Calcium Signaling in Dendrites and Spines: Practical and Functional Considerations

Neuron

Volumn 59, Issue 6, 2008, Pages 902-913

  Higley, Michael J ^a   Sabatini, Bernardo L ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BUFFER; CALCIUM;

CALCIUM CELL LEVEL; CALCIUM SIGNALING; CELL COMPARTMENTALIZATION; DENDRITIC SPINE; FLUORESCENCE; HUMAN; IMAGING SYSTEM; KINETICS; LINEAR SYSTEM; NEUROIMAGING; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REVIEW;

ANIMALS; CALCIUM; CALCIUM CHANNELS; CALCIUM SIGNALING; CYTOPLASM; DENDRITES; DENDRITIC SPINES; FLUORESCENT DYES; HUMANS; MEMBRANE MICRODOMAINS; MODELS, NEUROLOGICAL; SECOND MESSENGER SYSTEMS; SYNAPTIC TRANSMISSION;

EID: 52049092533     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2008.08.020     Document Type: Review

References (139)

1. Amitai Y., Friedman A., Connors B.W., and Gutnick M.J. Regenerative activity in apical dendrites of pyramidal cells in neocortex. Cereb. Cortex 3 (1993) 26-38
2. Bender V.A., Bender K.J., Brasier D.J., and Feldman D.E. Two coincidence detectors for spike timing-dependent plasticity in somatosensory cortex. J. Neurosci. 26 (2006) 4166-4177
3. Bezprozvanny I., Watras J., and Ehrlich B.E. Bell-shaped calcium-response curves of Ins(1,4,5)P3- and calcium-gated channels from endoplasmic reticulum of cerebellum. Nature 351 (1991) 751-754
4. Bi G.Q., and Poo M.M. Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type. J. Neurosci. 18 (1998) 10464-10472
5. Bloodgood B.L., and Sabatini B.L. Nonlinear regulation of unitary synaptic signals by CaV(2.3) voltage-sensitive calcium channels located in dendritic spines. Neuron 53 (2007) 249-260
6. Brenowitz S.D., Best A.R., and Regehr W.G. Sustained elevation of dendritic calcium evokes widespread endocannabinoid release and suppression of synapses onto cerebellar Purkinje cells. J. Neurosci. 26 (2006) 6841-6850
7. Brown S.P., Brenowitz S.D., and Regehr W.G. Brief presynaptic bursts evoke synapse-specific retrograde inhibition mediated by endogenous cannabinoids. Nat. Neurosci. 6 (2003) 1048-1057
8. Burnashev N., Monyer H., Seeburg P.H., and Sakmann B. Divalent ion permeability of AMPA receptor channels is dominated by the edited form of a single subunit. Neuron 8 (1992) 189-198
9. Buzsaki G., and Draguhn A. Neuronal oscillations in cortical networks. Science 304 (2004) 1926-1929
10. Cai X., Liang C.W., Muralidharan S., Muralidharan S., Kao J.P., Tang C.M., and Thompson S.M. Unique roles of SK and Kv4.2 potassium channels in dendritic integration. Neuron 44 (2004) 351-364
11. Callaway J.C., and Ross W.N. Frequency-dependent propagation of sodium action potentials in dendrites of hippocampal CA1 pyramidal neurons. J. Neurophysiol. 74 (1995) 1395-1403
12. Carter A.G., and Sabatini B.L. State-dependent calcium signaling in dendritic spines of striatal medium spiny neurons. Neuron 44 (2004) 483-493
13. Carter A.G., Soler-Llavina G.J., and Sabatini B.L. Timing and location of synaptic inputs determine modes of subthreshold integration in striatal medium spiny neurons. J. Neurosci. 27 (2007) 8967-8977
14. Christie B.R., Eliot L.S., Ito K., Miyakawa H., and Johnston D. Different Ca2+ channels in soma and dendrites of hippocampal pyramidal neurons mediate spike-induced Ca2+ influx. J. Neurophysiol. 73 (1995) 2553-2557
15. Clements J.D., Lester R.A., Tong G., Jahr C.E., and Westbrook G.L. The time course of glutamate in the synaptic cleft. Science 258 (1992) 1498-1501
