High-voltage-activated calcium currents in basal forebrain neurons during aging

Journal of Neurophysiology

Volumn 76, Issue 1, 1996, Pages 158-174

  Murchison, David ^a   Griffith, William H ^a  

^a TEXAS A M COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BARIUM ION; CADMIUM; CALCIUM CHANNEL; CALCIUM CHANNEL BLOCKING AGENT; CALCIUM ION; NIFEDIPINE; OMEGA CONOTOXIN GVIA;

AGING; ANIMAL CELL; ARTICLE; CALCIUM CURRENT; CALCIUM HOMEOSTASIS; CONTROLLED STUDY; FOREBRAIN; MALE; MEMBRANE CONDUCTANCE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; RAT;

EID: 0029896492     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.1996.76.1.158     Document Type: Article

References (91)

1. ALLEN, T. G. J., SIM, J. A., AND BROWN, D. A. The whole-cell calcium current in acutely dissociated magnocllular cholinergic basal forebrain neurones of the rat. J. Physiol. Lond. 460: 91-116, 1993.
2. AOSAKI, T. AND KASAI, H. Characterization of two kinds of high voltage-activated Ca-channel currents in chick sensory neurones. Differential sensitivity to dihydropyridines and ω-conotoxin GVIA. Pfluegers Arch. 414: 150-156, 1989.
3. ARMSTRONG, D. AND ECKERT, R. Voltage-activated calcium channels must be phosphorylated to respond to membrane depolarization. Proc. Natl. Acad. Sci. USA 84: 2518-2522, 1987.
4. 2+ currents in acutely isolated, adult rat neostriatal neurons. J. Neurosci. 14: 6667-6686, 1994.
5. BEAN, B. P. Classes of calcium channels in vertebrate cells. Annu. Rev. Physiol. 51: 367-384, 1989.
6. BERTOLINO, M. AND LLINÁS, R. R. The central role of voltage-activated calcium channels in neuronal cells. Annu. Rev. Pharmacol. Toxicol. 32: 399-421, 1992.
7. BIRNBAUMER, L., CAMPBELL, K. P., CATTERALL, W. A., HARPOLD, M. M., HOFMANN, F., HORNE, W. A., MORI, Y., SCHWARTZ, A., SNUTCH, T. P., TANABE, T., AND TSIEN, R. W. The naming of voltage-gated calcium channels. Neuron 13: 505-506, 1994.
8. BROWN, A. M., MORIMOTO, K., TSUDA, Y., AND WILSON, D. L. Calcium current-dependent and voltage-dependent inactivation of calcium channels in Helix aspersa. J. Physiol. Lond. 320: 193-218, 1981.
9. BYERLY, L. AND HAGIWARA, S. Calcium currents in internally perfused nerve cell bodies of Limnea stagnalis. J. Physiol. Lond. 322: 503-528, 1982.
10. CARBONE, E. AND LUX, H. D. A low voltage-activated, fully inactivating Ca channel in vertebrate sensory neurones. Nature Lond. 310: 501-502, 1984.
11. CHAD, J., ECKERT, R., AND EWALD, D. Kinetics of calcium-dependent inactivation of calcium current in voltage-clamped neurones of Aplysia californica. J. Physiol. Lond. 347: 279-300, 1984.
12. CHAD, J. E. AND ECKERT, R. An enzymatic mechanism for calcium current inactivation in dialyzed Helix neurones. J. Physiol. Lond. 378: 31-51, 1986.
13. 2+ in acutely isolated hippocampal neurons. J. Neurophysiol. 73: 515-524, 1995.
14. CHOI, D. W. Excitotoxic cell death. J. Neurobiol. 23: 1261-1276, 1992.
15. COX, D. AND DUNLAP, K. Inactivation of N-type calcium current in chick sensory neurons: calcium and voltage dependence. J. Gen. Physiol. 104: 311-336, 1994.
16. DATYNER, N. B. AND COHEN, I. S. Slow inactivation of L-type calcium current distorts the measurement of L- and T-type calcium current in Purkinje myocytes. J. Gen. Physiol. 102: 859-869, 1993.
