Transient changes in excitability of rabbit CA3 neurons with a time course appropriate to support memory consolidation

Journal of Neurophysiology

Volumn 76, Issue 3, 1996, Pages 1836-1849

  Thompson, L T ^a   Moyer Jr , J R ^a   Disterhoft, J F ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADOLESCENT; AFTERHYPERPOLARIZATION; ANIMAL EXPERIMENT; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CONTROLLED STUDY; HIPPOCAMPUS; LEARNING; MEMORY CONSOLIDATION; NERVE CELL EXCITABILITY; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RABBIT;

EID: 0029763504     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.1996.76.3.1836     Document Type: Article

References (100)

1. AGHAJANIAN, G. K. AND RASMUSSEN, K. Intracellular studies in the facial nucleus illustrating a simple new method for obtaining viable motorneurons in adult rat brain slices. Synapse 3: 331-338, 1989.
2. AKASE, E., ALKON, D. L., AND DISTERHOFT, J. F. Hippocampal lesions impair memory of short-delay conditioned eyeblink in rabbits. Behav. Neurosci. 103: 935-943, 1989.
3. AKASE, E., THOMPSON, L. T., AND DISTERHOFT, J. F. A system for quantitative analysis of associative learning. II. Real-time software for MS-DOS microcomputers. J. Neurosci. Methods 54: 119-130, 1994.
4. ALKON, D. L. Voltage-dependent calcium and potassium ion conductances: a contingency mechanism for an associative learning model. Science Wash. DC 205: 810-816, 1979.
5. ALKON, D. L. Calcium-mediated reduction of ionic currents: a biophysical memory trace. Science Wash. DC 226: 1037-1045, 1984.
6. ALKON, D. L., LEDERHENDLER, I., AND SHOUKIMAS, J. L. Primary changes of membrane currents during retention of associative learning. Science Wash. DC 215: 693-695, 1982.
7. BANK, B., DE WEER, A., KUZIRIAN, A. M., RASMUSSEN, H., AND ALKON, D. L. Classical conditioning induces long-term translocation of protein kinase C in rabbit hippocampal CA1 cells. Proc. Natl. Acad. Sci. USA 85: 1988-1992, 1988.
8. BARANYI, A., SZENTE, M. B., AND WOODY, C. D. Properties of associative long-lasting potentiation induced by cellular conditioning in the motor cortex of conscious cats. Neuroscience 42: 1-14, 1991.
9. BARNES, C. A. Involvement of LTP in memory: are we "searching under the street light"? Neuron 15: 751-754, 1995.
10. BENARDO, L. S. AND PRINCE, D. A. Cholinergic pharmacology of mammalian hippocampal pyramidal cells. Neuroscience 7: 1703-1712, 1982.
11. BERGER, T. W. Long-term potentiation of hippocampal synaptic transmission affects rate of behavioral learning. Science Wash. DC 224: 627-630, 1984.
12. BERGER, T. W., ALGER, B., AND THOMPSON, R. F. Neuronal substrates of classical conditioning in the hippocampus. Science Wash. DC 192: 483-485, 1976.
13. BERGER, T. W., RINALDI, P. C., WEISZ, D. J., AND THOMPSON, R. F. Single-unit analysis of different hippocampal cell types during classical conditioning of rabbit nictitating membrane response. J. Neurophysiol. 50: 1197-1219, 1983.
14. BLOCH, V. Facts and hypotheses concerning memory consolidation processes. Brain Res. 24: 561-575, 1970.
15. BLOCH, V. AND LAROCHE, S. Facts and hypotheses related to the search for the engram. In: Neurobiology of Learning and Memory, edited by G. Lynch, J. L. McGaugh, and N. M. Weinberger. New York: Guilford Press, 1994, p. 249-260.
16. BREESE, C. R., HAMPSON, R. E., AND DEADWYLER, S. A. Hippocampal place cells: stereotypy and plasticity. J. Neurosci. 9: 1097-1111, 1989.
17. BUZSAḰI, G. Two-stage model of memory trace formation: a role for "noisy" brain states. Neuroscience 31: 551-570, 1989.
18. BYRNE, J. H. Cellular analysis of associative learning. Physiol. Rev. 67: 329-439, 1987.
19. CAREW, T. J., CASTELLUCI, V. F., AND KANDEL, E. R. Sensitization in Aplysia: restoration of transmission in synapses inactivated by long-term habituation. Science Wash. DC 205: 417-419, 1979.