16. Colbran R.J., and Brown A.M. Calcium/calmodulin-dependent protein kinase II and synaptic plasticity. Curr. Opin. Neurobiol. 14 (2004) 318-327
17. Cormier R.J., Greenwood A.C., and Connor J.A. Bidirectional synaptic plasticity correlated with the magnitude of dendritic calcium transients above a threshold. J. Neurophysiol. 85 (2001) 399-406
18. In: Cowan W.M., Sudhof T.C., and Stevens C.F. (Eds). Synapses (2001), The Johns Hopkins University Press, Baltimore, MD
19. Cull-Candy S., Kelly L., and Farrant M. Regulation of Ca2+-permeable AMPA receptors: synaptic plasticity and beyond. Curr. Opin. Neurobiol. 16 (2006) 288-297
20. Dan Y., and Poo M.M. Spike timing-dependent plasticity of neural circuits. Neuron 44 (2004) 23-30
21. Day M., Wang Z., Ding J., An X., Ingham C.A., Shering A.F., Wokosin D., Ilijic E., Sun Z., Sampson A.R., et al. Selective elimination of glutamatergic synapses on striatopallidal neurons in Parkinson disease models. Nat. Neurosci. 9 (2006) 251-259
22. Denk W., Sugimori M., and Llinás R. Two types of calcium response limited to single spines in cerebellar Purkinje cells. Proc. Natl. Acad. Sci. USA 92 (1995) 8279-8282
23. Doering C.J., and Zamponi G.W. Molecular pharmacology of high voltage-activated calcium channels. J. Bioenerg. Biomembr. 35 (2003) 491-505
24. Dudman J.T., Tsay D., and Siegelbaum S.A. A role for synaptic inputs at distal dendrites: instructive signals for hippocampal long-term plasticity. Neuron 56 (2007) 866-879
25. Egger V., Svoboda K., and Mainen Z.F. Dendrodendritic synaptic signals in olfactory bulb granule cells: local spine boost and global low-threshold spike. J. Neurosci. 25 (2005) 3521-3530
26. Eilers J., Augustine G.J., and Konnerth A. Subthreshold synaptic Ca2+ signalling in fine dendrites and spines of cerebellar Purkinje neurons. Nature 373 (1995) 155-158
27. Emptage N., Bliss T.V., and Fine A. Single synaptic events evoke NMDA receptor-mediated release of calcium from internal stores in hippocampal dendritic spines. Neuron 22 (1999) 115-124
28. Faber E.S., Delaney A.J., and Sah P. SK channels regulate excitatory synaptic transmission and plasticity in the lateral amygdala. Nat. Neurosci. 8 (2005) 635-641
29. Farrant M., and Cull-Candy S.G. Excitatory amino acid receptor-channels in Purkinje cells in thin cerebellar slices. Proc. Biol. Sci. 244 (1991) 179-184
30. Fierro L., and Llano I. High endogenous calcium buffering in Purkinje cells from rat cerebellar slices. J. Physiol. 496 (1996) 617-625
31. Finch E.A., and Augustine G.J. Local calcium signalling by inositol-1,4,5-trisphosphate in Purkinje cell dendrites. Nature 396 (1998) 753-756
32. Finch E.A., Turner T.J., and Goldin S.M. Calcium as a coagonist of inositol 1,4,5-trisphosphate-induced calcium release. Science 252 (1991) 443-446
33. Fogelson A.L., and Zucker R.S. Presynaptic calcium diffusion from various arrays of single channels. Implications for transmitter release and synaptic facilitation. Biophys. J. 48 (1985) 1003-1017
34. Frick A., Magee J., Koester H.J., Migliore M., and Johnston D. Normalization of Ca2+ signals by small oblique dendrites of CA1 pyramidal neurons. J. Neurosci. 23 (2003) 3243-3250
35. Gabso M., Neher E., and Spira M.E. Low mobility of the Ca2+ buffers in axons of cultured Aplysia neurons. Neuron 18 (1997) 473-481
36. Gasparini S., Migliore M., and Magee J.C. On the initiation and propagation of dendritic spikes in CA1 pyramidal neurons. J. Neurosci. 24 (2004) 11046-11056
