Acute stress causes rapid synaptic insertion of Ca2+ -permeable AMPA receptors to facilitate long-term potentiation in the hippocampus

Garry Whitehead; Jihoon Jo; Ellen L Hogg; Thomas Piers; Dong-Hyun Kim; Gillian Seaton; Heon Seok; Gilles Bru-Mercier; Gi Hoon Son; Philip Regan; Lars Hildebrandt; Eleanor Waite; Byeong-Chae Kim; Talitha L Kerrigan; Kyungjin Kim; Daniel J Whitcomb; Graham L Collingridge; Stafford L Lightman; Kwangwook Cho

doi:10.1093/brain/awt293

Acute stress causes rapid synaptic insertion of Ca2+ -permeable AMPA receptors to facilitate long-term potentiation in the hippocampus

Garry Whitehead, Jihoon Jo, Ellen L Hogg, Thomas Piers, Dong-Hyun Kim, Gillian Seaton, Heon Seok, Gilles Bru-Mercier, Gi Hoon Son, Philip Regan, Lars Hildebrandt, Eleanor Waite, Byeong-Chae Kim, Talitha L Kerrigan, Kyungjin Kim, Daniel J Whitcomb, Graham L Collingridge, Stafford L Lightman, Kwangwook Cho

Department of Life Sciences

University of Bristol

Research output: Contribution to journal › Article › peer-review

80 Citations (SciVal)

Abstract

The neuroendocrine response to episodes of acute stress is crucial for survival whereas the prolonged response to chronic stress can be detrimental. Learning and memory are particularly susceptible to stress with cognitive deficits being well characterized consequences of chronic stress. Although there is good evidence that acute stress can enhance cognitive performance, the mechanism(s) for this are unclear. We find that hippocampal slices, either prepared from rats following 30 min restraint stress or directly exposed to glucocorticoids, exhibit an N-methyl-d-aspartic acid receptor-independent form of long-term potentiation. We demonstrate that the mechanism involves an NMDA receptor and PKA-dependent insertion of Ca2+ -permeable AMPA receptors into synapses. These then trigger the additional NMDA receptor-independent form of LTP during high frequency stimulation.

Original language	English
Pages (from-to)	3753-3765
Number of pages	13
Journal	Brain : A Journal of Neurology
Volume	136
Issue number	Pt 12
DOIs	https://doi.org/10.1093/brain/awt293
Publication status	Published - 10 Dec 2013

Keywords

Animals
Biotinylation
Calcium/metabolism
Dexamethasone/pharmacology
Electric Stimulation
Excitatory Amino Acid Antagonists/pharmacology
Gene Expression Regulation/drug effects
Glucocorticoids/pharmacology
Hippocampus/drug effects
Hormone Antagonists/pharmacology
In Vitro Techniques
Long-Term Potentiation/drug effects
Male
Mifepristone/pharmacology
Muscarinic Antagonists/pharmacology
Patch-Clamp Techniques
Phosphorylation/drug effects
Rats
Rats, Wistar
Receptors, AMPA/metabolism
Restraint, Physical/physiology
Valine/analogs & derivatives

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Whitehead, G., Jo, J., Hogg, E. L., Piers, T., Kim, D.-H., Seaton, G., Seok, H., Bru-Mercier, G., Son, G. H., Regan, P., Hildebrandt, L., Waite, E., Kim, B.-C., Kerrigan, T. L., Kim, K., Whitcomb, D. J., Collingridge, G. L., Lightman, S. L., & Cho, K. (2013). Acute stress causes rapid synaptic insertion of Ca2+ -permeable AMPA receptors to facilitate long-term potentiation in the hippocampus. Brain : A Journal of Neurology, 136(Pt 12), 3753-3765. https://doi.org/10.1093/brain/awt293

