Transient and persistent consequences of acute stress on long-term potentiation (LTP), synaptic efficacy, theta rhythms and bursts in area CA1 of the hippocampus

Synapse

Volumn 26, Issue 3, 1997, Pages 209-217

  Shors, Tracey J ^a   Gallegos, Roger A ^a   Breindl, Anette ^a  

^a PRINCETON UNIVERSITY   (United States)

Author keywords

electroencephalography (EEG); fear; hippocampus; learning; N methyl D aspartate (NMDA); stratum radiatum

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ELECTROENCEPHALOGRAPHY; EXCITATORY POSTSYNAPTIC POTENTIAL; FEAR; HIPPOCAMPUS; LEARNING; LONG TERM POTENTIATION; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; STRESS; SYNAPSE; THETA RHYTHM;

ACUTE DISEASE; ANIMALS; ELECTRIC STIMULATION; ELECTROPHYSIOLOGY; ELECTROSHOCK; EVOKED POTENTIALS; HIPPOCAMPUS; LONG-TERM POTENTIATION; MALE; RATS; RATS, SPRAGUE-DAWLEY; RESTRAINT, PHYSICAL; STRESS, PSYCHOLOGICAL; SYNAPSES; THETA RHYTHM;

EID: 0031004872     PISSN: 08874476     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1098-2396(199707)26:3<209::AID-SYN2>3.0.CO;2-B     Document Type: Article

References (56)

