The DOI matches its Crossref record; 72 of the 72 references it cites were found in a registry or an index.
Amygdalar Inactivation Blocks Stress-Induced Impairments in Hippocampal Long-Term Potentiation and Spatial Memory
Open accessAbstract
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.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“damage to, or inactivation of, the amygdala blocks stress effects on hippocampal LTP and spatial memory (Almaguer-Melian et al. [214]; Kim et al. [154]; Korz and Frey [215]; Kim and Jung [21]).”
From The Temporal Dynamics Model of Emotional Memory Processing: A Synthesis on the Neurobiological Basis of Stress-Induced Amnesia, Flashbulb and Traumatic Memories, and the Yerkes-Dodson Law (2007) · cites this paper as Kim et al. [154]
In the citing paper
“Overall, these findings, in conjunction with related work by Kim et al. [154] support our hypothesis that a strong stressor generates a powerful inhibitory influence on hippocampal memory processing for events occurring 30–60 minutes after the onset of a stressful experience.”
From The Temporal Dynamics Model of Emotional Memory Processing: A Synthesis on the Neurobiological Basis of Stress-Induced Amnesia, Flashbulb and Traumatic Memories, and the Yerkes-Dodson Law (2007) · cites this paper as Kim et al. [154]
Citations
Cites
Bliss, T. V. P., & Gardner-Medwin, A. R. (1973) · The Journal of Physiology · doi:10.1113/jphysiol.1973.sp010274 · Cited by 7,424
LOSS OF RECENT MEMORY AFTER BILATERAL HIPPOCAMPAL LESIONS
Scoville, W. B., & Milner, B. (1957) · Journal of Neurology, Neurosurgery & Psychiatry · doi:10.1136/jnnp.20.1.11 · Cited by 7,322
The Organization of Behavior; A Neuropsychological Theory.
Attneave, F., B., M., & Hebb, D. O. (1950) · The American Journal of Psychology · doi:10.2307/1418888 · Cited by 5,146
Memory - A century of consolidation
McGaugh, J. L. (2000) · Science · doi:10.1126/science.287.5451.248 · Cited by 4,250
Morris, R. G. M., Anderson, E., Lynch, G. S., & Baudry, M. (1986) · Nature · doi:10.1038/319774a0 · Cited by 3,640
Long-Term Potentiation--A Decade of Progress?
Malenka, R. C., & Nicoll, A. R. A. (1999) · Science · doi:10.1126/science.285.5435.1870 · Cited by 2,729
Two receptor systems for corticosterone in rat brain: Microdistribution and differential occupation
REUL, J. M. H. M., & KLOET, E. R. D. (1985) · Endocrinology · doi:10.1210/endo-117-6-2505 · Cited by 2,580
Learned helplessness: Theory and evidence
Maier, S. F., & Seligman, M. E. (1976) · Journal of Experimental Psychology: General · doi:10.1037/0096-3445.105.1.3 · Cited by 2,494
Failure to escape traumatic shock.
