Stress-facilitated LTD induces output plasticity through synchronized-spikes and spontaneous unitary discharges in the CA1 region of the hippocampus

Neuroscience Research

Volumn 49, Issue 2, 2004, Pages 229-239

  Cao, Jun ^a,b   Chen, Nanhui ^a   Xu, Tianle ^c   Xu, Lin ^a,b  

^a KUNMING INSTITUTE OF ZOOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

Author keywords

Evoked synchronized spikes; Hippocampus; Long term depression (LTD); Long term potentiation (LTP); Power spectrum; Spontaneous unitary discharges; Stress

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN REGION; CONTROLLED STUDY; CORTICAL SYNCHRONIZATION; DIATHERMY; ELECTROSTIMULATION; HIPPOCAMPUS; LONG TERM DEPRESSION; MALE; MENTAL STRESS; NERVE CELL PLASTICITY; NERVE CONDUCTION; NEUROTRANSMISSION; NONHUMAN; POWER SPECTRUM; PRIORITY JOURNAL; RAT; SYNAPSE;

ACTION POTENTIALS; ANALYSIS OF VARIANCE; ANIMALS; BEHAVIOR, ANIMAL; ELECTRIC STIMULATION; EXCITATORY POSTSYNAPTIC POTENTIALS; HIPPOCAMPUS; LONG-TERM DEPRESSION (PHYSIOLOGY); MALE; NEURONAL PLASTICITY; NEURONS; RATS; RATS, WISTAR; STRESS; TIME FACTORS;

EID: 2342462185     PISSN: 01680102     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neures.2004.03.001     Document Type: Article

References (63)

