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The Journal of Neuroscience, February 9, 2005, 25(6):1532-1539; doi:10.1523/JNEUROSCI.4623-04.2005

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Behavioral/Systems/Cognitive
Amygdalar Inactivation Blocks Stress-Induced Impairments in Hippocampal Long-Term Potentiation and Spatial Memory

Jeansok J. Kim,¹ Ja Wook Koo,² Hongjoo J. Lee,² and Jung-Soo Han³

¹Department of Psychology and Program in Neurobiology and Behavior, University of Washington, Seattle, Washington 98195-1525, ²Department of Psychology, Yale University, New Haven, Connecticut 06520-8205, and ³Department of Psychological and Brain Sciences, Johns Hopkins University, Baltimore, Maryland 21218

Electrolytic lesions to the amygdala, a limbic structure implicated in stress-related behaviors and memory modulation, have been shown to prevent stress-induced impairments of hippocampal long-term potentiation (LTP) and spatial memory in rats. The present study investigated the role of intrinsic amygdalar neurons in mediating stress effects on the hippocampus by microinfusing the GABA_A receptor agonist muscimol into the amygdala and examining stress effects on Schaffer collateral/commissural-CA1 LTP and spatial memory. The critical period of the amygdalar contribution to stress effects on hippocampal functions was determined by applying muscimol either before stress or immediately after stress. Our results indicate that intra-amygdalar muscimol infusions before uncontrollable restraint-tailshock stress effectively blocked stress-induced physiological and behavioral effects. Specifically, hippocampal slices prepared from vehicle-infused stressed animals exhibited markedly impaired LTP, whereas slices obtained from muscimol-infused stressed animals demonstrated robust LTP comparable with that of unstressed animals. Correspondingly, vehicle-infused stressed animals displayed impaired spatial memory (on a hidden platform version of the Morris water maze task), whereas muscimol-infused stressed animals revealed unimpaired spatial memory. In contrast to prestress muscimol effects, however, immediate poststress infusions of muscimol into the amygdala failed to interfere with stress impairments of LTP and spatial memory. Together, these results suggest that the amygdalar neuronal activity during stress, but not shortly after stress, is essential for the emergence of stress-induced alterations in hippocampal LTP and memory.

Key words: amygdala; hippocampus; GABA; glucocorticoids; corticosterone; long-term potentiation

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Received Nov 10, 2004; revised December 23, 2004; accepted December 28, 2004.

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