Chronic stress alters neural activity in medial prefrontal cortex during retrieval of extinction
Open accessAbstract
Chronic restraint stress produces morphological changes in medial prefrontal cortex and disrupts a prefrontally mediated behavior, retrieval of extinction. To assess potential physiological correlates of these alterations, we compared neural activity in infralimbic and prelimbic cortex of unstressed versus stressed rats during fear conditioning and extinction. After implantation of microwire bundles into infralimbic or prelimbic cortex, rats were either unstressed or stressed via placement in a plastic restrainer (3 h/day for 1 week). Rats then underwent fear conditioning and extinction while activity of neurons in infralimbic or prelimbic cortex was recorded. Percent freezing and neural activity were assessed during all phases of training. Chronic stress enhanced freezing during acquisition of conditioned fear, and altered both prelimbic and infralimbic activity during this phase. Stress did not alter initial extinction or conditioned stimulus (CS)-related activity during this phase. However, stress impaired retrieval of extinction assessed 24 h later, and this was accompanied by alterations in neuronal activity in both prelimbic and infralimbic cortex. In prelimbic cortex, unstressed rats showed decreased activity in response to CS presentation, whereas stressed rats showed no change. In infralimbic cortex, neurons in unstressed rats exhibited increased firing in response to the CS, whereas stressed rats showed no increase in infralimbic firing during the tone. Finally, CS-related firing in infralimbic but not prelimbic cortex was correlated with extinction retrieval. Thus, the stress-induced alteration of neuronal activity in infralimbic cortex may be responsible for the stress-induced deficit in retrieval of extinction.
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One consequence of stress-related PFC impairment is enhanced threat learning and impaired extinction retention in rodent models.
“One consequence of stress-related PFC impairment is enhanced threat learning and impaired extinction retention in rodent models [66, 70].”
From Prefrontal cortex, amygdala, and threat processing: implications for PTSD (2022) · cites this paper as [70]
The Discussion (page unavailable) reports increased freezing during fear-conditioning acquisition, impaired extinction retrieval 24 hours later, and altered medial PFC activity in stressed rats. But it says the increased freezing may reflect expression rather than enhanced learning, and it does not establish PFC impairment as the cause of both behavioral effects. (LLM, conf=0.84)
Experimental — accuracy not yet measuredChronic stress impacts neural activity in both PL and IL cortex and leads to structural changes in IL cortex.
“In rodents, chronic stress also impacts neural activity in both PL and IL cortex [70] and leads to structural changes in IL cortex [71].”
From Prefrontal cortex, amygdala, and threat processing: implications for PTSD (2022) · cites this paper as [70]
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Cites
Paxinos, G. (1985) · Cited by 3,715 · see citing works
Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex
McCormick, D. A., Connors, B. W., Lighthall, J. W., & Prince, D. A. (1985) · Journal of Neurophysiology · doi:10.1152/jn.1985.54.4.782 · Cited by 1,935 · see citing works
Neurons in medial prefrontal cortex signal memory for fear extinction
Milad, M. R., & Quirk, G. J. (2002) · Nature · doi:10.1038/nature01138 · Cited by 1,836 · see citing works
Vyas, A., Mitra, R., Shankaranarayana Rao, B. S., & Chattarji, S. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-15-06810.2002 · Cited by 1,662 · see citing works
Differential projections of the infralimbic and prelimbic cortex in the rat
Vertes, R. P. (2004) · Synapse · doi:10.1002/syn.10279 · Cited by 1,550 · see citing works
Intrinsic firing patterns of diverse neocortical neurons
Connors, B. W., & Gutnick, M. J. (1990) · Trends in Neurosciences · doi:10.1016/0166-2236(90)90185-d · Cited by 1,440 · see citing works
Reduction of Prefrontal Cortex Glucose Metabolism Common to Three Types of Depression
Baxter, L. R. (1989) · Archives of General Psychiatry · doi:10.1001/archpsyc.1989.01810030049007 · Cited by 1,320 · see citing works
A functional anatomical study of unipolar depression
Drevets, W., Videen, T., Price, J., Preskorn, S., Carmichael, S., & Raichle, M. (1992) · The Journal of Neuroscience · doi:10.1523/jneurosci.12-09-03628.1992 · Cited by 1,266 · see citing works
Homayoun, H., & Moghaddam, B. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.2213-07.2007 · Cited by 1,231 · see citing works
Designing Experiments and Analysing Data: A Model Comparison Perspective.
