Exposure to Acute Stress Blocks the Induction of Long-Term Potentiation of the Amygdala–Prefrontal Cortex Pathway In Vivo
Open accessAbstract
In recent years, attention has been given to the interaction between the emotional state of the animal and its ability to learn and remember. Studies into the neural mechanisms underlying these interactions have focused on stress-induced synaptic plasticity impairments in the hippocampus. However, other brain areas, including the amygdala and the prefrontal cortex (PFC), have been implicated in relation to stress-mediated effects on memory. The present study examined whether stress, which impairs hippocampal long-term potentiation (LTP), also affects LTP of the basolateral amygdala (BLA)–PFC pathway in vivo. We first confirmed that the stress protocol we used, i.e., the elevated platform stress, was effective in blocking LTP in the CA1 area of the hippocampus. We then characterized activity and established the ability to induce LTP at the BLA–PFC pathway. Finally, we examined the effects of an exposure to the elevated platform stress on the ability to induce LTP in this pathway. The results indicate that, at the same time when LTP is blocked in the hippocampus, it is also inhibited in the BLA–medial PFC pathway. These results call for a shift from a focused attention on the effects of stress on plasticity in the hippocampus to a system level approach that emphasizes the possible modification of interactions between relevant brain areas after an exposure to a stressful experience.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
Electrical stimulation of the amygdala produces LTP in the PFC.
“Maroun and Richter-Levin [401] showed that electrical stimulation of the amygdala produced LTP in the PFC.”
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 Maroun and Richter-Levin [401]
The same stress that blocks LTP in CA1 (elevated platform) also blocks LTP in the PFC.
“These researchers demonstrated that the same stress that blocked LTP in CA1 (placement of rats on an elevated platform) also blocked LTP in the PFC.”
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 Maroun and Richter-Levin [401]
Previous animal studies have shown that stress can modulate the nature of interactions among brain regions.
“as well as modulate the nature of interactions among brain regions.123,124”
From Preferential loss of dorsal-hippocampus synapses underlies memory impairments provoked by short, multimodal stress (2014) · cites this paper as [124]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
McEwen, 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
Modulation of memory fields by dopamine Dl receptors in prefrontal cortex
Williams, G. V., & Goldman-Rakic, P. S. (1995) · Nature · doi:10.1038/376572a0 · Cited by 1,593 · see citing works
The cortical projections of the mediodorsal nucleus and adjacent thalamic nuclei in the rat
Krettek, J. E., & Price, J. L. (1977) · The Journal of Comparative Neurology · doi:10.1002/cne.901710204 · Cited by 1,277 · see citing works
Adrenal steroid receptors and actions in the nervous system
McEwen, B. S., de Kloet, E. R., & Rostène, W. H. (1986) · Physiological Reviews · doi:10.1152/physrev.1986.66.4.1121 · Cited by 1,238 · see citing works
Stress and glucocorticoids impair retrieval of long-term spatial memory
de Quervain, D. J.-F., Roozendaal, B., & McGaugh, J. L. (1998) · Nature · doi:10.1038/29542 · Cited by 1,182 · see citing works
Selective activation of the mesocortical DA system by stress
Thierry, A. M., Tassin, J., BLANC, G., & Glowinski, J. (1976) · Nature · doi:10.1038/263242a0 · Cited by 1,033 · see citing works
Morgan, M. A., & LeDoux, J. E. (1995) · Behavioral Neuroscience · doi:10.1037//0735-7044.109.4.681 · Cited by 717 · see citing works
Morgan, M. A., & LeDoux, J. E. (1995) · Behavioral Neuroscience · doi:10.1037/0735-7044.109.4.681 · Cited by 717 · see citing works
Bodnoff, S., Humphreys, A., Lehman, J., Diamond, D. M., Rose, G., & Meaney, M. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-01-00061.1995 · Cited by 522 · see citing works
Behavioural stress facilitates the induction of long-term depression in the hippocampus
Xu, L., Anwyl, R., & Rowan, M. J. (1997) · Nature · doi:10.1038/387497a0 · Cited by 509 · see citing works
Direct and indirect pathways from the amygdala to the frontal-lobe in rhesus-monkeys
Porrino, L. J., Crane, A. M., & Goldman‐Rakic, P. S. (1981) · Journal of Comparative Neurology · doi:10.1002/cne.901980111 · Cited by 491 · see citing works
Organization of amygdaloid projections to the prefrontal cortex and associated striatum in the rat
McDonald, A. J. (1991) · Neuroscience · doi:10.1016/0306-4522(91)90247-l · Cited by 463 · see citing works
Inescapable versus escapable shock modulates long-term potentiation in the rat hippocampus
Shors, T. J., Seib, T. B., Levine, S., & Thompson, R. F. (1989) · Science · doi:10.1126/science.2704997 · Cited by 458 · 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
Behavioral stress modifies hippocampal plasticity through N-methyl-D-aspartate receptor activation.
