Glucocorticoids interact with the hippocampal endocannabinoid system in impairing retrieval of contextual fear memory
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There is extensive evidence that glucocorticoid hormones impair the retrieval of memory of emotionally arousing experiences. Although it is known that glucocorticoid effects on memory retrieval impairment depend on rapid interactions with arousal-induced noradrenergic activity, the exact mechanism underlying this presumably nongenomically mediated glucocorticoid action remains to be elucidated. Here, we show that the hippocampal endocannabinoid system, a rapidly activated retrograde messenger system, is involved in mediating glucocorticoid effects on retrieval of contextual fear memory. Systemic administration of corticosterone (0.3-3 mg/kg) to male Sprague-Dawley rats 1 h before retention testing impaired the retrieval of contextual fear memory without impairing the retrieval of auditory fear memory or directly affecting the expression of freezing behavior. Importantly, a blockade of hippocampal CB1 receptors with AM251 prevented the impairing effect of corticosterone on retrieval of contextual fear memory, whereas the same impairing dose of corticosterone increased hippocampal levels of the endocannabinoid 2-arachidonoylglycerol. We also found that antagonism of hippocampal β-adrenoceptor activity with local infusions of propranolol blocked the memory retrieval impairment induced by the CB receptor agonist WIN55,212-2. Thus, these findings strongly suggest that the endocannabinoid system plays an intermediary role in regulating rapid glucocorticoid effects on noradrenergic activity in impairing memory retrieval of emotionally arousing experiences.
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Elevated EC signaling during stress regulates the retrieval of traumatic memories.
“As part of this protective role under aversive conditions, elevated EC signaling during stress has been shown to dampen the development of anxiety [12] and to regulate the encoding [13], retrieval [14] and extinction [15] of traumatic memories.”
From Plasma concentrations of endocannabinoids and related primary fatty acid amides in patients with post-traumatic stress disorder (2013) · cites this paper as [14]
Cites
The rat brain in stereotaxic coordinates
Palkovits, M. (1983) · Neuropeptides · doi:10.1016/0143-4179(83)90049-5 · Cited by 28,959 · see citing works
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
THE AMYGDALA MODULATES THE CONSOLIDATION OF MEMORIES OF EMOTIONALLY AROUSING EXPERIENCES
McGaugh, J. L. (2004) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.27.070203.144157 · Cited by 2,296 · see citing works
Self-citationStress, memory and the amygdala
Roozendaal, B., McEwen, B. S., & Chattarji, S. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2651 · Cited by 1,760 · see citing works
Self-citationRole of Endogenous Cannabinoids in Synaptic Signaling
Freund, T. F., Katona, I., & Piomelli, D. (2003) · Physiological Reviews · doi:10.1152/physrev.00004.2003 · Cited by 1,567 · see citing works
Endocannabinoid-Mediated Control of Synaptic Transmission
Kano, M., Ohno‐Shosaku, T., Hashimotodani, Y., Uchigashima, M., & Watanabe, M. (2009) · Physiological Reviews · doi:10.1152/physrev.00019.2008 · Cited by 1,529 · see citing works
Stress and cognition: are corticosteroids good or bad guys?
de Kloet, E. R., Oitzl, M. S., & Joëls, M. (1999) · Trends in Neurosciences · doi:10.1016/s0166-2236(99)01438-1 · Cited by 1,258 · see citing works
Katona, I., Sperlágh, B., Sı́k, A., Käfalvi, A., Vizi, E. S., Mackie, K., & Freund, T. F. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-11-04544.1999 · Cited by 1,218 · 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
Self-citationRole of adrenal stress hormones in forming lasting memories in the brain
McGaugh, J. L., & Roozendaal, B. (2002) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(02)00306-9 · Cited by 818 · see citing works
Self-citationKirschbaum, C., Wolf, O. T., May, M., Wippich, W., & Hellhammer, D. H. (1996) · Life Sciences · doi:10.1016/0024-3205(96)00118-x · Cited by 815 · see citing works
Acute cortisone administration impairs retrieval of long-term declarative memory in humans
de Quervain, D. J.-F., Roozendaal, B., Nitsch, R. M., McGaugh, J. L., & Hock, C. (2000) · Nature Neuroscience · doi:10.1038/73873 · Cited by 745 · see citing works
Self-citationStress effects on memory: An update and integration
Schwabe, L., Joëls, M., Roozendaal, B., Wolf, O. T., & Oitzl, M. S. (2012) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2011.07.002 · Cited by 714 · see citing works
Self-citationImpaired Memory Retrieval after Psychosocial Stress in Healthy Young Men
Kuhlmann, S., Piel, M., & Wolf, O. T. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.5139-04.2005 · Cited by 680 · see citing works
Stress and Memory: Behavioral Effects and Neurobiological Mechanisms
Sandi, C., & Pinelo-Nava, M. T. (2007) · Neural Plasticity · doi:10.1155/2007/78970 · Cited by 611 · 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
Self-citationReversible neural inactivation reveals hippocampal participation in several memory processes
Riedel, G., Micheau, J., Lam, A. G. M., Roloff, E. V. L., Martin, S. J., Bridge, H., de Hoz, L., Poeschel, B., McCulloch, J., & Morris, R. (1999) · Nature Neuroscience · doi:10.1038/13202 · Cited by 478 · see citing works
Tanimura, A., Yamazaki, M., Hashimotodani, Y., Uchigashima, M., Kawata, S., Abe, M., Kita, Y., Hashimoto, K., Shimizu, T., Watanabe, M., et al. (2010) · Neuron · doi:10.1016/j.neuron.2010.01.021 · Cited by 472 · see citing works
Hippocampal Inactivation Disrupts Contextual Retrieval of Fear Memory after Extinction
Corcoran, K. A., & Maren, S. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-05-01720.2001 · Cited by 455 · cited 1× · see citing works
“There is extensive evidence that the hippocampus is involved in the retrieval of contextual, spatial, or declarative memory and is also a primary target for stress hormones (2, 40, 41).”
