Aging changes in voltage-gated calcium currents in hippocampal CA1 neurons

Journal of Neuroscience

Volumn 16, Issue 19, 1996, Pages 6286-6295

  Campbell, Lee W ^a,b   Hao, Su Yang ^a,c   Thibault, Olivier ^a   Blalock, Eric M ^a   Landfield, Philip W ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^c UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

Author keywords

afterhyperpolarization; aging; Alzheimer's disease; barium currents; calcium currents; calcium homeostasis; hippocampus; inactivation; neurotoxicity

Indexed keywords

CALCIUM ION; NIMODIPINE;

AGED; AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALCIUM CURRENT; CALCIUM TRANSPORT; CHANNEL GATING; CONTROLLED STUDY; HIPPOCAMPUS; MALE; NERVE CONDUCTION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; RAT; VOLTAGE CLAMP;

EID: 0029789056     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.16-19-06286.1996     Document Type: Article

References (92)

1. Armstrong DL, Eckert R (1987) Voltage-activated calcium channels that must be phosphorylated to respond to membrane depolarization. Proc Natl Acad Sci USA 84:2518-2522.
2. Barnes CA (1994) Normal aging: regionally specific changes in hippocampal synaptic transmission. Trends Neurosci 17:8-13.
3. Barnes CA, McNaughton BL (1980) Physiological compensation for loss of afferent synapses in rat hippocampal granule cells during senescence. J Physiol (Lond) 309:473-485.
4. Barnes CA, McNaughton BL, O'Keffe J (1983) Loss of place specificity in hippocampal complex spike cells of senescent rat. Neurobiol Aging 4:113-119.
5. Bean BP (1989) Classes of calcium channels in vertebrate cells. Annu Rev Physiol 51:367-384.
6. Bickford PC, Hoffer BJ, Freedman R (1986) Diminished interaction of norepinephrine with climbing fiber input to cerebellar purkinje neurons in aged Fischer 344 rats. Brain Res 385:405-410.
7. Bickford-Winer PC, Miller JA, Freedman R, Rose GM (1988) Age-related reduction in responses of rat hippocampal neurons to locally applied monoamines. Neurobiol Aging 9:173-179.
8. Brown TH, Jaffe DB (1994) Calcium imaging in hippocampal neurons using confocal microscopy. Ann NY Acad Sci 747:313-324.
9. Brown TH, Fricke RA, Perkel DH (1981) Passive electrical constants in three classes of hippocampal neurons. J Neurophysiol 46:812-827.
10. Catterall WA, De Jongh K, Rotman E, Hell J, Westenbroek R, Dubel SJ, Snutch TP (1993) Molecular properties of calcium channels in skeletal muscle and neurons. Ann NY Acad Sci 681:342-355.
11. Choi DW (1995) Calcium: still center-stage in hypoxic-ischemic neuronal death. Trends Neurosci 18:58-60.
12. Coleman PD, Flood DG (1987) Neuron numbers and dendritic extent in normal aging and Alzheimer's disease. Neurobiol Aging 8:521-545.
13. Deupree DL, Bradley J, Turner DA (1993) Age-related alterations in potentiation in the CA1 region in F344 rats. Neurobiol Aging 14:249-258.
14. Deyo RA, Straube KT, Disterhoft JF (1989) Nimodipine facilitates associative learning in aging rabbits. Science 243:809-811.
15. Dingledine R (1984) Brain slices. New York: Plenum.
16. 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 462:118-125.
17. Disterhoft JF, Moyer JR, Thompson LT, Kowalska M (1993) Functional aspects of calcium-channel modulation. Clin Neuropharmacol 16:S12-S24.
18. Disterhoft JF, Gispen WH, Traber J, Khatchaturian AS (1994) Calcium hypothesis of aging and dementia. Ann NY Acad Sci 747.