37. Gasparini S., Losonczy A., Chen X., Johnston D., and Magee J.C. Associative pairing enhances action potential back-propagation in radial oblique branches of CA1 pyramidal neurons. J. Physiol. 580 (2007) 787-800
38. Goldberg J.H., Tamas G., Aronov D., and Yuste R. Calcium microdomains in aspiny dendrites. Neuron 40 (2003) 807-821
39. Golding N.L., Jung H.Y., Mickus T., and Spruston N. Dendritic calcium spike initiation and repolarization are controlled by distinct potassium channel subtypes in CA1 pyramidal neurons. J. Neurosci. 19 (1999) 8789-8798
40. Golding N.L., Staff N.P., and Spruston N. Dendritic spikes as a mechanism for cooperative long-term potentiation. Nature 418 (2002) 326-331
41. Grynkiewicz G., Poenie M., and Tsien R.Y. A new generation of Ca2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 260 (1985) 3440-3450
42. Hartell N.A. Strong activation of parallel fibers produces localized calcium transients and a form of LTD that spreads to distant synapses. Neuron 16 (1996) 601-610
43. Helmchen F., Svoboda K., Denk W., and Tank D.W. In vivo dendritic calcium dynamics in deep-layer cortical pyramidal neurons. Nat. Neurosci. 2 (1999) 989-996
44. Henke W., Cetinsoy C., Jung K., and Loening S. Non-hyperbolic calcium calibration curve of Fura-2: implications for the reliability of quantitative Ca2+ measurements. Cell Calcium 20 (1996) 287-292
45. Hernandez-Cruz A., Sala F., and Adams P.R. Subcellular calcium transients visualized by confocal microscopy in a voltage-clamped vertebrate neuron. Science 247 (1990) 858-862
46. Hille B. Ion Channels of Excitable Membranes. Third Edition (2001), Sinauer Associates, Sunderland, MA
47. Holthoff K., Kovalchuk Y., Yuste R., and Konnerth A. Single-shock LTD by local dendritic spikes in pyramidal neurons of mouse visual cortex. J. Physiol. 560 (2004) 27-36
48. Hong M., and Ross W.N. Priming of intracellular calcium stores in rat CA1 pyramidal neurons. J. Physiol. 584 (2007) 75-87
49. Hoogland T.M., and Saggau P. Facilitation of L-type Ca2+ channels in dendritic spines by activation of beta2 adrenergic receptors. J. Neurosci. 24 (2004) 8416-8427
50. Inoue T., Kato K., Kohda K., and Mikoshiba K. Type 1 inositol 1,4,5-trisphosphate receptor is required for induction of long-term depression in cerebellar Purkinje neurons. J. Neurosci. 18 (1998) 5366-5373
51. Ismailov I., Kalikulov D., Inoue T., and Friedlander M.J. The kinetic profile of intracellular calcium predicts long-term potentiation and long-term depression. J. Neurosci. 24 (2004) 9847-9861
52. Isope P., and Murphy T.H. Low threshold calcium currents in rat cerebellar Purkinje cell dendritic spines are mediated by T-type calcium channels. J. Physiol. 562 (2005) 257-269
53. Jaffe D.B., Johnston D., Lasser-Ross N., Lisman J.E., Miyakawa H., and Ross W.N. The spread of Na+ spikes determines the pattern of dendritic Ca2+ entry into hippocampal neurons. Nature 357 (1992) 244-246
54. Jahr C.E., and Stevens C.F. A quantitative description of NMDA receptor-channel kinetic behavior. J. Neurosci. 10 (1990) 1830-1837
55. Kampa B.M., Letzkus J.J., and Stuart G.J. Requirement of dendritic calcium spikes for induction of spike-timing-dependent synaptic plasticity. J. Physiol. 574 (2006) 283-290
56. Kampa B.M., Letzkus J.J., and Stuart G.J. Dendritic mechanisms controlling spike-timing-dependent synaptic plasticity. Trends Neurosci. 30 (2007) 456-463