1. Abraham, W.C., Mason, S.E., Demmer, J., Williams, J.M., Richardson, C.L., Tate, W.P., Lawlor, P.A., and Dragunow, M. (1993) Correlations between immediate early gene induction and the persistence of long-term potentiation. Neuroscience, 56:717-727.
2. Balleine, B.W., and Curthoys, I.S. (1991) Differential effects of escapable and inescapable footshock on hippocampal theta activity. Behav. Neurosci., 105:202-209.
3. Berger, T.W. (1984) Long-term potentiation of hippocampal synaptic transmission affects rate of behavioral learning. Science, 224:627-630.
4. Berry, S.D., and Swain, R.A. (1989) Water deprivation optimizes hippocampal activity and facilitates nictitating membrane conditioning. Behav. Neurosci., 103:71-76.
5. Bland, B.H., Seto, M.G., Sinclair, B.R., and Fraser, S.M. (1984) The pharmacology of hippocampal theta cells: Evidence that the sensory processing correlate is cholinergic. Brain Res., 299:121-131.
6. Bliss, T.V.R. and Lomo, T. (1973) Long-lasting potentiation of synaptic transmission in the dentate gyrus of the anesthetized rabbit following stimulation of the perforant path. J. Physiol., 232:331-356.
7. Cole, A.J., Saffen, D.W., Baraban, J.M., and Worley, P.F. (1989) Rapid increase of an immediate early gene messenger RNA in hippocampal neurons by synaptic NMDA receptor activation. Nature, 340:474-476.
8. Collingridge, G.L., Kehl, S.J., and McLennan, H. (1983) Excitatory amino acids in synaptic transmission in the Schaffer-commissural pathway of the rat hippocampus. J. Physiol., 443:33-46.
9. Cullinan, W.E., Herman, J.P., Battaglia, D.F., Akil, H., and Watson, S.J. (1995) Pattern and time course of immediate early gene expression in rat brain following acute stress. Neuroscience, 64:477-505.
10. Diamond, D.M., Bennett, M.C., Stevens, K.E., Wilson, R.L., and Rose, G.M. (1990) Exposure to a novel environment interferes with the induction of hippocampal primed burst potentiation in the behaving rat. Psychobiology, 18:273-281.
11. Foy, M.R., Stanton, M.E., Levine, S., and Thompson, R.F. (1987) Behavioral stress impairs long-term potentiation in rodent hippocampus. Behav. Neural Biol., 48:138-149.
12. Foy, M.R., Shors, T.J., Levine, S., and Thompson, R.F. (1988) Time-course of stress-induced impairment of LTP in rodent hippocampus. Soc. Neurosci. Abstr., 12.8:19.
13. Henke, P.G. (1990) Granule cell potentials in the dentate gyrus of the hippocampus: Coping behavior and stress ulcers in rats. Behav. Brain Res., 36:97-103.
14. Huang, Y.Y., Colino, A., Selig, D.K., and Malenka, R.C. (1992) The influence of prior synaptic activity on the induction of long-term potentiation. Science, 255:730-733.
15. Kaczmarek, L. (1992) Expression of c-fos and other genes encoding transcription factors in long-term potentiation. Behav. Neural Biol., 57:263-266.
16. Kerr, D.S., Campbell, L.W., Applegate, M.D., Brodish, A., and Landfield, P.W. (1991) Chronic stress-induced acceleration of electrophysiologic and morphometric biomarkers of hippocampal aging. J. Neurosci., 11:1316-1324.
17. Khanna, S., and Sinclair, J.G. (1989) Noxious stimuli produce prolonged changes in the CA1 region of the rat hippocampus. Pain, 39:337-343.
18. Kim, J.J., Foy, M.R., Thompson, R.F. (1996) Behavioral stress modifies hippocampal plasticity through N-methyl-D-aspartate receptor activation. PNAS (USA), 93:4750-4753.
19. Kramis, R., Vanderwolf, C.H., and Bland, B.H. (1975) Two types of hippocampal rhythmical slow activity in both the rabbit and the rat: Relations to behavior and effects of atropine, diethyl ether, urethane, and pentobarbital. Exp. Neurol., 49:58-85.
20. Landfield, P. (1977) Differential effects of posttrial driving or blocking of the theta rhythm on avoidance learning in rats. Physiol. Behav., 18:439-445.
21. Larson, J., Lynch, G. (1988) Role of N-methyl-D-aspartate (NMDA) receptors in the induction of synaptic potentiation by burst stimulation patterned after the hippocampal theta rhythm. Brain Res., 441:111-118.
22. Larson, J., Wong, D., and Lynch, G. (1986) Patterned stimulation at the theta frequency is optimal for the induction of hippocampal long-term potentiation. Brain Res., 358:347-350.
23. Leung, L.W.S., and Desborough, K.A. (1988) APV, an NMDA receptor antagonist, blocks the hippocampal theta rhythm in behaving rats. Brain Res., 463:148-152.
24. Maier, S.F. (1990) Role of fear in mediating shuttle escape learning deficit produced by inescapable shock. J. Exp. Psychol., 16:137-149.
25. Maren, S., DeCola, J.P., Swain, R.A., Fanselow, M.S., and Thompson, R.F. (1994) Parallel augmentation of hippocampal long-term potentiation, theta rhythm, and contextual fear conditioning in water-deprived rats. Behav. Neurosci., 108:44-56.
26. Mark, G.P., Rada, P.V., and Shors, T.J. (1996) Inescapable stress enhances acetylcholine release in the hippocampus and prefrontal cortex, but not in the amygdala or nucleus accumbens. Neuroscience, 74:767-774.
27. McEwen, B.S. (1994) The plasticity of the hippocampus is the reason for its vulnerability. The Neurosci., 6:239-246.
