Abstract
The induction of activity-dependent persistent increases in synap-tic efficacy, such as long-term potentiation (LTP), is inhibited by behavioural stress1,2. The question arises whether stress also affects the ability to induce persistent decreases in synaptic efficacy, such as long-term depression (LTD)3–5. We now report that the induction of stable homosynaptic LTD in the CA1 area of the hippocampus of awake adult rats is facilitated, rather than inhibited, by exposure to mild naturalistic stress. The same stress blocked the induction of LTP. The effects of such stress were short lasting: acclimatization to, or removal from, the conditions that facilitated LTD induction led to a rapid loss of the ability to elicit this form of plasticity. The time window in which LTD could be reliably elicited was prolonged by inducing anaesthesia immediately after the stress. These data reveal that even brief exposure to mild stress can produce a striking shift in the susceptibility to synaptic plasticity in the awake animal.
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References
Diamond, D. M. et al. Exposure to a novel environment interferes with the induction of hippocampal primed burst potentiation. Psychobiology 18, 273–281 (1990).
Shors, T. J. et al. Inescapable versus escapable shock modulates long-term potentiation in the rat hippocampus. Science 244, 224–226 (1989).
Linden, D. J. & Connor, J. A. Long-term synaptic depression. Annu. Rev. Neurosci. 18, 319–357 (1995).
Bear, M. F. & Abraham, W. C. Long-term depression in hippocampus. Annu. Rev. Neurosci. 19, 437–462 (1996).
Dudek, S. M. & Bear, M. F. Bidirectional long-term modification of synaptic effectiveness in the adult and immature hippocampus. J. Neurosci. 13, 2910–2918 (1993).
Errington, M. L. et al. Stimulation at 1–5 Hz does not produce long-term depression or depotentiation in the hippocampus of the adult rat in vivo. J. Neurophysiol. 74, 1793–1799 (1995).
Staubli, U. & Lynch, G. Stable depression of potentiated synaptic responses in the hippocampus with 1–5 Hz stimulation. Brain Res. 513, 113–118 (1990).
Doyle, C. A. et al. Low-frequency stimulation induces homosynaptic depotentiation but not long-term depression of synaptic transmission in the adult anaesthetized and awake rat hippocampus in vivo. Neuroscience 77, 75–85 (1997).
Balfour, D. J. K. & Reid, A. Effects of betamethasone on the stimulation of corticosterone secretion in rats. Arch. Int. Pharmacodyn. Ther. 237, 67–74 (1979).
Barrionuevo, G., Shottler, F. & Lynch, G. The effects of repetitive low frequency stimulation on control and “potentiated” synaptic responses in the hippocampus. Life Sci. 27, 2385–2391 (1980).
Thiels, E., Barrionuevo, G. & Berger, T. W. Excitatory stimulation during postsynaptic inhibition induces long-term depression in hippocampus in vivo. J. Neurophysiol. 72, 3009–3016 (1994).
Heynen, A. J., Abraham, W. C. & Bear, M. F. Bidirectional modification of CA1 synapses in the adult hippocampus in vivo. Nature 381, 163–166 (1996).
Joëls, M. & de Kloet, E. R. Corticosteroid hormones: endocrine messengers in the brain. News Physiol. Sci. 10, 71–76 (1995).
Diamond, D. M. et al. Inverted-U relationship between the level of peripheral corticosterone and the magnitude of hippocampal primed burst potentiation. Hippocampus 2, 421–430 (1992).
Kerr, D. S. et al. Modulation of hippocampal long-term potentiation and long-term depression by corticosteroid receptor activation. Psychobiology 22, 123–133 (1994).
Pavlides, C. et al. Hippocampal homosynaptic long-term depression/depotentiation induced by adrenal steroids. Neurosdence 68, 379–385 (1995).
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. USA 93, 4750–4753 (1996).
Bear, M. F. Mechanism for a sliding synaptic modification threshold. Neuron 15, 1–4 (1995).
Doyle, C. A. et al. The selective neuronal NO synthase inhibitor 7-nitro-indazole blocks both long-term potentiation and depotentiation of field EPSPs in rat hippocampal CA1 in vivo. J. Neurosci. 16, 418–426 (1996).
O'Conor, J. J., Rowan, M. J. & Anwyl, R. Serotonergic involvement in the inhibitory effects of repeated buspirone treatment on synaptic transmission in the hippocampus of alert rats. Eur. J. Pharmacol. 167, 21–29 (1989).
Manahan-Vaughan, D., Anwyl, R. & Rowan, M. J. Adaptive changes in 5-HT1A receptor-mediated hippocampal inhibition in the alert rat produced by repeated 8-OH-DPAT treatment. Brit. J. Pharmacol. 112, 1083–1089 (1994).
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Xu, L., Anwyl, R. & Rowan, M. Behavioural stress facilitates the induction of long-term depression in the hippocampus. Nature 387, 497–500 (1997). https://doi.org/10.1038/387497a0
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DOI: https://doi.org/10.1038/387497a0
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