19. Eckert R, Chad JE (1984) Inactivation of Ca channels. Prog Biophys Mol Biol 44:215-267.
20. Eliot LE, Johnston D (1994) Multiple components of calcium current in acutely dissociated dentate gyrus granule neurons. J Neurophysiol 27:762-777.
21. Elliott EM, Malouf AT, Catterall WA (1995) Role of calcium channel subtypes in calcium transients in hippocampal CA3 neurons. J Neurosci 15:6433-6444.
22. Fedulova SA, Kostyuk PG, Veselovsky NS (1985) Two types of calcium channels in the somatic membrane of new-born rat dorsal root ganglion neurones, J Physiol (Lond) 359:431-446.
23. Finkel AS, Redman SJ (1985) Optimal voltage-clamping with single microelectrodes. In: Voltage and patch clamping with microelectrodes (Smith Jr TG, Lecar H, Redman SJ, Gage PW, eds), pp 95-120. Baltimore: Williams & Wilkins.
24. Fisher RE, Gray R, Johnston D (1990) Properties and distribution of single voltage-gated calcium channels in adult hippocampal neurons. J Neurophysiol 64:91-104.
25. Fox AP, Nowycky MC, Tsien RW (1987) Kinetics and pharmacological properties distinguishing three types of calcium currents in chick sensory neurons. J Physiol (Lond) 394:149-172.
26. Gähwiler BH, Brown DA (1987) Effects of dihydropyridines on calcium currents in CA3 pyramidal cells in slice cultures of rat hippocampus. Neuroscience 20:731-738.
27. Geinisman Y, deToledo-Morrell L, Morrell F, Heller RE (1995) Hippocampal markers of age-related memory dysfunction: behavioral, electrophysiological and morphological perspectives. Prog Neurobiol 45:223-252.
28. Gibson GE, Peterson C (1987) Calcium and the aging nervous system. Neurobiol Aging 8:329-343.
29. 2+ channels in guinea-pig ventricular myocytes through independent mechanisms. J Physiol (Lond) 444:257-268.
30. Hell JW, Westenbroek RE, Warner C, Ahlijanian MK, Prystay W, Gilbert MM, Snutch TP, Catterall WA (1993) Identification and differential subcellular localization of the neuronal Class C and Class D L-type calcium channel al subunits. J Cell Biol 123:949-962.
31. 2+ channels. Neuron 9:197-207.
32. Johnston D, Hablitz JJ, Wilson WA (1980) Voltage-clamp discloses slow inward current in hippocampal burst-firing neurones. Nature 286:391-393.
33. Johnston D, Brown TH (1983) Interpretation of voltage-clamp measurements in hippocampal neurons. J Neurophysiol 43:409-419.
34. Kavalali ET, Plummer MR (1996) Multiple voltage-dependent mechanisms potentiate calcium channel activity in hippocampal neurons. J Neurosci 16:1072-1082.
35. Kasai H, Aosaki T (1988) Divalent cation dependent inactivation of the high-voltage-activated Ca channel current in chick sensory neurons. Pflügers Arch 411:695-697.
36. Katzman R, Saitoh T (1991) Advances in Alzheimer's disease. FASEB J 5:278-286.
37. Kay AR (1991) Inactivation kinetics of calcium current of acutely dissociated CA1 pyramidal cells of the mature guinea-pig hippocampus. J Physiol (Lond) 437:27-48.
38. Kerr DS, Campbell LW, Hao S-Y, Landfield PW (1989) Corticosteroid modulation of hippocampal potentials: increased effect with aging. Science 245:1505-1509.
39. 2+ conductances: relevance to brain aging. Proc Natl Acad Sci USA 89:8527-8531.
40. Khachaturian ZS (1984) Towards theories of brain aging. In: Handbook of studies on psychiatry and old age (Kay D, Burrows GD, eds), pp 7-30. Amsterdam: Elsevier.
41. Khachaturian ZS (1989) The role of calcium regulation in brain aging: reexamination of a hypothesis. Aging 1:17-34.