Freeman, G. H., Maxwell, S. E., & Delaney, H. D. (1991) · Biometrics · doi:10.2307/2532173 · Cited by 1,229 · see citing works
Avison, W. R., Brown, G. W., & Harris, T. (1990) · Contemporary Sociology A Journal of Reviews · doi:10.2307/2072630 · Cited by 1,148 · see citing works
Designing Experiments and Analyzing Data: A Model Comparison Perspective, Third Edition
Maxwell, S. E., & Delaney, H. D. (1999) · Medical Entomology and Zoology · Cited by 975 · see citing works
The role of ventromedial prefrontal cortex in the recovery of extinguished fear
Quirk, G. J., Russo, G. K., Barron, J. L., & Lebron, K. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-16-06225.2000 · Cited by 957 · see citing works
Magarin˜os, A. M., & McEwen, B. S. (1995) · Neuroscience · doi:10.1016/0306-4522(95)00259-l · Cited by 863 · see citing works
Repeated Stress Induces Dendritic Spine Loss in the Rat Medial Prefrontal Cortex
Radley, J. J., Rocher, A. B., Miller, M., Janssen, W. G. M., Liston, C., Hof, P. R., McEwen, B. S., & Morrison, J. H. (2006) · Cerebral Cortex · doi:10.1093/cercor/bhi104 · Cited by 820 · see citing works
Chronic stress alters dendritic morphology in rat medial prefrontal cortex
Cook, S. C., & Wellman, C. L. (2004) · Journal of Neurobiology · doi:10.1002/neu.20025 · Cited by 750 · see citing works
Self-citationMorgan, 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
Vidal-Gonzalez, I., Vidal-Gonzalez, B., Rauch, S. L., & Quirk, G. J. (2006) · Learning & Memory · doi:10.1101/lm.306106 · Cited by 705 · see citing works
Prefrontal 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
Designing experiments and analyzing data: a model comparison perspective
(1990) · Choice Reviews Online · doi:10.5860/choice.28-2192 · Cited by 673 · see citing works
Conrad, C. D., Magariños, A. M., LeDoux, J. E., & McEwen, B. S. (1999) · Behavioral Neuroscience · doi:10.1037/0735-7044.113.5.902 · Cited by 664 · see citing works
Conrad, C. D., Magariños, A. M., LeDoux, J. E., & McEwen, B. S. (1999) · Behavioral Neuroscience · doi:10.1037//0735-7044.113.5.902 · Cited by 663 · see citing works
Activity in Prelimbic Cortex Is Necessary for the Expression of Learned, But Not Innate, Fears
Corcoran, K., & Quirk, G. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.5327-06.2007 · Cited by 580 · see citing works
Burgos-Robles, A., Vidal-Gonzalez, I., & Quirk, G. J. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.0378-09.2009 · Cited by 530 · see citing works
Burgos-Robles, A., Vidal-Gonzalez, I., Santini, E., & Quirk, G. J. (2007) · Neuron · doi:10.1016/j.neuron.2007.02.021 · Cited by 516 · see citing works
Dias, R. S., Robbins, T. W., & Roberts, A. (1996) · Behavioral Neuroscience · doi:10.1037//0735-7044.110.5.872 · Cited by 477 · see citing works
Dias, R., Robbins, T. W., & Roberts, A. C. (1996) · Behavioral Neuroscience · doi:10.1037/0735-7044.110.5.872 · Cited by 476 · 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
Self-citationOrganization 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
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
Self-citationCarter, C. S., MacDonald, A. W., Ross, L. L., & Stenger, V. A. (2001) · American Journal of Psychiatry · doi:10.1176/appi.ajp.158.9.1423 · Cited by 411 · see citing works
Milad, M. R., Vidal-Gonzalez, I., & Quirk, G. J. (2004) · Behavioral Neuroscience · doi:10.1037/0735-7044.118.2.389 · Cited by 354 · 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
Liu, R.-J., & Aghajanian, G. K. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0706679105 · Cited by 346 · see citing works
Mild, Short-term Stress Alters Dendritic Morphology in Rat Medial Prefrontal Cortex
Brown, S. M., Henning, S., & Wellman, C. L. (2005) · Cerebral Cortex · doi:10.1093/cercor/bhi048 · Cited by 335 · see citing works
Self-citationGoldwater, D. S., Pavlides, C., Hunter, R. G., Bloss, E. B., Hof, P. R., McEwen, B. S., & Morrison, J. H. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.08.053 · Cited by 333 · see citing works
Quantification, smoothing, and confidence limits for single-units' histograms
Abeles, M. (1982) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(82)90002-4 · Cited by 309 · see citing works
Jung, M. W., Qin, Y. F., McNaughton, B. L., & Barnes, C. A. (1998) · Cerebral Cortex · doi:10.1093/cercor/8.5.437 · Cited by 306 · see citing works
Prolonged behavioral stress enhances synaptic connectivity in the basolateral amygdala
Vyas, A., Jadhav, S., & Chattarji, S. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.08.003 · Cited by 299 · see citing works
