol. 2009, 7:e1000190.
9. Bollmann J.H., Engert F. Subcellular topography of visually driven dendritic activity in the vertebrate visual system. Neuron 2009, 61:895-905.
10. Boyden E.S., Zhang F., Bamberg E., Nagel G., Deisseroth K. Millisecond-timescale, genetically targeted optical control of neural activity. Nat. Neurosci. 2005, 8:1263-1268.
11. Branco T., Clark B.A., Hausser M. Dendritic discrimination of temporal input sequences in cortical neurons. Science 2010, 329:1671-1675.
12. Cavazzini M., Bliss T., Emptage N. Ca2+ and synaptic plasticity. Cell Calcium 2005, 38:355-367.
13. Chen X., Leischner U., Rochefort N.L., Nelken I., Konnerth A. Functional mapping of single spines in cortical neurons in vivo. Nature 2011, 475:501-505.
14. Cornelisse L.N., van Elburg R.A., Meredith R.M., Yuste R., Mansvelder H.D. High speed two-photon imaging of calcium dynamics in dendritic spines: consequences for spine calcium kinetics and buffer capacity. PLoS One 2007, 2:e1073.
15. Dan Y., Poo M.M. Spike timing-dependent plasticity of neural circuits. Neuron 2004, 44:23-30.
16. Denk W., Yuste R., Svoboda K., Tank D.W. Imaging calcium dynamics in dendritic spines. Curr. Opin. Neurobiol. 1996, 6:372-378.
17. Elyada Y.M., Haag J., Borst A. Different receptive fields in axons and dendrites underlie robust coding in motion-sensitive neurons. Nat. Neurosci. 2009, 12:327-332.
18. Fine A., Amos W.B., Durbin R.M., McNaughton P.A. Confocal microscopy: applications in neurobiology. Trends Neurosci. 1988, 11:346-351.
19. Goldberg J.H., Tamas G., Aronov D., Yuste R. Calcium microdomains in aspiny dendrites. Neuron 2003, 40:807-821.
20. Golding N.L., Jung H.Y., Mickus T., Spruston N. Dendritic calcium spike initiation and repolarization are controlled by distinct potassium channel subtypes in CA1 pyramidal neurons. J. Neurosci. 1999, 19:8789-8798.
21. Golding N.L., Staff N.P., Spruston N. Dendritic spikes as a mechanism for cooperative long-term potentiation. Nature 2002, 418:326-331.
22. Govindarajan A., Kelleher R.J., Tonegawa S. A clustered plasticity model of long-term memory engrams. Nat. Rev. Neurosci. 2006, 7:575-583.
23. Grewe B.F., Langer D., Kasper H., Kampa B.M., Helmchen F. High-speed in vivo calcium imaging reveals neuronal network activity with near-millisecond precision. Nat. Methods 2010, 7:399-405.
24. 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.
25. Harvey C.D., Svoboda K. Locally dynamic synaptic learning rules in pyramidal neuron dendrites. Nature 2007, 450:1195-1200.
26. Harvey C.D., Yasuda R., Zhong H., Svoboda K. The spread of ras activity triggered by activation of a single dendritic spine. Science 2008, 321:136-140.
27. Helmchen F., Imoto K., Sakmann B. Ca2+ buffering and action potential-evoked Ca2+ signaling in dendrites of pyramidal neurons. Biophys. J. 1996, 70:1069-1081.
28. Higley M.J., Sabatini B.L. Calcium signaling in dendrites and spines: practical and functional considerations. Neuron 2008, 59:902-913.
29. Holthoff K., Kovalchuk Y., Yuste R., Konnerth A. Single-shock LTD by local dendritic spikes in pyramidal neurons of mouse visual cortex. J. Physiol. 2004, 560:27-36.
30. Holtmaat A., De Paola V., Wilbrecht L., Knott G.W. Imaging of experience-dependent structural plasticity in the mouse neocortex in vivo. Behav. Brain Res. 2008, 192:20-25.
31. Homma R., Baker B.J., Jin L., Garaschuk O., Konnerth A., Cohen L.B., Zecevic D. Wide-field and two-photon imaging of brain activity with voltage- and calcium-sensitive dyes. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2009, 364:2453-2467.
32. Ji N., Magee J.C., Betzig E. High-speed, low-photodamage nonlinear imaging using passive pulse splitters. Nat. Methods 2008, 5:197-202.
33. Jia H., Rochefort N.L., Chen X., Konnerth A. Dendritic organization of sensory input to cortical neurons in vivo. Nature 2010, 464:1307-1312.