Seligman, M. E., & Maier, S. F. (1967) · Journal of Experimental Psychology · doi:10.1037/h0024514 · Cited by 1,981
McEwen, B. S., & Sapolsky, R. M. (1995) · Current Opinion in Neurobiology · doi:10.1016/0959-4388(95)80028-x · Cited by 1,889
Research works printed but not linked: 6
- 1999, Physiol Behav, 65, 739
- 1973, J Physiol (Lond), 232, 331, 10.1113/jphysiol.1973.sp010273 · DOI · Paper page
- 1990, Psychol Sci, 3, 201
- 10.1037/0735-7044.106.3.518 · DOI
- 10.1037/0735-7044.108.5.1005 · DOI
- 10.1037//0096-3445.105.1.3 · DOI · Paper page
Cited by
Sorted by citations
Items 101–184 of 184
Hippocampal astrocytes induce sex-dimorphic effects on memory
Meadows, S. M., Palaguachi, F., Jang, M. W., Licht-Murava, A., Barnett, D., Zimmer, T. S., Zhou, C. Q., McDonough, S. R., Orr, A. L., & Orr, A. G. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114278 · Cited by 35
Tripathi, S. J., Chakraborty, S., Srikumar, B. N., Raju, T. R., & Rao, B. S. S. (2017) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2017.12.006 · Cited by 32
MacDougall, M. J., & Howland, J. G. (2012) · Cerebral Cortex · doi:10.1093/cercor/bhs247 · Cited by 31
Liebmann, L., Karst, H., & Joëls, M. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06882.x · Cited by 31
Stress enhances hippocampal neuronal synchrony and alters ripple-spike interaction
Tomar, A., Polygalov, D., Chattarji, S., & McHugh, T. J. (2021) · Neurobiology of Stress · doi:10.1016/j.ynstr.2021.100327 · Cited by 29
Wang, W., Chen, Z., Liu, W., Chi, Z., He, L., & Liu, J. (2014) · British Journal of Pharmacology · doi:10.1111/bph.12671 · Cited by 28
Almonte, A. G., Ewin, S. E., Mauterer, M. I., Morgan, J. W., Carter, E. S., & Weiner, J. L. (2017) · Scientific Reports · doi:10.1038/s41598-017-12531-z · Cited by 29
Hegde, P., Jayakrishnan, H. R., Chattarji, S., Kutty, B. M., & Laxmi, T. R. (2011) · Brain Research · doi:10.1016/j.brainres.2011.01.055 · Cited by 27
Hirata, R., Matsumoto, M., Judo, C., Yamaguchi, T., Izumi, T., Yoshioka, M., & Togashi, H. (2009) · Synapse · doi:10.1002/syn.20631 · Cited by 27
Vouimba, R., & Richter‐Levin, G. (2013) · Frontiers in Neural Circuits · doi:10.3389/fncir.2013.00080 · Cited by 28
Dohanich, G. P., Korol, D. L., & Shors, T. J. (2009) · Elsevier eBooks · doi:10.1016/b978-008088783-8.00015-2 · Cited by 25
Kawamura, N., Katsuura, G., Yamada-Goto, N., Novianti, E., Inui, A., & Asakawa, A. (2021) · BMJ Open Diabetes Research & Care · doi:10.1136/bmjdrc-2020-001492 · Cited by 26
Karnik, V., Braun, M. H., Dalesman, S., & Lukowiak, K. (2012) · Journal of Experimental Biology · doi:10.1242/jeb.061432 · Cited by 25
Zoladz, P. R., O’Rear, A. E., Hoffman, M. M., Aufdenkampe, R. L., Burke, H. M., Woelke, S. A., Pisansky, J. M., & Talbot, J. N. (2014) · Brain and Cognition · doi:10.1016/j.bandc.2014.01.010 · Cited by 24
Passecker, J. (2011) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2011.00066 · Cited by 23
Tripathi, S. J., Chakraborty, S., Srikumar, B. N., Raju, T. R., & Rao, B. S. S. (2018) · Molecular Neurobiology · doi:10.1007/s12035-018-1057-1 · Cited by 24
Jeon, B. T., Hwang, Y. K., Lee, S.-Y., Kim, D., Chung, C., & Han, J. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.08.035 · Cited by 21
Self-citationSpatial object recognition memory formation under acute stress
da Cunha, P. L., Villar, M. E., Ballarini, F., Tintorelli, R., & Viola, H. (2018) · Hippocampus · doi:10.1002/hipo.23037 · Cited by 20