Maroun, M., & Richter-Levin, G. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-11-04406.2003 · Cited by 293 · see citing works
Stress-Induced Dendritic Remodeling in the Prefrontal Cortex is Circuit Specific
Shansky, R. M., Hamo, C., Hof, P. R., McEwen, B. S., & Morrison, J. H. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhp003 · Cited by 248 · see citing works
A History of Corticosterone Exposure Regulates Fear Extinction and Cortical NR2B, GluR2/3, and BDNF
Gourley, S. L., Kedves, A. T., Olausson, P., & Taylor, J. R. (2009) · Neuropsychopharmacology · doi:10.1038/npp.2008.123 · Cited by 218 · see citing works
Chronic stress impairs recall of extinction of conditioned fear
Miracle, A. D., BRACE, M., HUYCK, K., SINGLER, S., & Wellman, C. L. (2005) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2005.10.005 · Cited by 217 · see citing works
Self-citationAn fMRI study of differential neural response to affective pictures in schizophrenia
Takahashi, H., Koeda, M., Oda, K., Matsuda, T., Matsushima, E., Matsuura, M., Asai, K., & Okubo, Y. (2004) · NeuroImage · doi:10.1016/j.neuroimage.2004.03.028 · Cited by 205 · see citing works
Baeg, E. H. (2001) · Cerebral Cortex · doi:10.1093/cercor/11.5.441 · Cited by 205 · see citing works
Chronic stress and sex differences on the recall of fear conditioning and extinction
Baran, S. E., Armstrong, C. E., Niren, D. C., Hanna, J. J., & Conrad, C. D. (2009) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2008.11.005 · Cited by 200 · see citing works
A prospective study of stressful life events and schizophrenic relapse.
Ventura, J., Nuechterlein, K. H., Lukoff, D. G., & Hardesty, J. P. (1989) · Journal of Abnormal Psychology · doi:10.1037/0021-843x.98.4.407 · Cited by 191 · see citing works
Homayoun, H., Jackson, M., & Moghaddam, B. (2005) · Journal of Neurophysiology · doi:10.1152/jn.00875.2004 · Cited by 137 · 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
Garcia, R., Spennato, G., Nilsson-Todd, L., Moreau, J., & Deschaux, O. (2008) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2007.10.005 · Cited by 126 · see citing works
Monfils, M. (2004) · Cerebral Cortex · doi:10.1093/cercor/bhh020 · Cited by 124 · see citing works
Cunningham, M. G., Bhattacharyya, S., & Benes, F. M. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhm183 · Cited by 93 · see citing works
Prefrontal cortex lesions and sex differences in fear extinction and perseveration
Baran, S. E., Armstrong, C. E., Niren, D. C., & Conrad, C. D. (2010) · Learning & Memory · doi:10.1101/lm.1778010 · Cited by 90 · see citing works
Farinelli, M., Deschaux, O., Hugues, S., Thévenet, A., & Garcia, R. (2006) · Learning & memory (Cold Spring Harbor, N.Y.) · doi:10.1101/lm.204806 · Cited by 84 · see citing works
Stress, Synaptic Plasticity, and Psychopathology
Garcia, R. (2002) · Reviews in the Neurosciences · doi:10.1515/revneuro.2002.13.3.195 · Cited by 81 · see citing works
Garcia, R., Chang, C., & Maren, S. (2006) · Learning & Memory · doi:10.1101/lm.60406 · Cited by 70 · see citing works
Monfils, M., & Teskey, G. C. (2004) · Synapse · doi:10.1002/syn.20039 · Cited by 65 · see citing works
Apical tuft input efficacy in layer 5 pyramidal cells from rat visual cortex
Rhodes, P. A., & Llinás, R. R. (2001) · The Journal of Physiology · doi:10.1111/j.1469-7793.2001.00167.x · Cited by 56 · see citing works
Farrell, M. R., Sayed, J. A., Underwood, A. R., & Wellman, C. L. (2010) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2010.06.001 · Cited by 51 · see citing works
Self-citationJackson, M., & Moghaddam, B. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.05054.x · Cited by 46 · see citing works
Flagged first, then by citations
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Sorted by citations
Stress, serotonin, and hippocampal neurogenesis in relation to depression and antidepressant effects
Mahar, I., Bambico, F. R., Mechawar, N., & Nobrega, J. N. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.11.009 · Cited by 694 · see citing works
Maren, S., & Holmes, A. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2015.180 · Cited by 412 · see citing works
Prefrontal cortex, amygdala, and threat processing: implications for PTSD
Alexandra Kredlow, M., Fenster, R. J., Laurent, E. S., Ressler, K. J., & Phelps, E. A. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-021-01155-7 · Cited by 346 · see citing works
“In rodents, chronic stress also impacts neural activity in both PL and IL cortex [70] and leads to structural changes in IL cortex [71].”
