Dendritic calcium signaling triggered by spontaneous and sensory-evoked climbing fiber input to cerebellar purkinje cells in vivo

Journal of Neuroscience

Volumn 31, Issue 30, 2011, Pages 10847-10858

  Kitamura, Kazuo ^a   Häusser, Michael ^b  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CHANNEL; CALCIUM ION; SODIUM CHANNEL; VOLTAGE GATED CALCIUM CHANNEL;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CALCIUM SIGNALING; CELL MEMBRANE DEPOLARIZATION; CLIMBING FIBER; CONTROLLED STUDY; DENDRITIC CELL; ELECTROPHYSIOLOGY; EVOKED SOMATOSENSORY RESPONSE; EXCITATORY JUNCTION POTENTIAL; GABAERGIC SYSTEM; IN VIVO STUDY; MEMBRANE POTENTIAL; MULTIPHOTON MICROSCOPY; NERVE CELL PLASTICITY; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; PURKINJE CELL; RAT; SENSORY STIMULATION; SPIKE; SYNAPTIC TRANSMISSION;

ANIMALS; ANIMALS, NEWBORN; BENZYLAMINES; BIOPHYSICS; CALCIUM SIGNALING; CEREBELLUM; DENDRITES; ELECTRIC STIMULATION; FLUORESCENT DYES; GABA ANTAGONISTS; MEMBRANE POTENTIALS; NERVE FIBERS; PATCH-CLAMP TECHNIQUES; PHOSPHINIC ACIDS; PURKINJE CELLS; PYRIDAZINES; RATS; RATS, SPRAGUE-DAWLEY;

EID: 79960967881     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2525-10.2011     Document Type: Article

References (71)

