Stress-induced alterations in hippocampal plasticity, place cells, and spatial memory

doi:10.1073/pnas.0708644104

Stress-induced alterations in hippocampal plasticity, place cells, and spatial memory

*Department of Psychology, University of Washington, Seattle, WA 98195-1520;
^‡Department of Psychological and Brain Sciences, The Johns Hopkins University, Baltimore, MD 21218;
^§Department of Psychology, University of California, Los Angeles, CA 90095;
^¶Institute for Medical Sciences, Ajou University School of Medicine, Suwon 443-721, Korea;
^‖Center for Neural Science, Korea Institute of Science and Technology, Seoul 130-650, Korea; and
**Department of Psychology, Bowling Green State University, Bowling Green, OH 43403

Communicated by Richard F. Thompson, University of Southern California, Los Angeles, CA, September 28, 2007 (received for review January 4, 2007)

Abstract

Acute, inescapable, and unpredictable stress can profoundly modify brain and cognition in humans and animals. The present study investigated the ensuing effects of 2-h variable “audiogenic” stress on three related levels of hippocampal functions in rats: long-term potentiation, place cell activity, and spatial memory. In agreement with prior findings, we observed that stress reduced the magnitude of Schaffer collateral/commissural–Cornu Ammonis field 1 long-term potentiation in vitro, and selectively impaired spatial memory on a hidden platform version of the Morris water maze task. We also observed that stress impaired the stability of firing rates (but not firing locations) of place cells recorded from dorsal Cornu Ammonis field 1 in rats foraging freely on a novel open-field platform located in a familiar surrounding room. These findings suggest that stress-induced modifications in synaptic plasticity may prevent the storage of stable “rate maps” by hippocampal place cells, which in turn may contribute to spatial memory impairments associated with stress.

Footnotes

^†To whom correspondence should be addressed. E-mail: jeansokk{at}u.washington.edu
Author contributions: J.J.K., P.E.S., M.W.J., and H.T.B. designed research; J.J.K., H.J.L., A.C.W., E.S., J.C., and H.T.B. performed research; J.J.K., H.J.L., M.W.J., and H.T.B. analyzed data; and J.J.K. and H.T.B. wrote the paper.
The authors declare no conflict of interest.
This article contains supporting information online at www.pnas.org/cgi/content/full/0708644104/DC1.
Abbreviations:

LTP,

long-term potentiation;

CA1,

Cornu Ammonis field 1;

DG,

dentate gyrus;

f-EPSP,

field excitatory postsynaptic potential;

MWM,

Morris water maze.