Activation pattern of the limbic system following spatial learning under stress
Open accessAbstract
Anatomical evidence suggests an interplay between the dorsal CA1 of the hippocampus (CA1), the basolateral amygdala (BLA) and the entorhinal cortex (EC), but their specific interactions in the context of emotional memory remain obscure. Here, we sought to elucidate the activation pattern in these areas following spatial learning under different stress conditions in the Morris water maze, using cAMP response element‐binding protein (CREB) activation as a marker. Stress levels were manipulated by maintaining the water maze at one of two different temperatures: lower stress (warm water) or higher stress (cold water). Three groups of animals were tested under each condition: a Learning group, trained in the water maze with a hidden escape platform; a No‐Platform group, subjected to the maze without an escape platform; and a Naïve group. To evaluate the quality of the spatial memory formed, we also tested long‐term memory retention of the initial location of the platform following an interference procedure (reversal training). In the CA1 and EC, we found different CREB activation patterns for the lower‐ and higher‐stress groups. By contrast, in the BLA a similar pattern of activation was detected under both stress levels. The data reveal a difference in the sensitivity of the memory to interference, with reversal training interference affecting the memory of the initial platform location only under the higher‐stress condition. The results suggest that stress‐dependent alterations in limbic system activation patterns underlie differences in the quality of the memory formed.
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Previous animal studies have shown that stress can alter relative activation patterns within the limbic system.
“Previous animal studies have shown that stress can alter relative activation patterns within the limbic system,122”
From Preferential loss of dorsal-hippocampus synapses underlies memory impairments provoked by short, multimodal stress (2014) · cites this paper as [122]
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Cites
The Rat Brain in Stereotaxic Coordinates
Paxinos, G., & Watson, C. (1983) · Elsevier eBooks · doi:10.1016/c2009-0-63235-9 · Cited by 28,585 · see citing works
Place navigation impaired in rats with hippocampal lesions
Morris, R. G. M., Garrud, P., Rawlins, J. N. P., & O'Keefe, J. (1982) · Nature · doi:10.1038/297681a0 · Cited by 6,340 · see citing works
Memory - A century of consolidation
McGaugh, J. L. (2000) · Science · doi:10.1126/science.287.5451.248 · Cited by 4,250 · see citing works
Failure to escape traumatic shock.
Seligman, M. E., & Maier, S. F. (1967) · Journal of Experimental Psychology · doi:10.1037/h0024514 · Cited by 1,981 · cited 1× · see citing works
“…27, 715–722 It could be argued that the No-Platform animals actually experienced learned helplessness (LH), as they were exposed to an uncontrollable stress condition, resembling the uncontrollable and unpredictable foot shocks used in learned helplessness experiments (Seligman & Maier, 1967).”
MethodMcEwen, B. S., & Sapolsky, R. M. (1995) · Current Opinion in Neurobiology · doi:10.1016/0959-4388(95)80028-x · Cited by 1,889 · see citing works
Mechanisms of emotional arousal and lasting declarative memory.
Cahill, L., & McGaugh, J. L. (1998) · Trends in Neurosciences · doi:10.1016/s0166-2236(97)01214-9 · Cited by 1,575 · see citing works
Nibuya, M., Nestler, E., & Duman, R. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-07-02365.1996 · Cited by 1,206 · see citing works
The MAPK cascade is required for mammalian associative learning
Atkins, C. M., Selcher, J. C., Petraitis, J. J., Trzaskos, J. M., & Sweatt, J. D. (1998) · Nature Neuroscience · doi:10.1038/2836 · Cited by 1,083 · see citing works
Izquierdo, I., & Medina, J. H. (1997) · Neurobiology of Learning and Memory · doi:10.1006/nlme.1997.3799 · Cited by 959 · see citing works
LeDoux, J. E. (1994) · Scientific American · doi:10.1038/scientificamerican0694-50 · Cited by 892 · see citing works
The hippocampus—what does it do?
Eichenbaum, H., Otto, T., & Cohen, N. J. (1992) · Behavioral and Neural Biology · doi:10.1016/0163-1047(92)90724-i · Cited by 867 · see citing works
Involvement of the amygdala in memory storage: Interaction with other brain systems
McGaugh, J. L., Cahill, L. F., & Roozendaal, B. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.24.13508 · Cited by 747 · see citing works
Dolcos, F., LaBar, K. S., & Cabeza, R. (2004) · Neuron · doi:10.1016/s0896-6273(04)00289-2 · Cited by 714 · cited 1× · see citing works
“It has been suggested that the amygdala modulates memory formation processes in other brain regions under emotionally charged conditions (Bianchin et al., 1999; Quevedo et al., 2003; Dolcos et al., 2004, 2005; Smith et al., 2006).”