Kim, E. J., & Kim, J. J. (2019) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2019.00210 · Cited by 21
Self-citationChauveau, F., Piérard, C., Coutan, M., Drouet, I., Liscia, P., & Béracochéa, D. (2008) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2008.04.014 · Cited by 22
García‐Pérez, D., Ferenczi, S., Kovács, K., Laorden, M. L., Milanés, M. V., & Núñez, C. (2016) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2016.09.020 · Cited by 19
Reactivation of an aversive memory modulates learning strategy preference in male rats
Hawley, W. R., Grissom, E. M., Patel, J. M., Hodges, K. S., & Dohanich, G. P. (2012) · Stress · doi:10.3109/10253890.2012.683466 · Cited by 18
Considering the Rationality of African Ritual Behavior
Mort, J. G. (2006) · ScholarWorks - WMU (Western Michigan University) · Cited by 18
Cai, M., Park, H. R., & Yang, E. J. (2022) · Pharmaceuticals · doi:10.3390/ph15070898 · Cited by 17
Yang, C., Huang, C., & Hsu, K. (2008) · Hippocampus · doi:10.1002/hipo.20414 · Cited by 17
Briand, L. A., & Blendy, J. A. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.02.026 · Cited by 18
Neurobiological Basis of the Complex Effects of Stress on Memory and Synaptic Plasticity
Zoladz, P. R., Park, C. R., & Diamond, D. M. (2011) · Wiley eBooks · doi:10.1002/9781118083222.ch8 · Cited by 16
MacDougall, M. J., & Howland, J. G. (2013) · Physiological Reports · doi:10.1002/phy2.35 · Cited by 15
Mercerón‐Martínez, D., Almaguer‐Melian, W., Alberti‐Amador, E., Estupiñán, B., Fernández, I., & Bergado, J. A. (2016) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2016.05.017 · Cited by 15
Emotional Memory Formation Under Lower Versus Higher Stress Conditions
Kogan, I., & Richter‐Levin, G. (2010) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2010.00183 · Cited by 15
Zoladz, P. R., Woodson, J. C., Haynes, V. F., & Diamond, D. M. (2010) · Stress · doi:10.3109/10253890902853123 · Cited by 16
Sex-specific impairment of spatial memory in rats following a reminder of predator stress
Burke, H. M., Robinson, C. M., Wentz, B., McKay, J., Dexter, K. W., Pisansky, J. M., Talbot, J. N., & Zoladz, P. R. (2013) · Stress · doi:10.3109/10253890.2013.791276 · Cited by 14
Stress, Depression and NeuroplasticityPreprint
Singh, S. P., & Karkare, S. (2017) · arXiv (Cornell University) · doi:10.48550/arxiv.1711.09536 · Cited by 13
Hiraide, S., Saito, Y., Matsumoto, M., Yanagawa, Y., Ishikawa, S., Kubo, Y., Inoue, S., Yoshioka, M., & Togashi, H. (2012) · Journal of Pharmacological Sciences · doi:10.1254/jphs.12023fp · Cited by 13
Uncovering the neural circuitry involved in the stress-attenuation effects of chewing
Sasaguri, K., Yamada, K., & Yamamoto, T. (2018) · Japanese Dental Science Review · doi:10.1016/j.jdsr.2018.03.002 · Cited by 13
Park, J.-C., Jeon, Y.-J., Jang, Y.-S., Cho, J., Choi, D.-H., & Han, J.-S. (2021) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2021.02.012 · Cited by 12
Self-citationInoue, S., Kamiyama, H., Matsumoto, M., Yanagawa, Y., Hiraide, S., Saito, Y., Shimamura, K., & Togashi, H. (2013) · Journal of Pharmacological Sciences · doi:10.1254/jphs.13123fp · Cited by 11
Histone deacetylase inhibition abolishes stress-induced spatial memory impairment
Vargas-López, V., Lamprea, M. R., & Múnera, A. (2016) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2016.08.009 · Cited by 12
