Calcium-activated potassium channels: Multiple contributions to neuronal function

Neuroscientist

Volumn 9, Issue 3, 2003, Pages 181-194

  Louise Faber, E S ^a   Sah, Pankaj ^a  

^a Australian National University   (Australia)

Author keywords

Accommodation; AHP; SAHP; SK channel

Indexed keywords

CALCIUM; CALCIUM ACTIVATED POTASSIUM CHANNEL; CALCIUM CHANNEL;

ACTION POTENTIAL; CALCIUM TRANSPORT; CENTRAL NERVOUS SYSTEM; CHANNEL GATING; NERVE FUNCTION; PATHOGENESIS; PRIORITY JOURNAL; REVIEW;

AGING; ANIMALS; BRAIN DISEASES; CALCIUM; CENTRAL NERVOUS SYSTEM; LEARNING; NEURONS; POTASSIUM CHANNELS, CALCIUM-ACTIVATED;

EID: 0038175132     PISSN: 10738584     EISSN: None     Source Type: Journal    
DOI: 10.1177/1073858403009003011     Document Type: Review

References (170)

1. + current in vertebtrate sensory neurones. Nature 296:746-9.
2. Adelman JP, Shen K-Z, Kavanaugh MP, Warren RA, Wu Y-N, Lagrutta A, and others. 1992. Calcium-activated potassium channels expressed from cloned complementary DNAs. Neuron 9:209-16.
3. + channels in bovine chromaffin cells. Pflugers Arch 423:97-103.
4. Ashcroft FM. 2000. Ion channels and disease: channelopathies. New York: Academic Press.
5. Ashley CT Jr, Warren ST. 1995. Trinucleotide repeat expansion and human disease. Annu Rev Genet 29:703-28.
6. Atkinson NS, Robertson GA, Ganetzky B. 1992. A component of calcium-activated potassium channels encoded by the drosophila slo locus. Science 253:551-5.
7. Behnisch T, Reymann KG. 1998. Inhibition of apamin-sensitive calcium dependent potassium channels facilitate the induction of long-term potentiation in the CA1 region of rat hippocampus in vitro, Neurosci Lett 253:91-4.
8. Bekkers JM. 2000. Distribution of slow AHP channels on hippocampal CA1 pyramidal neurons. J Neurophysiol 83:1756-9.
9. Belcadi-Abbassi W, Destrade C. 1995. Post-test apamin injection suppresses a Kamin-like effect following a learning session in mice. Neuroreport 6:1293-6.
10. + channels of small conductance in cultured rat skeletal muscle. Nature 323:718-20.
11. Blatz AL, Magleby KL. 1987. Calcium-activated potassium channels. Trends Neurosci 10:463-7.
12. Bowden SE, Fletcher S, Loane DJ, Marrion NV. 2001. Somatic colocalization of rat SK1 and D class (Ca(v)1.2) L-type calcium channels in rat CA1 hippocampal pyramidal neurons. J Neurosci 21:RC175.
13. Brenner R, Jegla TJ, Wickenden A, Liu Y, Aldrich RW. 2000. Cloning and functional characterisation of novel large conductance calcium-activated potassium channel beta subunits, hKCNMB3 and hKCNMB4. J Biol Chem 275:6453-61.
14. Campbell LW, Hao SY, Thibault O, Blalock EM, Landfield PW. 1996. Aging changes in voltage-gated calcium currents in hippocampal CA1 neurons. J Neurosci 16:6286-95.
15. + channel. J Med Chem 43:420-31.
16. Cassell JF, McLachlan EM. 1987. Two calcium-activated potassium conductances in a subpopulation of coeliac neurones of guinea-pig and rabbit, J Physiol 394:331-49.
17. Chandy KG, Fantino E, Wittekindt O, Kalman K, Tong LL, Ho TH, and others. 1998. Isolation of a novel potassium channel gene hSKCa3 containing a polymorphic CAG repeat: a candidate for schizophrenia and bipolar disorder? Mol Psychiatry 3:32-7.
18. - channel. J Med Chem 43:3478-81.
19. Cohen AS, Coussens CM, Raymond CR, Abraham WC. 1999. Longlasting increase in cellular excitability associated with the priming of LTP induction in rat hippocampus. J Neurophysiol 82:3139-48.
20. Coulter DA, Lo Turco JJ, Kubota M, Disterhoft JF, Moore JW, Alkon DL. 1989. Classical conditioning reduces amplitude and duration of calcium-dependent afterhyperpolarization in rabbit hippocampal pyramidal cells. J Neurophysiol 61:971-81.