BackgroundA meta-analytic review of the effects of acute cortisol administration on human memory
Het, S., Ramlow, G., & Wolf, O. T. (2005) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2005.03.005 · Cited by 414 · see citing works
Status of Glucocorticoid Alterations in Post‐traumatic Stress Disorder
Yehuda, R. (2009) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2009.04979.x · Cited by 409 · see citing works
Rapid Glucocorticoid Signaling via Membrane-Associated Receptors
Tasker, J. G., Di, S., & Malcher‐Lopes, R. (2006) · Endocrinology · doi:10.1210/en.2006-0981 · Cited by 401 · see citing works
Roozendaal, B., Okuda, S., de Quervain, D. J.-F., & McGaugh, J. L. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2005.07.049 · Cited by 382 · see citing works
Self-citationStress and emotional memory: a matter of timing
Joëls, M., Fernández, G., & Roozendaal, B. (2011) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2011.04.004 · Cited by 372 · see citing works
Self-citationDe Quervain, D. J. ‐., Henke, K., Aerni, A., Treyer, V., McGaugh, J. L., Berthold, T., Nitsch, R. M., Buck, A., Roozendaal, B., & Hock, C. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02542.x · Cited by 342 · see citing works
Self-citationLow-Dose Cortisol for Symptoms of Posttraumatic Stress Disorder
Aerni, A., Traber, R., Höck, C., Roozendaal, B., Schelling, G., Papassotiropoulos, A., Nitsch, R. M., Schnyder, U., & de Quervain, D. J. ‐. (2004) · American Journal of Psychiatry · doi:10.1176/appi.ajp.161.8.1488 · Cited by 342 · see citing works
Self-citationFast Feedback Inhibition of the HPA Axis by Glucocorticoids Is Mediated by Endocannabinoid Signaling
Evanson, N. K., Tasker, J. G., Hill, M. N., Hillard, C. J., & Herman, J. P. (2010) · Endocrinology · doi:10.1210/en.2010-0285 · Cited by 324 · see citing works
Systemic or intrahippocampal cannabinoid administration impairs spatial memory in rats
Lichtman, A. H., Dimen, K. R., & Martin, B. R. (1995) · Psychopharmacology · doi:10.1007/bf02246292 · Cited by 311 · see citing works
Roozendaal, B., Hahn, E. L., Nathan, S. V., de Quervain, D. J.-F., & McGaugh, J. L. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.2574-04.2004 · Cited by 301 · see citing works
Self-citationCampolongo, P., Roozendaal, B., Trezza, V., Hauer, D., Schelling, G., McGaugh, J. L., & Cuomo, V. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0900835106 · Cited by 294 · see citing works
Self-citationRoozendaal, B., Griffith, Q. K., Buranday, J., de Quervain, D. J.-F., & McGaugh, J. L. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0337480100 · Cited by 291 · see citing works
Self-citationFraser, G. A. (2009) · CNS Neuroscience & Therapeutics · doi:10.1111/j.1755-5949.2008.00071.x · Cited by 283 · cited 1× · see citing works
“Although clinical studies have not yet investigated interactions between these two stress systems, recent findings indicate that administration of the synthetic cannabinoid nabilone to PTSD patients resulted in a highly comparable reduction of treatment-resistant daytime flashbacks and nightmares (56).”