BackgroundEpigenetics of stress adaptations in the brain
Stankiewicz, A. M., Swiergiel, A. H., & Lisowski, P. (2013) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2013.07.003 · Cited by 220 · see citing works
Single prolonged stress disrupts retention of extinguished fear in rats.Preprint
Knox, D., George, S. A., Fitzpatrick, C. J., Rabinak, C. A., Maren, S., & Liberzon, I. (2012) · Learning & memory (Cold Spring Harbor, N.Y.) · doi:10.1101/lm.024356.111 · Cited by 202 · see citing works
The interaction between stress and chronic pain through the lens of threat learning
Timmers, I., Quaedflieg, C., Hsu, C. M., Heathcote, L., Rovnaghi, C., & Simons, L. (2019) · Neuroscience and Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.10.007 · Cited by 171 · 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
Individual differences in recovery from traumatic fear
Holmes, A., & Singewald, N. (2012) · Trends in Neurosciences · doi:10.1016/j.tins.2012.11.003 · Cited by 141 · see citing works
Spadaro, P. A., Flavell, C. R., Widagdo, J., Ratnu, V. S., Troup, M., Ragan, C., Mattick, J. S., & Bredy, T. W. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.02.004 · Cited by 124 · see citing works
Czéh, B., Vardya, I., Varga, Z., Febbraro, F., Csabai, D., Martis, L., Højgaard, K., Henningsen, K., Bouzinova, E. V., Miseta, A., et al. (2018) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2018.00148 · Cited by 129 · see citing works
Glucocorticoid receptors and extinction retention deficits in the single prolonged stress model.
Knox, D., Nault, T., Henderson, C., & Liberzon, I. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.07.047 · Cited by 122 · see citing works
Fear conditioning and extinction: emotional states encoded by distinct signaling pathways
Tronson, N. C., Corcoran, K. A., Jovasevic, V., & Radulović, J. (2011) · Trends in Neurosciences · doi:10.1016/j.tins.2011.10.003 · Cited by 120 · see citing works
Giustino, T. F., Ramanathan, K. R., Totty, M. S., Miles, O. W., & Maren, S. (2020) · The Journal of Neuroscience · doi:10.1523/jneurosci.1092-19.2019 · Cited by 110 · see citing works
The dynamics of the stress neuromatrix
Sousa, N. (2016) · Molecular Psychiatry · doi:10.1038/mp.2015.196 · Cited by 105 · 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
Csabai, D., Wiborg, O., & Czéh, B. (2018) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2018.00024 · Cited by 100 · see citing works
Maroun, M. (2012) · The Neuroscientist · doi:10.1177/1073858412464527 · Cited by 105 · see citing works
Nature and causes of the immediate extinction deficit: A brief review
Maren, S. (2013) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2013.10.012 · Cited by 100 · see citing works
Walker, A. G., Wenthur, C. J., Xiang, Z., Rook, J. M., Emmitte, K. A., Niswender, C. M., Lindsley, C. W., & Conn, P. J. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1416196112 · Cited by 94 · 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
Durable fear memories require PSD-95
Fitzgerald, P. J., Pinard, C. R., Camp, M., Feyder, M. J., Sah, A., Bergstrom, H. C., Graybeal, C., Liu, Y., Schlüter, O. M., Grant, S. G. N., et al. (2014) · Molecular Psychiatry · doi:10.1038/mp.2014.161 · Cited by 85 · 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-citationSusceptibility and Resilience to Posttraumatic Stress Disorder–like Behaviors in Inbred Mice
Daws, S. E., Joseph, N. F., Jamieson, S., King, M. L., Chévere-Torres, I., Fuentes, I., Shumyatsky, G. P., Brantley, A. F., Rumbaugh, G., & Miller, C. A. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2017.06.030 · Cited by 84 · see citing works
Enhanced Extinction of Aversive Memories by High-Frequency Stimulation of the Rat Infralimbic Cortex
Maroun, M., Kavushansky, A., Holmes, A., Wellman, C., & Motanis, H. (2012) · PLoS ONE · doi:10.1371/journal.pone.0035853 · Cited by 79 · see citing works
Self-citationKopp, B., Wick, D., & Herman, J. P. (2013) · Physiology & Behavior · doi:10.1016/j.physbeh.2013.05.030 · Cited by 75 · see citing works
