Downregulation of Endocannabinoid Signaling in the Hippocampus Following Chronic Unpredictable Stress

Hill, Matthew N; Patel, Sachin; Carrier, Erica J; Rademacher, David J; Ormerod, Brandi K; Hillard, Cecilia J; Gorzalka, Boris B

doi:10.1038/sj.npp.1300601

Cited by 363Cannabis and Cannabinoid ResearchStress Responses and CortisolMemory and Neural Mechanisms

Downregulation of Endocannabinoid Signaling in the Hippocampus Following Chronic Unpredictable Stress

Hill, Matthew N, Patel, Sachin, Carrier, Erica J, Rademacher, David J, Ormerod, Brandi K, Hillard, Cecilia J, Gorzalka, Boris B·2005·Neuropsychopharmacology

DOI 10.1038/sj.npp.1300601

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Abstract

Deficits in cognitive functioning and flexibility are seen following both chronic stress and modulation of endogenous cannabinoid (eCB) signaling. Here, we investigated whether alterations in eCB signaling might contribute to the cognitive impairments induced by chronic stress. Chronic stress impaired reversal learning and induced perseveratory behavior in the Morris water maze without significant effect on task acquisition. These cognitive impairments were reversed by exogenous cannabinoid administration, suggesting deficient eCB signaling underlies these phenomena. In line with this hypothesis, chronic stress downregulated CB1 receptor expression and significantly reduced the content of the endocannabinoid 2-arachidonylglycerol within the hippocampus. CB1 receptor density and 2-arachidonylglycerol content were unaffected in the limbic forebrain. These data suggest that stress-induced downregulation of hippocampal eCB signaling contributes to problems in behavioral flexibility and could play a role in the development of perseveratory and ruminatory behaviors in stress-related neuropsychiatric disorders.

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Animal studies have shown that chronic stress is associated with decreased brain levels of the endocannabinoid anandamide and CB1 receptor adaptations.
“Animal studies17 have shown that chronic stress is associated with decreased brain levels of the endocannabinoid anandamide and CB1 receptor adaptations17–19”
From Elevated brain cannabinoid CB1 receptor availability in post-traumatic stress disorder: A positron emission tomography study (2013) · cites this paper as [17]
Chronic unpredictable stressors impair 2-AG signaling.
“chronic unpredictable stressors have been shown to impair 2-AG signaling (Hill et al., 2005; Zhang et al., 2015)”
From The endocannabinoid system as a target for novel anxiolytic drugs (2017) · cites this paper as Hill et al., 2005