BackgroundHill, M. N., Patel, S., Campolongo, P., Tasker, J. G., Wotjak, C. T., & Bains, J. S. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.4283-10.2010 · Cited by 255 · see citing works
Self-citationPostreactivation Glucocorticoids Impair Recall of Established Fear Memory
Cai, W.-H., Blundell, J. J., Han, J., Greene, R. W., & Powell, C. M. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.2397-06.2006 · Cited by 244 · see citing works
Hill, M. N., & McEwen, B. S. (2010) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2009.11.001 · Cited by 235 · see citing works
Kuhlmann, S., Kirschbaum, C., & Wolf, O. T. (2004) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2004.09.001 · Cited by 217 · see citing works
Yang, Y.-L., Chao, P.-K., & Lu, K. (2005) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300899 · Cited by 216 · see citing works
Di, S., Maxson, M. M., Franco, A. J., & Tasker, J. G. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.4546-08.2009 · Cited by 212 · see citing works
Arousal and cortisol interact in modulating memory consolidation in healthy young men.
Kuhlmann, S., & Wolf, O. T. (2006) · Behavioral Neuroscience · doi:10.1037/0735-7044.120.1.217 · Cited by 194 · see citing works
Preventive Effect of β-Adrenoceptor Blockade on Glucocorticoid-Induced Memory Retrieval Deficits
de Quervain, D. J. ‐., Aerni, A., & Roozendaal, B. (2007) · American Journal of Psychiatry · doi:10.1176/ajp.2007.164.6.967 · Cited by 181 · see citing works
Self-citationSchelling, G., Roozendaal, B., Krauseneck, T., Schmoelz, M., de Quervain, D. J. ‐., & Briegel, J. (2006) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1364.005 · Cited by 173 · see citing works
Self-citationRapid elevations in limbic endocannabinoid content by glucocorticoid hormones in vivo
Hill, M. N., Karatsoreos, I. N., Hillard, C. J., & McEwen, B. S. (2010) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2010.03.005 · Cited by 166 · see citing works
Légrádi, G., Das, M., Giunta, B. N., Hirani, K., Mitchell, E., & Diamond, D. M. (2007) · Neural Plasticity · doi:10.1155/2007/79102 · Cited by 164 · see citing works
Patel, S., & Hillard, C. J. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06266.x · Cited by 162 · see citing works
Oei, N. Y. L., Elzinga, B. M., Wolf, O. T., de Ruiter, M. B., Damoiseaux, J. S., Kuijer, J. P. A., Veltman, D. J., Scheltens, P., & Rombouts, S. A. R. B. (2007) · Brain Imaging and Behavior · doi:10.1007/s11682-007-9003-2 · Cited by 146 · see citing works
Roles of the Endocannabinoid System in Learning and Memory
Marsicano, G., & Lafenêtre, P. (2009) · Current topics in behavioral neurosciences · doi:10.1007/978-3-540-88955-7_8 · Cited by 140 · see citing works
The precision of remote context memories does not require the hippocampus
Wang, S., Teixeira, C. M., Wheeler, A. L., & Frankland, P. W. (2009) · Nature Neuroscience · doi:10.1038/nn.2263 · Cited by 138 · see citing works
Wang, M., Hill, M. N., Zhang, L., Gorzalka, B. B., Hillard, C. J., & Alger, B. E. (2011) · Journal of Psychopharmacology · doi:10.1177/0269881111409606 · Cited by 137 · see citing works
Can Posttraumatic Stress Disorder Be Prevented with Glucocorticoids?
SCHELLING, G., ROOZENDAAL, B., & de QUERVAIN, D. J. ‐. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1314.013 · Cited by 130 · see citing works
Self-citationRoozendaal, B., de Quervain, D. J. ‐., Schelling, G., & McGaugh, J. L. (2003) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2003.10.001 · Cited by 128 · see citing works
Self-citationMcReynolds, J. R., Donowho, K. M., Abdi, A., McGaugh, J. L., Roozendaal, B., & McIntyre, C. K. (2009) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2009.11.005 · Cited by 126 · see citing works
Self-citationSystemic administration of WIN 55,212-2 increases norepinephrine release in the rat frontal cortex
Oropeza, V. C., Page, M. E., & Bockstaele, E. J. V. (2005) · Brain Research · doi:10.1016/j.brainres.2005.03.036 · Cited by 121 · see citing works
Akirav, I. (2011) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2011.00034 · Cited by 100 · see citing works
Atsak, P., Roozendaal, B., & Campolongo, P. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2011.08.047 · Cited by 98 · see citing works
Self-citationEndocannabinoids: The silent partner of glucocorticoids in the synapse
Hill, M. N., & McEwen, B. S. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0901519106 · Cited by 98 · see citing works