Post-Traumatic Stress Disorder: The Relationship Between the Fear Response and Chronic Stress
Maeng, L. Y., & Milad, M. R. (2017) · Chronic Stress · doi:10.1177/2470547017713297 · Cited by 92 · see citing works
Negrón-Oyarzo, I., Aboitiz, F., & Fuentealba, P. (2016) · Neural Plasticity · doi:10.1155/2016/7539065 · Cited by 75 · see citing works
Prefrontal single-unit firing associated with deficient extinction in mice
Fitzgerald, P. J., Whittle, N., Flynn, S., Graybeal, C., Pinard, C. R., Gunduz‐Cinar, O., Kravitz, A. V., Singewald, N., & Holmes, A. (2013) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2013.11.002 · Cited by 71 · see citing works
Farrell, M. R., Sengelaub, D. R., & Wellman, C. L. (2013) · Physiology & Behavior · doi:10.1016/j.physbeh.2013.04.002 · Cited by 69 · see citing works
Self-citationBukalo, O., Pinard, C. R., & Holmes, A. (2014) · British Journal of Pharmacology · doi:10.1111/bph.12779 · Cited by 67 · see citing works
Herringa, R. J., Phillips, M. L., Fournier, J. C. J., Kronhaus, D. M., & Germain, A. (2012) · Psychological Medicine · doi:10.1017/s0033291712002310 · Cited by 65 · see citing works
Moench, K. M., & Wellman, C. L. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2017.05.049 · Cited by 63 · see citing works
Self-citationErk, S., Meyer‐Lindenberg, A., Schmierer, P., Mohnke, S., Grimm, O., Garbusow, M., Haddad, L., Pöhland, L., Mühleisen, T. W., Witt, S. H., et al. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.11.025 · Cited by 63 · see citing works
Post-extinction fluoxetine treatment prevents stress-induced reemergence of extinguished fear
Deschaux, O., Zheng, X., Lavigne, J., Nachon, O., Cleren, C., Moreau, J.-L., & Garcia, R. (2013) · Psychopharmacology · doi:10.1007/s00213-012-2806-x · Cited by 62 · see citing works
Guadagno, A., Kang, M. S., Devenyi, G. A., Mathieu, A. P., Rosa‐Neto, P., Chakravarty, M. M., & Walker, C. (2018) · Brain Structure and Function · doi:10.1007/s00429-018-1720-3 · Cited by 59 · see citing works
Knox, D., Stanfield, B. R., Staib, J. M., David, N., Keller, S. M., & DePietro, T. (2016) · Learning & memory (Cold Spring Harbor, N.Y.) · doi:10.1101/lm.043141.116 · Cited by 53 · see citing works
Conrad, C. D., McLaughlin, K. J., Huynh, T. N., El-Ashmawy, M., & Sparks, M. (2011) · Behavioral Neuroscience · doi:10.1037/a0025770 · Cited by 55 · see citing works
Nava, N., Treccani, G., Al‐Absi, A., Müller, H. K., Elfving, B., Popoli, M., Wegener, G., & Nyengaard, J. R. (2015) · Cerebral Cortex · doi:10.1093/cercor/bhv254 · Cited by 54 · see citing works
Wellman, C. L., Bollinger, J. L., & Moench, K. M. (2019) · International review of neurobiology · doi:10.1016/bs.irn.2019.11.007 · Cited by 53 · see citing works
Self-citationNegrón-Oyarzo, I., Pérez, M. Á., Terreros, G., Muñoz, P., & Dagnino‐Subiabre, A. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.11.001 · Cited by 52 · see citing works
Molecular Mechanisms of Stress-Induced Increases in Fear Memory Consolidation within the Amygdala
Aubry, A., Serrano, P. A., & Burghardt, N. S. (2016) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2016.00191 · Cited by 47 · see citing works
Exposure to stress attenuates fear retrieval in healthy men
Merz, C. J., Hamacher‐Dang, T. C., & Wolf, O. T. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.12.009 · Cited by 47 · see citing works
Binette, A. N., Liu, J., Bayer, H., Crayton, K. L., Melissari, L., Sweck, S. O., & Maren, S. (2023) · Journal of Neuroscience · doi:10.1523/jneurosci.1442-22.2023 · Cited by 45 · see citing works
Abe, R., Okada, S., Nakayama, R., Ikegaya, Y., & Sasaki, T. (2019) · Scientific Reports · doi:10.1038/s41598-019-45833-5 · Cited by 43 · see citing works
Moench, K. M., & Wellman, C. L. (2014) · Neuroscience Letters · doi:10.1016/j.neulet.2014.12.035 · Cited by 41 · see citing works
Self-citationMoench, K. M., Maroun, M., Kavushansky, A., & Wellman, C. (2016) · Neurobiology of Stress · doi:10.1016/j.ynstr.2015.12.002 · Cited by 41 · see citing works