Kim, J. J., Foy, M. R., & Thompson, R. F. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.10.4750 · Cited by 435 · 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
The amygdala modulates prefrontal cortex activity relative to conditioned fear
Garcia, R., Vouimba, R.-M., Baudry, M., & Thompson, R. F. (1999) · Nature · doi:10.1038/46286 · Cited by 347 · see citing works
Effects of Stress and Hippocampal NMDA Receptor Antagonism on Recognition Memory in RatsPreprint
Baker, K. B., & Kim, J. J. (2002) · Learning & Memory · doi:10.1101/lm.46102 · Cited by 292 · see citing works
Exposing Rats to a Predator Blocks Primed Burst Potentiation in the Hippocampus<i>In Vitro</i>
Mesches, M. H., Fleshner, M., Heman, K. L., Rose, G. M., & Diamond, D. M. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-14-j0004.1999 · Cited by 276 · see citing works
Akirav, I., & Richter-Levin, G. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-23-10530.1999 · Cited by 250 · see citing works
Self-citationXu, L., Hölscher, C., Anwyl, R., & Rowan, M. (1998) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.95.6.3204 · Cited by 248 · see citing works
Pavlides, C., Ogawa, S., Kimura, A., & McEwen, B. S. (1996) · Brain Research · doi:10.1016/s0006-8993(96)00776-7 · Cited by 234 · see citing works
Mechanisms of Amygdala Modulation of Hippocampal Plasticity
Akirav, I., & Richter‐Levin, G. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-22-09912.2002 · Cited by 225 · see citing works
Self-citationStress Impairs LTP and Hippocampal‐Dependent Memorya
Diamond, D. M., & ROSE, G. M. (1994) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1994.tb39271.x · Cited by 195 · see citing works
Retrograde transport of D-[3H]-aspartate injected into the monkey amygdaloid complex
Amaral, D. G., & Insausti, R. (1992) · Experimental Brain Research · doi:10.1007/bf02259113 · Cited by 187 · see citing works
McDonald, A. J. (1987) · The Journal of Comparative Neurology · doi:10.1002/cne.902620105 · Cited by 181 · see citing works
Jay, T. M., Burette, F., & Laroche, S. (1995) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1995.tb01060.x · Cited by 172 · see citing works
Attenuated hippocampal long-term potentiation in basolateral amygdala-lesioned rats
Ikegaya, Y., Saitō, H., & Abe, K. (1994) · Brain Research · doi:10.1016/0006-8993(94)91377-3 · Cited by 142 · see citing works
[3H]Dexamethasone binding in rat frontal cortex
Meaney, M. J., & Aitken, D. H. (1985) · Brain Research · doi:10.1016/0006-8993(85)91340-x · Cited by 133 · see citing works
Ikegaya, Y., Saitō, H., & Abe, K. (1995) · Neuroscience Research · doi:10.1016/0168-0102(95)00894-7 · Cited by 126 · see citing works
