Resilience against predator stress and dendritic morphology of amygdala neurons
Open accessAbstract
Individual differences in coping response lie at the core of vulnerability to conditions like post-traumatic stress disorder (PTSD). Like humans, not all animals exposed to severe stress show lasting change in affect. Predator stress is a traumatic experience inducing long-lasting fear, but not in all rodents. Thus, individual variation may be a cross species factor driving responsiveness to stressful events. The present study investigated neurobiological bases of variation in coping with severe stress. The amygdala was studied because it modulates fear and its function is affected by stress. Moreover, stress-induced plasticity of the amygdala has been related to induction of anxiety, a comorbid symptom of psychiatric conditions like PTSD. We exposed rodents to predator stress and grouped them according to their adaptability based on a standard anxiety test (the elevated plus maze). Subsequently we investigated if well-adapted (less anxious) and mal-adapted (extremely anxious) stressed animals differed in the structure of dendritic trees of their output neurons of the right basolateral amygdala (BLA). Two weeks after exposure to stress, well-adapted animals showed low anxiety levels comparable to unstressed controls, whereas mal-adapted animals were highly anxious. In these same animals, Golgi analysis revealed that BLA neurons of well-adapted rats exhibited more densely packed and shorter dendrites than neurons of mal-adapted or unstressed control animals, which did not differ. These data suggest that dendritic hypotrophy in the BLA may be a resilience marker against lasting anxiogenic effects of predator stress.
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?
Prevention of neuronal and synaptic remodeling in BLA PNs and enhanced glutamatergic transmission is paralleled by protection against stress-induced increases in anxiety-like behavior.
“Neuronal and synaptic remodeling in BLA PNs, along with enhanced glutamatergic transmission, has been repeatedly associated with the negative consequence of stress (14,33,34,40), and prevention of these changes is paralleled by a protection against stress-induced increases in anxiety-like behavior (26,41).”
From Chronic Stress Remodels Synapses in an Amygdala Circuit-Specific Manner (2019) · cites this paper as [26]
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
Kessler, R. C., Berglund, P., Demler, O., Jin, R., Merikangas, K. R., & Walters, E. E. (2005) · Archives of General Psychiatry · doi:10.1001/archpsyc.62.6.593 · Cited by 20,391 · see citing works
Posttraumatic Stress Disorder in the National Comorbidity Survey
Kessler, R. C. (1995) · Archives of General Psychiatry · doi:10.1001/archpsyc.1995.03950240066012 · Cited by 10,379 · see citing works
Physiology and neurobiology of stress and adaptation: central role of the brain
McEwen, B. S. (2007) · Physiological Reviews · doi:10.1152/physrev.00041.2006 · Cited by 4,981 · cited 1× · see citing works
“There is significant interest in understanding resilience, that is, the process of adapting well in face of adversity or trauma (16;21;26;35;41).”
BackgroundVyas, 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
Self-citationCharney, D. S. (2004) · American Journal of Psychiatry · doi:10.1176/appi.ajp.161.2.195 · Cited by 1,605 · see citing works
Rauch, S. L., Shin, L. M., & Phelps, E. A. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.06.004 · Cited by 1,397 · see citing works
The long-term behavioural consequences of prenatal stress
Weinstock, M. (2008) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.03.002 · Cited by 1,045 · see citing works
Correction of Fragile X Syndrome in Mice
Dölen, G., Osterweil, E., Rao, B. S. S., Smith, G. B., Auerbach, B. D., Chattarji, S., & Bear, M. F. (2007) · Neuron · doi:10.1016/j.neuron.2007.12.001 · Cited by 979 · see citing works
Shin, L. M., Wright, C. I., Cannistraro, P. A., Wedig, M. M., McMullin, K., Martis, B., Macklin, M. L., Lasko, N. B., Cavanagh, S. R., Krangel, T. S., et al. (2005) · Archives of General Psychiatry · doi:10.1001/archpsyc.62.3.273 · Cited by 960 · see citing works
A Susceptibility Gene for Affective Disorders and the Response of the Human Amygdala
Hariri, A. R., Drabant, E. M., Munoz, K. E., Kolachana, B. S., Mattay, V. S., Egan, M. F., & Weinberger, D. R. (2005) · Archives of General Psychiatry · doi:10.1001/archpsyc.62.2.146 · Cited by 815 · see citing works
