Small-conductance Ca2+-activated K+ channels modulate action potential-induced Ca2+ transients in hippocampal neurons

Journal of Neurophysiology

Volumn 109, Issue 6, 2013, Pages 1514-1524

  Tonini, Raffaella ^a,b   Ferraro, Teresa ^a   Sampedro Castañeda, Marisol ^a   Cavaccini, Anna ^b   Stocker, Martin ^a   Richards, Christopher D ^a   Pedarzani, Paola ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

Author keywords

Afterhyperpolarization; Apamin; Calcium imaging; Pyramidal neuron; SK channel

Indexed keywords

CALCIUM CHANNEL L TYPE; SMALL CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL; CALCIUM; CALCIUM CHANNEL STIMULATING AGENT; POTASSIUM CHANNEL BLOCKING AGENT;

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CELL STRUCTURE; CONTROLLED STUDY; DENDRITIC SPINE; ELECTROPHYSIOLOGY; FEEDBACK SYSTEM; HIPPOCAMPAL CA1 REGION; NERVE CELL PLASTICITY; NERVE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SYNAPSE; ACTION POTENTIAL; ANIMAL; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; HIPPOCAMPUS; METABOLISM; PHYSIOLOGY; RAT;

ACTION POTENTIALS; ANIMALS; CALCIUM; CALCIUM CHANNEL AGONISTS; CALCIUM CHANNELS, L-TYPE; CALCIUM SIGNALING; FEEDBACK, PHYSIOLOGICAL; HIPPOCAMPUS; POTASSIUM CHANNEL BLOCKERS; PYRAMIDAL CELLS; RATS; SMALL-CONDUCTANCE CALCIUM-ACTIVATED POTASSIUM CHANNELS;

EID: 84878501403     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00346.2012     Document Type: Article

References (72)