Pérez-Jaranay, J. M., & Vives, F. (1991) · Brain Research · doi:10.1016/0006-8993(91)91357-7 · Cited by 122 · see citing works
Ikegaya, Y., Saitō, H., & Abe, K. (1996) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1996.tb01327.x · Cited by 105 · see citing works
Plasticity in the Mediodorsal Thalamo-Prefrontal Cortical Transmission in Behaving Mice
Herry, C., Vouimba, R., & Garcia, R. (1999) · Journal of Neurophysiology · doi:10.1152/jn.1999.82.5.2827 · Cited by 104 · see citing works
Induction of stable long‐term depression in vivo in the hippocampal–prefrontal cortex pathway
Takita, M., Izaki, Y., Jay, T. M., Kaneko, H., & Suzuki, S. S. (1999) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1999.00870.x · Cited by 101 · see citing works
Time-dependent blockade of STP and LTP in hippocampal slices following acute stress in mice
Garcia, R., Musleh, W., Tocco, G., Thompson, R. F., & Baudry, M. (1997) · Neuroscience Letters · doi:10.1016/s0304-3940(97)00621-6 · Cited by 83 · see citing works
Burette, F., Jay, T. M., & Laroche, S. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.78.2.1155 · Cited by 71 · see citing works
Collateralization of the amygdaloid projections of the rat prelimbic and infralimbic cortices
Cassell, M. D., Chittick, C. A., Siegel, M. A., & Wright, D. J. (1989) · The Journal of Comparative Neurology · doi:10.1002/cne.902790207 · Cited by 63 · see citing works
Short-term behavioral and electrophysiological consequences of underwater trauma
Wang, J. (2000) · Physiology & Behavior · doi:10.1016/s0031-9384(00)00274-2 · Cited by 58 · see citing works
Stress‐Dependent Impairments of Spatial Memory. Role of 5‐HT
Luine, V. N., VILLEGAS, M., MARTINEZ, C., & McEwen, B. S. (1994) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1994.tb39268.x · Cited by 34 · see citing works
Diamond, D. M., Park, C. R., Puls, M. J., & Rose, G. M. (2000) · Cambridge University Press eBooks · doi:10.1017/cbo9780511529818.017 · Cited by 12 · see citing works
Yaniv, D., Vouimba, R., Diamond, D. M., & Richter‐Levin, G. (2003) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2003.tb07128.x · Cited by 6 · see citing works
Self-citationYaniv, D., Vouimba, R., Diamond, D. M., & Richter‐Levin, G. (2003) · Cited by 1 · see citing works
Self-citationLawson (1996) · doi:10.1002/(sici)1096-9861(19960212)365:3
Flagged first, then by citations
Research works printed but not linked: 1
- Diamond DM, Park CR, Puls MJ, Rose GM (2001) Differential effects of stress on hippocampal and amygdaloid LTP. In: Neuronal mechanisms of memory formation (Holscher C, ed), pp 379 -403. Cambridge, UK: Cam- bridge UP.