20. CAREW, T. J. AND SAHLEY, C. L. Invertebrate and memory: from behavior to molecules. Annu. Rev. Neurosci. 9: 435-487, 1986.
21. CASTELLUCCI, V. F., PINKSER, H., KUPFERMAN, I., AND KANDEL, E. R. Neuronal mechanisms of habituation and dishabituation of the gill-withdrawal reflex in Aplysia. Science Wash. DC 167: 1745-1748, 1970.
22. CASTRO, C. A., SILBERT, L. H., MCNAUGHTON, B. L., AND BARNES, C. A. Recovery of spatial learning deficits after decay of electrically induced synaptic enhancement in the hippocampus. Nature Lond. 342: 545-548, 1989.
23. CHRISTIAN, E. P. AND DEADWYLER, S. A. Behavioral functions and hippocampal cell types: evidence for two nonoverlapping populations in the rat. J. Neurophysiol. 55: 331-348, 1986.
24. COHEN, N. J. AND EICHENBAUM, H. Memory, Amnesia, and the Hippocampal System. Cambridge, MA: MIT Press, 1993.
25. COLE. A. E. AND NICOLL, R. A. Acetylcholine mediates a slow synaptic potential in hippocampal pyramidal cells. Science Wash. DC 221: 1299-1301, 1983.
26. COLE, A. E. AND NICOLL, R. A. Characterization of a slow cholinergic post-synaptic potential recorded in vitro from rat hippocampal pyramidal cells. J. Physiol. Lond. 352: 173-188, 1984.
27. +-conductances in hippocampal CA1 neurons by serotonin. Nature Land 328: 73-77, 1987.
28. COLINO, A. AND HALLIWELL, J. V. Carbachol potentiates Q current and activates a calcium-dependent non-specific conductance in rat hippocampus in vitro. Eur. J. Neurosci. 5: 1198-1209, 1994.
29. COULTER, D. A., Lo TURCO, J. J., KUBOTA, M., DISTERHOFT, J. F., MOORE, J. W., AND ALKON, D. L. Classical conditioning reduces amplitude and duration of calcium-dependent afterhyperpolarization in rabbit hippocampal pyramidal cells. J. Neumphysiol. 61: 971-981, 1989.
30. DE JONGE, M. C., BLACK, J., DLYO, R. A., AND DISTERHOFT, J. F. Learning-induced afterhyperpolarization reductions in hippocampus are specific for cell type and potassium conductance. Exp. Brain Res. 80: 456-462, 1990.
31. DEYO, R. A., STRAUBE, K. T., AND DISTERHOFF, J. F. Nimodipine facilitates associative learning in aging rabbits. Science Wash. DC 243: 809-811, 1989.
32. DISTERHOFT, J. F., COULTER, D. A., AND ALKON, D. L. Conditioning-specific membrane changes of rabbit hippocampal neurons measured in vitro. Proc. Nat. Acad. Sci. USA 83: 2733-2737, 1986.
33. DISTERHOFT, J. F., GOLDEN, D. T., READ, H. R., COULTER, D. A., AND ALKON, D. L. AHP reductions in rabbit hippocampal neurons during conditioning are correlated with acquisition of the learned response. Brain Res. 462: 118-125, 1988.
34. DISTERHOFT, J. F., KWAN, H. H., AND Lo, W. D. Nictitating membrane conditioning to tone in the immobilized albino rabbit. Brain Res. 137: 127-143, 1977.
35. DISTERHOFT, J. F., THOMPSON, L. T., AND MOYER, J. R., JR. Cellular mechanisms of associative learning in the hippocampus. In: Neural Bases of Learning and Memory in the Mammalian Brain, edited by J. Delacour. Paris: World Scientific Publishing, 1994.
36. EICHENBAUM, H., MATHEWS, P., AND COHEN, N. J. Further studies of hippocampal representation during odor discrimination learning. Behav. Neurosci. 103: 1207-1216, 1989a.
37. EICHENBAUM, H., WIENER, S. L. SHAPIRO, M. L., AND COHEN, N. J. The organization of spatial coding in the hippocampus: a study of neural ensemble activity. J. Neurosci. 9: 2764-2775, 1989b.
38. GORMEZANO, I. AND KEHOE, E. J. Classical conditioning and the law of contiguity. Adv. Anal. Behav. 2: 1-45, 1980.
39. GREEN, E. J. AND GREENOUGH, W. T. Altered synaptic transmission in dentate gyrus of rats reared in complex environments: evidence from hippocampal slices maintained in vitro. J. Neurophysiol. 55: 739-750, 1986.
