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Cited by 184Memory and Neural MechanismsStress Responses and CortisolNeuroscience and Neuropharmacology Research

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Amygdalar Inactivation Blocks Stress-Induced Impairments in Hippocampal Long-Term Potentiation and Spatial Memory

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Kim, Jeansok J., Koo, Ja Wook, Lee, Hongjoo J., Han, Jung-Soo·2005·The Journal of Neuroscience
DOI 10.1523/jneurosci.4623-04.2005PMC PMC6725997
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Abstract

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.

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Figure 1 Time intervals from intra-amygdalar MUSC infusions to stress presentation to hippocampal slice preparation in experiments 1 and 2.
Figure 1 Time intervals from intra-amygdalar MUSC infusions to stress presentation to hippocampal slice preparation in experiments 1 and 2.CC-BY-NC-SA · From the PDF
Figure 2 Photomicrograph showing a transverse brain section stained with cresyl violet from a rat infused with muscimol bilaterally into the amygdala and used in the hippocampal slice experiment. Arrowheads indicate infusion cannula tip positions.
Figure 2 Photomicrograph showing a transverse brain section stained with cresyl violet from a rat infused with muscimol bilaterally into the amygdala and used in the hippocampal slice experiment. Arrowheads indicate infusion cannula tip positions.CC-BY-NC-SA · From the PDF
Image 3
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Figure 4 Effects of intra-amygdalar infusions of muscimol and stress on Schaffer collateral/ commissural-CA1 LTP. Synaptic strength in the CA1 area of the hippocampus from ACSFCONTROL, ACSF-STRESS, MUSC-CONTROL, and MUSC-STRESS animals is expressed as a percentage of the average pretetanus f-EPSP over time (in minutes).
Figure 4 Effects of intra-amygdalar infusions of muscimol and stress on Schaffer collateral/ commissural-CA1 LTP. Synaptic strength in the CA1 area of the hippocampus from ACSFCONTROL, ACSF-STRESS, MUSC-CONTROL, and MUSC-STRESS animals is expressed as a percentage of the average pretetanus f-EPSP over time (in minutes).CC-BY-NC-SA · From the PDF
Figure 5 Prestress and immediate poststress intra-amygdalar infusions of muscimol and stress effects on Schaffer collateral/commissural-CA1 LTP. Synaptic strength in the CA1 area of the hippocampus from STRESS-ACSF, MUSC-STRESS, and STRESS-MUSC animals is expressed as a percentage of the average pretetanus f-EPSP over time (in minutes).
Figure 5 Prestress and immediate poststress intra-amygdalar infusions of muscimol and stress effects on Schaffer collateral/commissural-CA1 LTP. Synaptic strength in the CA1 area of the hippocampus from STRESS-ACSF, MUSC-STRESS, and STRESS-MUSC animals is expressed as a percentage of the average pretetanus f-EPSP over time (in minutes).CC-BY-NC-SA · From the PDF
Figure 6 Photomicrograph showing a transverse brain section stained with cresyl violet from a rat with bilateral guide cannulas implanted in the amygdala and used in the behavioral experiment. Arrowheads indicate infusion cannula tip positions.
Figure 6 Photomicrograph showing a transverse brain section stained with cresyl violet from a rat with bilateral guide cannulas implanted in the amygdala and used in the behavioral experiment. Arrowheads indicate infusion cannula tip positions.CC-BY-NC-SA · From the PDF
Figure 7 Effects of intra-amygdala infusions of muscimol and stress on spatial memory. A , Mean ( ± SE) latencies to find a submerged platform from ACSF-CONTROL, ACSF-STRESS, MUSC-CONTROL, MUSC-STRESS, and STRESS-MUSC animals during acquisition and a single retention test. B , Mean ( ± SE) swim speed of five groups during acquisition and a single retention test.
Figure 7 Effects of intra-amygdala infusions of muscimol and stress on spatial memory. A , Mean ( ± SE) latencies to find a submerged platform from ACSF-CONTROL, ACSF-STRESS, MUSC-CONTROL, MUSC-STRESS, and STRESS-MUSC animals during acquisition and a single retention test. B , Mean ( ± SE) swim speed of five groups during acquisition and a single retention test.CC-BY-NC-SA · From the PDF

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Metadata

Authors
Kim, J. J., Koo, J. W., Lee, H. J., & Han, J.-S.
Affiliations
  • University of Washington (US)
  • Yale University (US)
  • Johns Hopkins University (US)
ORCID
Venue
The Journal of Neuroscience
Publisher
Society for Neuroscience
Published
2005-02-09
Volume
25
Issue
6
Pages
1532-1539
ISSN
  • 0270-6474 (ISSN-L)
  • 1529-2401
DOI
10.1523/jneurosci.4623-04.2005
PMC
PMC6725997
OpenAlex
W2053502537
Cited by
184
References
71
Citations by year
2026: 2 · 2025: 2 · 2024: 1 · 2023: 2 · 2022: 4 · 2021: 8 · 2020: 3 · 2019: 4 · 2018: 6 · 2017: 6 · 2016: 12 · 2015: 6 · 2014: 14 · 2013: 19 · 2012: 16
FWCI
7.12
Type
journal article
Language
en
Open access
Licence
Locations
  • Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • Whitehall Foundation
  • National Institute of Mental Health (MH64457, R01MH064457, 1R01 MH64457)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords
amygdala, stress, hippocampal long-term potentiation, spatial memory, muscimol, GABAA receptor, stress-induced memory impairment, limbic system
MeSH terms
Amygdala, Animals, Corticosterone, Drug Administration Schedule, Electroshock, Hippocampus, Male, Memory Disorders, Muscimol, Stress, Physiological, Vocalization, Animal, Rats, Sprague-Dawley, Long-Term Potentiation, GABA Agonists, Maze Learning, Rats, GABA-A Receptor Agonists

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