21. + channels. J Gen Physiol 109:647-73.
22. Danober L, Pape H-C. 1998. Mechanisms and functional significance of a slow inhibitory potential in neurons of the lateral amygdala. Eur J Neurosci 10:853-67.
23. + conductances in neurones of the rat superior cervical ganglion. J Physiol 495:353-66.
24. de Jonge MC, Black J, Deyo RA, Disterhoft JF. 1990. Learning-induced afterhyperpolarization reductions in hippocampus are specific for cell type and potassium conductance. Exp Brain Res 80:456-62.
25. Deschaux O, Bizot JC, Goyffon M. 1997. Apamin improves learning in an object recognition task in rats. Neurosci Lett 222:159-62.
26. Deupree DL, Bradley J, Turner DA. 1993. Age-related alterations in potentiation in the CA1 region in F344 rats. Neurobiol Aging 14:249-58.
27. Deyo RA, Straube KT, Disterhoft JF. 1989. Nimodipine facilitates associative learning in aging rabbits. Science 243:809-11.
28. Ding JP, Li ZW, Lingle CJ. 1998. Inactivating BK channels in rat chromaffin cells may arise from heteromultimeric assembly of distinct inactivation-competent and noninactivating subunits. Biophys J 74:268-89.
29. Disterhoft JF, Coulter DA, Alkon DL. 1986. Conditioning-specific membrane changes of rabbit hippocampal neurons measured in vitro. Proc Natl Acad Sci U S A 83:2733-7.
30. Disterhoft JF, Golden DT, Read HL, Coulter DA, Alkon DL. 1988. AHP reductions in rabbit hippocampal neurons during conditioning correlate with acquisition of the learned response. Brain Res 462:118-25.
31. Disterhoft JF, Thompson LT, Moyer JR Jr, Mogul DJ. 1996. Calcium dependent afterhyperpolarization and learning in young and aging hippocampus. Life Sci 59:413-20.
32. Dror V, Shamir E, Ghanshani S, Kimhi R, Swartz M, Barak Y, and others. 1999. hKCa3/KCNN3 potassium channel gene: association of longer CAG repeats with schizophrenia in Israeli Ashkenazi Jews, expression in human tissues and localization to chromosome 1q21. Mol Psychiatry 4:254-60.
33. Dunn PM. 1994. Dequalinium, a selective blocker of the slow afterhyperpolarization in rat sympathetic neurones in culture. Eur J Pharmacol 252:189-94.
34. Dworetsky SI, Boissard CG, Lum-Ragan M, McKay C, Post-Munson DJ, Tronjnacki JT, and others. 1996. Phenotypic alteration of a human BK (hslo) channels by hslo-beta subunt coexpression: changes in blocker sensitivity, activation/relaxation and inactivation kinetics, and protein kinase A modulation. J Neurosci 16:4543-50.
35. Dworetzky SI, Trojnacki JT, Gribkoff VK. 1994. Cloning and expression of a human large-conductance calcium-activated potassium channel. Brain Res Mol Brain Res 27:189-93.
36. Engel J, Schultens HA, Schild D. 1999. Small conductance potassium channels cause an activity dependent spike frequency adaptation amd make the transfer function of neurons logarithmic. Biophys J 76:1310-19.
37. Faber ESL, Sah P. 2002. Physiological role of calcium-activated potassium currents in the rat lateral amygdala. J Neurosci 22:1618-28.
38. Fiorillo CD, Williams JT. 1998. Glutamate mediates an inhibitory postsynaptic potential in dopamine neurons. Nature 394:78-82.
39. + channels in an olfactory discrimination task. Behav Brain Res 121:81-93.
40. Gallagher M, Burwell R, Burchinal M. 1993. Severity of spatial learning impairment in aging: development of a learning index for performance in the Morris water maze. Behav Neurosci 107:618-26.
41. Galvez A, Gimenez-Gallego G, Reuben J, Roy-Contancin L, Feigenbaum P, Kaczorowski G, and others. 1990. Purification and characterization of a unique, potent, peptidyl probe for the high conductance calcium-activated potassium channel from venom of the scorpion Buthus tamulus. J Biol Chem 265:11083-90.
