Trace eyeblink conditioning increases CA1 excitability in a transient and learning-specific manner

Journal of Neuroscience

Volumn 16, Issue 17, 1996, Pages 5536-5546

  Moyer Jr , James R ^a,b   Thompson, Lucien T ^a   Disterhoft, John F ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b YALE UNIVERSITY   (United States)

Author keywords

afterhyperpolarization; associative learning; consolidation; hippocampus; in vitro; memory; spike frequency adaptation

Indexed keywords

ADAPTATION; AFTERHYPERPOLARIZATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL SPECIFICITY; CONTROLLED STUDY; ELECTROPHYSIOLOGY; EYELID REFLEX; HIPPOCAMPUS; INSTRUMENTAL CONDITIONING; LEARNING; MEMBRANE STEADY POTENTIAL; NONHUMAN; PRIORITY JOURNAL; RABBIT; STATE DEPENDENT LEARNING; STIMULUS RESPONSE;

EID: 0029822574     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.16-17-05536.1996     Document Type: Article

References (107)

1. Aghajanian GK, Rasmussen K (1989) Intracellular studies in the facial nucleus illustrating a simple new method for obtaining viable motoneurons in adult rat brain slices. Synapse 3:331-338.
2. Akase E, Alkon DL, Disterhoft JF (1989) Hippocampal lesions impair memory of short-delay conditioned eyeblink in rabbits. Behav Neurosci 103:935-943.
3. Akase E, Thompson LT, Disterhoft JF (1994) A system for quantitative analysis of associative learning. II. Real-time software for MS-DOS microcomputers. J Neurosci Methods 54:119-130.
4. Alkon DL (1984) Calcium-mediated reduction of ionic currents: a biophysical memory trace. Science 226:1037-1045.
5. Alvarez P, Squire LR (1994) Memory consolidation and the medial temporal lobe: a simple network model. Proc Natl Acad Sci USA 91:7041-7045.
6. Alvarez P, Zola-Morgan S, Squire LR (1995) Damage limited to the hippocampal region produces long-lasting memory impairment in monkeys. J Neurosci 15:3796-3807.
7. Bank B, deWeer A, Kuzirian AM, Rasmussen H, Alkon DL (1988) Classical conditioning induces long-term translocation of protein kinase C in rabbit hippocampal CA1 cells. Proc Natl Acad Sci USA 85:1988-1992.
8. Belcadi-Abbassi W, Destrade C (1995) Post-test apamin injection suppresses a Kamin-like effect following a learning session in mice. NeuroReport 6:1293-1296.
9. Benardo LS, Prince DA (1982) Ionic mechanisms of cholinergic excitation in mammalian hippocampal pyramidal cells. Brain Res 249:333-344.
10. Berger TW, Alger B, Thompson RF (1976) Neuronal substrate of classical conditioning in the hippocampus. Science 192:483-485.
11. Berger TW, Rinaldi PC, Weisz DJ, Thompson RF (1983) Single-unit analysis of different hippocampal cell types during classical conditioning of rabbit nictitating membrane response. J Neurophysiol 50:1197-1219.
12. +(Ca) into densely connected artificial neural networks. Network 2:1-6.
13. Buzsáki G (1989) Two-stage model of memory trace formation: a role for "noisy" brain states. Neuroscience 31:551-570.
14. Byrne JH (1987) Cellular analysis of associative learning. Physiol Rev 67:329-439.
15. Carew TJ, Sahley CL (1986) Invertebrate learning and memory: from behavior to molecules. Annu Rev Neurosci 9:435-487.
16. Carew TJ, Walters ET, Kandel ER (1981) Classical conditioning in a simple withdrawal reflex in Aplysia californica. J Neurosci 1:1426-1437.
17. Cohen NJ, Eichenbaum H (1993) Memory, amnesia, and the hippocampal system. Cambridge: MIT.
18. Cole AE, Nicoll RA (1983) Acetylcholine mediates a slow synaptic potential in hippocampal pyramidal cells. Science 221:1299-1301.