57. Kao J.P., and Tsien R.Y. Ca2+ binding kinetics of fura-2 and azo-1 from temperature-jump relaxation measurements. Biophys. J. 53 (1988) 635-639
58. Koester H.J., and 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. USA 95 (1998) 9596-9601
59. Koester H.J., and Sakmann B. 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 (2000) 625-646
60. Kovalchuk Y., Eilers J., Lisman J., and Konnerth A. NMDA receptor-mediated subthreshold Ca(2+) signals in spines of hippocampal neurons. J. Neurosci. 20 (2000) 1791-1799
61. Larkum M.E., Kaiser K.M., and Sakmann B. Calcium electrogenesis in distal apical dendrites of layer 5 pyramidal cells at a critical frequency of back-propagating action potentials. Proc. Natl. Acad. Sci. USA 96 (1999) 14600-14604
62. Larkum M.E., Zhu J.J., and Sakmann B. A new cellular mechanism for coupling inputs arriving at different cortical layers. Nature 398 (1999) 338-341
63. Lee S.H., Rosenmund C., Schwaller B., and Neher E. Differences in Ca2+ buffering properties between excitatory and inhibitory hippocampal neurons from the rat. J. Physiol. 525 (2000) 405-418
64. Lipscombe D., Helton T.D., and Xu W. L-type calcium channels: the low down. J. Neurophysiol. 92 (2004) 2633-2641
65. Llinás R., and Nicholson C. Electrophysiological properties of dendrites and somata in alligator Purkinje cells. J. Neurophysiol. 34 (1971) 532-551
66. Llinás R., and Hess R. Tetrodotoxin-resistant dendritic spikes in avian Purkinje cells. Proc. Natl. Acad. Sci. USA 73 (1976) 2520-2523
67. Llinás R.R., and Steriade M. Bursting of thalamic neurons and states of vigilance. J. Neurophysiol. 95 (2006) 3297-3308
68. Losonczy A., and Magee J.C. Integrative properties of radial oblique dendrites in hippocampal CA1 pyramidal neurons. Neuron 50 (2006) 291-307
69. Magee J.C., and Johnston D. A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons. Science 275 (1997) 209-213
70. Magee J.C., Christofi G., Miyakawa H., Christie B., Lasser-Ross N., and Johnston D. Subthreshold synaptic activation of voltage-gated Ca2+ channels mediates a localized Ca2+ influx into the dendrites of hippocampal pyramidal neurons. J. Neurophysiol. 74 (1995) 1335-1342
71. Mainen Z.F., Malinow R., and Svoboda K. Synaptic calcium transients in single spines indicate that NMDA receptors are not saturated. Nature 399 (1999) 151-155
72. Major G., Polsky A., Denk W., Schiller J., and Tank D.W. Spatiotemporally graded NMDA spike/plateau potentials in basal dendrites of neocortical pyramidal neurons. J. Neurophysiol. 99 (2008) 2584-2601
73. Maravall M., Mainen Z.F., Sabatini B.L., and Svoboda K. Estimating intracellular calcium concentrations and buffering without wavelength ratioing. Biophys. J. 78 (2000) 2655-2667
74. Markram H., and Sakmann B. Calcium transients in dendrites of neocortical neurons evoked by single subthreshold excitatory postsynaptic potentials via low-voltage-activated calcium channels. Proc. Natl. Acad. Sci. USA 91 (1994) 5207-5211
75. Markram H., Helm P.J., and Sakmann B. Dendritic calcium transients evoked by single back-propagating action potentials in rat neocortical pyramidal neurons. J. Physiol. 485 (1995) 1-20
76. Markram H., Lubke J., Frotscher M., and Sakmann B. Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 275 (1997) 213-215
77. McKay B.E., McRory J.E., Molineux M.L., Hamid J., Snutch T.P., Zamponi G.W., and Turner R.W. Ca(V)3 T-type calcium channel isoforms differentially distribute to somatic and dendritic compartments in rat central neurons. Eur. J. Neurosci. 24 (2006) 2581-2594