42. Garcia-Calvo M, Knaus HG, McManus OB, Giangiacomo KM, Kaczorowski GJ, Garcia ML, and others. 1994. Purification and reconstruction of the high-conductance, calcium-activated potassium channel from tracheal smooth muscle. J Biol Chem 269:676-82.
43. Gardos G. 1958. The function of calcium in the potassium permeability of human erythrocytes. Biochem Biophys Acta 30:653-4.
44. Gargus JJ, Fantino E, Gutman GA. 1998. A piece in the puzzle: an ion channel candidate gene for schizophrenia. Mol Med Today 4:518-24.
45. Goh JW, Pennefather PS. 1987. Pharmacological and physiological properties of the after-hyperpolarization current of bullfrog ganglion neurons. J Physiol 394:315-30.
46. Grissmer S, Nguyen AN, Cahalan MD. 1993. Calcium-activated potassium channels in resting and activated human T lymphocytes. Expression levels, calcium dependence, ion selectivity, and pharmacology. J Gen Physiol 102:601-30.
47. Gu N, Storm JF. 2002. Regulation of glutamate release by presynaptic calcium-activated potassium channels (BK channels) is enhanced under hypoxic conditions in rat hippocampus (CA1). Soc Neurosci Abs 340.15.
48. Heurteaux C, Messier C, Destrade C, Lazdunski M. 1993. Memory processing and apamin induce immediate early gene expression in mouse brain. Brain Res Mol Brain Res 18:17-22.
49. + channels by calcium. J Gen Physiol 111:565-81.
50. Hirst GDS, Johnson SM, van Helden DF. 1985. The slow calcium dependent potassium current in a myenteric neurone of the guineapig ileum. J Physiol 361:315-37.
51. 2+ binding and channel opening in large conductance (BK) potassium channels. J Gen Physiol 120:267-305.
52. + channels mediating the afterhyperpolarization in cultured rat SCG neurones. J Physiol 535:323-34.
53. + channels in glutamatergic hippocampal terminals and their role in spike repolarization and regulation of transmitter release. J Neurosci 21:9585-97.
54. Ikeda M, Dewar D, McCulloch J. 1991. Selective reduction of [125I]apamin binding sites in Alzheimer hippocampus: a quantitative autoradiographic study. Brain Res 567:51-6.
55. Ikonen S, Riekkinen P Jr. 1999. Effects of apamin on memory processing of hippocampal-lesioned mice. Eur J Pharmacol 382:151-6.
56. Ikonen S, Schmidt B, Riekkinen P Jr. 1998. Apamin improves spatial navigation in medial septal-lesioned mice. Eur J Pharmacol 347:13-21.
57. + channels. Neuron 31:1027-34.
58. Ishii TM, Maylie J, Adelman JP. 1997. Determinants of apamin and dtubocurarine block in SK potassium channels. J Biol Chem 272:23195-200.
59. Ishii TM, Silvia C, Hirschberg B, Bond CT, Adelman JP, Maylie J. 1997. A human intermediate conductance calcium-activated potassium†channel. Proc Natl Acad Sci U S A 94:11651-6.
60. Jan LY, Jan YN. 1997. Cloned potassium channels from eukaryotes and prokaryotes. Annu Rev Neurosci 20:91-123.
61. Jiang Y, Lee A, Chen J, Cadene M, Chair BT, MacKinnon R. 2002. Crystal structure and mechanism of a calcium-gated potassium channel. Nature 417:515-22.
62. + currents. Neurosci Lett 231:13-16.
63. Joiner WJ, Wang L-Y, Tang MD, Kaczmarek LK. 1997. hSK4, a member of a novel subfamily of calcium-activated potassium channels. Proc Natl Acad Sci U S A 94:11013-18.
64. 2+-activated potassium channels. J Neurosci 19:8830-8.
65. + channel from smooth muscle. J Biol Chem 269:17274-8.
66. Knaus HG, McManus OB, Lee SH, Schmalhofer WA, Garcia-Calvo M, Helms LM, and others. 1994. Tremorgenic indole alkaloids potently inhibit smooth muscle high-conductance calcium-activated potassium channels. Biochemistry 33:5819-28.