BackgroundSchafe, G. E., Atkins, C. M., Swank, M. W., Bauer, E. P., Sweatt, J. D., & LeDoux, J. E. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-21-08177.2000 · Cited by 674 · see citing works
Dolcos, F., LaBar, K. S., & Cabeza, R. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0409848102 · Cited by 601 · see citing works
Preclinical models: status of basic research in depression
Nestler, E. J., Gould, E., & Manji, H. K. (2002) · Biological Psychiatry · doi:10.1016/s0006-3223(02)01405-1 · Cited by 571 · see citing works
Beck, C., & Fibiger, H. (1995) · The Journal of Neuroscience · doi:10.1523/jneurosci.15-01-00709.1995 · Cited by 547 · see citing works
Kim, J. J., Lee, H. J., Han, J.-S., & Packard, M. G. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-14-05222.2001 · Cited by 537 · see citing works
Blum, S., Moore, A. N., Adams, F., & Dash, P. K. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-09-03535.1999 · Cited by 522 · see citing works
cAMP Response Element-Mediated Gene Transcription Is Upregulated by Chronic Antidepressant Treatment
Thome, J., Sakai, N., Shin, K.-H., Steffen, C., Zhang, Y.-J., Impey, S., Storm, D. R., & Duman, R. S. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-11-04030.2000 · Cited by 507 · see citing works
Guzowski, J. F., & McGaugh, J. L. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.6.2693 · Cited by 481 · see citing works
Pittenger, C., Huang, Y. Y., Paletzki, R. F., Bourtchouladze, R., Scanlin, H., Vronskaya, S., & Kandel, E. R. (2002) · Neuron · doi:10.1016/s0896-6273(02)00684-0 · Cited by 464 · see citing works
Impaired spatial and sequential learning in rats treated neonatally with d ‐fenfluramine
Morford, L. L., Inman-Wood, S. L., Gudelsky, G. A., Williams, M. T., & Vorhees, C. V. (2002) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2002.02100.x · Cited by 454 · see citing works
Sandi, C., Loscertales, M., & Guaza, C. (1997) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1997.tb01412.x · Cited by 447 · see citing works
Behavioral stress impairs long-term potentiation in rodent hippocampus
Foy, M. R., Stanton, M. E., Levine, S., & Thompson, R. F. (1987) · Behavioral and Neural Biology · doi:10.1016/s0163-1047(87)90664-9 · Cited by 436 · see citing works
Stress: metaplastic effects in the hippocampus
Kim, J. J., & Yoon, K. S. (1998) · Trends in Neurosciences · doi:10.1016/s0166-2236(98)01322-8 · Cited by 403 · see citing works
Kelly, A. M., Laroche, S., & Davis, S. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-12-05354.2003 · Cited by 361 · see citing works
Li, S., Wang, C., Wang, M., Murakami, Y., & Matsumoto, K. (2006) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2006.01.004 · Cited by 329 · see citing works
Chen, A. C. H., Shirayama, Y., Shin, K.-H., Neve, R. L., & Duman, R. S. (2001) · Biological Psychiatry · doi:10.1016/s0006-3223(00)01114-8 · Cited by 311 · see citing works
Memory systems in the brain and localization of a memory
Thompson, R. F., & Kim, J. J. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.24.13438 · Cited by 291 · see citing works
Lathe, R. (2001) · Journal of Endocrinology · doi:10.1677/joe.0.1690205 · Cited by 272 · see citing works
Lamprecht, R., Hazvi, S., & Dudai, Y. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-21-08443.1997 · Cited by 263 · see citing works
Task and Content Modulate Amygdala-Hippocampal Connectivity in Emotional Retrieval
Smith, A. P. R., Stephan, K. E., Rugg, M. D., & Dolan, R. J. (2006) · Neuron · doi:10.1016/j.neuron.2005.12.025 · Cited by 252 · see citing works
Gesing, A., Bilang‐Bleuel, A., Droste, S. K., Linthorst, A. C. E., Holsboer, F., & Reul, J. M. H. M. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-13-04822.2001 · Cited by 211 · see citing works
Mizuno, M., Yamada, K., Maekawa, N., Saito, K., Seishima, M., & Nabeshima, T. (2002) · Behavioural Brain Research · doi:10.1016/s0166-4328(01)00470-3 · Cited by 211 · see citing works
Vermetten, E., & Bremner, J. D. (2002) · Depression and Anxiety · doi:10.1002/da.10017 · Cited by 210 · see citing works
Phillips, R. G., & LeDoux, J. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-07-05308.1995 · Cited by 194 · see citing works
Emotional tagging of memory formation—in the search for neural mechanisms
Richter‐Levin, G., & Akirav, I. (2003) · Brain Research Reviews · doi:10.1016/j.brainresrev.2003.08.005 · Cited by 194 · see citing works
Self-citationKim, J. J., Koo, J. W., Lee, H. J., & Han, J.-S. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.4623-04.2005 · Cited by 184 · see citing works
A Facilitative Role for Corticosterone in the Acquisition of a Spatial Task Under Moderate StressPreprint
Akirav, I., Kozenicky, M., Tal, D., Sandi, C., Venero, C., & Richter‐Levin, G. (2004) · Learning & Memory · doi:10.1101/lm.61704 · Cited by 170 · see citing works
Self-citationMcDonald, A., & Mascagni, F. (1997) · Neuroscience · doi:10.1016/s0306-4522(96)00478-2 · Cited by 142 · see citing works
Differential activation of hippocampus and amygdala following spatial learning under stress
Akirav, I., Sandi, C., & Richter‐Levin, G. (2001) · European Journal of Neuroscience · doi:10.1046/j.0953-816x.2001.01687.x · Cited by 140 · see citing works
Self-citationBianchin, M. M., Souza, T. M. E., Medina, J. H., & Izquierdo, I. (1999) · Neurobiology of Learning and Memory · doi:10.1006/nlme.1998.3881 · Cited by 109 · see citing works
Alberini, C. M. (1999) · Journal of Experimental Biology · doi:10.1242/jeb.202.21.2887 · Cited by 99 · see citing works
Differential effects of emotional arousal in short- and long-term memory in healthy adults.