Xue, L., Li, Z. D., Chen, Z. X., Wang, X. G., Shi, Y., & Zhao, H. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.12.014 · Cited by 11
PTSD: From Neurons to Networks
Rao, R. P., Suvrathan, A., Miller, M. M., McEwen, B. S., & Chattarji, S. (2009) · Humana Press eBooks · doi:10.1007/978-1-60327-329-9_7 · Cited by 11
Hajisoltani, R., & Meftahi, G. H. (2023) · Neuroscience Letters · doi:10.1016/j.neulet.2023.137590 · Cited by 9
Rodríguez-Fernández, J. M., García-Acero, M., & Franco, P. (2013) · Universitas Médica · doi:10.11144/javeriana.umed54-4.neac · Cited by 9
Park, J.-C., Jeon, Y.-J., Kim, J. J., Cho, J., Choi, D.-H., & Han, J. (2020) · Neuroscience Letters · doi:10.1016/j.neulet.2020.135245 · Cited by 8
Self-citationPochwat, B., Nowak, G., & Szewczyk, B. (2016) · Pharmacological Reports · doi:10.1016/j.pharep.2016.04.011 · Cited by 8
A role of anterior cingulate cortex in the emergence of worker–parasite relationship
Ahn, S., Kang, Y., Lee, J. W., Jeong, S. J., Lee, Y. J., Lee, S., Kim, J., Kim, J. J., Kim, J. J., & Jung, M. W. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2111145118 · Cited by 7
Self-citationMercerón‐Martínez, D., Almaguer‐Melian, W., & Bergado, J. A. (2021) · Behavioural Brain Research · doi:10.1016/j.bbr.2021.113589 · Cited by 6
Fluoxetine reverses stress-induced fimbria–prefrontal long-term potentiation facilitation
Kessal, K., Deschaux, O., Chessel, A., Xu, L., Moreau, J., & Garcia, R. (2006) · Neuroreport · doi:10.1097/01.wnr.0000201507.68997.52 · Cited by 7
Differential Effects of Controllable Stress Exposure on Subsequent Extinction Learning in Adult Rats
Hadad-Ophir, O., Brande-Eilat, N., & Richter‐Levin, G. (2016) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2015.00366 · Cited by 6
Patarroyo, W., García-Perez, M., Lamprea, M. R., Múnera, A., & Troncoso, J. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.11.045 · Cited by 6
“Unpredictable Stress”: Ambiguity of Stress Reactivity in Studies of Long-Term Plasticity
Kudryashova, I. V., & Gulyaeva, N. V. (2017) · Neuroscience and Behavioral Physiology · doi:10.1007/s11055-017-0496-x · Cited by 5
Dissociating effects of acute photic stress on spatial, episodic-like and working memory in the rat
Passecker, J., Barlow, S. H., & O’Mara, S. M. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.07.007 · Cited by 5
Classification Based on Configuration Objects by Using Procrustes Analysis
Ananda, R., & Prasetiadi, A. (2021) · JURNAL INFOTEL · doi:10.20895/infotel.v13i2.637 · Cited by 5
Alizadeh, K., Moghimi, H., Golbabaei, A., Alijanpour, S., & Rezayof, A. (2022) · Neurochemical Research · doi:10.1007/s11064-022-03625-w · Cited by 4
Alexander Bain'sMind and Body(1872): An underappreciated contribution to early neuropsychology
Harper, K. (2019) · Journal of the History of the Behavioral Sciences · doi:10.1002/jhbs.21963 · Cited by 4
Neural-Cognitive Effects of Stress in the Hippocampus
Kim, J. J., Pellman, B. A., & Kim, E. J. (2014) · Springer eBooks · doi:10.1007/978-1-4939-1056-4_9 · Cited by 3
Self-citationJones, K., Teliska, L. H., Mirrione, M. M., & Betz, A. J. (2025) · Experimental Brain Research · doi:10.1007/s00221-025-07204-7 · Cited by 3
Fernandes, C. E. M., Serafim, K. R., Gianlorenço, A. C., & Mattioli, R. (2019) · Brazilian Journal of Medical and Biological Research · doi:10.1590/1414-431x20198334 · Cited by 2