Hashimotodani, Y., Ohno‐Shosaku, T., Maejima, T., Fukami, K., & Kano, M. (2007) · Neuropharmacology · doi:10.1016/j.neuropharm.2007.06.002 · Cited by 90 · see citing works
Egashira, N., 三島, 健., Iwasaki, K., & Fujiwara, M. (2002) · Brain Research · doi:10.1016/s0006-8993(02)03247-x · Cited by 83 · see citing works
Repeated cannabinoid administration increases indices of noradrenergic activity in rats
Page, M. E., Oropeza, V. C., Sparks, S. E., Qian, Y., Menko, A. S., & Bockstaele, E. J. V. (2007) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2006.12.020 · Cited by 81 · see citing works
Release of anandamide from blood cells
Vogeser, M., Hauer, D., Azad, S. C., Huber, E., Storr, M., & Schelling, G. (2006) · Clinical Chemistry and Laboratory Medicine (CCLM) · doi:10.1515/cclm.2006.065 · Cited by 77 · see citing works
Self-citationRodent Stereotaxic Surgery and Animal Welfare Outcome Improvements for Behavioral Neuroscience
Fornari, R. V., Wichmann, R., Atsak, P., Atucha, E., Barsegyan, A., Beldjoud, H., Messanvi, F., Thuring, C. M. A., & Roozendaal, B. (2012) · Journal of Visualized Experiments · doi:10.3791/3528 · Cited by 61 · see citing works
Self-citationWegener, N., Kuhnert, S., Thüns, A., Roese, R., & Koch, M. (2008) · Psychopharmacology · doi:10.1007/s00213-008-1148-1 · Cited by 57 · see citing works
Schutsky, K., Ouyang, M., Castelino, C. B., Zhang, L., & THOMAS, S. A. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.2122-11.2011 · Cited by 56 · see citing works
Pitfalls in measuring the endocannabinoid 2-arachidonoyl glycerol in biological samples
Vogeser, M., & Schelling, G. (2007) · Clinical Chemistry and Laboratory Medicine (CCLM) · doi:10.1515/cclm.2007.197 · Cited by 51 · see citing works
Self-citationCalhoun, P., Sampson, W. S., Bosworth, H., Feldman, M., Kirby, A., Hertzberg, M. A., Wampler, T. P., Tate-Williams, F., Moore, S. D., & Beckham, J. (2000) · Journal of Consulting and Clinical Psychology · doi:10.1037/0022-006x.68.5.923 · Cited by 26 · see citing works
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The Brain on Stress: Vulnerability and Plasticity of the Prefrontal Cortex over the Life Course
McEwen, B. S., & Morrison, J. H. (2013) · Neuron · doi:10.1016/j.neuron.2013.06.028 · Cited by 1,079 · see citing works
Neurobiological Interactions Between Stress and the Endocannabinoid System
Morena, M., Patel, S., Bains, J. S., & Hill, M. N. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.166 · Cited by 663 · see citing works
Stress, glucocorticoids and memory: implications for treating fear-related disorders
de Quervain, D., Schwabe, L., & Roozendaal, B. (2017) · Nature Reviews Neuroscience · doi:10.1038/nrn.2016.155 · Cited by 484 · see citing works
Self-citationMaren, S., & Holmes, A. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2015.180 · Cited by 412 · see citing works
Cannabis and adolescent brain development.
Lubman, D. I., Cheetham, A., & Yücel, M. (2015) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2014.11.009 · Cited by 360 · 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
Hill, M. N., Bierer, L. M., Makotkine, I., Golier, J. A., Galea, S., McEwen, B. S., Hillard, C. J., & Yehuda, R. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.08.004 · Cited by 256 · see citing works
Corticotropin-releasing hormone drives anandamide hydrolysis in the amygdala to promote anxiety
Gray, J. M., Vecchiarelli, H. A., Morena, M., Lee, T. T. Y., Hermanson, D. J., Kim, A. B., McLaughlin, R. J., Hassan, K. I., Kühne, C., Wotjak, C. T., et al. (2015) · The Journal of Neuroscience · doi:10.1523/jneurosci.2737-14.2015 · Cited by 246 · see citing works
The hypothalamic-pituitary-adrenal axis in PTSD: Pathophysiology and treatment interventions
Dunlop, B. W., & Wong, A. (2018) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2018.10.010 · Cited by 245 · see citing works
Hill, M. N., Campolongo, P., Yehuda, R., & Patel, S. (2017) · Neuropsychopharmacology · doi:10.1038/npp.2017.162 · Cited by 239 · see citing works
Self-citationHauer, D., Schelling, G., Gola, H., Campolongo, P., Morath, J., Roozendaal, B., Hamuni, G., Karabatsiakis, A., Atsak, P., Vogeser, M., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0062741 · Cited by 200 · see citing works