Cited by
Sorted by citations
Stress and the brain: from adaptation to disease
de Kloet, E. R., Joëls, M., & Holsboer, F. (2005) · Nature Reviews Neuroscience · doi:10.1038/nrn1683 · Cited by 4,621 · see citing works
Stress, Depression, and Neuroplasticity: A Convergence of Mechanisms
Pittenger, C., & Duman, R. S. (2008) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301574 · Cited by 1,795 · see citing works
The stressed synapse: the impact of stress and glucocorticoids on glutamate transmission
Popoli, M., Yan, Z., McEwen, B. S., & Sanacora, G. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3138 · Cited by 1,393 · see citing works
Diamond, D. M., Campbell, A. M., Park, C. R., Halonen, J., & Zoladz, P. R. (2007) · Neural Plasticity · doi:10.1155/2007/60803 · Cited by 762 · see citing works
“Our findings are consistent with recent work from other laboratories indicating that acute stress or corticosterone administration blocks hippocampal LTP (Shors et al. [141]; Shors and Thompson [142]; Pavlides et al. [143]; Pavlides et al. [144]; Pavlides et al. [145]; Garcia et al. [146]; Pavlides and McEwen [147]; Ak…”
BackgroundInfluentialPrefrontal mechanisms in extinction of conditioned fear
Quirk, G. J., Garcia, R., & González-Lima, F. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.03.010 · Cited by 682 · see citing works
Chiba, S., Numakawa, T., Ninomiya, M., Richards, M. C., Wakabayashi, C., & Kunugi, H. (2012) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2012.05.018 · Cited by 673 · see citing works
A review of adversity, the amygdala and the hippocampus: a consideration of developmental timing
Tottenham, N. (2009) · Frontiers in Human Neuroscience · doi:10.3389/neuro.09.068.2009 · Cited by 651 · see citing works
Stress prompts habit behavior in humans
Schwabe, L., & Wolf, O. T. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.0979-09.2009 · Cited by 606 · see citing works
Stress effects on the hippocampus: a critical review
Kim, E. J., Pellman, B., & Kim, J. J. (2015) · Learning & Memory · doi:10.1101/lm.037291.114 · Cited by 620 · see citing works
Cognitive impairment associated to HPA axis hyperactivity after maternal separation in rats
Aisa, B., Tordera, R. M., Lasheras, B., Rı́o, J. D., & Ramírez, M. J. (2007) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2006.12.013 · Cited by 534 · see citing works
Glucocorticoids and the regulation of memory in health and disease
de Quervain, D. J. ‐., Aerni, A., Schelling, G., & Roozendaal, B. (2009) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2009.03.002 · Cited by 496 · see citing works
Stress-induced prefrontal reorganization and executive dysfunction in rodents
Holmes, A., & Wellman, C. L. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.11.005 · Cited by 469 · see citing works
Izquierdo, A., Wellman, C. L., & Holmes, A. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.0474-06.2006 · Cited by 459 · see citing works
The Influence of Stress Hormones on Fear Circuitry
Rodrigues, S. M., LeDoux, J. E., & Sapolsky, R. M. (2009) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.051508.135620 · Cited by 556 · see citing works
The effects of acute stress on episodic memory: A meta-analysis and integrative review.
Shields, G. S., Sazma, M. A., McCullough, A. M., & Yonelinas, A. P. (2017) · Psychological Bulletin · doi:10.1037/bul0000100 · Cited by 450 · see citing works
Joëls, M., Sarabdjitsingh, R. A., & Karst, H. (2012) · Pharmacological Reviews · doi:10.1124/pr.112.005892 · Cited by 425 · see citing works
Corticosteroid hormones in the central stress response: Quick-and-slow
de Kloet, E. R., Karst, H., & Joëls, M. (2008) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2007.10.002 · Cited by 391 · see citing works
Maren, S., & Holmes, A. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2015.180 · Cited by 412 · see citing works
Chronic stress: Implications for neuronal morphology, function and neurogenesis
Joëls, M., Karst, H., Krugers, H. J., & Lucassen, P. J. (2007) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2007.04.001 · Cited by 381 · see citing works
Sex differences in anxiety disorders: Interactions between fear, stress, and gonadal hormones
Maeng, L. Y., & Milad, M. R. (2015) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.04.002 · Cited by 374 · see citing works
Mechanisms contributing to prefrontal cortex maturation during adolescence
Caballero, A., Granberg, R., & Tseng, K. Y. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.05.013 · Cited by 357 · 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
Myers, B., McKlveen, J. M., & Herman, J. P. (2014) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2013.12.003 · Cited by 318 · see citing works
Goto, Y., Yang, C. R., & Otani, S. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2009.08.026 · Cited by 305 · see citing works
Acute Stress-induced Changes in Hippocampal/Prefrontal Circuits in Rats: Effects of Antidepressants
Rocher, C. (2004) · Cerebral Cortex · doi:10.1093/cercor/bhg122 · Cited by 307 · see citing works
Stress, anxiety, and dendritic spines: What are the connections?