1. Bekkers JM, Hausser M (2007) Targeted dendrotomy reveals active and passive contributions of the dendritic tree to synaptic integration and neuronal output. Proc Natl Acad Sci USA 104:11447-11452.
2. Bower JM, Woolston DC (1983) Congruence of spatial organization of tactile projections to granule cell and Purkinje cell layers of cerebellar hemispheres of the albino rat: vertical organization of cerebellar cortex. J Neurophysiol 49:745-766.
3. Brenowitz SD, Regehr WG (2005) Associative short-term synaptic plasticity mediated by endocannabinoids. Neuron 45:419-431.
4. Broser PJ, Schulte R, Lang S, Roth A, Helmchen F, Waters J, Sakmann B, Wittum G (2004) Nonlinear anisotropic diffusion filtering of three-dimensional image data from two-photon microscopy. J Biomed Opt 9:1253-1264.
5. Brown IE, Bower JM (2001) Congruence of mossy fiber and climbing fiber tactile projections in the lateral hemispheres of the rat cerebellum. J Comp Neurol 429:59-70.
6. Callaway JC, Lasser-Ross N, Ross WN (1995) IPSPs strongly inhibit climbing fiber-activated [Ca2+]i increases in the dendrites of cerebellar Purkinje neurons. J Neurosci 15:2777-2787.
7. Chan CY, Hounsgaard J, Midtgaard J (1989) Excitatory synaptic responses in turtle cerebellar Purkinje cells. J Physiol 409:143-156.
8. Chen X, Kovalchuk Y, Adelsberger H, Henning HA, Sausbier M, Wietzorrek G, Ruth P, Yarom Y, Konnerth A (2010) Disruption of the olivocerebellar circuit by Purkinje neuron-specific ablation of BK channels. Proc Natl Acad Sci USA 107:12323-12328.
9. Coesmans M, Weber JT, De Zeeuw CI, Hansel C (2004) Bidirectional parallel fiber plasticity in the cerebellum under climbing fiber control. Neuron 44:691-700.
10. Davie JT, Clark BA, Hausser M (2008) The origin of the complex spike in cerebellar Purkinje cells. J Neurosci 28:7599-7609.
11. Denk W, Strickler JH, Webb WW (1990) Two-photon laser scanning fluorescence microscopy. Science 248:73-76.
12. Denk W, Sugimori M, Llinas R (1995) Two types of calcium response limited to single spines in cerebellar Purkinje cells. Proc Natl Acad Sci USA 92:8279-8282.
13. Dzubay JA, Otis TS (2002) Climbing fiber activation of metabotropic glu-tamate receptors on cerebellar Purkinje neurons. Neuron 36:1159-1167.
14. Eilers J, Augustine GJ, Konnerth A (1995) Subthreshold synaptic Ca + signalling in fine dendrites and spines of cerebellar Purkinje neurons. Nature 373:155-158.
15. Fernandez FR, Engbers JD, Turner RW (2007) Firing dynamics of cerebellar Purkinje cells. J Neurophysiol 98:278-294.
16. Fujita Y (1968) Activity of dendrites of single Purkinje cells and its relationship to so-called inactivation response in rabbit cerebellum. J Neurophysiol 31:131-141.
17. Hansel C, Linden DJ (2000) Long-term depression of the cerebellar climbing fiber-Purkinje neuron synapse. Neuron 26:473-482.
18. Hartell NA (1996) Strong activation of parallel fibers produces localized calcium transients and a form of LTD that spreads to distant synapses. Neuron 16:601-610.
19. Hausser M, Clark BA (1997) Tonic synaptic inhibition modulates neuronal output pattern and spatiotemporal synaptic integration. Neuron 19:665-678.
20. Helmchen F, Svoboda K, Denk W, Tank DW (1999) In vivo dendritic calcium dynamics in deep-layer cortical pyramidal neurons. Nat Neurosci 2:989-996.
21. Holt GR, Softky WR, Koch C, Douglas RJ (1996) Comparison of discharge variability in vitro and in vivo in cat visual cortex neurons. J Neurophysiol 75:1806-1814.
22. Hounsgaard J, Midtgaard J (1989) Synaptic control of excitability in turtle cerebellar Purkinje cells. J Physiol 409:157-170.
23. Hounsgaard J, Yamamoto C (1979) Dendritic spikes in Purkinje cells of the guinea pig cerebellum studied in vitro. Exp Brain Res 37:387-398.
24. Isope P, Murphy TH (2005) Low threshold calcium currents in rat cerebellar Purkinje cell dendritic spines are mediated by T-type calcium channels. J Physiol 562:257-269.
25. Ito M (1984) The cerebellum and neural control. New York: Raven.