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Micale, V., & Drago, F. (2018) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2018.07.039 · Cited by 189 · see citing works
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Self-citationBeckers, T., & Kindt, M. (2017) · Annual Review of Clinical Psychology · doi:10.1146/annurev-clinpsy-032816-045209 · Cited by 172 · see citing works
McPartland, J. M., Guy, G. W., & Marzo, V. D. (2014) · PLoS ONE · doi:10.1371/journal.pone.0089566 · Cited by 161 · see citing works
Morena, M., Roozendaal, B., Trezza, V., Ratano, P., Peloso, A., Hauer, D., Atsak, P., Trabace, L., Cuomo, V., McGaugh, J. L., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1420285111 · Cited by 146 · see citing works
Self-citationThe endocannabinoid system: An emotional buffer in the modulation of memory function
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Self-citationWolf, O. T., Atsak, P., de Quervain, D. J. ‐., Roozendaal, B., & Wingenfeld, K. (2015) · Journal of Neuroendocrinology · doi:10.1111/jne.12353 · Cited by 97 · see citing works
Self-citationMorena, M., Berardi, A., Colucci, P., Palmery, M., Trezza, V., Hill, M. N., & Campolongo, P. (2017) · Neuropsychopharmacology · doi:10.1038/npp.2017.305 · Cited by 94 · see citing works
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Stockhorst, U., & Antov, M. I. (2016) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2015.00359 · Cited by 86 · see citing works
Atsak, P., Hauer, D., Campolongo, P., Schelling, G., Fornari, R. V., & Roozendaal, B. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.334 · Cited by 85 · see citing works
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Self-citationMorena, M., Castro, V. D., Gray, J. M., Palmery, M., Trezza, V., Roozendaal, B., Hill, M. N., & Campolongo, P. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.1983-15.2015 · Cited by 70 · see citing works
Self-citationCampolongo, P., Morena, M., Scaccianoce, S., Trezza, V., Chiarotti, F., Schelling, G., Cuomo, V., & Roozendaal, B. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2013.26 · Cited by 68 · see citing works
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THOMAS, S. A. (2014) · Hippocampus · doi:10.1002/hipo.22394 · Cited by 63 · see citing works
Pedraza, L. K., Sierra, R. O., Boos, F. Z., Haubrich, J., Quillfeldt, J. A., & Alvares, L. D. O. (2015) · Hippocampus · doi:10.1002/hipo.22527 · Cited by 62 · see citing works
Micale, V., Stepan, J., Jurik, A., Pamplona, F. A., Marsch, R., Drago, F., Eder, M., & Wotjak, C. T. (2017) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2017.02.002 · Cited by 62 · see citing works
Zhong, F., Liu, L., Wei, J., Hu, Z., Li, L., Wang, S., Xu, J., Zhou, X., Li, C.-Q., Yang, Z., et al. (2019) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2018.00776 · Cited by 61 · see citing works
Corrêa, M. D. S., Vaz, B. D. S., Grisanti, G. D. V., de Paiva, J. P. Q., Tiba, P. A., & Fornari, R. V. (2019) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2019.104447 · Cited by 59 · see citing works
Short and Long-Term Effects of Cannabis on Symptoms of Post-Traumatic Stress Disorder
LaFrance, E. M., Glodosky, N. C., Bonn‐Miller, M. O., & Cuttler, C. (2020) · Journal of Affective Disorders · doi:10.1016/j.jad.2020.05.132 · Cited by 59 · see citing works
The Endocannabinoid System and Anxiety
Lisboa, S. F. D. S., Gomes, F. V., Terzian, A. L. B., de Aguiar, D. C., Moreira, F. A., Resstel, L. B. M., & Guimarães, F. S. (2016) · Vitamins and hormones · doi:10.1016/bs.vh.2016.09.006 · Cited by 56 · see citing works
Kotler, S., Mannino, M., Kelso, S., & Huskey, R. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104956 · Cited by 52 · see citing works
Glucocorticoids mediate stress-induced impairment of retrieval of stimulus-response memory
Atsak, P., Guenzel, F. M., Kantar, D., Zalachoras, I., Yargıçoğlu, P., Meijer, O. C., Quirarte, G. L., Wolf, O. T., Schwabe, L., & Roozendaal, B. (2016) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2016.02.006 · Cited by 52 · see citing works
Self-citationIntegrating endocannabinoid signaling in the regulation of anxiety and depression
Yin, A., Wang, F., & Zhang, X. (2018) · Acta Pharmacologica Sinica · doi:10.1038/s41401-018-0051-5 · Cited by 52 · see citing works
Yi, B., Ничипорук, И. А., Nicolas, M., Schneider, S., Feuerecker, M., Vassilieva, G. Y., Thieme, D., Schelling, G., & Choukèr, A. (2016) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2016.01.004 · Cited by 51 · see citing works