Farmer, G. E., Park, C. R., Bullard, L. A., & Diamond, D. M. (2014) · Springer eBooks · doi:10.1007/978-1-4939-1056-4_10 · Cited by 2
Stress and Spatial Maze Performance in the Rat
Taylor, S. B., Conrad, C. D., & Olive, M. F. (2014) · Neuromethods · doi:10.1007/978-1-4939-2159-1_8 · Cited by 2
Howland, J. G., & Davies, D. A. (2014) · Springer eBooks · doi:10.1007/978-1-4939-1056-4_11 · Cited by 1
Corticosteroid Actions on Electrical Activity in the Limbic Brain
Joëls, M., Karst, H., Krugers, H. J., & de Kloet, E. R. (2009) · Elsevier eBooks · doi:10.1016/b978-008088783-8.00042-5 · Cited by 1
Neurocognitive effects of stress on the hippocampus: a systems level analysis
Kim, E., & 김진석 (2012) · 한국심리학회지: 인지 및 생물 · doi:10.22172/cogbio.2012.24.1.004 · Cited by 1
Hosseinmardi, L., Meftahi, G. H., Shiravi, A., Shirvani, H., & Sharafi, S. (2020) · Brazilian Archives of Biology and Technology · doi:10.1590/1678-4324-2020190113 · Cited by 1
How Does Stress Work? The Role of Memes in Epigenesis
Leigh, H. (2010) · Springer eBooks · doi:10.1007/978-1-4419-5671-2_2 · Cited by 1
The Effects of Chronic Stress on Neuroanatomy and Cognitive Function
Viradia, N., Paredes, J. M. G., & Hassan, S. A. (2022) · Scholarly Research In Progress · doi:10.64057/001c.142181
Perusini, J. N. (2014) · eScholarship (California Digital Library) · Cited by 1
Fanselow, & Ponnusamy, R. (2007) · Elsevier eBooks · doi:10.1016/b978-012373947-6.00031-3 · Cited by 1
Zoladz, P. R. (2006) · Digital Commons - University of South Florida (University of South Florida)
MacDougall, M. J. (2012) · University Library - University of Saskatchewan (University of Saskatchewan)
Modesti, A. (2014) · Digital Commons @ Butler University (Butler University)
Der Einfluss von Stress auf abrufinduziertes Vergessen
Sektion, M.-N., & Psychologie, F. (2010)
Gaskins, D. L. (2012) · IUScholarWorks (Indiana University) · doi:10.7912/c2/2044
The effects of acute stress on spatial navigation in men and women.
van Gerven, D. (2016) · UVic’s Research and Learning Repository (University of Victoria)
Chahua, J. Z. C., & Díaz-Murillo, H. (2019) · Veritas · doi:10.35286/veritas.v20i2.251
Stress enhances hippocampal neuronal synchrony and prolongs sharp-wave ripplesPreprint
Tomar, A., Polygalov, D., Chattarji, S., & McHugh, T. J. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.06.19.162487
Estudio de biodisponibilidad de una mezcla de hidrocarburos en suelo modelo
Flores, A. P. G. (2016) · doi:10.24275/uami.pv63g030k
McEwen, B. S., & Chattarji, S. (2025) · Oxford University Press eBooks · doi:10.1093/med/9780190065324.003.0017
Calandreau, L. (2006) · Oskar-Bordeaux (Universite de Bordeaux)
The Role of Chewing and Chronic Stress in Breast Cancer Progression and Metastasis: A Review
Azuma, K., Ochi, S., Kajimoto, K., Suzuki, A., Iinuma, M., Yamada, K., Tamaki, T., & Kubo, K. (2026) · Stresses · doi:10.3390/stresses6020016
Jeon, Y.-J., Kim, N.-H., Yoon, S. J., Lyoo, I. K., Kim, J.-M., & Han, J. (2026) · Neuropharmacology · doi:10.1016/j.neuropharm.2026.111158
Self-citation
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)
- 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
- 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
- hybrid
- doi.org
- 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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review