78. Milojkovic B.A., Zhou W.L., and Antic S.D. Voltage and calcium transients in basal dendrites of the rat prefrontal cortex. J. Physiol. 585 (2007) 447-468
79. Miyakawa H., Ross W.N., Jaffe D., Callaway J.C., Lasser-Ross N., Lisman J.E., and Johnston D. Synaptically activated increases in Ca2+ concentration in hippocampal CA1 pyramidal cells are primarily due to voltage-gated Ca2+ channels. Neuron 9 (1992) 1163-1173
80. Miyata M., Finch E.A., Khiroug L., Hashimoto K., Hayasaka S., Oda S.I., Inouye M., Takagishi Y., Augustine G.J., and Kano M. Local calcium release in dendritic spines required for long-term synaptic depression. Neuron 28 (2000) 233-244
81. Müller W., and Connor J.A. Dendritic spines as individual neuronal compartments for synaptic Ca2+ responses. Nature 354 (1991) 73-76
82. Nakamura T., Barbara J.G., Nakamura K., and Ross W.N. Synergistic release of Ca2+ from IP3-sensitive stores evoked by synaptic activation of mGluRs paired with backpropagating action potentials. Neuron 24 (1999) 727-737
83. Naraghi M. T-jump study of calcium binding kinetics of calcium chelators. Cell Calcium 22 (1997) 255-268
84. Neher E. Usefulness and limitations of linear approximations to the understanding of Ca++ signals. Cell Calcium 24 (1998) 345-357
85. Neher E., and Augustine G.J. Calcium gradients and buffers in bovine chromaffin cells. J. Physiol. 450 (1992) 273-301
86. Nevian T., and 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. 24 (2004) 1689-1699
87. Nevian T., and Sakmann B. Spine Ca2+ signaling in spike-timing-dependent plasticity. J. Neurosci. 26 (2006) 11001-11013
88. Ngo-Anh T.J., Bloodgood B.L., Lin M., Sabatini B.L., Maylie J., and Adelman J.P. SK channels and NMDA receptors form a Ca2+-mediated feedback loop in dendritic spines. Nat. Neurosci. 8 (2005) 642-649
89. Nishiyama M., Hong K., Mikoshiba K., Poo M.M., and Kato K. Calcium stores regulate the polarity and input specificity of synaptic modification. Nature 408 (2000) 584-588
90. Noguchi J., Matsuzaki M., Ellis-Davies G.C., and Kasai H. Spine-neck geometry determines NMDA receptor-dependent Ca2+ signaling in dendrites. Neuron 46 (2005) 609-622
91. Nowak L., Bregestovski P., Ascher P., Herbet A., and Prochiantz A. Magnesium gates glutamate-activated channels in mouse central neurones. Nature 307 (1984) 462-465
92. Oakley J.C., Schwindt P.C., and Crill W.E. Dendritic calcium spikes in layer 5 pyramidal neurons amplify and limit transmission of ligand-gated dendritic current to soma. J. Neurophysiol. 86 (2001) 514-527
93. Plant K., Pelkey K.A., Bortolotto Z.A., Morita D., Terashima A., McBain C.J., Collingridge G.L., and Isaac J.T. Transient incorporation of native GluR2-lacking AMPA receptors during hippocampal long-term potentiation. Nat. Neurosci. 9 (2006) 602-604
94. Rancz E.A., and Häusser M. Dendritic calcium spikes are tunable triggers of cannabinoid release and short-term synaptic plasticity in cerebellar Purkinje neurons. J. Neurosci. 26 (2006) 5428-5437
95. Regehr W.G., and Tank D.W. Postsynaptic NMDA receptor-mediated calcium accumulation in hippocampal CA1 pyramidal cell dendrites. Nature 345 (1990) 807-810
96. Regehr W.G., and Tank D.W. Calcium concentration dynamics produced by synaptic activation of CA1 hippocampal pyramidal cells. J. Neurosci. 12 (1992) 4202-4223