17. DECKER, M. W. The effects of aging on hippocampal and cortical projections of the forebrain cholinergic system. Brain Res. Rev. 12: 423-438, 1987.
18. 2+ channel expressed in Xenopus oocytes. J. Physiol. Lond. 485: 619-634, 1995.
19. DINOPOULOS, A., PARNAVELAS, J. F., AND ECKENSTEIN, F. Morphological characterization of cholinergic neurons in the horizontal limb of the diagonal band of Broca in the basal forebrain of the rat. J. Neurocytol. 15: 619-628, 1986.
20. DINOPOULOS, A., PARNAVELAS, J. G., UYLINGS, H. B. M., AND VAN EDEN, C. G. Morphology of neurons in the basal forebrain nuclei of the rat: a golgi study. J. Comp. Neurol. 272: 461-474, 1988.
21. DISTERHOFT, J. F., MOYER, J. R., JR., AND THOMPSON, L. T. The calcium rationale in aging and Alzheimer's disease. Evidence from an animal model of normal aging. In: Calcium Hypothesis of Aging and Dementia, edited by J. F. Disterhoft, W. H. Gispen, J. Traber, and Z. S. Khachaturian. New York: NY Acad. Sci., 1994, p. 382-406.
22. DOROSHENKO, P. A., KOSTYUK, P. G., AND MARTYNYUK, A. E. Intracellular metabolism of adenosine 3′,5′-cyclic monophosphate and calcium inward current in perfused neurones of Helix pomatia. Neuroscience 7: 2125-2134, 1982.
23. ECKERT, R. AND CHAD, J. E. Inactivation of Ca channels. Prog. Biophys. Mol. Biol. 44: 215-267, 1984.
24. FIBIGER, H. C. The organization and some projections of cholinergic neurons of the mammalian forebrain. Brain Res. Rev. 4: 327-388, 1982.
25. FIFKOVA, E. AND MORALES, M. Aging and the neurocytoskeleton. Exp. Gerontol. 26: 125-136, 1992.
26. FISCHER, W., GAGE, F. H., AND BJÖRKLUND, A. Degenerative changes in forebrain cholinergic nuclei correlate with cognitive impairments in aged rats. Eur. J. Neurosci. 1: 34-45, 1989.
27. FOX, A. P., NOWYCKY, M. C., AND TSIEN, R. W. Kinetic and pharmacological properties distinguishing three types of calcium currents in chick sensory neurones. J. Physiol. Lond. 394: 149-172, 1987.
28. GIBSON, G. E. AND PETERSON, C. Calcium and the aging nervous system. Neurobiol. Aging 8: 329-343, 1987.
29. GRIFFITH, W. H. Membrane properties of cells types within guinea pig basal forebrain in vitro. J. Neurophysiol. 1590-1612, 1988.
30. GUTNICK, M. J., LUX, H. D., SWANDULLA, D., AND ZUCKER, H. Voltage-dependent and calcium-dependent inactivation of calcium channel current in identified snail neurones. J. Physiol. Lond. 412: 197-220, 1989.
31. HALL, S. C. AND GRIFFITH, W. H. Calcium channel subtypes mediating synaptic transmission during aging. Soc. Neurosci. Abstr. 21: 332, 1995.
32. HAMILL, O. P., MARTY, A. R., NEHER, E., SAKMANN, B., AND SIGWORTH, F. J. Improved patch techniques for high-resolution current recordings from cells and cell-free patches. Pfluegers Arch. 391: 85-100, 1981.
33. HILLE, B. Ionic Channels of Excitable Membranes. Sunderland, MA: Sinauer, 1992.
34. 2+ channels. Neuron 9: 69-77, 1992.
35. HOCKBERGER, P. E. AND NAM, S. C. High-voltage-activation calcium current in developing neurons is insensitive to nifedipine. Pfluegers Arch. 426: 402-411, 1994.