19. Cole AE, Nicoll RA (1984) Characterization of a slow cholinergic post-synaptic potential recorded in vitro from rat hippocampal pyramidal cells. J Physiol (Lond) 352:173-188.
20. Colino A, Halliwell JV (1987) Differential modulation of three separate K-conductances in hippocampal CA1 neurons by serotonin. Nature 328:73-77.
21. Colino A, Halliwell JV (1993) Carbachol potentiates Q current and activates a calcium-dependent non-specific conductance in rat hippocampus in vitro. Eur J Neurosci 5:1198-1209.
22. Coulter DA, LoTurco JJ, Kubota M, Disterhoft JF, Moore JW, Alkon DL (1989) Classical conditioning reduces the amplitude and duration of the calcium-dependent afterhyperpolarization in rabbit hippocampal pyramidal cells. J Neurophysiol 61:971-981.
23. Crow T (1985a) Conditioned modification of phototactic behavior in Hermissenda. I. Analysis of light intensity. J Neurosci 5:209-214.
24. Crow T (1985b) Conditioned modification of phototactic behavior in Hermissenda. II. Differential adaptation of B photoreceptors. J Neurosci 5:215-223.
25. deJonge MC, Black JP, Deyo RA, Disterhoft JF (1990) Learning-induced afterhyperpolarization reductions in hippocampus are specific for cell type and potassium conductance. Exp Brain Res 80:456-462.
26. Deyo RA, Straube KT, Disterhoft JF (1989) Nimodipine facilitates associative learning in aging rabbits. Science 243:809-811.
27. Disterhoft JF, Coulter DA, Alkon DL (1986) Conditioning-specific membrane changes of rabbit hippocampal neurons measured in vitro. Proc Natl Acad Sci USA 83:2733-2737.
28. Disterhoft JF, Coulter DA, Alkon DL (1988a) Conditioning-specific biophysical alterations in rabbit hippocampus. In: Cellular mechanisms of conditioning and behavioral plasticity (Woody CD, Alkon DL, McGaugh JL, eds), pp 89-104. New York: Plenum.
29. Disterhoft JF, Golden DT, Read HL, Coulter DA, Alkon DL (1988b) AHP reductions in rabbit hippocampal neurons during conditioning correlate with acquisition of the learned response. Brain Res 462:118-125.
30. Disterhoft JF, Deyo RA, Moyer Jr JR, Straube KT, Thompson LT (1989) Calcium blockers and memory in the aging brain. Cardiovasc Rev Rep 10:22-29.
31. Disterhoft JF, Moyer Jr JR, Thompson LT, Cutting FB, Power JM (1994a) In vitro analyses of aging-related learning deficits. Soc Neurosci Abstr 20:796.
32. Disterhoft JF, Thompson LT, Moyer Jr JR (1994b) Cellular mechanisms of associative learning in the hippocampus. In: The memory system of the brain (Delacour J, ed), pp 431-492. Singapore: World Scientific.
33. Frysztak RJ, Crow T (1994) Enhancement of type B and A photoreceptor inhibitory synaptic connections in conditioned Hermissenda. J Neurosci 14:1245-1250.
34. Gustafsson B, Wigström H (1981) Evidence for two types of afterhyperpolarization in CA1 pyramidal cells in the hippocampus. Brain Res 206:462-468.
35. Haas H, Greene R (1984) Adenosine enhances AHP and accommodation in hippocampal pyramidal cells. Pflügers Arch 402:244-247.
36. Haas HL, Konnerth A (1983) Histamine and noradrenaline decrease calcium-activated potassium conductance in hippocampal pyramidal cells. Nature 302:432-434.
37. Halliwell JV, Adams PR (1982) Voltage-clamp analysis of muscarinic excitation in hippocampal neurons. Brain Res 250:71-92.
38. Harvey JA, Gormezano I, Cool-Hauser VA (1985) Relationship between heterosynaptic reflex facilitation and acquisition of the nictitating membrane response in control and scopolamine-injected rabbits. J Neurosci 5:595-602.