34. Katona G., Kaszas A., Turi G.F., Hajos N., Tamas G., Vizi E.S., Rozsa B. Roller coaster scanning reveals spontaneous triggering of dendritic spikes in CA1 interneurons. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:2148-2153.
35. Katz Y., Menon V., Nicholson D.A., Geinisman Y., Kath W.L., Spruston N. Synapse distribution suggests a two-stage model of dendritic integration in CA1 pyramidal neurons. Neuron 2009, 63:171-177.
36. Kitamura K., Judkewitz B., Kano M., Denk W., Hausser M. Targeted patch-clamp recordings and single-cell electroporation of unlabeled neurons in vivo. Nat. Methods 2008, 5:61-67.
37. Kleindienst T., Lohmann C. Simultaneous patch-clamping and calcium imaging in developing dendrites. Imaging in Developmental Biology 2010, 491-499. Cold Spring Harbor Laboratory Press. J. Sharpe, R.O. Wong, R. Yuste (Eds.).
38. Kleindienst, T., Winnubst, J., Roth-Alpermann, C., Bonhoeffer, T., Lohmann, C., 2011. Activity-dependent clustering of functional synaptic inputs on developing hippocampal dendrites. Neuron. 72, 1012-1024.
39. Koester H.J., Sakmann B. Calcium dynamics in single spines during coincident pre- and postsynaptic activity depend on relative timing of back-propagating action potentials and subthreshold excitatory postsynaptic potentials. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:9596-9601.
40. Komiyama T., Sato T.R., 'Connor D.H., Zhang Y.X., Huber D., Hooks B.M., Gabitto M., Svoboda K. Learning-related fine-scale specificity imaged in motor cortex circuits of behaving mice. Nature 2010, 464:1182-1186.
41. Kovalchuk Y., Eilers J., Lisman J., Konnerth A. NMDA receptor-mediated subthreshold Ca(2+) signals in spines of hippocampal neurons. J. Neurosci. 2000, 20:1791-1799.
42. Larkum M.E., Nevian T. Synaptic clustering by dendritic signalling mechanisms. Curr. Opin. Neurobiol. 2008, 18:321-331.
43. Larkum M.E., Nevian T., Sandler M., Polsky A., Schiller J. Synaptic integration in tuft dendrites of layer 5 pyramidal neurons: a new unifying principle. Science 2009, 325:756-760.
44. Lee S.J., Escobedo-Lozoya Y., Szatmari E.M., Yasuda R. Activation of CaMKII in single dendritic spines during long-term potentiation. Nature 2009, 458:299-304.
45. Lohmann C. Calcium signaling and the development of specific neuronal connections. Prog. Brain Res. 2009, 175:443-452.
46. Losonczy A., Magee J.C. Integrative properties of radial oblique dendrites in hippocampal CA1 pyramidal neurons. Neuron 2006, 50:291-307.
47. Losonczy A., Makara J.K., Magee J.C. Compartmentalized dendritic plasticity and input feature storage in neurons. Nature 2008, 452:436-441.
48. Magee J.C., Johnston D. Plasticity of dendritic function. Curr. Opin. Neurobiol. 2005, 15:334-342.
49. Mainen Z.F., Maletic-Savatic M., Shi S.H., Hayashi Y., Malinow R., Svoboda K. Two-photon imaging in living brain slices. Methods 1999, 18(231-9):181.
50. Mainen Z.F., Malinow R., Svoboda K. Synaptic calcium transients in single spines indicate that NMDA receptors are not saturated. Nature 1999, 399:151-155.
51. Majewska A., Brown E., Ross J., Yuste R. Mechanisms of calcium decay kinetics in hippocampal spines: role of spine calcium pumps and calcium diffusion through the spine neck in biochemical compartmentalization. J. Neurosci. 2000, 20:1722-1734.
52. Major G., Polsky A., Denk W., Schiller J., Tank D.W. Spatiotemporally graded NMDA spike/plateau potentials in basal dendrites of neocortical pyramidal neurons. J. Neurophysiol. 2008, 99:2584-2601.
53. Malenka R.C., Bear M.F. LTP and LTD: an embarrassment of riches. Neuron 2004, 44:5-21.
54. Maravall M., Mainen Z.F., Sabatini B.L., Svoboda K. Estimating intracellular calcium concentrations and buffering without wavelength ratioing. Biophys. J. 2000, 78:2655-2667.
55. Markram H., Lubke J., Frotscher M., Sakmann B. Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 1997, 275:213-215.
56. Mrsic-Flogel T.D., Hofer S.B., Ohki K., Reid R.C., Bonhoeffer T., Hubener M. Homeostatic regulation of eye-specific responses in visual cortex during ocular dominance plasticity. Neuron 2007, 54:961-972.