67. Knuttinen MG, Power JM, Preston AR, Disterhoft JF. 2001. Awareness in classical differential eyeblink conditioning in young and aging humans. Behav Neurosci 115:747-57.
68. Kohler M, Hischberg B, Bond CT, Kinzie JM, Marrion NM, Maylie J, and others. 1996. Small-conductance, calcium-activated potassium channels from mammalian brain. Science 273:1709-14.
69. Kronforst-Collins MA, Moriearty PL, Schmidt B, Disterhoft JF. 1997. Metrifonate improves associative learning and retention in aging rabbits. Behav Neurosci 111:1031-40.
70. Lancaster B, Adams PR. 1986. Calcium-dependent current generating the afterhyperpolarization of hippocampal neurons. J Neurophysiol 55:1268-82.
71. Lancaster B, Hu H, Ramakers GM, Storm JF. 2001. Interaction between synaptic excitation and slow afterhyperpolarization current in rat hippocampal pyramidal cells. J Physiol 536:809-23.
72. Lancaster B, Nicoll RA. 1987. Properties of two calcium-activated hyperpolarizations in rat hippocampal neurones. J Physiol 389:187-204.
73. 2+-dependent afterhyperpolarizations in hippocampal neurons of aged rats. Science 226:1089-92.
74. Lang EJ, Paré D. 1997. Synaptic and synaptically activated intrinsic conductances underlie inhibitory potentials in cat lateral amygdaloid projection neurons in vivo. J Neurophysiol 77:353-63.
75. Latorre R, Oberhauser A, Labarca P, Alvarez O. 1989. Varieties of calcium-activated potassium channels. Ann Rev Physiol 51:385-99.
76. Levitan IB. 1994. Modulation of ion channels by protein phosphorylation and dephosphorylation. Annu Rev Physiol 56:193-212.
77. Logsdon NJ, Kang J, Togo JA, Christian EP, Aiyar J. 1997. A novel gene, hKCa4, encodes the calcium-activated potassium channel in human T lymphocytes. J Biol Chem 272:32723-6.
78. Lovell PV, McCobb DP. 2001. Pituitary control of BK potassium channel function and intrinsic firing properties of adrenal chromaffin cells. J Neurosci 21:3429-42.
79. Madison DV, Nicoll RA. 1982. Noradrenaline blocks accommodation of pyramidal cell discharge in the hippocampus. Nature 299:636-8.
80. 2+ channels in hippocampal neurons. Nature 395:900-5.
81. + current in hippocampal CA1 pyramidal neurons: implication in epileptogenesis. J Neurophysiol 86:2878-86.
82. Marty A. 1981. Ca-dependent K channels with large unitary conductance in chromaffin cell membranes. Nature 291:497-500.
83. Matsumoto H, Ajmone-Marsan C. 1964. Cortical cellular phenomena in experimental epilepsy: ictal manifestations. Exp Neurol 9:305-26.
84. McManus OB. 1991. Calcium-activated potassium channels: regulation by calcium. J Bioenerg Biomembr 23:537-60.
85. McManus OB, Harris GH, Giangiacomo KM, Feigenbaum P, Reuben JP, Addy ME, and others. 1993. An activator of calcium-dependent potassium channels isolated from a medicinal herb. Biochemistry 32:128-33.
86. McManus OB, Helms LM, Pallanck L, Ganetzky B, Swanson R, Leonard RJ. 1995. Functional role of the beta subunit of high conductance calcium-activated potassium channels. Neuron 14:645-50.
87. Meech RW, Strumwasser F. 1970. Intracellular calcium injection activates potassium conductance in aplysia nerve cells. Fed Proc 29:834.
88. + channel, a distinct member of voltage-dependent ion channels with seven N-terminus transmembrane segments (S0-S6), and extracellular N terminus, and an intracellular (S9-S10) C terminus. Proc Natl Acad Sci U S A 94:14066-71.
89. + channel resistant to charybdotoxin and iberiotoxin. Proc Natl Acad Sci U S A 97:5562-7.
90. + channels, on learning and memory processes. Brain Res 551:322-6.
91. Moore CI, Browning MD, Rose GM. 1993. Hippocampal plasticity induced by primed burst, but not long-term potentiation, stimulation is impaired in area CA1 of aged Fischer 344 rats. Hippocampus 3:57-66.