36. HOLLIDAY, J. AND SPITZER, N. Calcium channels in the regulation of cell development and cellular interactions. In: Calcium Channels: Their Properties, Functions, Regulation and Clinical Relevance, edited by L. Hurwitz, L. D. Partridge, and J. K. Leach. Boca Raton, FL: CRC, 1991, p. 137-155.
37. HONG, S. J. AND LNENICKA, G. A. Activity-dependent reduction in voltage-dependent calcium current in a crayfish motoneuron. J. Neurosci. 15: 3539-3547, 1995.
38. HORN, R. AND MARTY, A. Muscarinic activation of ionic currents measured by a new whole-cell recording method. J. Gen. Physiol. 92: 145-159, 1988.
39. JASSAR, B. S., PENNEFATHER, P. S., AND SMITH, P. A. Changes in sodium and calcium channel activity following axotomy of B-cells in bullfrog sympathetic ganglion. J. Physiol. Lond. 472: 203-231, 1993.
40. JASSAR, B. S. AND SMITH, P. A. Slow frequency-dependence of action potential afterhyperpolarization in bullfrog sympathetic ganglion neurones. Pfluegers Arch. 419: 478-485, 1991.
41. JIN, L.-W. AND SAITOH, T. Changes in protein kinases in brain aging and Alzheimer's disease: Implications for drug therapy. Drugs Aging 6: 136-149, 1995.
42. 2+-dependent inactivation in a mammalian central neuron involves the cytoskeleton. Pfluegers Arch. 429: 14-21, 1994.
43. JOHNSTON, D. AND WU, S. M.-S. Foundations of Cellular Neurophysiology. Cambridge, MA: MIT Press, 1995.
44. JONES, S. W. AND MARKS, T. N. Calcium currents in bullfrog sympathetic neurons. II. Inactivation. J. Gen. Physiol. 94: 169-182, 1989.
45. KAY, A. R. AND WONG, R. K. S. Isolation of neurons suitable for patch-clamping from adult mammalian central nervous systems. J. Neurosci. Methods 16: 227-238, 1986.
46. KHACHATURIAN, Z. Towards theories of brain aging. In: Handbook of Studies on Psychiatry and Old Age, edited by D. W. Kay and G. D. Burrows. Amsterdam: Elsevier, 1984, p. 7-30.
47. KHACHATURIAN, Z. S. Calcium hypothesis of Alzheimer's disease and brain aging. In: Calcium Hypothesis of Aging and Dementia, edited by J. F. Disterhoft, W. H. Gispen, J. Traber, and Z. S. Khachaturian. New York: NY Acad. Sci., 1994, p. 1-11.
48. KHATEB, A., MÜHLETHALER, M., ALONSO, A., SERAFIN, M., MAINVILLE, L., AND JONES, B. E. Cholinergic nucleus basalis neurons display the capacity for rhythmic bursting activity mediated by low-threshold calcium spikes. Neuroscience 51: 489-494, 1992.
49. KIRISCHUK, S., PRONCHUK, N., AND VERKHRATSKY, A. Measurements of intracellular calcium in sensory neurons of adult and old rats. Neuroscience 50: 947-951, 1992.
50. KOSTYUK, P. G. Diversity of calcium ion channels in cellular membranes. Neuroscience. 28: 253-261, 1989.
51. KOSTYUK, P., PRONCHUK, N., SAVCHENKO, A., AND VERKHRATSKY, A. Calcium currents in aged rat dorsal root ganglion neurones. J. Physiol. Lond. 461: 467-483, 1993.
52. LANDFIELD, P. W. "Increased calcium-current" hypothesis of brain aging. Neurobiol. Aging 8: 346-347, 1987.
53. 2+ channel activity in brain aging and dementia. Hormonal and pharmacologic modulation. In: Calcium Hypothesis of Aging and Dementia, edited by J. F. Disterhoft, W. H. Gispen, J. Traber, and Z. S. Khachaturian. New York: NY Acad. Sci., 1994, p. 351-364.