39. Hasselmo ME (1993) Acetylcholine and learning in a cortical associative memory. Neural Comput 5:32-44.
40. Hasselmo ME, Barkai E (1995) Cholinergic modulation of activity-dependent synaptic plasticity in the piriform cortex and associative memory function in a network biophysical simulation. J Neurosci 15:6592-6604.
41. Hasselmo ME, Bower JM (1993) Acetylcholine and memory. Trends Neurosci 16:218-222.
42. Hawkins RD, Abrams TW, Carew TJ, Kandel ER (1983) A cellular mechanism of classical conditioning in Aplysia: activity-dependent amplification of presynaptic facilitation. Science 219:400-404.
43. Hawkins RD, Kandel ER, Siegelbaum SA (1993) Learning to modulate transmitter release: themes and variations in synaptic plasticity. Annu Rev Neurosci 16:625-665.
44. Hebb DO (1949) The organization of behavior: a neurophysiological theory. New York: Wiley.
45. Hedlund B, Andersen P (1989) Alaproclate increases the excitability of hippocampal CA1 pyramidal cells and blocks the slow afterhyperpolarization. Pharmacol Toxicol 65:185-188.
46. Hotson JR, Prince DA (1980) A calcium-activated hyperpolarization follows repetitive firing in hippocampal neurons. J Neurophysiol 43:409-419.
47. Kaneko T, Thompson RF (1995) Suppression of rabbit's trace-conditioning nictitating membrane response by scopolamine. Soc Neurosci Abstr 21:1222.
48. Kim JJ, Fanselow MS (1992) Modality-specific retrograde amnesia of fear. Science 256:675-677.
49. Kim JJ, Clark RE, Thompson RF (1995) Hippocampectomy impairs the memory of recently, but not remotely, acquired trace eyeblink conditioned responses. Behav Neurosci 109:195-203.
50. 2+ current: mechanism for behavioral sensitization in Aplysia californica. Proc Natl Acad Sci USA 75:3512-3516.
51. Klein M, Kandel ER (1980) Mechanism of calcium current modulation underlying presynaptic facilitation and behavioral sensitization in Aplysia. Proc Natl Acad Sci USA 77:6912-6916.
52. 2+ transients. Proc Natl Acad Sci USA 87:4083-4087.
53. Kowalska M, Disterhoft JF (1994) Dose- and concentration-dependent effect of nimodipine on learning rate of aging rabbits. Exp Neurol 127:159-166.
54. Kruppa DJ, Thompson JK, Thompson RF (1993) Localization of a memory trace in the mammalian brain. Science 260:989-991.
55. Lancaster B, Adams PR (1986) Calcium-dependent current generating the afterhyperpolarization of hippocampal neurons. J Neurophysiol 55:1268-1282.
56. 2+-dependent afterhyperpolarizations in hippocampal neurons of aged rats. Science 226:1089-1092.
57. Liu YB, Disterhoft JF, Slater NT (1993) Activation of metabotropic glutamate receptors induces long-term depression of GABAergic inhibition in hippocampus. J Neurophysiol 69:1000-1004.
58. LoTurco JJ, Coulter DA, Alkon DL (1988) Enhancement of synaptic potentials in rabbit CA1 pyramidal neurons following classical conditioning. Proc Natl Acad Sci USA 85:1672-1676.
59. Madison DV, Nicoll RA (1986) Actions of noradrenaline recorded intracellularly in rat hippocampal CA1 pyramidal neurones, in vitro. J Physiol (Lond) 372:221-244.
60. Malenka RC, Nicoll RA (1986) Dopamine decreases the calcium-activated afterhyperpolarization in hippocampal CA1 pyramidal cells. Brain Res 379:210-215.
61. Malenka RC, Madison DV, Andrade R, Nicoll RA (1986) Phorbol esters mimic some cholinergic actions in hippocampal pyramidal neurons. J Neurosci 6:475-480.