1. + channels: form and function. Annu Rev Physiol 74: 245-269, 2012.
2. Bloodgood BL, Sabatini BL. Nonlinear regulation of unitary synaptic signals by CaV2.3 voltage-sensitive calcium channels located in dendritic spines. Neuron 53: 249-260, 2007.
3. + channel knock-out mice reveal the identity of calcium-dependent afterhyperpolarization currents. J Neurosci 24: 5301-5306, 2004.
4. Bosurgi R, Pedarzani P. High voltage-activated calcium channel types responsible for the activation of the SK-mediated IAHP in rat hippocampal CA1 pyramidal neurons (Abstract). FENS Forum Abstr 3: A084.5, 2006.
5. Budde T, Meuth S, Pape HC. Calcium-dependent inactivation of neuronal calcium channels. Nat Rev Neurosci 3: 873-883, 2002.
6. Cai X, Liang CW, Muralidharan S, Kao JP, Tang CM, Thompson SM. Unique roles of SK and Kv4.2 potassium channels in dendritic integration. Neuron 44: 351-364, 2004.
7. Cai X, Wei DS, Gallagher SE, Bagal A, Mei YA, Kao JP, Thompson SM, Tang CM. Hyperexcitability of distal dendrites in hippocampal pyramidal cells after chronic partial deafferentation. J Neurosci 27: 59-68, 2007.
8. Callaway JC, Ross WN. Frequency-dependent propagation of sodium action potentials in dendrites of hippocampal CA1 pyramidal neurons. J Neurophysiol 74: 1395-1403, 1995.
9. Caporale N, Dan Y. Spike timing-dependent plasticity: a Hebbian learning rule. Annu Rev Neurosci 31: 25-46, 2008.
10. 2+ influx. J Neurophysiol 73: 2553-2557, 1995.
11. Christie BR, Magee JC, Johnston D. Dendritic calcium channels and hippocampal long-term depression. Hippocampus 6: 17-23, 1996.
12. + channel expression and function in rat Purkinje neurons. J Neurosci 22: 4456-4467, 2002.
13. Coetzee WA, Amarillo Y, Chiu J, Chow A, Lau D, McCormack T, Moreno H, Nadal MS, Ozaita A, Pountney D, Saganich M, de Vega-Saenz Miera E, Rudy B. Molecular diversity of K channels. Ann NY Acad Sci 868: 233-285, 1999.
14. 2+ channels, SK2 channels and SERCAs gate sleep-related oscillations in thalamic dendrites. Nat Neurosci 11: 683-692, 2008.
15. 2+ signaling requirements for long-term depression in the hippocampus. Neuron 16: 825-833, 1996.
16. Dragoi G, Buzsaki G. Temporal encoding of place sequences by hippocampal cell assemblies. Neuron 50: 145-157, 2006.
17. 2+ dependent afterhyperpolarisation in hippocampal CA3. Neuroscience 102: 297-306, 2001.
18. Faber ES, Delaney AJ, Sah P. SK channels regulate excitatory synaptic transmission and plasticity in the lateral amygdala. Nat Neurosci 8: 635-641, 2005.
19. Fakler B, Adelman JP. Control of KCa channels by calcium nano/microdomains. Neuron 59: 873-881, 2008.
20. Fernandez de Sevilla D, Garduno J, Galvan E, Buno W. Calcium-activated afterhyperpolarizations regulate synchronization and timing of epileptiform bursts in hippocampal CA3 pyramidal neurons. J Neurophysiol 96: 3028-3041, 2006.
21. Forti L, Pietrobon D. Functional diversity of L-type calcium channels in rat cerebellar neurons. Neuron 10: 437-450, 1993.
22. Golding NL, Jung HY, Mickus T, Spruston N. Dendritic calcium spike initiation and repolarization are controlled by distinct potassium channel subtypes in CA1 pyramidal neurons. J Neurosci 19: 8789-8798, 1999.
23. Goslin K, Banker G. Rat hippocampal neurons in low-density culture. In: Culturing Nerve Cells, edited by Banker G, Goslin K. Cambridge, MA: MIT Press, 1991, p. 251-281.
24. Gu N, Vervaeke K, Hu H, Storm JF. Kv7/KCNQ/M and HCN/h, but not KCa2/SK channels, contribute to the somatic medium after-hyperpolarization and excitability control in CA1 hippocampal pyramidal cells. J Physiol 566: 689-715, 2005.
25. 2+ signaling in dendrites of pyramidal neurons. Biophys J 70: 1069-1081, 1996.
26. 2+ influx by D2 dopamine and A2A adenosine receptors. Nat Neurosci 13: 958-966, 2010.
27. Hoffman DA, Magee JC, Colbert CM, Johnston D. K channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons. Nature 387: 869-875, 1997.
28. 2+ entry into hippocampal neurons. Nature 357: 244-246, 1992.
29. Johnston D, Hoffman DA, Magee JC, Poolos NP, Watanabe S, Colbert CM, Migliore M. Dendritic potassium channels in hippocampal pyramidal neurons. J Physiol 525: 75-81, 2000.
30. Jones SL, Stuart GJ. Different calcium sources control somatic and dendritic SK channel activation in cortical pyramidal neurons (Abstract). FENS Forum Abstr 6: P030.12, 2012.
31. Kaczorowski CC, Disterhoft J, Spruston N. Stability and plasticity of intrinsic membrane properties in hippocampal CA1 pyramidal neurons: effects of internal anions. J Physiol 578: 799-818, 2007.
32. Kavalali ET, Plummer MR. Selective potentiation of a novel calcium channel in rat hippocampal neurones. J Physiol 480: 475-484, 1994.
33. 2+ exchangers in hippocampal CA1 neurons. Neuroreport 15: 2113-2116, 2004.
34. Kip SN, Gray NW, Burette A, Canbay A, Weinberg RJ, Strehler EE. Changes in the expression of plasma membrane calcium extrusion systems during the maturation of hippocampal neurons. Hippocampus 16: 20-34, 2006.
35. Koschak A, Obermair GJ, Pivotto F, Sinnegger-Brauns MJ, Striessnig J, Pietrobon D. Molecular nature of anomalous L-type calcium channels in mouse cerebellar granule cells. J Neurosci 27: 3855-3863, 2007.
36. Kramar EA, Lin B, Lin CY, Arai AC, Gall CM, Lynch G. A novel mechanism for the facilitation of theta-induced long-term potentiation by brain-derived neurotrophic factor. J Neurosci 24: 5151-5161, 2004.