54. LANDFIELD, P. W., CAMPBELL, L. W., HAO, S.-Y., AND KERR, D. S. Aging-related increases in voltage-sensitive, inactivating calcium currents in rat hippocampus. In: Calcium, Membranes, Aging and Alzheimer's Disease, edited by Z. Khachaturian, C. W. Cotman, and J. W. Pettegrew. New York: NY Acad. Sci., 1989, p. 95-105.
55. 2+-dependent afterhyperpolarizations in hippocampal neurons of aged rats. Science Wash. DC 226: 1089-1092, 1984.
56. 2+ ratios on frequency potentiation in hippocampal slices of young and aged rats. J. Neurophysiol. 56: 797-811, 1986.
57. LETERRIER, J. F. AND EYER, J. Age-dependent changes in the ultrastructure and in the molecular composition of rat brain microtubles. J. Neurochem. 59: 1126-1137, 1992.
58. LEVITAN, I. B. Modulation of ion channels in neurons and other cells. Annu. Rev. Neurosci. 11: 119-136, 1988.
59. LLINÁS, R., SUGIMORI, M., LIN, J.-W., AND CHERKSEY, B. 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, 1989.
60. LORENZON, N. M. AND FOEHRING, R. C. Characterization of pharmacologically identified voltage-gated calcium channel currents in acutely isolated rat neocortical neurons. I. Adult neurons. J. Neurophysiol. 73: 1430-1442, 1995a.
61. LORENZON, N. M. AND FOEHRING, R. C. Characterization of pharmacologically identified voltage-gated calcium channel currents in acutely isolated rat neocortical neurons. II. Postnatal development. J. Neurophysiol. 73: 1443-1450, 1995b.
62. MALENKA, R. C., KAUER, J. A., PERKEL, D. J., AND NICOLL, R. A. The impact of postsynaptic calcium on synaptic transmission. Trends Neurosci. 12: 444-450, 1989.
63. MARTINEZ, A., VITORICA, J., AND SATRUSTEGUI, J. Cytosolic free calcium levels increase with age in rat brain synaptosomes. Neurosci. Lett. 88: 336-342, 1988.
64. MCCOBB, D. P., BEST, P. M., AND BEAM, K. G. Development alters the expression of calcium currents in chick limb motoneurons. Neuron 2: 1633-1643, 1989.
65. MESULAM, M.-M., MUFSON, E. J., WAINER, B. H., AND LEVY, A. I. Central cholinergic pathways in the rat: an overview based on an alternative nomenclature (Ch1-Ch6). Neuroscience 10: 1185-1201, 1983.
66. MEYERS, D. E. R. AND BARKER, J. L. Whole-cell patch-clamp analysis of voltage-dependent calcium conductances in cultured embryonic rat hippocampal neurons. J. Neurophysiol. 61: 467-477, 1989.
67. MIETTINEN, R., SIRVIÖ, J., RIEKKINEN, P., SR., LAAKSO, M. P., RIEKKINEN, M., AND RIEKKINEN, P., JR. Neocortical, hippocampal and septal parvalbumin- and somatostatin-containing neurons in young and aged rats: correlation with passive avoidance and water maze performance. Neuroscience 53: 367-378, 1993.
68. MILIJANICH, G. P. AND RAMACHANDRAN, J. Antagonists of neuronal calcium channels: structure, function, and therapeutic implications. Annu. Rev. Pharmacol. Toxicol. 35: 707-734, 1995.
69. 2+ homeostasis. Prog. Neurobiol. 37: 255-285, 1991.
70. MINTZ, I. M., ADAMS, M. E., AND BEAN, B. P. P-type calcium channels in rat central and peripheral neurons. Neuron 9: 85-95, 1992.
71. MORI, Y., FRIEDRICH, T., KIM, M.-S., MIKAMI, A., NAKAI, J., RUTH, P., BOSSE, E., HOFMANN, F., FLOCKERZI, V., FURUICHI, T., MIKOSHIBA, K., IMOTO, K., TANABE, T., AND NUMA, S. Primary structure and functional expression from complementary DNA of a brain calcium channel. Nature Lond. 350: 398-402, 1991.
72. MURCHISON, D. AND GRIFFITH, W. H. Low-voltage activated calcium currents increase in basal forebrain neurons from aged rats. J. Neurophysiol. 74: 876-887, 1995.