42. Kostyuk P, Pronchuk N, Savchenko A, Verkhratsky A (1993) Calcium currents in aged rat dorsal root ganglion neurones. J Physiol (Lond) 461:467-483.
43. + current in rat hippocampal neurones. J Physiol (Lond) 475:229-239.
44. Landfield PW (1987) "Increased calcium current" hypothesis of brain aging. Neurobiol Aging 8:346-347.
45. Landfield PW (1988) Hippocampal neurobiological mechanisms of age-related memory dysfunction. Neurobiol Aging 9:571-579.
46. 2+ channel activity in brain aging and dementia. Ann NY Acad Sci 747:351-364.
47. 2+-dependent afterhyperpolarizations in hippocampal neurons of aged rats. Science 226:1089-1092.
48. 2+ ratios on frequency potentiation in hippocampal slices of young and aged animals. J Neurophysiol 56:797-811.
49. Landfield PW, Thibault O, Mazzanti ML, Porter NM, Kerr DS (1992) Mechanisms of neuronal death in brain aging and Alzheimer's disease: role of endocrine-mediated calcium dyshomeostasis. J Neurobiol 23:1247-1260.
50. 2+. J Gen Physiol 88:321-347.
51. Llinas R, Sugimori M, Lin JW, Cherskey B (1989) Blocking and isolation of a calcium channel from neurons in mammals and cephalopods utilizing a toxin fraction (FTX) from funnel-web spider poison. Proc Natl Acad Sci USA 86:1689-1693.
52. Madison DV, Nicoll RA (1984) Control of the repetitive discharge of rat CA1 pyramidal neurons in vitro. J Physiol (Lond) 354:319-331.
53. Magee JC, Johnston D (1995) Synaptic activation of voltage-gated channels in the dendrites of hippocampal pyramidal neurons. Science 268:301-304.
54. Martinez-Serrano A, Blanco P, Satrustegui J (1992) Calcium binding to the cytosol and calcium extrusion mechanisms in intact synaptosomes and their alterations with aging. J Biol Chem 267:4672-4679.
55. Mayer ML, Westbrook GL (1987) Permeation and block of N-methyl-D-aspartic acid receptor channels by divalent cations in mouse cultured central neurones. J Physiol (Lond) 394:501-527.
56. 2+ channels in embryonic chick ventricle cells: dependence on voltage, current and channel density. J Physiol (Lond) 443:307-334.
57. Mazzanti ML, Thibault O, Landfield PW (1991b) Dihydropyridine modulation of normal hippocampal physiology in young and aged rats. Neurosci Res Commun 9:117-125.
58. McCarthy RT, TanPiengco PE (1992) Multiple types of high-threshold calcium channels in rabbit sensory neurons: high-affinity block of neuronal calcium L-type by nimodipine. J Neurosci 12:2225-2234.
59. McMonagle-Strucko K, Fanelli RJ (1993) Enhanced acquisition of reversal training in a spatial learning task in rats treated with chronic nimodipine. Pharmacol Biochem Behav 44:827-835.
60. 2+ regulation in aging neurons. Ann NY Acad Sci 747:407-418.
61. 2+ regulation. Mech Ageing Dev 25:215-225.
62. Michaelis ML, Foster CT, Jayawickreme C (1992) Regulation of calcium levels in brain tissue from adult and aged rats. Mech Ageing Dev 62:291-306.
63. 2+ channels. J Biol Chem 267:1403-1406.
64. 2+ channels. Neuron 9:1163-1173.
65. 2+ channels in acutely isolated hippocampal CA3 neurons of the guinea-pig. J Physiol (Lond) 433:259-281.
66. Moyer JR, Disterhoft JF (1994) Nimodipine decreases calcium action potentials in an age- and concentration-dependent manner. Hippocampus 4:11-18.
67. Moyer JR, Thompson LT, Black JP, Disterhoft JF (1992) Nimodipine increases excitability of rabbit CA1 pyramidal neurons in an age- and concentration-dependent manner. J Neurophysiol 68:2100-2109.