Self-citationAmbeskovic, M., Soltanpour, N., Falkenberg, E. A., Zucchi, F. C. R., Kolb, B. E., & Metz, G. A. S. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhw063 · Cited by 39 · see citing works
Ambeskovic, M., Babenko, O., Ilnytskyy, Y., Kovalchuk, I., Kolb, B., & Metz, G. A. S. (2019) · Scientific Reports · doi:10.1038/s41598-019-42691-z · Cited by 36 · see citing works
New insights on brain‐derived neurotrophic factor epigenetics: from depression to memory extinction
Poon, C. H., Heng, B. C., & Lim, L. W. (2021) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.14458 · Cited by 40 · see citing works
Ye, D., Li, Y., Zhang, X., Guo, F., Geng, L., Zhang, Q., & Zhang, Z. (2015) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2015.09.007 · Cited by 38 · see citing works
Gururajan, A., Hill, R., & van den Buuse, M. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.10.009 · Cited by 36 · see citing works
Involvement of CRFR 1 in the Basolateral Amygdala in the Immediate Fear Extinction Deficit
Hollis, F., Sevelinges, Y., Grosse, J., Zanoletti, O., & Sandi, C. (2016) · eNeuro · doi:10.1523/eneuro.0084-16.2016 · Cited by 35 · see citing works
Unrelenting Fear Under Stress: Neural Circuits and Mechanisms for the Immediate Extinction Deficit
Maren, S. (2022) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2022.888461 · Cited by 33 · see citing works
Song, C., Orlandi, C., Sutton, L. P., & Martemyanov, K. A. (2019) · Journal of Biological Chemistry · doi:10.1074/jbc.ra119.007533 · Cited by 30 · see citing works
Schayek, R., & Maroun, M. (2014) · Biological Psychiatry · doi:10.1016/j.biopsych.2014.10.004 · Cited by 32 · see citing works
Wellman, C. L., & Moench, K. M. (2018) · Psychopharmacology · doi:10.1007/s00213-018-5023-4 · Cited by 31 · see citing works
Self-citationPredictable Chronic Mild Stress during Adolescence Promotes Fear Memory Extinction in Adulthood
Deng, J., Yan, W., Han, Y., Chen, C., Meng, S., Sun, C., Xu, L., Xue, Y.-X., Gao, X., Chen, N., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-08017-7 · Cited by 29 · see citing works
Graybeal, C., Kiselycznyk, C., & Holmes, A. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.02.042 · Cited by 29 · see citing works
Barrera, G., Fagnani, J., Carballo, F., Giamal, Y., & Bentosela, M. (2015) · Journal of Veterinary Behavior · doi:10.1016/j.jveb.2015.03.005 · Cited by 28 · see citing works
Raise‐Abdullahi, P., Vafaei, A. A., Ghanbari, A., Dadkhah, M., & Rashidy‐Pour, A. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.01.058 · Cited by 26 · see citing works
Wei, J., Cheng, J., Waddell, N. J., Wang, Z.-J., Pang, X., Cao, Q., Liu, A., Chitaman, J. M., Abreu, K., Jasrotia, R. S., et al. (2020) · Cerebral Cortex · doi:10.1093/cercor/bhaa337 · Cited by 26 · see citing works
On making (and turning adaptive to) maladaptive aversive memories in laboratory rodents
Gazarini, L., Stern, C. A. J., & Bertoglio, L. J. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105101 · Cited by 25 · see citing works
Cingulate subregions in posttraumatic stress disorder, chronic stress, and treatment
Hinojosa, C. A., Kaur, N., VanElzakker, M. B., & Shin, L. M. (2019) · Handbook of clinical neurology · doi:10.1016/b978-0-444-64196-0.00020-0 · Cited by 25 · see citing works
Cumulative Effects of Social Stress on Reward-Guided Actions and Prefrontal Cortical Activity
Barthas, F., Hu, M. Y., Siniscalchi, M. J., Ali, F., Mineur, Y. S., Picciotto, M. R., & Kwan, A. C. (2019) · Biological Psychiatry · doi:10.1016/j.biopsych.2020.02.008 · Cited by 25 · see citing works
Stress enhances the consolidation of extinction memory in a predictive learning task
Hamacher‐Dang, T. C., Engler, H., Schedlowski, M., & Wolf, O. T. (2013) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2013.00108 · Cited by 25 · see citing works
Knox, D., Stanfield, B. R., Staib, J. M., David, N. P., DePietro, T., Chamness, M., Schneider, E. K., Keller, S. M., & Lawless, C. (2017) · Behavioural Brain Research · doi:10.1016/j.bbr.2017.12.037 · Cited by 23 · see citing works
Retrieval-Extinction and Relapse Prevention: Rewriting Maladaptive Drug Memories?