Leuner, B., & Shors, T. J. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2012.04.021 · Cited by 284 · see citing works
Larson, J., & Munkácsy, E. (2015) · Brain Research · doi:10.1016/j.brainres.2014.10.034 · Cited by 285 · see citing works
Morphological Correlates of Corticosteroid-Induced Changes in Prefrontal Cortex-Dependent Behaviors
Cerqueira, J., Pêgo, J. M., Taipa, R. J. F., Bessa, J. M., Almeida, O. F. X., & Sousa, N. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.1598-05.2005 · Cited by 285 · see citing works
McCutcheon, J. E., & Marinelli, M. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06648.x · Cited by 279 · see citing works
Akirav, I., & Maroun, M. (2007) · Neural Plasticity · doi:10.1155/2007/30873 · Cited by 277 · see citing works
Self-citationManzanares, P. A. R., Isoardi, N. A., Carrer, H. F., & Molina, V. A. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.2260-05.2005 · Cited by 262 · see citing works
Neighborhood matters: divergent patterns of stress-induced plasticity across the brain
Chattarji, S., Tomar, A., Suvrathan, A., Ghosh, S., & Rahman, M. M. (2015) · Nature Neuroscience · doi:10.1038/nn.4115 · Cited by 248 · see citing works
Stress, neurotransmitters, corticosterone and body–brain integration
Mora, F., Segovia, G., del Arco, A., de Blas, M., & Garrido, P. (2012) · Brain Research · doi:10.1016/j.brainres.2011.12.049 · Cited by 253 · see citing works
Roozendaal, B., McReynolds, J. R., & McGaugh, J. L. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.4664-03.2004 · Cited by 327 · see citing works
Akirav, I., & Maroun, M. (2005) · Cerebral Cortex · doi:10.1093/cercor/bhj114 · Cited by 240 · see citing works
Self-citationRole of stress, corticotrophin releasing factor (CRF) and amygdala plasticity in chronic anxiety
Shekhar, A., Truitt, W., Rainnie, D., & Sajdyk, T. (2005) · Stress · doi:10.1080/10253890500504557 · Cited by 237 · see citing works
McCormick, C. M., & Mathews, I. Z. (2010) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2009.09.019 · Cited by 230 · see citing works
Acute stress impairs spatial memory in male but not female rats: influence of estrous cycle
Conrad, C. D., Jackson, J. L., Wieczorek, L., Baran, S. E., Harman, J. S., Wright, R. L., & Korol, D. L. (2004) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2004.04.025 · Cited by 211 · see citing works
BDNF protects against stress‐induced impairments in spatial learning and memory and LTP
Radecki, D. T., Brown, L. M., Martinez, J., & Teyler, T. J. (2004) · Hippocampus · doi:10.1002/hipo.20048 · Cited by 209 · see citing works
Floresco, S. B., & Tse, M. T. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.5474-06.2007 · Cited by 204 · 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-citationRegulation of dopamine system responsivity and its adaptive and pathological response to stress
Belujon, P., & Grace, A. A. (2015) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2014.2516 · Cited by 185 · see citing works
The Amygdala, the Hippocampus, and Emotional Modulation of Memory
Richter‐Levin, G. (2004) · The Neuroscientist · doi:10.1177/1073858403259955 · Cited by 182 · see citing works
Self-citationManipulating fear associations via optogenetic modulation of amygdala inputs to prefrontal cortex
Klavir, O., Prigge, M., Sarel, A., Paz, R., & Yizhar, O. (2017) · Nature Neuroscience · doi:10.1038/nn.4523 · Cited by 163 · see citing works
Tsoory, M., Cohen, H., & Richter‐Levin, G. (2006) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2006.06.007 · Cited by 165 · see citing works