97. Reid C.A., Fabian-Fine R., and Fine A. Postsynaptic calcium transients evoked by activation of individual hippocampal mossy fiber synapses. J. Neurosci. 21 (2001) 2206-2214
98. Remy S., and Spruston N. Dendritic spikes induce single-burst long-term potentiation. Proc. Natl. Acad. Sci. USA 104 (2007) 17192-17197
99. Roberts W.M. Spatial calcium buffering in saccular hair cells. Nature 363 (1993) 74-76
100. Ross W.N., and Werman R. Mapping calcium transients in the dendrites of Purkinje cells from the guinea-pig cerebellum in vitro. J. Physiol. 389 (1987) 319-336
101. Sabatini B.L., and Regehr W.G. Optical measurement of presynaptic calcium currents. Biophys. J. 74 (1998) 1549-1563
102. Sabatini B.L., and Svoboda K. Analysis of calcium channels in single spines using optical fluctuation analysis. Nature 408 (2000) 589-593
103. Sabatini B.L., Maravall M., and Svoboda K. Ca(2+) signaling in dendritic spines. Curr. Opin. Neurobiol. 11 (2001) 349-356
104. Sabatini B.L., Oertner T.G., and Svoboda K. The life cycle of Ca(2+) ions in dendritic spines. Neuron 33 (2002) 439-452
105. Safo P.K., and Regehr W.G. Endocannabinoids control the induction of cerebellar LTD. Neuron 48 (2005) 647-659
106. Sarkisov D.V., and Wang S.S. Order-dependent coincidence detection in cerebellar Purkinje neurons at the inositol trisphosphate receptor. J. Neurosci. 28 (2008) 133-142
107. Scheuss V., Yasuda R., Sobczyk A., and Svoboda K. Nonlinear [Ca2+] signaling in dendrites and spines caused by activity-dependent depression of Ca2+ extrusion. J. Neurosci. 26 (2006) 8183-8194
108. Schiller J., Helmchen F., and Sakmann B. Spatial profile of dendritic calcium transients evoked by action potentials in rat neocortical pyramidal neurones. J. Physiol. 487 (1995) 583-600
109. Schiller J., Schiller Y., Stuart G., and Sakmann B. Calcium action potentials restricted to distal apical dendrites of rat neocortical pyramidal neurons. J. Physiol. 505 (1997) 605-616
110. Schiller J., Schiller Y., and Clapham D.E. NMDA receptors amplify calcium influx into dendritic spines during associative pre- and postsynaptic activation. Nat. Neurosci. 1 (1998) 114-118
111. Schiller J., Major G., Koester H.J., and Schiller Y. NMDA spikes in basal dendrites of cortical pyramidal neurons. Nature 404 (2000) 285-289
112. Schwaller B., Meyer M., and Schiffmann S. 'New' functions for 'old' proteins: the role of the calcium-binding proteins calbindin D-28k, calretinin and parvalbumin, in cerebellar physiology. Studies with knockout mice. Cerebellum 1 (2002) 241-258
113. Schwartzkroin P.A., and Slawsky M. Probable calcium spikes in hippocampal neurons. Brain Res. 135 (1977) 157-161
114. Simon S.M., and Llinás R.R. Compartmentalization of the submembrane calcium activity during calcium influx and its significance in transmitter release. Biophys. J. 48 (1985) 485-498
115. Sjöström P.J., Rancz E.A., Roth A., and Häusser M. Dendritic excitability and synaptic plasticity. Physiol. Rev. 88 (2008) 769-840
116. Sobczyk A., Scheuss V., and Svoboda K. NMDA receptor subunit-dependent [Ca2+] signaling in individual hippocampal dendritic spines. J. Neurosci. 25 (2005) 6037-6046
117. Soderling T.R. CaM-kinases: modulators of synaptic plasticity. Curr. Opin. Neurobiol. 10 (2000) 375-380
118. Soler-Llavina G.J., and Sabatini B.L. Synapse-specific plasticity and compartmentalized signaling in cerebellar stellate cells. Nat. Neurosci. 9 (2006) 798-806