Kuijer, E. J., Ferragud, A., & Milton, A. L. (2020) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2020.00023 · Cited by 23 · see citing works
D1 receptors regulate dendritic morphology in normal and stressed prelimbic cortex
Lin, G. L., Borders, C. B., Lundewall, L. J., & Wellman, C. L. (2015) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.09.020 · Cited by 27 · see citing works
Self-citationEnvironmental certainty influences the neural systems regulating responses to threat and stress
Meyer, H. C., Sangha, S., Radley, J. J., LaLumiere, R. T., & Baratta, M. V. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.10.014 · Cited by 20 · see citing works
Wellman, C. L., Camp, M., Jones, V. M., MacPherson, K. P., Ihne, J. L., Fitzgerald, P. J., Maroun, M., Drabant, E. M., Bogdan, R., Hariri, A. R., et al. (2013) · Experimental Neurology · doi:10.1016/j.expneurol.2013.09.025 · Cited by 20 · see citing works
Self-citationShimizu, T., Minami, C., & Mitani, A. (2018) · Behavioural Brain Research · doi:10.1016/j.bbr.2018.07.005 · Cited by 21 · see citing works
Lamanna, J., Isotti, F., Ferro, M., Racchetti, G., Anchora, L., Rucco, D., & Malgaroli, A. (2020) · Journal of Neuroscience Research · doi:10.1002/jnr.24732 · Cited by 20 · see citing works
Poon, K., Ho, M. S. H., & Chou, K. (2022) · Heliyon · doi:10.1016/j.heliyon.2022.e11121 · Cited by 23 · see citing works
Zoladz, P. R., Reneau, K. E., Weiser, J. N., Cordes, C. N., Virden, E. M., Helwig, S., Thebeault, C. K., Pfister, C. L., Getnet, B. A., Boaz, K. M., et al. (2022) · Brain Sciences · doi:10.3390/brainsci12111536 · Cited by 17 · see citing works
Pase, C. S., Roversi, K., Roversi, K., Vey, L. T., Dias, V. T., Veit, J. C., Maurer, L. H., Duarte, T., Emanuelli, T., Duarte, M. M. M. F., et al. (2016) · Physiology & Behavior · doi:10.1016/j.physbeh.2016.11.009 · Cited by 19 · see citing works
Dorze, C. L., Borreca, A., Pignataro, A., Ammassari‐Teule, M., & Gisquet-Verrier, P. (2020) · Translational Psychiatry · doi:10.1038/s41398-020-0714-0 · Cited by 16 · see citing works
Namkung, H., Thomas, K. L., Hall, J., & Sawa, A. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.12.025 · Cited by 14 · see citing works
de Souza-Júnior, F. J. C., Cunha, L. C., & Lisboa, S. F. D. S. (2022) · Exploration of Neuroprotective Therapy · doi:10.37349/ent.2022.00028 · Cited by 14 · see citing works
History of chronic stress modifies acute stress-evoked fear memory and acoustic startle in male rats
Schmeltzer, S. N., Vollmer, L. L., Rush, J., Weinert, M., Dolgas, C. M., & Sah, R. (2015) · Stress · doi:10.3109/10253890.2015.1016495 · Cited by 14 · see citing works
Timing is everything: differential effects of chronic stress on fear extinction
Chakraborty, P., & Chattarji, S. (2018) · Psychopharmacology · doi:10.1007/s00213-018-5053-y · Cited by 14 · see citing works
Microglial sex differences in innate high anxiety and modulatory effects of minocycline
Ugursu, B., Sah, A., Sartori, S. B., Popp, O., Mertins, P., Dunay, I. R., Kettenmann, H., Singewald, N., & Wolf, S. A. (2024) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2024.03.035 · Cited by 13 · see citing works
Gentry, R. N., & Roesch, M. R. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.2579-17.2018 · Cited by 14 · see citing works
Bender, C. L., Giachero, M., Mutis, R. C., Molina, V. A., & Calfa, G. D. (2018) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2018.09.002 · Cited by 12 · see citing works
Evidence for impaired extinction learning in humans after distal stress exposure
Klinke, C. M., Fiedler, D., Lange, M. D., & Andreatta, M. (2019) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2019.107127 · Cited by 11 · see citing works
Chronic stress and anticipatory event-related potentials: the moderating role of resilience
Shi, X., & Wu, J. (2020) · Stress · doi:10.1080/10253890.2020.1766019 · Cited by 12 · see citing works
Intra‐amygdala metaplasticity modulation of fear extinction learning
Saha, R., Kriebel, M., Anunu, R., Volkmer, H., & Richter‐Levin, G. (2020) · European Journal of Neuroscience · doi:10.1111/ejn.15080 · Cited by 10 · see citing works
Wallace, T., & Myers, B. (2021) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2021.737960 · Cited by 8 · see citing works