Posttraumatic stress disorder: a state-of-the-science review
Nemeroff, C. B., Bremner, J. D., Foa, E. B., Mayberg, H. S., North, C. S., & Stein, M. B. (2006) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2005.07.005 · Cited by 675 · see citing works
Validity of head-dipping as a measure of exploration in a modified hole-board
File, S. E., & Wardill, A. G. (1975) · Psychopharmacology · doi:10.1007/bf00421184 · Cited by 670 · see citing works
Stress duration modulates the spatiotemporal patterns of spine formation in the basolateral amygdala
Mitra, R., Jadhav, S., McEwen, B. S., Vyas, A., & Chattarji, S. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0504011102 · Cited by 663 · see citing works
Self-citationAntipredator defensive behaviors in a visible burrow system
Blanchard, R. J., & Blanchard, D. C. (1989) · Journal of comparative psychology · doi:10.1037/0735-7036.103.1.70 · Cited by 663 · see citing works
Champagne, D. L., Bagot, R. C., van Hasselt, F., Ramakers, G., Meaney, M. J., de Kloet, E. R., Joels, M., & Krugers, H. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.0526-08.2008 · Cited by 661 · see citing works
Vyas, A., Pillai, A. G., & Chattarji, S. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2004.07.013 · Cited by 445 · see citing works
Acute corticosterone treatment is sufficient to induce anxiety and amygdaloid dendritic hypertrophy
Mitra, R., & Sapolsky, R. M. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0705615105 · Cited by 409 · see citing works
Self-citationKilpatrick, D. G., Koenen, K. C., Ruggiero, K. J., Acierno, R. E., Galea, S., Resnick, H. S., Roitzsch, J. C., Boyle, J. M., & Gelernter, J. E. (2007) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2007.06122007 · Cited by 405 · see citing works
Lasting effects on rodent anxiety of a single exposure to a cat
Adamec, R. E., & Shallow, T. (1993) · Physiology & Behavior · doi:10.1016/0031-9384(93)90050-p · Cited by 348 · see citing works
Self-citationHeinrichs, M., Wagner, D., Schoch, W., Soravia, L. M., Hellhammer, D. H., & Ehlert, U. (2005) · American Journal of Psychiatry · doi:10.1176/appi.ajp.162.12.2276 · Cited by 337 · see citing works
The relevance of differential response to trauma in an animal model of posttraumatic stress disorder
Cohen, H., Zohar, J., & Matar, M. A. (2003) · Biological Psychiatry · doi:10.1016/s0006-3223(02)01909-1 · Cited by 268 · see citing works
Cohen, H., Zohar, J., Matar, M. A., Kaplan, Z., Loewenthal, U., & Richter‐Levin, G. (2004) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300523 · Cited by 254 · see citing works
Lee, H., Lee, M.-S., Kang, R.-H., Kim, H., Kim, S.-D., Kee, B. S., Kim, Y., Kim, Y., Kim, J. B., Yeon, B. K., et al. (2005) · Depression and Anxiety · doi:10.1002/da.20064 · Cited by 236 · see citing works
PTSD and stress sensitisation: A tale of brain and body
Stam, R. (2007) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2006.11.010 · Cited by 211 · see citing works
Psychological mechanisms in acute response to trauma
McNally, R. J. (2003) · Biological Psychiatry · doi:10.1016/s0006-3223(02)01663-3 · Cited by 211 · see citing works
The reliability of the hole-board apparatus
File, S. E., & Wardill, A. G. (1975) · Psychopharmacology · doi:10.1007/bf00421183 · Cited by 210 · see citing works
Muller, J. F., Mascagni, F., & McDonald, A. J. (2005) · The Journal of Comparative Neurology · doi:10.1002/cne.20832 · Cited by 203 · see citing works
Corticosteroid receptor polymorphisms: Determinants of vulnerability and resilience
DeRijk, R. H., & de Kloet, E. R. (2008) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2007.11.072 · Cited by 184 · see citing works
Kozlovsky, N., Matar, M. A., Kaplan, Z., Kotler, M., Zohar, J., & Cohen, H. (2007) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145707007560 · Cited by 165 · see citing works
Adamec, R., Kent, P., Anisman, H., Shallow, T., & Merali, Z. (1998) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(98)00032-3 · Cited by 154 · see citing works
Self-citationDendritic pruning of the medial amygdala during pubertal development of the male Syrian hamster
Zehr, J. L., Todd, B. J., Schulz, K. M., McCarthy, M. M., & Sisk, C. L. (2006) · Journal of Neurobiology · doi:10.1002/neu.20251 · Cited by 145 · see citing works
Adamec, R., Head, D., Blundell, J., Burton, P., & Berton, O. (2006) · Physiology & Behavior · doi:10.1016/j.physbeh.2006.03.005 · Cited by 145 · see citing works