40. HAAS, H. L. AND GREENE, R. W. Adenosine enhances atterhyperpolarizalion and accommodation in hippocampal pyramidal cells. Pfleugers Arch. 402: 244-247, 1984.
41. HAAS, H. L. AND KONNERTH, A. Histamine and noradrenaline decrease calcium-activated potassium conductance in hippocampal pyramidal cells. Nature Lond. 302: 432-434, 1983.
42. HAMPSON, R. E., HEYSER, C. J., AND DEADWYLER, S. A. Hippocampal cell firing correlates of delayed-match-to-sample performance in the rat. Behav. Neurosci. 107: 715-739, 1993.
43. HARVEY, J. A., GORMEZANO, I., AND COOL-HAUSER, V. A. Relationship between heterosynaptic reflex facilitation and acquisition of the niclitating membrane response in control and scopolamine-injected rabbits. J. Neurosci. 5: 596-602, 1985.
44. HASSELMO, M. E. Neuromodulation and cortical function: modeling the physiological basis of behavior. Behav. Brain Res. 67: 1-27, 1995.
45. HASSELMO, M. E. AND SCHNELL, E. Laminar selectivity of the cholinergic suppression of synaptic transmission in rat hippocampal region CA1: computational modeling and brain slice physiology. J. Neurosci. 14: 3898-3914, 1994.
46. HAWKINS, R. D., ABRAMS, T. W., CAREW, T. J., AND KANDEL, E. R. A cellular mechanism of classical conditioning in Aplysia: activity-dependent amplification of presynaptic facilitation. Science Wash. DC 219: 400-405, 1983.
47. HAWKINS, R. D., KANDEL, E. R., AND SIEGELBAUM, S. A. Learning to modulate transmitter release: themes and variations in synaptic plasticity. Annu. Rev. Neurosci. 16: 625-665, 1993.
48. HEBB, D. O. The Organization of Behavior: A Neurophvsiological Theory. New York: Wiley, 1949.
49. HEDLUND, B. AND ANDERSEN, P. Alaproclate increases the excitability of hippocampal CA1 pyramidal cells and blocks the slow after-hyperpolarization. Pharmacol. Toxicol. 65: 185-188, 1989.
50. HOTSON, J. R. AND PRINCE, D. A. A calcium-activated hyperpolarization follows repetitive firing in hippocampal neurons. J. Neumphysiol. 43: 409-419, 1980.
51. JEFFERY, K. J. AND MORRIS, R. G. M. Cumulative long-term potentiation in the rat dentate gyrus correlates with, but does not modify, performance in the water maze. Hippocampus 3: 133-140, 1993.
52. KIM, J. J. AND FANESLOW, M. S. Modality-specific retrograde amnesia of fear. Science Wash. DC 256: 675-677, 1992
53. KIM, J. J., CLARK, R. E., AND THOMPSON, R. F. Hippocampectomy impairs the memory of recently, but not remotely, acquired trace eyeblink conditioned responses. Behav. Neurosci. 109: 195-203, 1995.
54. KIRK, R. E. Introductory Statistics. Monterey, CA: Brooks/Cole, 1978.
55. 2+ current: mechanism for behavioral sensitization in Aplysia californica. Proc. Natl. Acad. Sci. USA 75: 3512-3516, 1978.
56. 2+ transients. Proc. Natl. Acad. Sci. USA 87: 4083-4087, 1990.
57. KOROL, D. L., ABEL, T. W., CHURCH, L. T., BARNES, C. A., AND MCNAUGHTON, B. L. Hippocampal synaptic enhancement and spatial learning in the Morris swim task. Hippocampus 3: 127-132, 1993.
58. LANCASTER, B. AND ADAMS, P. R. Calcium-dependent current generating the afterhypetpolarization of hippocampal neurons. J. Neurophysiol. 55: 1268-1282, 1986.
59. LIU, Y. B., DISTERHOFT, J. F., AND SLATER, N. T. Activation of metabotropic glutamate receptors induces long-term depression of GABAergic inhibition in hippocampus. J. Neurophysiol. 69: 1000-1004, 1993.
60. LORENTE DE Nó, R. Studies on the structure of the cerebral cortex. II. Continuation of the study of the Ammonic system. J. Physiol. Neurol. 46: 113-177, 1934.