Whitehead, G, Jo, J, Hogg, EL, Piers, T, Kim, D-H, Seaton, G, Seok, H, Bru-Mercier, G, Son, GH, Regan, P, Hildebrandt, L, Waite, E, Kim, B-C, Kerrigan, TL, Kim, K, Whitcomb, DJ, Collingridge, GL, Lightman, SL & Cho, K 2013, 'Acute stress causes rapid synaptic insertion of Ca2+ -permeable AMPA receptors to facilitate long-term potentiation in the hippocampus', Brain : A Journal of Neurology, vol. 136, no. Pt 12, pp. 3753-3765. https://doi.org/10.1093/brain/awt293

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abstract = "The neuroendocrine response to episodes of acute stress is crucial for survival whereas the prolonged response to chronic stress can be detrimental. Learning and memory are particularly susceptible to stress with cognitive deficits being well characterized consequences of chronic stress. Although there is good evidence that acute stress can enhance cognitive performance, the mechanism(s) for this are unclear. We find that hippocampal slices, either prepared from rats following 30 min restraint stress or directly exposed to glucocorticoids, exhibit an N-methyl-d-aspartic acid receptor-independent form of long-term potentiation. We demonstrate that the mechanism involves an NMDA receptor and PKA-dependent insertion of Ca2+ -permeable AMPA receptors into synapses. These then trigger the additional NMDA receptor-independent form of LTP during high frequency stimulation.",

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AU - Kim, Dong-Hyun

AU - Seaton, Gillian

AU - Seok, Heon

AU - Bru-Mercier, Gilles

AU - Son, Gi Hoon

AU - Regan, Philip

AU - Hildebrandt, Lars

AU - Waite, Eleanor

AU - Kim, Byeong-Chae

AU - Kerrigan, Talitha L

AU - Kim, Kyungjin

AU - Whitcomb, Daniel J

AU - Collingridge, Graham L

AU - Lightman, Stafford L

AU - Cho, Kwangwook

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N2 - The neuroendocrine response to episodes of acute stress is crucial for survival whereas the prolonged response to chronic stress can be detrimental. Learning and memory are particularly susceptible to stress with cognitive deficits being well characterized consequences of chronic stress. Although there is good evidence that acute stress can enhance cognitive performance, the mechanism(s) for this are unclear. We find that hippocampal slices, either prepared from rats following 30 min restraint stress or directly exposed to glucocorticoids, exhibit an N-methyl-d-aspartic acid receptor-independent form of long-term potentiation. We demonstrate that the mechanism involves an NMDA receptor and PKA-dependent insertion of Ca2+ -permeable AMPA receptors into synapses. These then trigger the additional NMDA receptor-independent form of LTP during high frequency stimulation.

AB - The neuroendocrine response to episodes of acute stress is crucial for survival whereas the prolonged response to chronic stress can be detrimental. Learning and memory are particularly susceptible to stress with cognitive deficits being well characterized consequences of chronic stress. Although there is good evidence that acute stress can enhance cognitive performance, the mechanism(s) for this are unclear. We find that hippocampal slices, either prepared from rats following 30 min restraint stress or directly exposed to glucocorticoids, exhibit an N-methyl-d-aspartic acid receptor-independent form of long-term potentiation. We demonstrate that the mechanism involves an NMDA receptor and PKA-dependent insertion of Ca2+ -permeable AMPA receptors into synapses. These then trigger the additional NMDA receptor-independent form of LTP during high frequency stimulation.

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KW - Mifepristone/pharmacology

KW - Muscarinic Antagonists/pharmacology

KW - Patch-Clamp Techniques

KW - Phosphorylation/drug effects

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KW - Receptors, AMPA/metabolism

KW - Restraint, Physical/physiology

KW - Valine/analogs & derivatives

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JO - Brain : A Journal of Neurology

JF - Brain : A Journal of Neurology

IS - Pt 12

ER -

Acute stress causes rapid synaptic insertion of Ca2+ -permeable AMPA receptors to facilitate long-term potentiation in the hippocampus

Abstract

Keywords

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