119. Spruston N., Schiller Y., Stuart G., and Sakmann B. Activity-dependent action potential invasion and calcium influx into hippocampal CA1 dendrites. Science 268 (1995) 297-300
120. Stevens C.F., and Zador A.M. Input synchrony and the irregular firing of cortical neurons. Nat. Neurosci. 1 (1998) 210-217
121. Stuart G., Schiller J., and Sakmann B. Action potential initiation and propagation in rat neocortical pyramidal neurons. J. Physiol. 505 (1997) 617-632
122. Svoboda K., Denk W., Kleinfeld D., and Tank D.W. In vivo dendritic calcium dynamics in neocortical pyramidal neurons. Nature 385 (1997) 161-165
123. Svoboda K., Helmchen F., Denk W., and Tank D.W. Spread of dendritic excitation in layer 2/3 pyramidal neurons in rat barrel cortex in vivo. Nat. Neurosci. 2 (1999) 65-73
124. Takechi H., Eilers J., and Konnerth A. A new class of synaptic response involving calcium release in dendritic spines. Nature 396 (1998) 757-760
125. Tank D.W., Sugimori M., Connor J.A., and Llinás R.R. Spatially resolved calcium dynamics of mammalian Purkinje cells in cerebellar slice. Science 242 (1988) 773-777
126. Thiagarajan T.C., Lindskog M., and Tsien R.W. Adaptation to synaptic inactivity in hippocampal neurons. Neuron 47 (2005) 725-737
127. Tsay D., Dudman J.T., and Siegelbaum S.A. HCN1 channels constrain synaptically evoked Ca2+ spikes in distal dendrites of CA1 pyramidal neurons. Neuron 56 (2007) 1076-1089
128. Vicini S., Wang J.F., Li J.H., Zhu W.J., Wang Y.H., Luo J.H., Wolfe B.B., and Grayson D.R. Functional and pharmacological differences between recombinant N-methyl-D-aspartate receptors. J. Neurophysiol. 79 (1998) 555-566
129. Wang S.S., Denk W., and Häusser M. Coincidence detection in single dendritic spines mediated by calcium release. Nat. Neurosci. 3 (2000) 1266-1273
130. Watanabe S., Hong M., Lasser-Ross N., and Ross W.N. Modulation of calcium wave propagation in the dendrites and to the soma of rat hippocampal pyramidal neurons. J. Physiol. 575 (2006) 455-468
131. Waters J., Larkum M., Sakmann B., and Helmchen F. Supralinear Ca2+ influx into dendritic tufts of layer 2/3 neocortical pyramidal neurons in vitro and in vivo. J. Neurosci. 23 (2003) 8558-8567
132. Wei D.S., Mei Y.A., Bagal A., Kao J.P., Thompson S.M., and Tang C.M. Compartmentalized and binary behavior of terminal dendrites in hippocampal pyramidal neurons. Science 293 (2001) 2272-2275
133. Westenbroek R.E., Ahlijanian M.K., and Catterall W.A. Clustering of L-type Ca2+ channels at the base of major dendrites in hippocampal pyramidal neurons. Nature 347 (1990) 281-284
134. Yasuda R., Sabatini B.L., and Svoboda K. Plasticity of calcium channels in dendritic spines. Nat. Neurosci. 6 (2003) 948-955
135. Yuste R., and Denk W. Dendritic spines as basic functional units of neuronal integration. Nature 375 (1995) 682-684
136. Yuste R., Gutnick M.J., Saar D., Delaney K.R., and Tank D.W. Ca2+ accumulations in dendrites of neocortical pyramidal neurons: an apical band and evidence for two functional compartments. Neuron 13 (1994) 23-43
137. Yuste R., Majewska A., Cash S.S., and Denk W. Mechanisms of calcium influx into hippocampal spines: heterogeneity among spines, coincidence detection by NMDA receptors, and optical quantal analysis. J. Neurosci. 19 (1999) 1976-1987
138. Zhou Z., and Neher E. Mobile and immobile calcium buffers in bovine adrenal chromaffin cells. J. Physiol. 469 (1993) 245-273
139. Zucker R.S. Calcium- and activity-dependent synaptic plasticity. Curr. Opin. Neurobiol. 9 (1999) 305-313