Self-citationAdamec, R. E., Burton, P., Shallow, T., & Budgell, J. (1998) · Physiology & Behavior · doi:10.1016/s0031-9384(98)00225-x · Cited by 137 · see citing works
Self-citationThe contribution of behavioural studies to the neuropharmacology of anxiety
File, S. E. (1987) · Neuropharmacology · doi:10.1016/0028-3908(87)90065-7 · Cited by 132 · see citing works
Neural circuit changes mediating lasting brain and behavioral response to predator stress
Adamec, R. E., Blundell, J., & Burton, P. (2005) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.05.007 · Cited by 121 · see citing works
Self-citationLong-lasting, selective, anxiogenic effects of feline predator stress in mice
Adamec, R. E., WALLING, S., & Burton, P. (2004) · Physiology & Behavior · doi:10.1016/j.physbeh.2004.08.029 · Cited by 120 · see citing works
Self-citationVulnerability to mild predator stress in serotonin transporter knockout mice
Adamec, R. E., Burton, P., BLUNDELL, J., MURPHY, D., & HOLMES, A. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.02.012 · Cited by 119 · see citing works
Self-citationPTSD and stress sensitisation: A tale of brain and body Part 2: Animal models
Stam, R. (2007) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2007.01.001 · Cited by 114 · see citing works
Cohen, H., Geva, A. B., Matar, M. A., Zohar, J., & Kaplan, Z. (2007) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145707007912 · Cited by 89 · see citing works
Neural plasticity and stress induced changes in defense in the rat
Adamec, R. E., Blundell, J. J., & Collins, A. (2001) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(01)00053-7 · Cited by 89 · see citing works
Self-citationAdamec, R. E., Holmes, A., & Blundell, J. J. (2008) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.05.005 · Cited by 86 · see citing works
Self-citationMorphine withdrawal‐induced morphological changes in the nucleus accumbens
Spiga, S., Puddu, M. C., Pisano, M., & Diana, M. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.04416.x · Cited by 86 · see citing works
Chakravarthy, S., Saiepour, M. H., Bence, M., Perry, S., Hartman, R., Couey, J. J., Mansvelder, H. D., & Levelt, C. N. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0506305103 · Cited by 79 · see citing works
Whitcher, L. T., & Klintsova, A. Y. (2008) · Synapse · doi:10.1002/syn.20532 · Cited by 77 · see citing works
CRMP3 is required for hippocampal CA1 dendritic organization and plasticity
Quach, T., Massicotte, G., Belin, M., et al. (2007) · The FASEB Journal · doi:10.1096/fj.07-9012com · Cited by 70 · see citing works
Mitra, R., Ferguson, D., & Sapolsky, R. M. (2009) · Molecular Psychiatry · doi:10.1038/mp.2009.9 · Cited by 70 · see citing works
Self-citationProtein synthesis and the mechanisms of lasting change in anxiety induced by severe stress
Adamec, R. E., Strasser, K. J., BLUNDELL, J., Burton, P., & MCKAY, D. (2005) · Behavioural Brain Research · doi:10.1016/j.bbr.2005.09.019 · Cited by 67 · see citing works
Self-citationAdamec, R. E., Blundell, J. J., & Burton, P. (2005) · Physiology & Behavior · doi:10.1016/j.physbeh.2005.06.026 · Cited by 66 · see citing works
Self-citationEvidence of resilience: Neuroimaging in former prisoners of war
Freeman, T., Kimbrell, T. A., Booe, L. Q., Myers, M. W., Cardwell, D. A., Lindquist, D. M., Hart, J., & Komoroski, R. A. (2005) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2005.07.007 · Cited by 65 · see citing works
Adamec, R. E. (2001) · Behavioural Brain Research · doi:10.1016/s0166-4328(00)00366-1 · Cited by 59 · see citing works
Self-citationKozlovsky, N., Matar, M. A., Kaplan, Z., Kotler, M., Zohar, J., & Cohen, H. (2007) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2007.04.009 · Cited by 56 · see citing works
PTSD : brain mechanisms and clinical implications
加藤, 進., 河田, 光., & Pitman, R. K. (2006) · Springer eBooks · Cited by 38 · see citing works
Sherren, N., & Pappas, B. A. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.08.053 · Cited by 31 · see citing works
Mechanisms of Lasting Change in Anxiety Induced by Severe Stress
Adamec, R. E., Blundell, J. J., Strasser, K. J., & Burton, P. (2007) · Springer eBooks · doi:10.1007/4-431-29567-4_7 · Cited by 16 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Stress, immunity, and the management of calves
Hulbert, L. E., & Moisá, S. J. (2016) · Journal of Dairy Science · doi:10.3168/jds.2015-10198 · Cited by 370 · see citing works
The mesoaccumbens dopamine in coping with stress