37. Leitch B, Szostek A, Lin R, Shevtsova O. Subcellular distribution of L-type calcium channel subtypes in rat hippocampal neurons. Neuroscience 164: 641-657, 2009.
38. Lin MT, Lujan R, Watanabe M, Adelman JP, Maylie J. SK2 channel plasticity contributes to LTP at Schaffer collateral-CA1 synapses. Nat Neurosci 11: 170-177, 2008.
39. Lorincz A, Rozsa B, Katona G, Vizi ES, Tamas G. Differential distribution of NCX1 contributes to spine-dendrite compartmentalization in CA1 pyramidal cells. Proc Natl Acad Sci USA 104: 1033-1038, 2007.
40. Lujan R, Maylie J, Adelman JP. New sites of action for GIRK and SK channels. Nat Rev Neurosci 10: 475-480, 2009.
41. Magee JC, Carruth M. Dendritic voltage-gated ion channels regulate the action potential firing mode of hippocampal CA1 pyramidal neurons. J Neurophysiol 82: 1895-1901, 1999.
42. Mainen ZF, Malinow R, Svoboda K. Synaptic calcium transients in single spines indicate that NMDA receptors are not saturated. Nature 399: 151-155, 1999.
43. 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 20: 1722-1734, 2000.
44. Maravall M, Mainen ZF, Sabatini BL, Svoboda K. Estimating intracellular calcium concentrations and buffering without wavelength ratioing. Biophys J 78: 2655-2667, 2000.
45. Markram H, Helm PJ, Sakmann B. Dendritic calcium transients evoked by single back-propagating action potentials in rat neocortical pyramidal neurons. J Physiol 485: 1-20, 1995.
46. 2+ channels in hippocampal neurons. Nature 395: 900-905, 1998.
47. Nazzaro C, Greco B, Cerovic M, Baxter P, Rubino T, Trusel M, Parolaro D, Tkatch T, Benfenati F, Pedarzani P, Tonini R. SK channel modulation rescues striatal plasticity and control over habit in cannabinoid tolerance. Nat Neurosci 15: 284-293, 2012.
48. 2+-mediated feedback loop in dendritic spines. Nat Neurosci 8: 642-649, 2005.
49. O'Keefe J, Dostrovsky J. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res 34: 171-175, 1971.
50. Oh MM, Power JM, Thompson LT, Disterhoft JF. Apamin increases excitability of CA1 hippocampal pyramidal neurons. Neurosci Res Commun 27: 135-142, 2000.
51. + channels controls fast inhibitory synaptic transmission at auditory outer hair cells. Neuron 26: 595-601, 2000.
52. Papp E, Leinekugel X, Henze DA, Lee J, Buzsaki G. The apical shaft of CA1 pyramidal cells is under GABAergic interneuronal control. Neuroscience 102: 715-721, 2001.
53. Parvez S, Ramachandran B, Frey JU. Functional differences between and across different regions of the apical branch of hippocampal CA1 dendrites with respect to long-term depression induction and synaptic cross-tagging. J Neurosci 30: 5118-5123, 2010.
54. Pedarzani P, McCutcheon JE, Rogge G, Jensen BS, Christophersen P, Hougaard C, Strobaek D, Stocker M. Specific enhancement of SK channel activity selectively potentiates the afterhyperpolarizing current IAHP and modulates the firing properties of hippocampal pyramidal neurons. J Biol Chem 280: 41404-41411, 2005.
55. + channels. J Biol Chem 276: 9762-9769, 2001.
56. Pedarzani P, Stocker M. Molecular and cellular basis of small- and intermediate-conductance, calcium-activated potassium channel function in the brain. Cell Mol Life Sci 65: 3196-3217, 2008.
57. Pravettoni E, Bacci A, Coco S, Forbicini P, Matteoli M, Verderio C. Different localizations and functions of L-type and N-type calcium channels during development of hippocampal neurons. Dev Biol 227: 581-594, 2000.
58. Regehr WG, Connor JA, Tank DW. Optical imaging of calcium accumulation in hippocampal pyramidal cells during synaptic activation. Nature 341: 533-536, 1989.
59. Regehr WG, Tank DW. Calcium concentration dynamics produced by synaptic activation of CA1 hippocampal pyramidal cells. J Neurosci 12: 4202-4223, 1992.
60. Regehr WG, Tank DW. Dendritic calcium dynamics. Curr Opin Neurobiol 4: 373-382, 1994.
61. 2+ ions in dendritic spines. Neuron 33: 439-452, 2002.
62. + channels in rat brain. J Neurosci 22: 9698-9707, 2002.
63. 2+ extrusion. J Neurosci 26: 8183-8194, 2006.
64. Schjott JM, Plummer MR. Sustained activation of hippocampal Lp-type voltage-gated calcium channels by tetanic stimulation. J Neurosci 20: 4786-4797, 2000.
65. Shah MM, Javadzadeh-Tabatabaie M, Benton DC, Ganellin CR, Haylett DG. Enhancement of hippocampal pyramidal cell excitability by the novel selective slow-afterhyperpolarization channel blocker 3-(triphenylmethylaminomethyl)pyridine (UCL2077). Mol Pharmacol 70: 1494-1502, 2006.
66. Spruston N, Schiller Y, Stuart G, Sakmann B. Activity-dependent action potential invasion and calcium influx into hippocampal CA1 dendrites. Science 268: 297-300, 1995.
67. + channels: molecular determinants and function of the SK family. Nat Rev Neurosci 5: 758-770, 2004.
68. + current in hippocampal pyramidal neurons. Proc Natl Acad Sci USA 96: 4662-4667, 1999.
69. 2+ channels in the rat hippocampus. J Comp Neurol 506: 569-583, 2008.
70. 2+ channels at the base of major dendrites in hippocampal pyramidal neurons. Nature 347: 281-284, 1990.
71. Xia XM, Fakler B, Rivard A, Wayman G, Johnson-Pais T, Keen JE, Ishii T, Hirschberg B, Bond CT, Lutsenko S, Maylie J, Adelman JP. Mechanism of calcium gating in small-conductance calcium-activated potassium channels. Nature 395: 503-507, 1998.
72. Yasuda R, Nimchinsky EA, Scheuss V, Pologruto TA, Oertner TG, Sabatini BL, Svoboda K. Imaging calcium concentration dynamics in small neuronal compartments. Sci STKE 219: p l5, 2004.