1. Abraham W.C., Bliss T.V. An analysis of the increase in granule cell excitability accompanying habituation in the dentate gyrus of the anesthetized rat. Brain Res. 331:1985;303-313
2. Abraham W.C., Bliss T.V., Goddard G.V. Heterosynaptic changes accompany long-term but not short-term potentiation of the perforant path in the anaesthetized rat. J Physiol. 363:1985;335-349
3. Alfarez D.N., Wiegert O., Joels M., Krugers H.J. Corticosterone and stress reduce synaptic potentiation in mouse hippocampal slices with mild stimulation. Neuroscience. 115:2002;1119-1126
4. Arieli A., Shoham D., Hildesheim R., Grinvald A. Coherent spatiotemporal patterns of ongoing activity revealed by real-time optical imaging coupled with single-unit recording in the cat visual cortex. J. Neurophysiol. 73:1995;2072-2093
5. Arieli A., Sterkin A., Grinvald A., Aertsen A.D. Dynamics of ongoing activity: explanation of the large variability in evoked cortical responses. Science. 273:1996;1868-1871
6. Ashwood T.J., Lancaster B., Wheal H.V. In vivo and in vitro studies on putative interneurones in the rat hippocampus: possible mediators of feed-forward inhibition. Brain Res. 293:1984;279-291
7. Bernard C., Wheal H.V. Expression of EPSP/spike potentiation following low frequency and tetanic stimulation in the CA1 area of the rat hippocampus. J. Neurosci. 15:1995;6542-6551
8. Bi G., Poo M. Synaptic modification by correlated activity: Hebb's postulate revisited. Annu. Rev. Neurosci. 24:2001;139-166
9. Bliss T.V., Collingridge G.L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature. 361:1993;31-39
10. Bontempi B., Laurent-Demir C., Destrade C., Jaffard R. Time-dependent reorganization of brain circuitry underlying long-term memory storage. Nature. 400:1999;671-675
11. Buzsaki G., Leung L.W., Vanderwolf C.H. Cellular bases of hippocampal EEG in the behaving rat. Brain Res. 287:1983;139-171
12. Chen N.H., White I.M., Wise S.P. Neuronal activity in dorsomedial frontal cortex and prefrontal cortex reflecting irrelevant stimulus dimensions. Exp. Brain Res. 139:2001;116-119
13. Daoudal G., Hanada Y., Debanne D. Bidirectional plasticity of excitatory postsynaptic potential (EPSP)-spike coupling in CA1 hippocampal pyramidal neurons. Proc. Natl. Acad. Sci. U.S.A. 99:2002;14512-14517
14. Deadwyler S.A., Gribkoff V., Cotman C., Lynch G. Long lasting changes in the spontaneous activity of hippocampal neurons following stimulation of the entorhinal cortex. Brain Res. Bull. 1:1976;1-7
15. Debiec J., LeDoux J.E., Nader K. Cellular and systems reconsolidation in the hippocampus. Neuron. 36:2002;527-538
16. Decharms R.C., Merzenich M.M. Primary cortical representation of sounds by the coordination of action-potential timing. Nature. 381:1996;610-613
17. Diamond D.M., Bennett M.C., Fleshner M., Rose G.M. Inverted-U relationship between the level of peripheral corticosterone and the magnitude of hippocampal primed burst potentiation. Hippocampus. 2:1992;421-430
18. Dinse H.R., Recanzone G.H., Merzenich M.M. Alterations in correlated activity parallel ICMC-induced representational plasticity. NeuroReport. 5:1993;173-176
19. Dudek S.M., Bear M.F. Bidirectional long-term modification of synaptic effectiveness in the adult and immature hippocampus. J. Neurosci. 13:1993;2910-2918
20. Frankland P.W., O'Brien C., Ohno M., Kirkwood A., Silva A.J. Alpha-CaMKII-dependent plasticity in the cortex is required for permanent memory. Nature. 411:2001;309-313
21. Fries P., Fernandez G., Jensen O. When neurons form memories. Trends Neurosci. 26:2003;123-124
22. Fujii S., Kuroda Y., Ito K., Kaneko K., Kato H. Effects of adenosine receptors on the synaptic and EPSP-spike components of long-term potentiation and depotentiation in the guinea-pig hippocampus. J. Physiol. 521(Pt 2):1999;451-466
23. Hollup S.A., Molden S., Donnett J.G., Moser M.B., Moser E.I. Accumulation of hippocampal place fields at the goal location in an annular watermaze task. J. Neurosci. 21:2001;1635-1644
24. Izaki Y., Arita J. Long-term potentiation in the rat hippocampal CA1 region is inhibited selectively at the acquisition stage of discriminatory avoidance learning. Brain Res. 723:1996;162-168
25. Johnson M.J., Alloway K.D. Cross-correlation analysis reveals laminar differences in thalamocortical interactions in the somatosensory system. J. Neurophysiol. 75:1996;1444-1457
26. Kapur N., Brooks D.J. Temporally-specific retrograde amnesia in two cases of discrete bilateral hippocampal pathology. Hippocampus. 9:1999;247-254
27. Kim J.J., Foy M.R., Thompson R.F. Behavioral stress modifies hippocampal plasticity through N-methyl-D-aspartate receptor activation. Proc. Natl. Acad. Sci. U.S.A. 93:1996;4750-4753
28. Kimura A., Pavlides C. Long-term potentiation/depotentiation are accompanied by complex changes in spontaneous unit activity in the hippocampus. J. Neurophysiol. 84:2000;1894-1906
29. Lee H.K., Takamiya K., Han J.S., Man H., Kim C.H., Rumbaugh G., Yu S., Ding L., He C., Petralia R.S., Wenthold R.J., Gallagher M., Huganir R.L. Phosphorylation of the AMPA receptor GluR1 subunit is required for synaptic plasticity and retention of spatial memory. Cell. 112:2003;631-643
30. Malenka R.C. Synaptic plasticity and AMPA receptor trafficking. Ann. N.Y. Acad. Sci. 1003:2003;1-11
31. Malenka R.C., Nicoll R.A. Long-term potentiation - a decade of progress? Science. 285:1999;1870-1874
32. Martin S.J., Grimwood P.D., Morris R.G. Synaptic plasticity and memory: an evaluation of the hypothesis. Annu. Rev. Neurosci. 23:2000;649-711