28. McNaughton, B.L. (1982) Long-term synaptic enhancement and short-term potentiation in rat fascia dentata act through different mechanisms. J. Physiol., 324:249-262.
29. Moser, E., Moser, M.D., and Andersen, P. (1993) Association between brain temperature and dentate field potentials in exploring and swimming rats. Science, 259:1324-1326.
30. Otto, T., Eichenbaum, H., Wiener, S.I., and Wible, C.G. (1991) Learning-related patterns of CA1 spike trains parallel stimulation parameters optimal for inducing hippocampal long-term potentiation. Hippocampus, 1:181-192.
31. Overmier, J.B., Seligman, and M.E.P. (1967) Effects of inescapable shock upon subsequent escape and avoidance learning. J. Comp. Physiol. Psychol., 63:23-33.
32. Pavlides, C., Greenstein, Y.J., Grudman, M., and Winson, J. (1988) Long-term potentiation in the dentate gyrus is induced preferentially on the positive phase of theta-rhythm. Brain Res., 439:383-387.
33. Pavlides, C., Watanabe, Y., and McEwen, B. (1993) Effects of glucocorticoids on hippocampal long-term potentiation. Hippocampus, 3:183-192.
34. Reymann, K.G., Malisch, R., Schulzeck, K., Brodemann, R., Otto, T., and Matthies, H. (1985) The duration of long-term potentiation in the CA1 region of the hippocampal slice. Brain Res. Bull 15:249-255.
35. Rossellini, R.A. (1978) Inescapable shock interferes with the acquisition of a free appetitive operant. Animal Learn Behav., 6:155-159.
36. Rose, G.M., and Dunwiddie, T.V. (1986) Induction of hippocampal long-term potentiation using physiologically patterned stimulation. Neurosci. Lett., 69:244-248.
37. Sainsbury, R.S., Heynen, A., and Montoya, C.P. (1987) Behavioral correlates of hippocampal type 2 theta in the rat. Physiol. Behav. 39:513-519.
38. Sapolsky, R.M. (1992) Stress, the Aging Brain, and the Mechanisms of Neuron Death. The MIT Press, Cambridge, Massachusetts.
39. Schreiber, S., Tocco, G., Shors, T.J., and Thompson, R.F. (1991) Immediate early gene induction after acute stress. Neuroreport, 2:17-20.
40. Shors, T.J., and Dryver, E. (1992) Stress impedes exploration and the acquisition of spatial information in the eight-arm radial maze. Psychobiology, 20:247-253.
41. Shors, T.J., and Dryver, E. (1994) Effects of stress and long-term potentiation (LTP) on subsequent LTP and the theta burst response in the dentate gyrus. Brain Res., 666:232-238.
42. Shors, T.J., and Servatius, R.J. (1995) Stress-induced sensitization and facilitated learning require NMDA receptor activation. Neuroreport, 6:677-680.
43. Shors, T.J., and Thompson, R.F. (1992) Stress impairs (or induces) synaptic LTP, but does not affect paired-pulse facilitation in the stratum radiatum of the rat hippocampus. Synapse, 11:262-265.
44. Shors, T.J., Seib, T.B., Levine, S., and Thompson, R.F. (1989) Inescapable versus escapable shock modulates long-term potentiation (LTP) in rat hippocampus. Science, 244:224-226.
45. Shors, T.J., Levine, S., Thompson, R.F. (1990) Effect of adrenalectomy and demedullation on the stress-induced impairment of long-term potentiation (LTP). Neuroendocrinology, 51:70-75.
46. Shors, T.J., Weiss, C., and Thompson, R.F. (1992) Stress-induced facilitation of classical conditioning. Science, 257:537-539.
47. Smith, M.A., Makino, S., Kvetnansky, R., and Post, R.M. (1995) Stress and glucocorticoids affect the expression of brain-derived neurotrophic factor and neurotrophin-3 mRNAs in the hippocampus. J. Neurosci., 15:1768-1777.
48. Staubli, U., Lynch, G. (1987) Stable hippocampal long-term potentiation elicited by "theta" pattern stimulation. Brain Res., 435:227-234.
49. Stewart, D.J., and Vanderwolf, C.H. (1987) Hippocampal rhythmical slow activity following ibotenic acid lesions of the septal region. I. Relations to behavior and effects of atropine and urethane. Brain Res., 423:88-100.
50. Tocco, G., Shors, T.J., Baudry, M., and Thompson, R.F. (1991) Selective increase of AMPA binding to the AMPA/quisqualate receptor in the hippocampus in response to acute stress. Brain Res., 559:168-171.
51. Tocco, G., Maren, S., Shors, T.J., Baudry, M., and Thompson, R.F. (1992) Long-term potentiation is associated with increased [H]AMPA binding in rat hippocampus. Brain Res., 573:228-234.
52. Vanderwolf, C.H. (1969) Hippocampal electrical activity and voluntary movement in the rat. Electroenceph. Clin. Neurophysiol., 26:407-418.
53. Vanderwolf, C.H. (1988) Cerebral activity and behavior: Control by central cholinergic and serotonergic systems. Inter. Rev. Neurobiol., 30:225-340.
54. Wilson, D.A., Willner, E.M., Kurz, E.M., and Nadel, L. (1986) Early handling increases hippocampal long-term potentiation in young rats. Behav. Brain Res., 531:225-231.
55. Winson, J. (1974) Patterns of hippocampal theta rhythm in the freely moving rat. Electroenceph. Clin. Neurophysiol., 36:291-301.
56. Ylinen, A., Soltesz, I., Bregin, A., Penttonen, M., Sik, A., and Buzsaki, G. (1995) Intracellular correlates of hippocampal theta rhythm in identified pyramidal cells, granule cells, and basket cells. Hippocampus, 5:78-90.