61. LOTURCO, J. J., COULTER, D. A., AND ALKON, D. L. Enhancement of synaptic potentials in rabbit CA1 pyramidal neurons following classical conditioning. Proc. Natl. Acad Sci. USA 85: 1672-1676, 1988.
62. MADISON, D. V. AND NICOLL, R. A. Control of the repetitive discharge of rat CA1 pyramidal neurones in vitro. J. Physiol. Lond. 372: 221-244, 1986a.
63. MADISON, D. V. AND NICOLL, R. A. Actions of noradrenaline recorded intracellularly in rat hippocampal CA1 pyramidal neurones, in vitro. J. Physiol. Lond. 372: 221-244, 1986b.
64. MADISON, D. V., LANCASTER, B., AND NICOLI., R. A. Voltage clamp analysis of cholinergic action in the hippocampus. J. Neurosci. 7: 733-741, 1987.
65. MALENKA, R. C. AND NICOLL, R. A. Dopamine decreases the calcium-activated afterhyperpolarization in hippocampal CA1 pyramidal cells. Brain Res. 379: 210-215, 1986.
66. MCCORMICK, D. A., CLARK, G. A., LAVOND, D. G.. AND THOMPSON, R. F. Initial localization of the memory trace for a basic form of learning. Proc. Natl. Acad. Sci. USA 79: 2731-2735, 1982.
67. MCGAUGH, J. L. Time-dependent processes in memory storage. Science Wash. DC 153: 1351-1358, 1966.
68. MCGAUGH, J. L. AND ALPERIN, H. P. Effects of electroshock on memory: amnesia without convulsions. Science Wash. DC 152: 665-666, 1966.
69. MIZUMORI, S. J. Y., MCNAUGHTON, B. L., BARNES, C. A., AND Fox, K. B. Preserved spatial coding in hippocampal CA1 pyramidal cells during reversible suppression of CA3c output: evidence for pattern completion in hippocampus. J. Neurosci. 9: 3915-3928, 1989.
70. MOYER, J. R., JR., DEYO, R. A., AND DISTERHOFT, J. F. Hippocampectomy disrupts trace eye-blink conditioning in rabbits. Behav. Neurosci. 104: 243-252, 1990.
71. MOYER, J. R., JR. AND DISTERHOFT, J. F. Nimodipine decreases calcium action potentials in rabbit hippocampal CA1 neurons in an age- and concentration-dependent manner. Hippocampus 4: 11-18, 1994.
72. MOYER, J. R., JR., DISTERHOFT, J. F., BLACK, J. P., AND YEH, J. Dihydropyridine-sensitive calcium channels in acutely-dissociated hippocampal CA1 neurons. Neurosci. Res. Commun. 15: 39-48, 1994.
73. MOYER, J. R., JR., THOMPSON, L. T., BLACK, J. P., AND DISTERHOFT, J. F. Nimodipine increases excitability of rabbit CA1 pyramidal in an age-and concentration-dependent manner. J. Neurophvsiol. 68: 2100-2109, 1992.
74. MOYER, J. R., JR., THOMPSON, L. T., AND DISTERHOFT, J. F. Trace eyeblink conditioning increases CA1 excitability in a transient and learning-specific manner. J. Neurosci. In press.
75. OLDS, J., DISTERHOFT, J. F., SEGAL, M., KONBLITH, C. L., AND HIRSH, R. Learning centers of rat brain mapped by measuring latencies of conditioned unit responses. J. Neurophysiol. 35: 202-219, 1972.
76. OLDS, J. L., ANDERSON, M. L., MCPHIE, D. L., STATEN, L. D., AND ALKON, D. L. Imaging of memory-specific changes in the distribution of protein kinase-C in the hippocampus. Science Wash. DC 245: 866-869, 1989.
77. OLMSTEAD, C. E., BEST, P. J., AND MAYS, L. E. Neural activity in the dorsal hippocampus during paradoxical sleep, slow wave sleep, and waking. Brain Res. 60: 381-391, 1973.
78. POWER, J. M., THOMPSON, L. T., MOYER, J. R., JR., AND DISTERHOFT, J. F. Increased synaptic responsiveness between CA3 and CA1 after trace eyeblink conditioning recorded in vitro. Soc. Neurosci. Abstr. 21: 1931, 1995.
79. Rioux, G. F. AND ROBINSON, G. B. Hippocampal long-term potentiation does not affect either discrimination learning or reversal learning of the rabbit nictitating membrane response. Hippocampus 5: 165-170, 1995.