Self-citationHauer, D., Kaufmann, I., Strewe, C., Briegel, I., Campolongo, P., & Schelling, G. (2013) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2013.10.003 · Cited by 49 · see citing works
Self-citationde Oliveira, A. R., Reimer, A. E., Reis, F. M., & Brandão, M. L. (2012) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2012.05.007 · Cited by 44 · see citing works
Gould, G. G., Burke, T. F., Osorio, M. D., Smolik, C. M., Zhang, W. Q., Onaivi, E. S., Gu, T.-T., DeSilva, M., & Hensler, J. G. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.09.003 · Cited by 43 · see citing works
Papini, S., Sullivan, G. M., Hien, D. A., Shvil, E., & Neria, Y. (2014) · Biological Psychology · doi:10.1016/j.biopsycho.2014.10.010 · Cited by 37 · see citing works
Kruk-Słomka, M., & Biała, G. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.12.023 · Cited by 37 · see citing works
Drug discovery strategies that focus on the endocannabinoid signaling system in psychiatric disease
Wyrofsky, R. R., McGonigle, P., & Bockstaele, E. J. V. (2014) · Expert Opinion on Drug Discovery · doi:10.1517/17460441.2014.966680 · Cited by 35 · see citing works
The role of the cannabinoid system in fear memory and extinction in male and female mice
Mizuno, I., Matsuda, S., Tohyama, S., & Mizutani, A. (2022) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2022.105688 · Cited by 35 · see citing works
Effects of rTMS on Hippocampal Endocannabinoids and Depressive-like Behaviors in Adolescent Rats
Fang, G., & Wang, Y. (2018) · Neurochemical Research · doi:10.1007/s11064-018-2591-y · Cited by 34 · see citing works
Giachero, M., Bustos, S. G., Calfa, G. D., & Molina, V. A. (2013) · Learning & Memory · doi:10.1101/lm.029306.112 · Cited by 34 · see citing works
Hauer, D., Weis, F., Campolongo, P., Schopp, M., Beiras-Fernandez, A., Strewe, C., Giehl, M., Toth, R., Kilger, E., & Schelling, G. (2012) · Reviews in the Neurosciences · doi:10.1515/revneuro-2012-0058 · Cited by 33 · see citing works
Self-citationMemory Under Stress: From Adaptation to Disorder
Schwabe, L. (2024) · Biological Psychiatry · doi:10.1016/j.biopsych.2024.06.005 · Cited by 33 · see citing works
Aisenberg, N., Serova, L. I., Sabban, E. L., & Akirav, I. (2017) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2017.06.006 · Cited by 33 · see citing works
Shoshan, N., & Akirav, I. (2017) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2017.08.004 · Cited by 32 · see citing works
Translation of animal endocannabinoid models of PTSD mechanisms to humans: Where to next?
Ney, L. J., Crombie, K. M., Mayo, L. M., Felmingham, K. L., Bowser, T. A., & Matthews, A. J. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.11.040 · Cited by 30 · see citing works
The neuroendocrine impact of acute stress on synaptic plasticity
dos-Santos, R. C., Sweeten, B. L. W., Stelly, C. E., & Tasker, J. G. (2023) · Endocrinology · doi:10.1210/endocr/bqad149 · Cited by 29 · see citing works
Malcher‐Lopes, R. (2014) · Revista da Biologia · doi:10.7594/revbio.13.01.07 · Cited by 29 · see citing works
Niloy, N., Hediyal, T. A., Vichitra, C., Sharma, S., Chidambaram, S. B., Gorantla, V. R., & Mahalakshmi, A. M. (2023) · Biomolecules · doi:10.3390/biom13010162 · Cited by 28 · see citing works
Photobiomodulation prevents PTSD-like memory impairments in rats
Li, Y., Dong, Y., Yang, L., Tucker, L. D., Zong, X., Brann, D. W., Hamblin, M. R., Vazdarjanova, A. I., & Zhang, Q. (2021) · Molecular Psychiatry · doi:10.1038/s41380-021-01088-z · Cited by 28 · see citing works
Yoshida, M., Takayanagi, Y., & Onaka, T. (2014) · Endocrinology · doi:10.1210/en.2013-1411 · Cited by 27 · see citing works
Segev, A., & Akirav, I. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.238 · Cited by 26 · see citing works
Reis, F. M., Almada, R. C., Fogaça, M. V., & Brandão, M. L. (2015) · Cerebral Cortex · doi:10.1093/cercor/bhv103 · Cited by 26 · see citing works
Fattore, L., Piva, A., Zanda, M. T., Fumagalli, G. F., & Chiamulera, C. (2017) · Psychopharmacology · doi:10.1007/s00213-017-4793-4 · Cited by 26 · see citing works
Longaretti, A., Forastieri, C., Gabaglio, M., Rubino, T., Battaglioli, E., & Rusconi, F. (2020) · Journal of Neurochemistry · doi:10.1111/jnc.15000 · Cited by 25 · see citing works
Barsegyan, A., Atsak, P., Hornberger, W., Jacobson, P. B., van Gaalen, M. M., & Roozendaal, B. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.48 · Cited by 25 · see citing works