Cabib, S., & Puglisi-Allegra, S. (2012) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2011.04.012 · Cited by 329 · 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
Chronic Stress Remodels Synapses in an Amygdala Circuit-Specific Manner
Zhang, J.-Y., Liu, T.-H., He, Y., Pan, H.-Q., Zhang, W.-H., Yin, X.-P., Tian, X.-L., Li, B.-M., Wang, X.-D., Holmes, A., et al. (2019) · Biological Psychiatry · doi:10.1016/j.biopsych.2018.06.019 · Cited by 183 · see citing works
Rao, R. P., Anilkumar, S., McEwen, B. S., & Chattarji, S. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.04.008 · Cited by 131 · see citing works
Boldrini, M., Galfalvy, H., Dwork, A. J., Rosoklija, G. B., Trencevska-Ivanovska, I., Pavlovski, G., Hen, R., Arango, V., & Mann, J. J. (2019) · Biological Psychiatry · doi:10.1016/j.biopsych.2018.12.022 · Cited by 116 · see citing works
Daskalakis, N. P., Cohen, H., Nievergelt, C. M., Baker, D. G., Buxbaum, J. D., Russo, S. J., & Yehuda, R. (2016) · Experimental Neurology · doi:10.1016/j.expneurol.2016.07.024 · Cited by 105 · see citing works
Localization of Mineralocorticoid Receptors at Mammalian Synapses
Prager, E. M., Brielmaier, J., Bergstrom, H. C., McGuire, J., & Johnson, L. R. (2010) · PLoS ONE · doi:10.1371/journal.pone.0014344 · Cited by 81 · see citing works
The Neurological Ecology of Fear: Insights Neuroscientists and Ecologists Have to Offer one Another
Clinchy, M., Schulkin, J., Zanette, L. Y., Sheriff, M. J., McGowan, P. O., & Boonstra, R. (2011) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2011.00021 · Cited by 81 · see citing works
“…and pharmacological agents known to affect symptoms in human patients should correct, with equal efficacy, comparable symptoms in the animal (Rosen and Schulkin, 1998; Roseboom et al., 2007; Stam, 2007; Armario et al., 2008; Masini et al., 2009; Mitra et al., 2009; Cohen et al., 2010).”
BackgroundInfluentialAdamec, R., Hebert, M., Blundell, J., & Mervis, R. F. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.09.009 · Cited by 74 · see citing works
Self-citationMolecular and cell signaling targets for PTSD pathophysiology and pharmacotherapy
Hauger, R. L., Olivares-Reyes, J. A., Dautzenberg, F. M., Lohr, J. B., Braun, S., & Oakley, R. H. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.11.007 · Cited by 71 · see citing works
Hetzel, A., & Rosenkranz, J. A. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.60 · Cited by 62 · see citing works
Miklós, I. H., & Kovács, K. J. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.10.027 · Cited by 51 · see citing works
Adamec, R., Toth, M., Haller, J., Halasz, J., & Blundell, J. (2012) · Physiology & Behavior · doi:10.1016/j.physbeh.2011.09.016 · Cited by 37 · see citing works
Self-citationBergstrom, H. C., Smith, R. F., Mollinedo, N. S., & McDonald, C. G. (2010) · Synapse · doi:10.1002/syn.20783 · Cited by 31 · see citing works
Genome to Phenome: A Systems Biology Approach to PTSD Using an Animal Model
Chakraborty, N., Meyerhoff, J., Jett, M., & Hammamieh, R. (2017) · Methods in Molecular Biology · doi:10.1007/978-1-4939-6952-4_6 · Cited by 14 · see citing works
- Authors
- Mitra, R., Adamec, R., & Sapolsky, R.
- Affiliations
- Stanford University (US)
- Memorial University of Newfoundland (CA)
- Corresponding author
- Mitra, Rupshi
- Venue
- Behavioural Brain Research
- Publisher
- Elsevier BV
- Published
- 2009-12-28
- Volume
- 205
- Issue
- 2
- Pages
- 535-543
- ISSN
- 0166-4328 (ISSN-L)
- PMC
- PMC4022315
- OpenAlex
- W2010163307
- Cited by
- 80
- References
- 55
- Citations by year
- 2026: 2 · 2025: 1 · 2023: 3 · 2022: 1 · 2021: 5 · 2020: 6 · 2019: 3 · 2018: 3 · 2017: 10 · 2016: 9 · 2015: 6 · 2014: 2 · 2013: 2 · 2012: 13
- FWCI
- 3.43
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Behavioural Brain Research (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- U.S. Public Health Service (AGO20633)
- National Institute on Aging (R01AG020633)
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Social Sciences › Psychology › Clinical Psychology › Posttraumatic Stress Disorder Research
- Keywords
- predator stress, resilience, basolateral amygdala, dendritic morphology, anxiety, post-traumatic stress disorder, stress-induced plasticity, Golgi staining, elevated plus maze
- MeSH terms
- Adaptation, Psychological, Amygdala, Analysis of Variance, Animals, Anxiety, Cats, Cell Count, Dendrites, Exploratory Behavior, Male, Neurons, Neuropsychological Tests, Random Allocation, Stress, Psychological, Time Factors, Maze Learning, Rats, Long-Evans, 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