26. Jaeger D, Bower JM (1994) Prolonged responses in rat cerebellar Purkinje cells following activation of the granule cell layer: an intracellular in vitro and in vivo investigation. Exp Brain Res 100:200-214.
27. Jia H, Rochefort NL, Chen X, Konnerth A (2010) Dendritic organization of sensory input to cortical neurons in vivo. Nature 464:1307-1312.
28. Kitamura K, Judkewitz B, Kano M, Denk W, Hausser M (2008) Targeted patch-clamp recordings and single-cell electroporation of unlabeled neurons in vivo. Nat Methods 5:61-67.
29. Konnerth A, Dreessen J, Augustine GJ (1992) Brief dendritic calcium signals initiate long-lasting synaptic depression in cerebellar Purkinje cells. Proc Natl Acad Sci USA 89:7051-7055.
30. Kulik A, Nakadate K, Hagiwara A, Fukazawa Y, Lujan R, Saito H, Suzuki N, Futatsugi A, Mikoshiba K, Frotscher M, Shigemoto R (2004) Immuno-cytochemical localization of the alpha 1A subunit of the P/Q-type calcium channel in the rat cerebellum. Eur J Neurosci 19:2169-2178.
31. Lev-Ram V, Miyakawa H, Lasser-Ross N, Ross WN (1992) Calcium transients in cerebellar Purkinje neurons evoked by intracellular stimulation. J Neurophysiol 68:1167-1177.
32. Llinas R, Sasaki K (1989) The functional organization of the olivo-cerebellar system as examined by multiple Purkinje cell recordings. Eur J Neurosci 1:587-602.
33. Llinas R, Sugimori M (1980a) Electrophysiological properties of in vitro Purkinje cell somata in mammalian cerebellar slices. J Physiol 305:171-195.
34. Llinas R, Sugimori M (1980b) Electrophysiological properties of in vitro Purkinje cell dendrites in mammalian cerebellar slices. J Physiol 305:197-213.
35. Loewenstein Y, Mahon S, Chadderton P, Kitamura K, Sompolinsky H, Yarom Y, Hausser M (2005) Bistability of cerebellar Purkinje cells modulated by sensory stimulation. Nat Neurosci 8:202-211.
36. Maeda H, Ellis-Davies GC, Ito K, Miyashita Y, Kasai H (1999) Supralinear Ca + signaling by cooperative and mobile Ca + buffering in Purkinje neurons. Neuron 24:989-1002.
37. Margrie TW, Brecht M, Sakmann B (2002) In vivo, low-resistance, whole-cell recordings from neurons in the anaesthetized and awake mammalian brain. Pflugers Arch 444:491-498.
38. McKay BE, Turner RW (2004) Kv3 K + channels enable burst output in rat cerebellar Purkinje cells. Eur J Neurosci 20:729-739.
39. McKay BE, Engbers JD, Mehaffey WH, Gordon GR, Molineux ML, Bains JS, Turner RW (2007) Climbing fiber discharge regulates cerebellar functions by controlling the intrinsic characteristics of Purkinje cell output. J Neurophysiol 97:2590-2604.
40. Midtgaard J, Lasser-Ross N, Ross WN (1993) Spatial distribution of Ca2+ influx in turtle Purkinje cell dendrites in vitro: role of a transient outward current. J Neurophysiol 70:2455-2469.
41. Miyakawa H, Lev-Ram V, Lasser-Ross N, Ross WN (1992) Calcium transients evoked by climbing fiber and parallel fiber synaptic inputs in guinea pig cerebellar Purkinje neurons. J Neurophysiol 68:1178-1189.
42. Miyashita Y, Nagao S (1984) Contribution of cerebellar intracortical inhibition to Purkinje cell response during vestibulo-ocular reflex of alert rabbits. J Physiol 351:251-262.
43. Miyata M, Finch EA, Khiroug L, Hashimoto K, Hayasaka S, Oda SI, Inouye M, Takagishi Y, Augustine GJ, Kano M (2000) Local calcium release in dendritic spines required for long-term synaptic depression. Neuron 28:233-244.
44. Mukamel EA, Nimmerjahn A, Schnitzer MJ (2009) Automated analysis of cellular signals from large-scale calcium imaging data. Neuron 63: 747-760.
45. Murayama M, Perez-Garci E, Nevian T, Bock T, Senn W, Larkum ME (2009) Dendritic encoding of sensory stimuli controlled by deep cortical in-terneurons. Nature 457:1137-1141.
46. Nevian T, Helmchen F (2007) Calcium indicator loading of neurons using single-cell electroporation. Pflugers Arch 454:675-688.
47. Ozden I, Sullivan MR, Lee HM, Wang SS (2009) Reliable coding emerges from coactivation of climbing fibers in microbands of cerebellar Purkinje neurons. J Neurosci 29:10463-10473.