92. Moser EI, Krobert KA, Moser MB, Morris RG. 1998. Impaired spatial learning after saturation of long-term potentiation. Science 281:2038-42.
93. Moyer JR Jr, Disterhoft JF. 1994. Nimodipine decreases calcium action potentials in rabbit hippocampal CA1 neurons in an age-dependent and concentration-dependent manner. Hippocampus 4:11-17.
94. Moyer JR Jr, Power JM, Thompson LT, Disterhoft JF. 2000. Increased excitability of aged rabbit CA1 neurons after trace eyeblink conditioning. J Neurosci 20:5476-82.
95. Moyer JR Jr, Thompson LT, Black JP, Disterhoft JF. 1992. Nimodipine increases excitability of rabbit CA1 pyramidal neurons in an ageand concentration-dependent manner. J Neurophysiol 68:2100-9.
96. Moyer JR Jr, Thompson LT, Disterhoft JF. 1996. Trace eyeblink conditioning increases CA1 excitability in a transient and learning-specific manner. J Neurosci 16:5536-46.
97. 2+-calmodulin kinase II in cholinergic modulation of neuronal responsiveness. J Neurophysiol 68:2264-8.
98. + channel splice variants among hair cells along the tonotopic axis of the chick cochlea. Neuron 19:1077-85.
99. Nicoll RA. 1988. The coupling of neurotransmitter receptors to ion channels in the brain. Science 241:545-51.
100. 2+-activated potassium channels by retaining the gating the bursting states. J Gen Physiol 113:425-39.
101. 2+ channels. J Neurosci 18:3171-9.
102. Oh MM, Gamelli AE, Wu WW, Sametsky E, Disterhoft JF. 2001. Morris watermaze learning enhances neuronal excitability of CA1 hippocampal pyramidal neurons in rats. Soc Neurosci Abs 27:921.921.
103. Oh MM, Power JM, Thompson LT, Moriearty PL, Disterhoft JF. 1999. Metrifonate increases neuronal excitability in CA1 pyramidal neurons from both young and aging rabbit hippocampus. J Neurosci 19:1814-23.
104. + channels by novel benzimidazolone. Eur J Pharmacol 251:53-9.
105. Osmanovic SS, Schefner SA. 1993. Calcium-activated hyperpolarizations in rat locus coeruleus neurons in vitro. J Physiol 469:89-109.
106. + channels in cultured rat adrenal chromaffin cells. J Physiol 481:555-70.
107. + channel function in rat dorsal vagal neurones. J Physiol 527:283-90.
108. + channels. J Biol Chem 276:9762-9.
109. + current underlying the slow spike frequency adaptation in hippocampal neurons. Neuron 11:1023-35.
110. + current IAHP by acetlycholine, but not by glutamate, in hippocampal neurons. Pflugers Arch 431:723-8.
111. Pennefather P, Lancaster B, Adams PR, Nicoll RA. 1985. Two distinct Ca-dependent K currents in bullfrog sympathetic ganglionic cells. Proc Natl Acad Sci U S A 82:3040-4.
112. Piskorowski R, Aldrich RW. 2002. Calcium activation of BK(Ca) potassium channels lacking the calcium bowl and RCK domains. Nature 420:499-502.
113. Pitler TA, Landfield PW. 1990. Aging-related prolongation of calcium spike duration in rat hippocampal slice neurons. Brain Res 508:1-6.
114. Power JM, Wu WW, Sametsky E, Oh MM, Disterhoft JF. 2002. Agerelated enhancement of the slow outward calcium-activated potassium current in hippocampal CA1 pyramidal neurons in vitro. J Neurosci 22:7234-43.
115. Rapp PR, Gallagher M. 1996. Preserved neuron number in the hippocampus of aged rats with spatial learning deficits. Proc Natl Acad Sci U S A 93:9926-30.
116. Reinhart PH, Levitan IB. 1995. Kinase and phosphatase activities intimately associated with a reconstituted calcium-dependent potassium channel. J Neurosci 15:4572-9.
117. Ritsner M, Modai I, Ziv H, Amir S, Halperin T, Weizman A, and others. 2002. An association of CAG repeats at the KCNN3 locus with symptom dimensions of schizophrenia. Biol Psychiatry 51:788-94.