Isolation and Structure of a Brain Constituent That Binds to the Cannabinoid Receptor
Devane, W. A., Hanuš, L., Breuer, A., Pertwee, R. G., Stevenson, L. A., Griffin, G., Gibson, D., Mandelbaum, A., Etinger, A., & Mechoulam, R. (1992) · Science · doi:10.1126/science.1470919 · Cited by 5,633 · see citing works
2-Arachidonoylgylcerol: A Possible Endogenous Cannabinoid Receptor Ligand in Brain
Sugiura, T., Kondo, S., Sukagawa, A., Nakane, S., Shinoda, A., Itoh, K., Yamashita, A., & Waku, K. (1995) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1995.2437 · Cited by 2,196 · see citing works
Characterization and localization of cannabinoid receptors in rat brain: a quantitative in vitro autoradiographic study
Herkenham, M., Lynn, A., Johnson, M., Melvin, L., de Costa, B., & Rice, K. (1991) · The Journal of Neuroscience · doi:10.1523/jneurosci.11-02-00563.1991 · Cited by 2,159 · see citing works
The prefontral cortex and cognitive control
Miller, E. K. (2000) · Nature Reviews Neuroscience · doi:10.1038/35036228 · Cited by 2,016 · see citing works
Validity, reliability and utility of the chronic mild stress model of depression: a 10-year review and evaluation
Willner, P. (1997) · Psychopharmacology · doi:10.1007/s002130050456 · Cited by 1,832 · see citing works
The endogenous cannabinoid system controls extinction of aversive memories
Marsicano, G., Wotjak, C. T., Azad, S. C., Bisogno, T., Rammes, G., Cascio, M. G., Hermann, H., Tang, J., Hofmann, C., Zieglgänsberger, W., et al. (2002) · Nature · doi:10.1038/nature00839 · Cited by 1,728 · see citing works
Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons
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
Leptin-regulated endocannabinoids are involved in maintaining food intake
Di Marzo, V., Goparaju, S. K., Wang, L., Liu, J., Bátkai, S., Járai, Z., Fezza, F., Miura, G. I., Palmiter, R. D., Sugiura, T., et al. (2001) · Nature · doi:10.1038/35071088 · Cited by 1,559 · see citing works
A second endogenous cannabinoid that modulates long-term potentiation
Stella, N., Schweitzer, P., & Piomelli, D. (1997) · Nature · doi:10.1038/42015 · Cited by 1,496 · see citing works
Organization of the stress system and its dysregulation in melancholic and atypical depression: high vs low CRH/NE states
Gold, P. W., & Chrousos, G. P. (2002) · Molecular Psychiatry · doi:10.1038/sj.mp.4001032 · Cited by 1,274 · see citing works
Presynaptically Located CB1 Cannabinoid Receptors Regulate GABA Release from Axon Terminals of Specific Hippocampal Interneurons
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
Mood disorders and allostatic load
McEwen, B. S. (2003) · Biological Psychiatry · doi:10.1016/s0006-3223(03)00177-x · Cited by 1,135 · see citing works
Plasticity of the Hippocampus: Adaptation to Chronic Stress and Allostatic Load
McEwen, B. S. (2001) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2001.tb05830.x · Cited by 875 · see citing works
Repeated stress causes reversible impairments of spatial memory performance.
Luine, V., Villegas, M., Martinez, C., & McEwen, B. (1994) · Brain Research · doi:10.1016/0006-8993(94)91778-7 · Cited by 813 · see citing works
Nongenomic Glucocorticoid Inhibition via Endocannabinoid Release in the Hypothalamus: A Fast Feedback Mechanism
Di, S., Malcher‐Lopes, R., Halmos, K. C., & Tasker, J. G. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-12-04850.2003 · Cited by 801 · see citing works
Cognitive Functioning of Long-term Heavy Cannabis Users Seeking Treatment
Solowij, N. (2002) · JAMA · doi:10.1001/jama.287.9.1123 · Cited by 798 · see citing works
Regulation of Serotonin1A, Glucocorticoid, and Mineralocorticoid Receptor in Rat and Human Hippocampus: Implications for the Neurobiology of Depression
López, J. F., Chalmers, D. T., Little, K. Y., & Watson, S. J. (1998) · Biological Psychiatry · doi:10.1016/s0006-3223(97)00484-8 · Cited by 700 · see citing works
Neuropsychological Performance in Long-term Cannabis Users
Pope, H. G., Gruber, A. J., Hudson, J. I., Huestis, M. A., & Yurgelun-Todd, D. A. (2001) · Archives of General Psychiatry · doi:10.1001/archpsyc.58.10.909 · Cited by 647 · see citing works
Sex differences in dendritic atrophy of CA3 pyramidal neurons in response to chronic restraint stress