Negrón-Oyarzo, I., Dib, T., Chacana-Véliz, L., Quilodrán, N. L., & Urrutia-Piñones, J. (2024) · Frontiers in Neural Circuits · doi:10.3389/fncir.2024.1286111 · Cited by 7 · see citing works
Taslimi, Z., Komaki, A., Sarihi, A., & Haghparast, A. (2019) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2019.01.013 · Cited by 9 · see citing works
Wang, M., Zhang, A., Qin, Z., Xu, S., Ban, S., Zhang, J., Ma, J., & Du, X. (2018) · European Child & Adolescent Psychiatry · doi:10.1007/s00787-018-1255-4 · Cited by 9 · see citing works
Effects of constant darkness on behaviour and physiology of male and female mice
Singh, D., Pandey, S., Ghosh, A., & Aich, P. (2023) · European Journal of Neuroscience · doi:10.1111/ejn.15972 · Cited by 8 · see citing works
Zalewska, K., Hood, R. J., Pietrogrande, G., Sanchez‐Bezanilla, S., Ong, L. K., Johnson, S. J., Young, K. M., Nilsson, M., & Walker, F. R. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22136693 · Cited by 8 · see citing works
Locus coeruleus–amygdala circuit disrupts prefrontal control to impair fear extinction
Bayer, H., Binette, A. N., Sweck, S. O., Juliano, V. A. L., Plas, S. L., Ferst, L. M., Hassell, J. E., Mourão, F. A. G., & Maren, S. (2026) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2528250123 · Cited by 6 · see citing works
Gender dependent contribution of muscarinic receptors in memory retrieval under sub-chronic stress
Rashid, H., & Ahmed, T. (2018) · Neuroscience Letters · doi:10.1016/j.neulet.2018.05.024 · Cited by 7 · see citing works
Ball, K. T., Bennardo, G. M., Roe, J., & Wunderlich, K. J. (2021) · Behavioural Brain Research · doi:10.1016/j.bbr.2021.113583 · Cited by 7 · see citing works
Novel potent blockers for TWIK-1/TREK-1 heterodimers as potential antidepressants
Lee, E. H., Park, J.-E., Gotina, L., Han, Y., Viswanath, A. N. I., Yoo, S., Moon, B., Hwang, J., Park, W., Cho, Y., et al. (2023) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2023.115139 · Cited by 6 · see citing works
Bergosh, M., Medvidovic, S., Zepeda, N., Crown, L. M., Ipe, J., Debattista, L., Romero, L., Amjadi, E., Lam, T., Hakopian, E., et al. (2024) · Frontiers in Neuroscience · doi:10.3389/fnins.2024.1389096 · Cited by 6 · see citing works
Pillai, A. G., Henckens, M. J. A. G., Fernández, G., & Joëls, M. (2014) · PLoS ONE · doi:10.1371/journal.pone.0099208 · Cited by 5 · see citing works
Centella asiatica increases B-cell lymphoma 2 expression in rat prefrontal cortex
Kuswati, K., Prakosa, D., Wasita, B., & Wiyono, N. (2016) · Universa Medicina · doi:10.18051/univmed.2015.v34.10-16 · Cited by 2 · see citing works
Chronic Stress Effects on Corticolimbic Morphology
Wellman, C. L. (2011) · Wiley eBooks · doi:10.1002/9781118083222.ch10 · Cited by 4 · see citing works
Self-citation
- Authors
- Wilber, A. A., Walker, A. G., Southwood, C. J., Farrell, M. R., Lin, G. L., Rebec, G. V., & Wellman, C. L.
- Affiliations
- Indiana University Bloomington (US)
- Corresponding author
- Wellman, C.L.
- Venue
- Neuroscience
- Publisher
- Elsevier BV
- Published
- 2011-02
- Volume
- 174
- Pages
- 115-131
- ISSN
- 0306-4522 (ISSN-L)
- PMC
- PMC3020264
- OpenAlex
- W2039543325
- Semantic Scholar
- ec3c2ff6cfebae04751b5903c47df5b3116789fa
- Cited by
- 115
- References
- 59
- Citations by year
- 2026: 3 · 2025: 2 · 2024: 4 · 2023: 6 · 2022: 4 · 2021: 7 · 2020: 8 · 2019: 12 · 2018: 10 · 2017: 5 · 2016: 8 · 2015: 8 · 2014: 11 · 2013: 14 · 2012: 10
- FWCI
- 5.16
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- U.S. Public Health Service (MHR03087794)
- National Institute of Mental Health (F31MH085415, R03MH087794)
- National Institute of Neurological Disorders and Stroke (F31NS066603, F31NS064791)
- 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 › Neurotransmitter Receptor Influence on Behavior
- Keywords
- chronic restraint stress, medial prefrontal cortex, infralimbic cortex, prelimbic cortex, extinction retrieval, fear extinction, fear conditioning, neuronal firing, conditioned stimulus, neuronal activity
- MeSH terms
- Action Potentials, Animals, Conditioning, Operant, Extinction, Psychological, Fear, Male, Neurons, Restraint, Physical, Stress, Psychological, Rats, Sprague-Dawley, Prefrontal Cortex, Rats
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