118. + channels. J Physiol 79:259-64.
119. + channels with different pharmacological properties and different physiological functions. Biochem Biophys Res Commun 118:669-74.
120. + channel isoforms along the tonotopic gradient of the chickens cochlea. Neuron 19:1061-75.
121. Rosenzweig ES, Rao G, McNaughton BL, Barnes CA. 1997. Role of temporal summation in age-related long-term potentiation-induction deficits. Hippocampus 7:549-58.
122. Saar D, Grossman Y, Barkai E. 1998. Reduced after-hyperpolarization in rat piriform cortex pyramidal neurons is associated with increased learning capability during operant conditioning. Eur J Neurosci 10:1518-23.
123. + current in rat vagal motoneurons. J Neurophysiol 68:2237-48.
124. Sah P. 1995a. Different calcium channels are coupled to potassium channels with distinct physiological roles in vagal neurons. Proc R Soc Lond B 260:105-11.
125. Sah P. 1995b. Properties of channels mediating the apamin-insensitive afterhyperpolarization in vagal motoneurons. J Neurophysiol 74:1772-6.
126. + currents in neurones: types, physiological roles and modulation. Trends Neurosci 19:150-4.
127. Sah P, Bekkers JM. 1996. Apical dendritic location of slow-afterhyperpolarization current in hippocampal pyramidal neurons: implications for the integration of LTP. J Neurosci 16:4537-42.
128. Sah P, Faber ESL. 2002. Channels underlying neuronal calcium activated potassium currents. Prog Neurobiol 66:345-53.
129. Sah P, Isaacson JS. 1995. Channels underlying the slow afterhyperpolarization in hippocampal pyramidal neurons: neurotransmitters modulate the open probability. Neuron 15:435-41.
130. 2+ release. Neuron 7:257-64.
131. Sah P, McLachlan EM. 1992. Potassium currents contributing to action potential repolarization and the afterhyperpolarization in rat vagal motoneurons. J Neurophysiol 68:1834-41.
132. + channels in rat brain. J Neurosci 22:9698-707.
133. Sanchez M, McManus OB. 1996. Paxilline inhibition of the alphasubunit of the high conductance calcium-activated potassium channel. Neuropharmacology 35:963-8.
134. Sansom SC, Stockland JD, Hall D, Williams B. 1997. Regulation of calcium-activated potassium channels by protein phosphatase 2A. J Biol Chem 272:9902-6.
135. Schreiber M, Salkoff L. 1997. A novel calcium-sensing domain in the BK channel. Biophys J 73:1355-63.
136. 2+/calmodulin. Nature 410:1120-4.
137. Schwindt PC, Spain WJ, Foehring RC, Stafstrom CE, Chubb MC, Crill WE. 1988. Multiple potassium conductances and their functions in neurons from cat sensorimotor cortex in vitro. J Neurophysiol 59:424-49.
138. Seutin V, Johnson SW. 1999. Recent advances in the pharmacology of quaternary salts of bicuculline. Trends Pharmacol Sci 20:268-70.
139. + channels expressed in mammalian cell lines. Br J Pharmacol 129:627-30.
140. + channels in spike broadening during repetitive firing in rat hippocampal pyramidal cells. J Physiol 521:135-46.
141. Shen KZ, Lagrutta A, Davies NW, Standen NB, Adelman JP, North RA. 1994. Tetraethylammonium block of Slowpoke calcium-activated potassium channels expressed in Xenopus oocytes: evidence for tetrameric channel formation. Pflugers Arch 426:440-5.
142. Shmukler BE, Bond CT, Wilhelm S, Bruening-Wright A, Maylie J, Adelman JP, and others. 2001. Structure and complex transcription pattern of the mouse SK1 K(Ca) channel gene, KCNN1. Biochim Biophys Acta 1518:36-46.
143. + channels modulate synaptic plasticity and memory encoding. J Neurosci 22:10163-71.
144. + current in hippocampal pyramidal neurons. Proc Natl Acad Sci U S A 96:4662-7.