62. Mazzanti ML, Thibault O, Landfield PW (1991) Dihydropyridine modulation of normal hippocampal physiology in young and aged rats. Neurosci Res Commun 9:117-126.
63. McGaugh JL (1966) Time-dependent processes in memory storage. Science 153:1351-1358.
64. McGaugh JL, Alperin HP (1966) Effects of electroshock on memory: amnesia without convulsions. Science 152:665-666.
65. McGaugh JL, Herz MJ (1972) Memory consolidation. San Francisco: Albion.
66. Moyer Jr JR, Disterhoft JF (1994) Nimodipine decreases calcium action potentials in an age- and concentration-dependent manner. Hippocampus 4:11-18.
67. Moyer Jr JR, Deyo RA, Disterhoft JF (1990) Hippocampectomy disrupts trace eye-blink conditioning in rabbits. Behav Neurosci 104:243-252.
68. Moyer Jr 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.
69. Moyer Jr JR, Thompson LT, Disterhoft JF (1993) Hippocampally-dependent trace eyeblink conditioning increases excitability of rabbit CA1 neurons in vitro. Soc Neurosci Abstr 19:801.
70. Moyer Jr JR, Disterhoft JF, Black JP, Yeh JZ (1994a) Dihydropyridine-sensitive calcium channels in acutely-dissociated hippocampal CA1 neurons. Neurosci Res Commun 15:39-48.
71. Moyer Jr JR, Thompson LT, Disterhoft JF (1994b) The hippocampus as an intermediate storage buffer after associative learning: in vitro evidence from rabbit CA1. Soc Neurosci Abstr 20:796.
72. Müller GE, Pilzecker A (1900) Experimentelle beiträge zur lehre vom gedächtniss. Z Psychol 1:1-288.
73. 2+-calmodulin kinase II in cholinergic modulation of neuronal responsiveness. J Neurophysiol 68:2264-2269.
74. Olds JL, Anderson ML, McPhie DL, Staten LD, Alkon DL (1989) Imaging of memory-specific changes in the distribution of protein kinase-C in the hippocampus. Science 245:866-869.
75. + current underlying slow spike frequency adaptation in hippocampal neurons. Neuron 11:1023-1035.
76. Power JM, Thompson LT, Moyer Jr JR, Disterhoft JF (1995) Increased synaptic responsiveness between CA3 and CA1 after trace eyeblink conditioning recorded in vitro. Soc Neurosci Abstr 21:1931.
77. Rawlins JNP (1985) Associations across time: the hippocampus as a temporary memory store. Behav Brain Sci 8:479-496.
78. Runyon RP, Haber A, Pittenger DJ, Coleman KA (1996) Fundamentals of behavioral statistics, 8th Ed. New York: McGraw-Hill.
79. 2+/calmodulin-dependent protein kinase II. Biophys J 50:319-327.
80. Sanchez-Andres JV, Alkon DL (1991) Voltage-clamp analysis of the effects of classical conditioning on the hippocampus. J Neurophysiol 65:796-807.
81. Schmaltz LW, Theios J (1972) Acquisition and extinction of a classically conditioned response in hippocampectomized rabbits (Oryctolagus cuniculus). J Comp Physiol Psychol 79:328-333.
82. Scholz KP, Byrne JH (1987) Long-term sensitization in Aplysia: biophysical correlates in tail sensory neurons. Science 235:685-687.
83. Schwindt P, Spain WJ, Crill WE (1992) Calcium-dependent potassium currents in neurons from cat sensorimotor cortex. J Neurophysiol 67:216-226.
84. Scoville WB, Milner B (1957) Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psychiatry 20:11-21.
85. Solomon PR (1980) A time and a place for everything? Temporal processing views of hippocampal function with special reference to attention. Physiol Psychol 8:254-261.
86. Solomon PR, Solomon SD, vander Schaff EV, Perry HE (1983) Altered activity in the hippocampus is more detrimental to classical conditioning than removing the structure. Science 220:329-331.