Self-citationCorticolimbic Blood Flow During Nontraumatic Emotional Processing in Posttraumatic Stress Disorder
Phan, K. L., Britton, J. C., Taylor, S. F., Fig, L. M., & Liberzon, I. (2006) · Archives of General Psychiatry · doi:10.1001/archpsyc.63.2.184 · Cited by 161 · see citing works
Roozendaal, B., McReynolds, J. R., van der Zee, E. A., Lee, S., McGaugh, J. D., & McIntyre, C. K. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.3626-09.2009 · Cited by 182 · see citing works
Time-dependent corticosteroid modulation of prefrontal working memory processing
Henckens, M. J. A. G., van Wingen, G. A., Joëls, M., & Fernández, G. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1019128108 · Cited by 155 · see citing works
Disconnection and reconnection: The morphological basis of (mal)adaptation to stress
Sousa, N., & Almeida, O. F. X. (2012) · Trends in Neurosciences · doi:10.1016/j.tins.2012.08.006 · Cited by 159 · see citing works
Human amygdala development in the absence of species‐expected caregiving
Tottenham, N. (2012) · Developmental Psychobiology · doi:10.1002/dev.20531 · Cited by 149 · see citing works
Akirav, I., Raizel, H., & Maroun, M. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.04603.x · Cited by 161 · see citing works
Self-citationStress‐induced dynamic routing of hippocampal connectivity: A hypothesis
Segal, M., Richter‐Levin, G., & Maggio, N. (2010) · Hippocampus · doi:10.1002/hipo.20751 · Cited by 146 · see citing works
Self-citationArousal and Stress Effects on Consolidation and Reconsolidation of Recognition Memory
Maroun, M., & Akirav, I. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301401 · Cited by 146 · see citing works
Self-citationJay, T. M., Rocher, C., Hotte, M., Naudon, L., Gurden, H., & Spedding, M. (2004) · Neurotoxicity Research · doi:10.1007/bf03033225 · Cited by 141 · see citing works
Stress-induced metaplasticity: From synapses to behavior
Schmidt, M. V., Abraham, W. C., Maroun, M., Stork, O., & Richter‐Levin, G. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.06.059 · Cited by 134 · see citing works
Self-citationGabbott, P. L. A., Warner, T., & Busby, S. J. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.01.026 · Cited by 133 · see citing works
Synaptic Plasticity, Metaplasticity and Depression
Vose, L. R., & Stanton, P. K. (2016) · Current Neuropharmacology · doi:10.2174/1570159x14666160202121111 · Cited by 127 · see citing works
Tsoory, M., & Richter‐Levin, G. (2005) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145705006255 · Cited by 132 · see citing works
Self-citationDel’Arco, A. E., Segovia, G., GARRIDO, P., DEBLAS, M., & MORA, F. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.10.006 · Cited by 127 · see citing works
Sandi, C., Woodson, J. C., Haynes, V. F., Park, C. R., Touyarot, K., Lopez-Fernandez, M. A., Venero, C., & Diamond, D. M. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2004.12.034 · Cited by 122 · see citing works
Maras, 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
Chronic stress alters neural activity in medial prefrontal cortex during retrieval of extinction
Wilber, A. A., Walker, A. G., Southwood, C. J., Farrell, M. R., Lin, G. L., Rebec, G. V., & Wellman, C. L. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2010.10.070 · Cited by 115 · see citing works
Kavushansky, A., Vouimba, R., Cohen, H., & Richter‐Levin, G. (2006) · Hippocampus · doi:10.1002/hipo.20130 · Cited by 141 · see citing works
Self-citationCzéh, B., Perez‐Cruz, C., Fuchs, E., & Flügge, G. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.02.031 · Cited by 117 · see citing works