73. NEUMANN, T., LINKE, R., AND FROTSCHER, M. Fine structure of rat septohippocampal neurons. I. Identification of septohippocampal projection neurons by retrograde tracing combined with electron microscopic immunocytochemistry and intracellular staining. J. Comp. Neurol. 325: 207-218, 1992.
74. NICOTERA, P., BELLOMO, G., AND ORRENIUS, S. Calcium-mediated mechanisms in chemically induced cell death. Annu. Rev. Pharmacol. Toxicol. 32: 449-470, 1992.
75. NOWYCKY, M. C., FOX, A. P., AND TSIEN, R. W. Three types of neuronal calcium channel with different calcium agonist sensitivity. Nature Lond. 316: 440-443, 1985.
76. OLCESE, R., QIN, N., SCHNEIDER, T., NEELY, A., WEI, X., STEFANI, E., AND BIRNBAUMER, L. The amino terminus of a calcium channel β subunit sets rates of channel inactivation independently of the subunit's effect on activation. Neuron 13: 1433-1438, 1994.
77. ORRENIUS, S. AND NICOTERA, P. The calcium ion and cell death. J. Neural Transm. 43: 1-11, 1994.
78. PEREZ-REYES, E. AND SCHNEIDER, T. Calcium channels: structure, function and classification. Drug Dev. Res. 33: 295-318, 1994.
79. PITLER, T. A. AND LANDFIELD, P. W. Aging-related prolongation of calcium spike duration in rat hippocampal slice neurons. Brain Res. 508: 1-6, 1990.
80. PLUMMER, M. R. AND HESS, P. Reversible uncoupling of inactivation in N-type calcium channels. Nature Lond. 351: 657-659, 1991.
81. 1-subunit. Nature Lond. 368: 67-70, 1994.
82. 2+ channel currents in rat cerebellar granule neurons. J. Neurosci. 15: 2995-3012, 1995.
83. REYNOLDS, J. N. AND CARLEN, P. L. Diminished calcium currents in aged hippocampal dentate gyrus granule neurones. Brain Res. 479: 384-390, 1989.
84. ROSSI, P., D'ANGELO, E., MAGISTRETTI, J., TOSELLI, M., AND TAGLIETTI, V. Age-dependent expression of high-voltage activated calcium currents during cerebellar granule cell development in situ. Pfluegers Arch. 429: 107-116, 1994.
85. ROTHE, T. AND GRANTYN, R. Retinal ganglion neurons express a toxin-resistant developmentally regulated novel type of high-voltage-activated calcium channel. J. Neurophysiol. 72: 2542-2546, 1994.
86. SCHANNE, F. A. X., KANE, A. B., YOUNG, E. E., AND FARBER, J. L. Calcium dependence of toxic cell death: a final common pathway. Science Wash. DC 206: 700-702, 1979.
87. 2+ current. J. Neurophysiol. 71: 1272-1280, 1994.
88. THOMPSON, S. M. AND WONG, R. K. S. Development of calcium current subtypes in isolated rat hippocampal pyramidal cells. J. Physiol. Lond. 439: 671-689, 1991.
89. TILLOTSON, D. Inactivation of Ca conductance dependent on entry of Ca ions in molluscan neurons. Proc. Natl. Acad. Sci. USA 76: 1497-1500, 1979.
90. VERKHRATSKY, A., SHMIGOL, A., KIRISCHUK, S., PRONCHUK, N., AND KOSTYUK, P. Age-dependent changes in calcium currents and calcium homeostasis in mammalian neurons. In: Calcium Hypothesis of Aging and Dementia, edited by J. F. Disterhoft, W. H. Gispen, J. Traber, and Z. S. Khachaturian. New York: NY Acad. Sci., 1994, p. 365-381.
91. WERZ, M. A., ELMSLIE, K. S., AND JONES, S. W. Phosphorylation enhances inactivation of N-type calcium channel current in bullfrog sympathetic neurons. Pfluegers Arch. 424: 424-538, 1993.