87. Solomon PR, vander Schaff E, Thompson RF, Weisz DJ (1986) Hippocampus and trace conditioning of the rabbit's classically conditioned nictitating membrane response. Behav Neurosci 100:729-744.
88. Squire LR (1986) Mechanisms of memory. Science 232:1612-1619.
89. Squire LR (1987) Memory and brain. New York: Oxford UP.
90. Storm JF (1990) Potassium currents in hippocampal pyramidal cells. Prog Brain Res 83:161-187.
91. Storm JF, Pedarzani P (1995) Norepinephrine and cyclic AMP modulates the Q/H-current independently of protein kinase A in hippocampal neurons. Soc Neurosci Abstr 21:505.
92. Thompson LT, Deyo RA, Disterhoft JF (1990) Nimodipine enhances spontaneous activity of hippocampal pyramidal cells in aging rabbits at a dose that facilitates learning. Brain Res 535:119-130.
93. Thompson LT, Moskal JR, Disterhoft JF (1992) Hippocampus-dependent learning facilitated by a monoclonal antibody or D-cycloserine. Nature 359:638-641.
94. Thompson LT, Moyer Jr JR, Akase E, Disterhoft JF (1994) A system for quantitative analysis of associative learning. I. Hardware interfaces with cross-species applications. J Neurosci Methods 54:109-117.
95. Thompson LT, Moyer Jr JR, Disterhoft JF (1996a) Trace eyeblink conditioning in rabbits demonstrates heterogeneity of learning ability both between and within age groups. Neurobiol Aging 17:619-629.
96. Thompson LT, Moyer Jr JR, Disterhoft JF (1996b) Transient changes in excitability of rabbit CA3 neurons with a time-course appropriate to support memory consolidation. J Neurophysiol, in press.
97. Thompson RF (1967) Foundations of physiological psychology, pp 599-625. New York; Harper & Row.
98. Thompson RF (1988) The neural basis of basic associative learning of discrete behavioral responses. Trends Neurosci 11:152-155.
99. Tocco G, Ramirez O, Nordholm A, Baudry M, Thompson RF (1993) Abolition of the rabbit nictitating membrane conditioned response by reversible inactivation of brain structures. Soc Neurosci Abstr 19:999.
100. Van den Kerckhoff W, Drewes LR (1989) Transfer of nimodipine and another calcium antagonist across the blood-brain barrier and their regional distribution in vivo. In: Diagnosis and treatment of senile dementia (Bergener M, Reisberg B, eds), pp 308-321. Berlin: Springer.
101. Van der Zee EA, Kronforst MA, Disterhoft JF (1994) Hippocampally-dependent trace eyeblink conditioning changes the immunoreactivity for muscarinic acetylcholine receptors and PKCγ in the rabbit hippocampus. Soc Neurosci Abstr 20:1433.
102. Victor M, Agamanolis D (1990) Amnesia due to lesions confined to the hippocampus: a clinical-pathologic study. J Cognit Neurosci 2:246-257.
103. Walters ET, Byrne JH (1983) Associative conditioning of single sensory neurons suggests a cellular mechanism for learning. Science 219:405-408.
104. Weiss C, Kronforst-Collins MA, Disterhoft JF (1996) Activity of hippocampal pyramidal neurons during trace eyeblink conditioning. Hippocampus 6:192-209.
105. Woody CD, Gruen E, Birt D (1991) Changes in membrane currents during Pavlovian conditioning of single cortical neurons. Brain Res 539:76-84.
106. Zola-Morgan S, Squire LR (1990) The primate hippocampal formation: evidence for a time-limited role in memory storage. Science 250:288-290.
107. Zola-Morgan S, Squire LR, Amaral DG (1986) Human amnesia and the medial temporal region: enduring memory impairment following a bilateral lesion limited to field CA1 of the hippocampus. J Neurosci 6:2950-2967.