33. McEwen B.S. Stress and hippocampal plasticity. Annu. Rev. Neurosci. 22:1999;105-122
34. Nakazawa K., Quirk M.C., Chitwood R.A., Watanabe M., Yeckel M.F., Sun L.D., Kato A., Carr C.A., Johnston D., Wilson M.A., Tonegawa S. Requirement for hippocampal CA3 NMDA receptors in associative memory recall. Science. 297:2002;211-218
35. Okada T., Yamada N., Tsuzuki K., Horikawa H.P., Tanaka K., Ozawa S. Long-term potentiation in the hippocampus CA1 area and dentate gyrus plays different roles in spatial learing. Eur. J. Neurosci. 17:2003;341-349
36. Reed J.M., Squire L.R. Retrograde amnesia for facts and events: findings from four new cases. J. Neurosci. 18:1998;3943-3954
37. Rocher C., Spedding M., Munoz C., Jay T.M. Acute stress-induced changes in hippocampal/prefrontal circuits in rats: effects of antidepressants. Cereb. Cortex. 14:2004;224-229
38. Saal D., Dong Y., Bonci A., Malenka R.C. Drugs of abuse and stress trigger a common synaptic adaptation in dopamine neurons. Neuron. 37:2003;577-582
39. Shimizu E., Tang Y.P., Rampon C., Tsien J.Z. NMDA receptor-dependent synaptic reinforcement as a crucial process for memory consolidation. Science. 290:2000;1170-1174
40. Shors T.J., Seib T.B., Levine S., Thompson R.F. Inescapable versus escapable shock modulates long-term potentiation in the rat hippocampus. Science. 244:1989;224-226
41. Silva A.J. Molecular and cellular cognitive studies of the role of synaptic plasticity in memory. J. Neurobiol. 54:2003;224-237
42. Simonov P.V., Rusalova M.N. Electroencephalographic correlates of human emotional stress. Aviat. Space Environ. Med. 51:1980;1109-1111
43. Skaggs W.E., McNaughto B.L., Wilson M.A., Barnes C.A. Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus. 6:1996;149-172
44. Soderling T.R., Derkach V.A. Postsynaptic protein phosphorylation and LTP. Trends Neurosci. 23:2000;75-80
45. Squire L.R., Clark R.E., Knowlton B.J. Retrograde amnesia. Hippocampus. 11:2001;50-55
46. Staff N.P., Spruston N. Intracellular correlate of EPSP-spike potentiation in CA1 pyramidal neurons is controlled by GABAergic modulation. Hippocampus. 13:2003;801-805
47. Tang Y.P., Shimizu E., Dube G.R., Rampon C., Kerchner G.A., Zhuo M., Liu G., Tsien J.Z. Genetic enhancement of learning and memory in mice. Nature. 401:1999;63-69
48. Thompson L.T., Best P.J. Long-term stability of the place-field activity of single units recorded from the dorsal hippocampus of freely behaving rats. Brain Res. 509:1990;299-308
49. Wagner J.J., Alger B.E. GABAergic and developmental influences on homosynaptic LTD and depotentiation in rat hippocampus. J. Neurosci. 15:1995;1577-1586
50. Wang J., Liu S., Haditsch U., Tu W., Cochrane K., Ahmadian G., Tran L., Paw J., Wang Y., Mansuy I., Salter M.M., Lu Y.M. Interaction of calcineurin and type-A GABA receptor gamma 2 subunits produces long-term depression at CA1 inhibitory synapses. J. Neurosci. 23:2003;826-836
51. Wasling P., Hanse E., Gustafsson B. Long-term depression in the developing hippocampus: low induction threshold and synapse nonspecificity. J. Neurosci. 22:2002;1823-1830
52. Wei H., Xiong W., Yang S., Zhou Q., Liang C., Zeng B., Xu L. Propofol facilitates the development of long-term depression (LTD) and impairs the maintenance of long-term potentiation (LTP) in the CA1 region of the hippocampus of anesthetized rats. Neurosci. Lett. 324:2002;181-184
53. Wiener S.I. Spatial, behavioral and sensory correlates of hippocampal CA1 complex spike cell activity: implications for information processing functions. Prog. Neurobiol. 49:1996;335-361
54. Wittenberg G.M., Sullivan M.R., Tsien J.Z. Synaptic reentry reinforcement based network model for long-term memory consolidation. Hippocampus. 12:2002;637-647
55. Xiong W., Yang Y., Cao J., Wei H., Liang C., Yang S., Xu L. The stress experience dependent long-term depression disassociated with stress effect on spatial memory task. Neurosci. Res. 46:2003;415-421
56. Xiong W.Y., Wei H.M., Xiang X.J., Dong Z.F., Cao J., Wang Y.F., Xu T.L., Xu L. The effect of acute stress on LTP and LTD induction in the hippocampal CA1 region of anesthetized rats at three different ages. Brain Res. 1005:2004;187-192
57. Xu L., Anwyl R., Rowan M.J. Behavioural stress facilitates the induction of long-term depression in the hippocampus. Nature. 387:1997;497-500
58. Xu L., Anwyl R., Rowan M.J. Spatial exploration induces a persistent reversal of long-term potentiation in rat hippocampus. Nature. 394:1998a;891-894
59. Xu L., Holscher C., Anwyl R., Rowan M.J. Glucocorticoid receptor and protein/RNA synthesis-dependent mechanisms underlie the control of synaptic plasticity by stress. Proc. Natl. Acad. Sci. U.S.A. 95:1998b;3204-3208
60. Yamamoto J. Relationship between hippocampal theta-wave frequency and emotional behaviors in rabbits produced with stresses or psychotropic drugs. Jpn. J. Pharmacol. 76:1998;125-127
61. Yang Y., Cao J., Xiong W., Zhang J., Zhou Q., Wei H., Liang C., Deng J., Li T., Yang S., Xu L. Both stress experience and age determine the impairment or enhancement effect of stress on spatial memory retrieval. J. Endocrinol. 178:2003;45-54
62. Yang Y., Zheng X.G., Wang Y.F., Cao J., Dong Z.F., Cai J.X., Sui N., Xu L. Stress enable synaptic depression in CA1 synapse by acute and chronic morphine: possible mechanisms for corticosterone on opiate addiction. J. Neurosci. 24:2004;2412-2420
63. Zhou T.L., Tamura R., Kuriwaki J., Ono T. Comparison of medial and lateral septal neuron activity during performance of spatial tasks in rats. Hippocampus. 9:1999;220-234