Self-citationFeltes, P. K., de Vries, E. F. J., Juárez‐Orozco, L. E., Kurtys, E., Dierckx, R., Jeckel, C. M. M., & Doorduin, J. (2017) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x17747189 · Cited by 24 · see citing works
Joëls, M., Karst, H., & Tasker, J. G. (2024) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2024.101146 · Cited by 23 · see citing works
Medical cannabis for treatment-resistant combat PTSD
Nacasch, N., Avni, C., & Toren, P. (2023) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2022.1014630 · Cited by 23 · see citing works
Corticosteroid–endocannabinoid loop supports decrease of fear-conditioned response in rats
de Bitencourt, R. M., Pamplona, F. A., & Takahashi, R. N. (2014) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2014.01.010 · Cited by 23 · see citing works
Deng, L., Lee, W.-H., Xu, Z., Makriyannis, A., & Hohmann, A. G. (2016) · Pharmacological Research · doi:10.1016/j.phrs.2016.10.007 · Cited by 23 · see citing works
Atsak, P., Morena, M., Schoenmaker, C., Tabak, E., Oomen, C. A., Jamil, S., Hill, M. N., & Roozendaal, B. (2018) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2018.02.021 · Cited by 22 · see citing works
Self-citationAnandamide modulation of circadian- and stress-dependent effects on rat short-term memory
Santori, A., Colucci, P., Mancini, G. F., Morena, M., Palmery, M., Trezza, V., Puglisi‐Allegra, S., Hill, M. N., & Campolongo, P. (2019) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2019.06.018 · Cited by 22 · see citing works
Self-citationSink, K. S., Davis, M., & Walker, D. L. (2013) · Learning & Memory · doi:10.1101/lm.032482.113 · Cited by 22 · see citing works
Liu, X.-H., Zhu, R., Hao, B., Shi, Y., Wang, X., Xue, L., & Zhao, H. (2019) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2019.00043 · Cited by 21 · see citing works
An endocannabinoid receptor polymorphism modulates affective processing under stress
Wirz, L., Reuter, M., Felten, A., & Schwabe, L. (2018) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsy083 · Cited by 21 · see citing works
How do stupendous cannabinoids modulate memory processing via affecting neurotransmitter systems?
Vaseghi, S., Nasehi, M., & Zarrindast, M. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.10.018 · Cited by 21 · see citing works
Chu, S., Zhang, Z., Zhou, X., He, W., Yang, B., Cui, L., He, H.-Y., Wang, Z., & Chen, N. (2020) · Acta Pharmacologica Sinica · doi:10.1038/s41401-020-00536-w · Cited by 20 · see citing works
Endocannabinoid regulation of hippocampus-dependent memory
Figueiredo, A. M. P. D., & Cheer, J. F. (2023) · Experimental Neurology · doi:10.1016/j.expneurol.2023.114384 · Cited by 20 · see citing works
Basolateral amygdala GABA-A receptors mediate stress-induced memory retrieval impairment in rats
Sardari, M., Rezayof, A., Khodagholi, F., & Zarrindast, M. (2013) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145713001363 · Cited by 20 · see citing works
Santori, A., Morena, M., Hill, M. N., & Campolongo, P. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21197316 · Cited by 16 · see citing works
Self-citationIn it together? The case for endocannabinoid–noradrenergic interactions in fear extinction
Warren, W. G., Papagianni, E. P., Stevenson, C. W., & Stubbendorff, C. (2021) · European Journal of Neuroscience · doi:10.1111/ejn.15200 · Cited by 16 · see citing works
Omoumi, S., Rashidy‐Pour, A., Seyedinia, S. A., Tarahomi, P., Vafaei, A. A., & Raise‐Abdullahi, P. (2023) · Physiology & Behavior · doi:10.1016/j.physbeh.2023.114156 · Cited by 16 · see citing works
Propranolol can induce PTSD ‐like memory impairments in rats
Zhu, R., Liu, X., Shi, Y., Wang, X., Xue, L., & Zhao, H. (2018) · Brain and Behavior · doi:10.1002/brb3.905 · Cited by 16 · see citing works
Singh, M., Agarwal, V., Jindal, D., Pancham, P., Agarwal, S., Mani, S., Tiwari, R. K., Das, K., Alghamdi, B. S. A., Abujamel, T. S., et al. (2023) · Diagnostics · doi:10.3390/diagnostics13030337 · Cited by 15 · see citing works
Circadian regulation of memory under stress: Endocannabinoids matter
Morena, M., Santori, A., & Campolongo, P. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104712 · Cited by 14 · see citing works
Self-citationHuzard, D., Vouros, A., Monari, S., Astori, S., Vasilaki, E., & Sandi, C. (2019) · Stress · doi:10.1080/10253890.2019.1625885 · Cited by 14 · see citing works