57. Muller W., Connor J.A. Dendritic spines as individual neuronal compartments for synaptic Ca2+ responses. Nature 1991, 354:73-76.
58. Nagayama S., Zeng S., Xiong W., Fletcher M.L., Masurkar A.V., Davis D.J., Pieribone V.A., Chen W.R. In vivo simultaneous tracing and ca(2+) imaging of local neuronal circuits. Neuron 2007, 53:789-803.
59. Nevian T., Sakmann B. Single spine Ca2+ signals evoked by coincident EPSPs and backpropagating action potentials in spiny stellate cells of layer 4 in the juvenile rat somatosensory barrel cortex. J. Neurosci. 2004, 24:1689-1699.
60. Nevian T., Sakmann B. Spine Ca2+ Signaling in Spike-Timing-Dependent Plasticity. J. Neurosci. 2006, 26:11001-11013.
61. Nimchinsky E.A., Sabatini B.L., Svoboda K. Structure and function of dendritic spines. Annu. Rev. Physiol. 2002, 64:313-353.
62. Nimchinsky E.A., Yasuda R., Oertner T.G., Svoboda K. The number of glutamate receptors opened by synaptic stimulation in single hippocampal spines. J. Neurosci. 2004, 24:2054-2064.
63. Noguchi J., Matsuzaki M., Ellis-Davies G.C., Kasai H. Spine-neck geometry determines NMDA receptor-dependent Ca2+ signaling in dendrites. Neuron 2005, 46:609-622.
64. Oertner T.G., Sabatini B.L., Nimchinsky E.A., Svoboda K. Facilitation at single synapses probed with optical quantal analysis. Nat. Neurosci. 2002, 5:657-664.
65. Ohki K., Chung S., Ch'ng Y.H., Kara P., Reid R.C. Functional imaging with cellular resolution reveals precise micro-architecture in visual cortex. Nature 2005, 433:597-603.
66. Peterka D.S., Takahashi H., Yuste R. Imaging voltage in neurons. Neuron 2011, 69:9-21.
67. Petrozzino J.J., Pozzo Miller L.D., Connor J.A. Micromolar Ca2+ transients in dendritic spines of hippocampal pyramidal neurons in brain slice. Neuron 1995, 14:1223-1231.
68. Poirazi P., Mel B.W. Impact of active dendrites and structural plasticity on the memory capacity of neural tissue. Neuron 2001, 29:779-796.
69. Polsky A., Mel B.W., Schiller J. Computational subunits in thin dendrites of pyramidal cells. Nat. Neurosci. 2004, 7:621-627.
70. Qiu D.L., Akemann W., Chu C.P., Araki R., Knopfel T. Targeted optical probing of neuronal circuit dynamics using fluorescent protein sensors. Neurosignals 2008, 16:289-299.
71. Regehr W.G., Tank D.W. Calcium concentration dynamics produced by synaptic activation of CA1 hippocampal pyramidal cells. J. Neurosci. 1992, 12:4202-4223.
72. Rickgauer J.P., Tank D.W. Two-photon excitation of channelrhodopsin-2 at saturation. Proc. Natl. Acad. Sci. 2009, 106:15025-15030.
73. Rochefort N.L., Garaschuk O., Milos R.I., Narushima M., Marandi N., Pichler B., Kovalchuk Y., Konnerth A. Sparsification of neuronal activity in the visual cortex at eye-opening. Proc. Natl. Acad. Sci. 2009, 106:15049-15054.
74. Ross W.N., Nakamura T., Watanabe S., Larkum M., Lasser-Ross N. Synaptically activated ca2+ release from internal stores in CNS neurons. Cell. Mol. Neurobiol. 2005, 25:283-295.
75. Sabatini B.L., Svoboda K. Analysis of calcium channels in single spines using optical fluctuation analysis. Nature 2000, 408:589-593.
76. Sabatini B.L., Oertner T.G., Svoboda K. The life cycle of Ca(2+) ions in dendritic spines. Neuron 2002, 33:439-452.
77. Scanziani M., Hausser M. Electrophysiology in the age of light. Nature 2009, 461:930-939.
78. Schiller J., Schiller Y., Stuart G., Sakmann B. Calcium action potentials restricted to distal apical dendrites of rat neocortical pyramidal neurons. J. Physiol. 1997, 505(Pt 3):605-616.
79. Schiller J., Schiller Y., Clapham D.E. NMDA receptors amplify calcium influx into dendritic spines during associative pre- and postsynaptic activation. Nat. Neurosci. 1998, 1:114-118.