Aleksandrova, L. R., Wang, Y. T., & Phillips, A. G. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.07.007 · Cited by 114 · see citing works
Stress-induced alterations in large-scale functional networks of the rodent brain
Henckens, M. J. A. G., van der Marel, K., van der Toorn, A., Pillai, A. G., Fernández, G., Dijkhuizen, R. M., & Joëls, M. (2014) · NeuroImage · doi:10.1016/j.neuroimage.2014.10.037 · Cited by 110 · see citing works
Ilin, Y., & Richter‐Levin, G. (2009) · PLoS ONE · doi:10.1371/journal.pone.0004329 · Cited by 112 · see citing works
Self-citationAbush, H., & Akirav, I. (2012) · PLoS ONE · doi:10.1371/journal.pone.0031731 · Cited by 114 · see citing works
Tan, H., Zhong, P., & Yan, Z. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.0143-04.2004 · Cited by 112 · see citing works
Contrasting Roles of Corticosteroid Receptors in Hippocampal Plasticity
Avital, A., Segal, M., & Richter‐Levin, G. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.1628-06.2006 · Cited by 109 · see citing works
Self-citationOpen questions in current models of antidepressant action
Tanti, A., & Belzung, C. (2010) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2009.00585.x · Cited by 109 · see citing works
Réus, G. Z., Stringari, R. B., Ribeiro, K. F., Cipriano, A. L., Panizzutti, B., Stertz, L., Lersch, C., Kapczinski, F. P., & Quevedo, J. (2010) · Neurochemical Research · doi:10.1007/s11064-010-0364-3 · Cited by 108 · see citing works
Vouimba, R., Yaniv, D., Diamond, D., & Richter‐Levin, G. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03294.x · Cited by 114 · see citing works
Self-citationChang, C., Berke, J. D., & Maren, S. (2010) · PLoS ONE · doi:10.1371/journal.pone.0011971 · Cited by 105 · see citing works
Noradrenergic blockade stabilizes prefrontal activity and enables fear extinction under stress
Fitzgerald, P. J., Giustino, T. F., Seemann, J. R., & Maren, S. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1500682112 · Cited by 101 · see citing works
The influence of acute stress on the regulation of conditioned fear
Raio, C. M., & Phelps, E. A. (2015) · Neurobiology of Stress · doi:10.1016/j.ynstr.2014.11.004 · Cited by 121 · see citing works
Gilmartin, M. R., Kwapis, J. L., & Helmstetter, F. J. (2012) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2012.03.009 · Cited by 102 · see citing works
Diabetes as a chronic metabolic stressor: Causes, consequences and clinical complications
Reagan, L. P. (2011) · Experimental Neurology · doi:10.1016/j.expneurol.2011.02.004 · Cited by 101 · see citing works
Goto, Y., & Grace, A. A. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.05.046 · Cited by 100 · see citing works
Maroun, M. (2012) · The Neuroscientist · doi:10.1177/1073858412464527 · Cited by 105 · see citing works
Self-citationGanon-Elazar, E., & Akirav, I. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.01.014 · Cited by 98 · see citing works
Lack of Medial Prefrontal Cortex Activation Underlies the Immediate Extinction Deficit
Kim, S. C., Jo, Y. S., Kim, I. H., Kim, H., & Choi, J.-S. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.4145-09.2010 · Cited by 96 · see citing works
Zhang, Y., Fukushima, H., & Kida, S. (2011) · Molecular Brain · doi:10.1186/1756-6606-4-4 · Cited by 95 · see citing works
Ritov, G., Boltyansky, B., & Richter-Levin, G. (2016) · Molecular Psychiatry · doi:10.1038/mp.2015.169 · Cited by 92 · see citing works
Self-citationEmotional tagging--a simple hypothesis in a complex reality.