68. Murchison D, Griffith WH (1995) Low-voltage activated calcium currents increase in basal forebrain neurons from aged rats. J Neurophysiol 74:876-887.
69. 2+ current in CA1 neurones of the adult rat hippocampal slice. Neurosci Lett 111:102-108.
70. Obejero-Paz CA, Jones SW, Scarpa A (1991) Calcium currents in the A7r5 smooth muscle- derived cell line. J Gen Physiol 98:1127-1140.
71. Peterson C, Gibson GE (1984) Aging and 3,4-diaminopyridine ameliorates deficits in calcium uptake during hypoxia. J Neurochem 42:248-252.
72. 2+ currents in mammalian brain neurons. Brain Res 410:147-153.
73. Pitler TA, Landfield PW (1990) Aging-related prolongation of calcium spike duration in rat hippocampal slice neurons. Brain Res 508:1-6.
74. Plummer MR, Logothetis DE, Hess P (1989) Elementary properties and pharmacological sensitivities of calcium channels in mammalian peripheral neurons. Neuron 2:1453-1463.
75. Potier B, Lamour Y, Dutar P (1993) Age-related alterations in the properties of hippocampal pyramidal neurons among rat strains. Neurobiol Aging 14:17-25.
76. 2+ channel currents in rat cerebellar granule neurons. J Neurosci 15:2995-3012.
77. 2+ channels in rat central and peripheral neurons: high-threshold current resistant to dihydropyridine blockers and ω-conotoxin. Neuron 6:269-280.
78. Regehr WG, Connor JA, Tank DW (1989) Optical imaging of calcium accumulation in hippocampal pyramidal cells during synaptic activation. Nature 341:533-536.
79. Reynolds JN, Carlen PL (1989) Diminished calcium currents in aged hippocampal dentate gyrus granule neurones. Brain Res 479:384-390.
80. Rose GM, Gerhardt GA, Conboy GL, Hoffer BJ (1986) Age-related alterations in monoamine release from rat striatum: an in vivo electrochemical study. Neurobiol Aging 7:77-82.
81. Scriabine A, Schuurman T, Traber J (1989) Pharmacological basis for the use of nimodipine in central nervous system disorders. FASEB J 3:1799-1806.
82. Smith DO, Rosenheimer JL (1984) Aging at the neuromuscular junction. In: Aging and cell structure (Johnson JE, ed), pp 113-139. New York: Plenum.
83. Spruston N, Jaffe DB, Johnston D (1994) Dendritic attenuation of synaptic potentials and currents: the role of passive membrane properties. Trends Neurosci 17:161-166.
84. Storm JF (1990) Potassium currents in hippocampal pyramidal cells. In: Progress in brain research (Storm-Mathisen J, Zimmer J, Ottersen OP, eds), pp 161-187. New York: Elsevier.
85. Swartz KJ, Bean BP (1992) Inhibition of calcium channels in rat CA3 pyramidal neurons by a metabotropic glutamate receptor. J Neurosci 12:4358-4371.
86. Thibault O, Landfield PW (1996) Increase in single L-type calcium channels in hippocampal neurons during aging. Science 272:1017-1020.
87. 2+ channels in hippocampal neurons: physiological implications. Proc Natl Acad Sci USA 90:11792-11796.
88. Thibault O, Mazzanti ML, Blalock EM, Porter NM, Landfield PW (1994) Brain neuron preparations for the study of aging changes in calcium potentials and currents. Neuroprotocols 4:177-181.
89. 2+ channel activity at resting potential. Soc Neurosci Abstr 21:1577.
90. Tsien RW, Lipscombe D, Madison DV, Bley KR, Fox AP (1988) Multiple types of neuronal calcium channels and their selective modulation. Trends Neurosci 11:431-437.
91. 2+ channels. Trends Pharmacol Sci 12:349-354.
92. Turner DA, Schwartzkroin PA (1984) Passive electrotonic structure and dendritic properties of hippocampal neurons. In: Brain slices (Dingledine R, ed), pp 25-50. New York: Plenum.