80. Schiller J., Major G., Koester H.J., Schiller Y. NMDA spikes in basal dendrites of cortical pyramidal neurons. Nature 2000, 404:285-289.
81. Schoenenberger P., Scharer Y.P., Oertner T.G. Channelrhodopsin as a tool to investigate synaptic transmission and plasticity. Exp. Physiol. 2011, 96:34-39.
82. Segal M. Changing views of Cajal's neuron: the case of the dendritic spine. Prog. Brain Res. 2002, 136(101-7):101-107.
83. Segev I., Rall W. Computational study of an excitable dendritic spine. J. Neurophysiol. 1988, 60:499-523.
84. Smith S.L., Hausser M. Parallel processing of visual space by neighboring neurons in mouse visual cortex. Nat. Neurosci. 2010, 13:1144-1149.
85. Stosiek C., Garaschuk O., Holthoff K., Konnerth A. In vivo two-photon calcium imaging of neuronal networks. Proc. Natl. Acad. Sci. 2003, 100:7319-7324.
86. 2+]: intracellular stores spill their guts. Neuron 1999, 22:427-430.
87. Svoboda K., Yasuda R. Principles of two-photon excitation microscopy and its applications to neuroscience. Neuron 2006, 50:823-839.
88. Svoboda K., Tank D.W., Denk W. Direct measurement of coupling between dendritic spines and shafts. Science 1996, 272:716-719.
89. Svoboda K., Denk W., Kleinfeld D., Tank D.W. In vivo dendritic calcium dynamics in neocortical pyramidal neurons. Nature 1997, 385:161-165.
90. Tao H.W., Zhang L.I., Engert F., Poo M. Emergence of input specificity of ltp during development of retinotectal connections in vivo. Neuron 2001, 31:569-580.
91. Waters J., Helmchen F. Boosting of action potential backpropagation by neocortical network activity in vivo. J. Neurosci. 2004, 24:11127-11136.
92. Wei D.S., Mei Y.A., Bagal A., Kao J.P., Thompson S.M., Tang C.M. Compartmentalized and binary behavior of terminal dendrites in hippocampal pyramidal neurons. Science 2001, 293:2272-2275.
93. Wilt B.A., Burns L.D., Wei Ho E.T., Ghosh K.K., Mukamel E.A., Schnitzer M.J. Advances in light microscopy for neuroscience. Annu. Rev. Neurosci. 2009, 32:435-506.
94. Yasuda R., Nimchinsky E.A., Scheuss V., Pologruto T.A., Oertner T.G., Sabatini B.L., Svoboda K. Imaging calcium concentration dynamics in small neuronal compartments. Sci. STKE 2004, 2004:l5.
95. Yuste R., Denk W. Dendritic spines as basic functional units of neuronal integration. Nature 1995, 375:682-684.
96. Yuste R., Majewska A., Cash S.S., Denk W. Mechanisms of calcium influx into hippocampal spines: heterogeneity among spines, coincidence detection by NMDA receptors, and optical quantal analysis. J. Neurosci. 1999, 19:1976-1987.
97. Yuste R., Majewska A., Holthoff K. From form to function: calcium compartmentalization in dendritic spines. Nat. Neurosci. 2000, 3:653-659.
98. Zhang Y.P., Oertner T.G. Optical induction of synaptic plasticity using a light-sensitive channel. Nat. Methods 2007, 4:139-141.
99. Zhang F., Aravanis A.M., Adamantidis A., de Lecea L., Deisseroth K. Circuit-breakers: optical technologies for probing neural signals and systems. Nat. Rev. Neurosci. 2007, 8:577-581.
100. Zhang Y.P., Holbro N., Oertner T.G. Optical induction of plasticity at single synapses reveals input-specific accumulation of alpha CaMKII. Proc. Natl. Acad. Sci. 2008, 105:12039-12044.
101. Zhu P., Narita Y., Bundschuh S.T., Fajardo O., Scharer Y.P., Chattopadhyaya B., Bouldoires E.A., Stepien A.E., Deisseroth K., Arber S., Sprengel R., Rijli F.M., Friedrich R.W. Optogenetic dissection of neuronal circuits in zebrafish using viral gene transfer and the tet system. Front. Neural Circ. 2009, 3:21.
102. Zito K., Scheuss V., Knott G., Hill T., Svoboda K. Rapid functional maturation of nascent dendritic spines. Neuron 2009, 61:247-258.
103. Zucker R.S. Calcium- and activity-dependent synaptic plasticity. Curr. Opin. Neurobiol. 1999, 9:305-313.