Bergado, J., Lucas, M., & Richter-Levin, G. (2011) · Progress in neurobiology · doi:10.1016/j.pneurobio.2011.03.004 · Cited by 85 · see citing works
Self-citationAcute stress impairs the retrieval of extinction memory in humans
Raio, C. M., Brignoni-Perez, E., Goldman, R., & Phelps, E. A. (2014) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2014.01.015 · Cited by 90 · see citing works
The Influence of Organized Violence and Terror on Brain and Mind: A Co-Constructive Perspective
Elbert, T. R., Rockstroh, B. S., Kolassa, I., Schauer, M., & Neuner, F. (2006) · Cambridge University Press eBooks · doi:10.1017/cbo9780511499722.017 · Cited by 88 · see citing works
Vouimba, R., & Maroun, M. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2011.115 · Cited by 88 · see citing works
Self-citationTsoory, M., Guterman, A., & Richter‐Levin, G. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301397 · Cited by 88 · see citing works
Self-citationLane, R. D., & Garfield, D. (2005) · Neuropsychoanalysis · doi:10.1080/15294145.2005.10773468 · Cited by 89 · see citing works
Maroun, M., Ioannides, P. J., Bergman, K. L., Kavushansky, A., Holmes, A., & Wellman, C. L. (2013) · European Journal of Neuroscience · doi:10.1111/ejn.12259 · Cited by 86 · see citing works
Self-citationHugues, S., & Garcia, R. (2007) · Learning & Memory · doi:10.1101/lm.625407 · Cited by 83 · see citing works
Maroun, M. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.05169.x · Cited by 82 · see citing works
Self-citationNR2B-containing NMDA receptor is required for morphine-but not stress-induced reinstatement
Ma, Y., Chu, N.-N., Guo, C., Han, J., & Cui, C. (2006) · Experimental Neurology · doi:10.1016/j.expneurol.2006.08.014 · Cited by 83 · see citing works
Caballero, A. C., Thomases, D. R., Flores-Barrera, E., Cass, D. K., & Tseng, K. Y. (2013) · Psychopharmacology · doi:10.1007/s00213-013-3216-4 · Cited by 82 · see citing works
Tan, H., Lauzon, N. M., Bishop, S. F., Bechard, M. A., & Laviolette, S. R. (2010) · Cerebral Cortex · doi:10.1093/cercor/bhp210 · Cited by 81 · see citing works
Corticosteroid Induced Decoupling of the Amygdala in Men
Henckens, M. J. A. G., van Wingen, G. A., Joëls, M., & Fernández, G. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhr313 · Cited by 80 · see citing works
Hippocampal network oscillations at the interplay between innate anxiety and learned fear
Çalışkan, G., & Stork, O. (2019) · Psychopharmacology · doi:10.1007/s00213-018-5109-z · Cited by 72 · see citing works
Physiological Dissociation in Hippocampal Subregions in Response to Amygdala Stimulation
Vouimba, R., & Richter‐Levin, G. (2005) · Cerebral Cortex · doi:10.1093/cercor/bhi058 · Cited by 80 · see citing works
Self-citationZoladz, P. R., Park, C. R., Halonen, J. D., Salim, S., Alzoubi, K. H., Srivareerat, M., Fleshner, M., Alkadhi, K. A., & Diamond, D. M. (2011) · Hippocampus · doi:10.1002/hipo.20922 · Cited by 79 · see citing works
- Authors
- Maroun, M., & Richter-Levin, G.
- Affiliations
- University of Haifa (IL)
- ORCID
- Maroun, Mouna
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2003-06-01
- Volume
- 23
- Issue
- 11
- Pages
- 4406-4409
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6740777
- OpenAlex
- W1784991500
- Cited by
- 293
- References
- 43
- Citations by year
- 2025: 4 · 2024: 4 · 2023: 5 · 2022: 5 · 2021: 10 · 2020: 6 · 2019: 8 · 2018: 11 · 2017: 5 · 2016: 12 · 2015: 21 · 2014: 19 · 2013: 19 · 2012: 23
- FWCI
- 8.63
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- acute stress, long-term potentiation, basolateral amygdala, medial prefrontal cortex, stress-induced memory impairment, hippocampal CA1, synaptic plasticity, stress and learning
- MeSH terms
- Acute Disease, Amygdala, Analysis of Variance, Animals, Behavior, Animal, Electric Stimulation, Hippocampus, Male, Neural Pathways, Neuronal Plasticity, Stress, Physiological, Theta Rhythm, Receptors, N-Methyl-D-Aspartate, Rats, Sprague-Dawley, Prefrontal Cortex, Long-Term Potentiation, Excitatory Postsynaptic Potentials, Rats
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