Wang, H., Xing, X., Liang, J., Bai, Y.-J., Lui, Z., & Zheng, X.-G. (2014) · Pharmacology, Biochemistry and Behavior · doi:10.1016/j.pbb.2014.06.003 · Cited by 12 · see citing works
Li, Y., Zhi, W.-J., Qi, B., Wang, L.-F., & Hu, X. (2023) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2023.1216524 · Cited by 10 · see citing works
Habenula orphan G-protein coupled receptors in the pathophysiology of fear and anxiety
Roy, N., & Parhar, I. S. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.11.008 · Cited by 11 · see citing works
Multiplexed membrane signaling by glucocorticoids
Harrison, L. M., & Tasker, J. G. (2022) · Current Opinion in Endocrine and Metabolic Research · doi:10.1016/j.coemr.2022.100390 · Cited by 11 · see citing works
de Bitencourt, R. M., Alpár, A., Cinquina, V., Ferreira, S. G., Pinheiro, B. S., Lemos, C., Ledent, C. A., Takahashi, R. N., Sialana, F. J., Lübec, G., et al. (2015) · Neurochemistry International · doi:10.1016/j.neuint.2015.07.014 · Cited by 11 · see citing works
Targeting the endocannabinoid system to treat haunting traumatic memories
Akirav, I. (2013) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2013.00124 · Cited by 11 · see citing works
Genetic stress-reactivity, sex, and conditioning intensity affect stress-enhanced fear learning
Przybyl, K. J., Jenz, S. T., Lim, P. H., Ji, M. T., Wert, S. L., Luo, W., Gacek, S. A., Schaack, A. K., & Redei, E. E. (2021) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2021.107523 · Cited by 11 · see citing works
Yu, J. Q., Ren, L., Su, M., Lv, F., Luo, J., Li, P., & Zhang, Y. (2021) · Psychiatry Research · doi:10.1016/j.psychres.2021.113917 · Cited by 10 · see citing works
Chu, L., Zheng, S., Gu, X., Wu, Y., Yang, J., & Deng, H. (2023) · Cannabis and Cannabinoid Research · doi:10.1089/can.2022.0267 · Cited by 10 · see citing works
Scienza-Martin, K., Lotz, F. N., Zanona, Q. K., Santana, F., Crestani, A. P., Boos, F. Z., Calcagnotto, M. E., & Quillfeldt, J. A. (2022) · Neuroscience · doi:10.1016/j.neuroscience.2022.04.009 · Cited by 10 · see citing works
Nasehi, M., Shahbazzadeh, S., Ebrahimi-Ghiri, M., & Zarrindast, M. (2018) · Journal of Psychopharmacology · doi:10.1177/0269881118760654 · Cited by 9 · see citing works
Dai, Z., Xu, X., Chen, W., Nie, L.-N., Liu, Y., Sui, N., & Liang, J. (2022) · Current Addiction Reports · doi:10.1007/s40429-022-00407-w · Cited by 8 · see citing works
- Authors
- Atsak, P., Hauer, D., Campolongo, P., Schelling, G., McGaugh, J. L., & Roozendaal, B.
- Affiliations
- University Medical Center Groningen (NL)
- Sapienza University of Rome (IT)
- Ludwig-Maximilians-Universität München (DE)
- University of California, Irvine (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2012-02-13
- Volume
- 109
- Issue
- 9
- Pages
- 3504-3509
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3295257
- OpenAlex
- W2147317037
- Cited by
- 140
- References
- 64
- Citations by year
- 2026: 3 · 2025: 6 · 2024: 8 · 2023: 11 · 2022: 8 · 2021: 7 · 2020: 7 · 2019: 9 · 2018: 9 · 2017: 13 · 2016: 12 · 2015: 16 · 2014: 14 · 2013: 11 · 2012: 5
- FWCI
- 7.54
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (publishedVersion)
- IRIS Research product catalog (Sapienza University of Rome) (submittedVersion)
- Radboud Repository (Radboud University) (submittedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Health Sciences › Medicine › Pharmacology › Cannabis and Cannabinoid Research
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- glucocorticoids, endocannabinoid system, hippocampus, contextual fear memory, corticosterone, CB1 receptor, 2-arachidonoylglycerol, noradrenergic activity, propranolol, beta-adrenoceptor antagonism, WIN 55,212-2, emotional arousal, retrograde signaling
- MeSH terms
- Acoustic Stimulation, Adrenergic beta-Antagonists, Animals, Arachidonic Acids, Arousal, Conditioning, Classical, Corticosterone, Electroshock, Emotions, Fear, Glucocorticoids, Glycerides, Hippocampus, Male, Memory, Morpholines, Naphthalenes, Piperidines, Propranolol, Pyrazoles, Receptors, Glucocorticoid, Rats, Sprague-Dawley, Receptor, Cannabinoid, CB1, Freezing Reaction, Cataleptic, Benzoxazines, Rats, Cannabinoid Receptor Modulators, Endocannabinoids
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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.
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