145. + channel subunits, SK1, Sk2 and SK3 in the adult rat centrl nervous system. Mol Cell Neurosci 15:476-93.
146. Storm JF. 1987. Action potential repolarization and a fast after-hyperpolarization in rat hippocampal pyramidal cells. J Physiol 385:733-59.
147. Storm JF. 1990. Potassium currents in hippocampal pyramidal cells. Prog Brain Res 83:161-87.
148. + channels stably expressed in HEK 293 cells. Br J Pharmacol 129:991-9.
149. + channels. Am J Physiol 278:C570-81.
150. 2+-dependent afterhyperpolariation current in rat CA3 pyramidal cells in vitro. J Neurophysiol 80:2268-73.
151. Thibault O, Landfield PW. 1996. Increase in single L-type calcium channels in hippocampal neurons during aging. Science 272:1017-20.
152. Thompson LT, Moyer JR Jr, Disterhoff JF. 1996. Transient changes in excitability of rabbit CA3 neurons with a time course appropriate to support memory consolidation. J Neurophysiol 76:1836-49.
153. + channels: metabolic regulation. J Bioenerg Biomembr 23:561-76.
154. Torres GE, Arfken CL, Andrade R. 1996. 5-Hydroxytryptamine4 receptors reduce afterhyperpolarization in hippocampus by inhibiting calcium-induced calcium release. Mol Pharmacol 50:1316-22.
155. + channel beta-subunitfrom human brain. Proc Natl Acad Sci U S A 93:9200-5.
156. Valiante TA, Abdul-Ghani MA, Carlen PL, Pennefather P. 1997. Analysis of current fluctuations during after-hyperpolarization current in dentate granule neurones of the rat hippocampus. J Physiol 499:121-34.
157. van der Staay FJ, Fanelli RJ, Blokland A, Schmidt BH. 1999. Behavioral effects of apamin, a selective inhibitor of the SK(Ca)channel, in mice and rats. Neurosci Biobehav Rev 23:1087-110.
158. Vegara C, Latorre R, Marrion NV, Adelman JP. 1998. Calcium-activated potassium channels. Curr Opin Neurobiol 8:321-9.
159. Viana F, Bayliss DA, Berger AJ. 1993. Calcium conductances and their role in the firing behavior of neonatal rat hypoglossal motoneurons. J Neurophysiol 69:2137-49.
160. Vogalis F, Harvey JR, Furness JB. 2002. TEA- and apamin-resistant K(Ca) channels in guinea-pig myenteric neurons: slow AHP channels. J Physiol 538:421-33.
161. + channels: a transmembrane betasubunit homolog. Proc Natl Acad Sci U S A 96:4137-42.
162. Ca channels determined by a separable domain. Neuron 13:671-81.
163. Weiss C, Preston AR, Oh MM, Schwarz RD, Welty D, Disterhoft JE 2000. The M1 muscarinic agonist CI-1017 facilitates trace eyeblink conditioning in aging rabbits and increases the excitability of CA1 pyramidal neurons. J Neurosci 20:783-90.
164. Wilkinson D, Murray J. 2001. Galantamine: a randomized, double-blind, dose comparison in patients with Alzheimer's disease. Int J Geriatr Psychiatry 16:852-7.
165. Wolfart J, Neuhoff H, Franz O, Roepe J. 2001. Differential expression of the small-conductance, calcium-activated potassium channel SK3 is critical for pacemaker control in dopaminergic midbrain neurons. J Nerosci 21:3443-56.
166. Wu WW, Oh MM, Disterhoft FF. 2002. Age-related biophysical alterations of hippocampal pyramidal neurons: implications for learning and memory. Ageing Res Rev 1:181-207.
167. 2+- and voltage-dependent BK channels in adrenal chromaffin cells and rat insulinoma tumor cells. J Neurosci 19:5255-64.
168. Xia X-M, Falker B, Rivard A, Wayman G, Johnson-Pais T, Keen JE, and others. 1998. Mechanism of calcium gating in small-conductance calcium-activated potassium channels. Nature 395:503-7.
169. Xie J, McCobb DP. 1998. Control of alternative splicing of potassium channels by stress hormones. Science 280:443-6.
170. 2+ release and its activation in response to a single action potential in rabbit otic ganglion cells. J Physiol 486.1:177-87.