48. Palay S, Chan-Palay V (1974) Cerebellar cortex: cytology and organization. New York: Springer.
49. Palmer LM, Clark BA, Grundemann J, Roth A, Stuart G, Hausser M (2010) Initiation of simple and complex spikes in cerebellar Purkinje cells. J Physiol 588:1709-1717.
50. Pologruto TA, Sabatini BL, Svoboda K (2003) ScanImage: flexible software for operating laser scanning microscopes. Biomed Eng Online 2:13.
51. Rancz EA, Hausser M (2006) Dendritic calcium spikes are tunable triggers of cannabinoid release and short-term synaptic plasticity in cerebellar Purkinje neurons. J Neurosci 26:5428-5437.
52. Rokni D, Tal Z, Byk H, Yarom Y (2009) Regularity, variability and bi-stability in the activity of cerebellar Purkinje cells. Front Cell Neurosci 3:12.
53. Sakurai M (1990) Calcium is an intracellular mediator of the climbing fiber in induction of cerebellar long-term depression. Proc Natl Acad Sci U S A 87:3383-3385.
54. Sasaki K, Bower JM, Llinás R (1989) Multiple Purkinje cell recording in rodent cerebellar cortex. Eur J Neurosci 1:572-586.
55. Schonewille M, Khosrovani S, Winkelman BH, Hoebeek FE, De Jeu MT, Larsen IM, Van der Burg J, Schmolesky MT, Frens MA, De Zeeuw CI (2006) Purkinje cells in awake behaving animals operate at the upstate membrane potential. Nat Neurosci 9:459-461; author reply 461.
56. Schultz SR, Kitamura K, Post-Uiterweer A, Krupic J, Häusser M (2009) Spatial pattern coding of sensory information by climbing fiber-evoked calcium signals in networks of neighboring cerebellar Purkinje cells. J Neurosci 29:8005-8015.
57. Stuart G, Häusser M (1994) Initiation and spread of sodium action potentials in cerebellar Purkinje cells. Neuron 13:703-712.
58. Sullivan MR, NimmerjahnA,Sarkisov DV, HelmchenF, Wang SS (2005) In vivo calcium imaging of circuit activity in cerebellar cortex. J Neuro-physiol 94:1636-1644.
59. Svoboda K, Denk W, Kleinfeld D, Tank DW (1997) In vivo dendritic calcium dynamics in neocortical pyramidal neurons. Nature 385:161-165.
60. Svoboda K, Helmchen F, Denk W, Tank DW (1999) Spread of dendritic excitation in layer 2/3 pyramidal neurons in rat barrel cortex in vivo. Nat Neurosci 2:65-73.
61. Takechi H, Eilers J, Konnerth A (1998) A new class of synaptic response involving calcium release in dendritic spines. Nature 396:757-760.
62. Tal Z, Chorev E, Yarom Y (2008) State-dependent modification of complex spike waveforms in the cerebellar cortex. Cerebellum 7:577-582.
63. Tank DW, Sugimori M, Connor JA, Llinas RR (1988) Spatially resolved calcium dynamics of mammalian Purkinje cells in cerebellar slice. Science 242:773-777.
64. Vetter P, Roth A, Hausser M (2001) Propagation of action potentials in dendrites depends on dendritic morphology. J Neurophysiol 85:926-937.
65. Wang SS, Denk W, Hausser M (2000) Coincidence detection in single dendritic spines mediated by calcium release. Nat Neurosci 3:1266-1273.
66. Waters J, Helmchen F (2004) Boosting of action potential backpropagation by neocortical network activity in vivo. J Neurosci 24:11127-11136.
67. Waters J, Larkum M, Sakmann B, Helmchen F (2003) Supralinear Ca + influx into dendritic tufts of layer 2/3 neocortical pyramidal neurons in vitro and in vivo. J Neurosci 23:8558-8567.
68. Weber JT, De Zeeuw CI, Linden DJ, Hansel C (2003) Long-term depression of climbing fiber-evoked calcium transients in Purkinje cell dendrites. Proc Natl Acad Sci USA 100:2878-2883.
69. Williams SR, Christensen SR, Stuart GJ, Hausser M (2002) Membrane potential bistability is controlled by the hyperpolarization-activated current I(H) in rat cerebellar Purkinje neurons in vitro. J Physiol 539:469-483.
70. Yartsev MM, Givon-Mayo R, Maller M, Donchin O (2009) Pausing Purkinje cells in the cerebellum of the awake cat. Front Syst Neurosci 3:2.
71. Yasuda R, Sabatini BL, Svoboda K (2003) Plasticity of calcium channels in dendritic spines. Nat Neurosci 6:948-955.