80. ROBINSON, G. B. Maintained saturation of hippocampal long-term potentiation does not disrupt acquisition of the eight-arm radial maze. Hippocampus 2: 389-395, 1992.
81. SANCHEZ-ANDRES, J. V. AND ALKON, D. L. Voltage-clamp analysis of the effects of classical conditioning on the hippocampus. J. Neurophysiol. 65: 796-807, 1991.
82. SCHARFMAN, H. E. Evidence from simultaneous intracellular recordings in rat hippocampal slices that area CA3 pyramidal cells innervate dentate hilar mossy cells. J. Neurophysiol. 72: 2167-2180, 1994.
83. SCHMALTZ, L. W. AND THEIOS, J. Acquisition and extinction of a classically conditioned reflex in hippocampectomized rabbits (Oryctolagus cuniculus). J. Comp. Physiol. Psych. 79: 328-333, 1972.
84. SCHOLZ, K. P. AND BYRNE, J. H. Long-term sensitization in Aplysia: biophysical correlates in tail sensory neurons. Science Wash. DC 235: 685-687, 1987.
85. SEGAL, M., DISTERHOFT, J. F., AND OLDS, J. Hippocampal unit activity during classical aversive and appetitive conditioning. Science Wash DC 175: 792-794, 1972.
86. SHARP, P. E., MCNAUOHTON, B. L., AND BARNES, C. A. Enhancement of hippocampal field potentials in rats exposed to a novel, complex environment. Brain Res. 339: 361-365, 1985.
87. SOLOMON, P. R., SOLOMON, S. D., VANDER SCHAAF, E. V., AND PERRY, H. E. Altered activity in the hippocampus is more detrimental to classical conditioning than removing the structure. Science Wash. DC 220: 329-331, 1983.
88. SOLOMON, P. R., VANDER SCHAAF, E. V., THOMPSON, R. F., AND WEISZ, D. J. Hippocampus and trace conditioning of the rabbit's classically conditioned nictitating membrane response. Behav. Neurosci. 100: 729-744, 1986.
89. SQUIRE, L. Memory and Brain. New York: Oxford, 1987.
90. STORM, J. F. Potassium currents in hippocampal pyramidal cells. Prog. Brain Res. 83: 161-187, 1990.
91. SUTHERLAND, R. J., DRINCENBERG, H. C., AND HOESING, J. M. Induction of long-term potentiation at perforant path dentate synapses does not affect place learning or memory. Hippocampus 3: 141-148, 1993.
92. THOMPSON, L. T. AND BEST, P. J. Place cells and silent cells in the hippocampus of freely-behaving rats. J. Neurosci. 9: 2382-2390, 1989.
93. THOMPSON, L. T., DISTERHOFT, J. F., AND DEYO, R. A. Nimodipine enhances spontaneous activity of hippocampal pyramidal cells in aging rabbits at a dose that facilitates learning. Brain Res. 535: 119-130, 1990.
94. THOMPSON, L. T., MOSKAL, J. R., AND DISTERHOFT, J. F. Hippocampus-dependent learning facilitated by a monoclonal antibody or D-cycloserine. Nature Lond. 359: 638-641, 1992.
95. THOMPSON, L. T., MOYER, J. R., JR., AKASE, E., AND DISTERHOFT, J. F. A system for quantitative analysis of associative learning. I. Hardware interfaces with cross-species applications. J. Neurosci. Methods 54: 109-117, 1994.
96. THOMPSON, L. T., MOYER, J. R., JR., AND DISTERHOFT, J. F. Trace eyeblink conditioning in rabbits demonstrates heterogeneity of learning ability both between and within age groups. Neurobiol. Aging. In press.
97. THOMPSON, R. F. The neurobiology of learning and memory. Science Wash. DC 233: 941-947, 1986.
98. WALTERS, E. T. AND BYRNE, J. H. Associative conditioning of single sensory neurons suggests a cellular mechanism for learning. Science Wash. DC 219: 405-408, 1983.
99. WOODY, C. D., GRUEN, E., AND BIRT, D. Changes in membrane currents during Pavlovian conditioning of single cortical neurons. Brain Res. 539: 76-84, 1991.
100. ZOLA-MORGAN, S., SQUIRE, L. R., AND AMARAL, D. G. Lesions of the hippocampal formation but not lesions of the fornix or the mammillary nuclei produce long-lasting memory impairment in monkeys. J. Neurosci. 9: 898-913, 1989.