Quevedo, J., Sant'Anna, M. K., Madruga, M., Lovato, I., de-Paris, F., Kapczinski, F., Izquierdo, I., & Cahill, L. (2003) · Neurobiology of Learning and Memory · doi:10.1016/s1074-7427(02)00034-5 · Cited by 98 · see citing works
Roesler, R., Roozendaal, B., & McGaugh, J. L. (2002) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2002.01924.x · Cited by 87 · see citing works
Hebert, A. E., & Dash, P. K. (2002) · Learning & Memory · doi:10.1101/lm.48502 · Cited by 82 · see citing works
Roozendaal, B., Sapolsky, R. M., & McGaugh, J. L. (1998) · Neuroscience · doi:10.1016/s0306-4522(97)00538-1 · Cited by 56 · see citing works
Activation of the amygdalo‐entorhinal pathway in fear‐conditioning in rat
Majak, K., & Pitkänen, A. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02854.x · Cited by 52 · see citing works
Yaniv, D., Vouimba, R., Diamond, D. M., & Richter‐Levin, G. (2003) · Neuroscience · doi:10.1016/s0306-4522(03)00386-5 · Cited by 50 · see citing works
Self-citationMoses, S. N., Cole, C., & Ryan, J. D. (2005) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2005.02.029 · Cited by 33 · see citing works
Plasticity in the Entorhinal Cortex Suppresses Memory for Contextual Fear
Hebert, A. E., & Dash, P. K. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.3491-04.2004 · Cited by 17 · see citing works
Umegaki, H., Zhu, W., Nakamura, A., Suzuki, Y., Takada, M., Endo, H., & Iguchi, A. (2003) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2003.00979.x · Cited by 14 · see citing works
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Sandi, C., & Richter‐Levin, G. (2009) · Trends in Neurosciences · doi:10.1016/j.tins.2009.02.004 · Cited by 227 · see citing works
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Self-citationMaras, P. M., Molet, J., Chen, Y., Rice, C., Ji, S. G., Solodkin, A., & Baram, T. Z. (2014) · Molecular Psychiatry · doi:10.1038/mp.2014.12 · Cited by 118 · see citing works
Morales-Medina, J. C., Sanchez, F., Flores, G., Dumont, Y., & Quirion, R. (2009) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2009.05.009 · Cited by 111 · see citing works
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Wingard, J. C., & Packard, M. G. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.05.002 · Cited by 103 · see citing works
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- Authors
- Kogan, I., & Richter‐Levin, G.
- Affiliations
- University of Haifa (IL)
- Corresponding author
- Richter‐Levin, Gal
- ORCID
- Richter‐Levin, Gal
- Venue
- European Journal of Neuroscience
- Publisher
- Wiley
- Published
- 2008-02
- Volume
- 27
- Issue
- 3
- Pages
- 715-722
- ISSN
- 0953-816X (ISSN-L)
- 1460-9568
- OpenAlex
- W2015644952
- Cited by
- 34
- References
- 54
- Citations by year
- 2024: 1 · 2023: 2 · 2020: 1 · 2018: 1 · 2016: 1 · 2015: 3 · 2014: 5 · 2013: 1 · 2012: 5
- FWCI
- 2.41
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- European Journal of Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Charles H. Revson Foundation
- Israel Science Foundation
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- limbic system, spatial learning, stress, hippocampal CA1, basolateral amygdala, entorhinal cortex, CREB activation, emotional memory, memory interference, reversal learning, water temperature stress, memory quality
- MeSH terms
- Amygdala, Animals, Avoidance Learning, Cold Temperature, Emotions, Hippocampus, Learning, Limbic System, Male, Memory Disorders, Neural Pathways, Neuropsychological Tests, Orientation, Space Perception, Stress, Psychological, Biomarkers, Rats, Wistar, Cyclic AMP Response Element-Binding Protein, Entorhinal Cortex, Maze Learning, Rats
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