Galea, L. A. M., McEwen, B. S., Tanapat, P., Deak, T., Spencer, R. L., & Dhabhar, F. S. (1997) · Neuroscience · doi:10.1016/s0306-4522(97)00233-9 · Cited by 540 · see citing works
Involvement of CB1 cannabinoid receptors in emotional behaviour
Martín, M., Ledent, C. A., Parmentier, M., Maldonado, R. J., & Valverde, O. (2002) · Psychopharmacology · doi:10.1007/s00213-001-0946-5 · Cited by 507 · see citing works
Chronic Stress Induces Impairment of Spatial Working Memory Because of Prefrontal Dopaminergic Dysfunction
Mizoguchi, K., Yuzurihara, M., Ishige, A., Sasaki, H., Chui, D.-H., & Tabira, T. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-04-01568.2000 · Cited by 481 · see citing works
Stress Effects on Morphology and Function of the Hippocampusa
McEwen, B. S., & Magariños, A. M. (1997) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1997.tb48286.x · Cited by 393 · see citing works
Endocannabinoids facilitate the induction of LTP in the hippocampus
Carlson, G. C., Wang, Y., & Alger, B. E. (2002) · Nature Neuroscience · doi:10.1038/nn879 · Cited by 336 · see citing works
Effects of chronic stress on hippocampal long‐term potentiation
Pavlides, C., Nivón, L. G., & McEwen, B. S. (2002) · Hippocampus · doi:10.1002/hipo.1116 · Cited by 316 · see citing works
Behavioral Effects of Cannabinoid Agents in Animals
Chaperon, F., & Thiébot, M.-H. (1999) · Critical Reviews in Neurobiology · doi:10.1615/critrevneurobiol.v13.i3.20 · Cited by 311 · see citing works
Improvement of memory in rodents by the selective CB1 cannabinoid receptor antagonist, SR 141716
Terranova, J.-P., Storme, J.-J., Lafon, N., Perio, A., Rinaldi, M. L., Fur, G. L., & Soubrié, P. (1996) · Psychopharmacology · doi:10.1007/bf02246352 · Cited by 283 · see citing works
Chronic ▵ 9 ‐Tetrahydrocannabinol Treatment Produces a Time‐Dependent Loss of Cannabinoid Receptors and Cannabinoid Receptor‐Activated G Proteins in Rat Brain
Breivogel, C. S., Childers, S. R., Deadwyler, S. A., Hampson, R. E., Vogt, L. J., & Sim‐Selley, L. J. (1999) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1999.0732447.x · Cited by 273 · see citing works
Chronic unpredictable stress impairs long‐term potentiation in rat hippocampal CA1 area and dentate gyrus <i>in vitro</i>
Alfarez, D. N., Joëls, M., & Krugers, H. J. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02622.x · Cited by 258 · see citing works
Evaluation of CB1 Receptor Knockout Mice in the Morris Water Maze
Varvel, S. A., & Lichtman, A. H. (2002) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.301.3.915 · Cited by 245 · see citing works
Cannabinoids, hippocampal function and memory
Hampson, R. E., & Deadwyler, S. A. (1999) · Life Sciences · doi:10.1016/s0024-3205(99)00294-5 · Cited by 221 · see citing works
Pilot controlled trial of d-serine for the treatment of post-traumatic stress disorder
Heresco‐Levy, U., Vass, Á., Bloch, B., Wolosker, H., Dumin, E., Balan, L., Deutsch, L., & Kremer, I. (2009) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145709000339 · Cited by 171 · see citing works
Synergistic interactions between cannabinoids and environmental stress in the activation of the central amygdala
Patel, S., Cravatt, B. F., & Hillard, C. J. (2005) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300535 · Cited by 164 · see citing works
Self-citation
Differential Regulation of the Endocannabinoids Anandamide and 2-Arachidonylglycerol within the Limbic Forebrain by Dopamine Receptor Activity
Patel, S., Rademacher, D. J., & Hillard, C. J. (2003) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.103.054270 · Cited by 153 · see citing works
Self-citation
Stress-induced disturbances in Morris water-maze performance: Interstrain variability
Francis, D. D. (1995) · Physiology & Behavior · doi:10.1016/0031-9384(95)00009-8 · Cited by 148 · see citing works
Endocannabinoids in cognition and dependence
Lichtman, A. H., Varvel, S. A., & Martin, B. R. (2002) · Prostaglandins Leukotrienes and Essential Fatty Acids · doi:10.1054/plef.2001.0351 · Cited by 135 · see citing works
Pilot-controlled trial of D-cycloserine for the treatment of post-traumatic stress disorder
Heresco-Levy, U., Kremer, I., Javitt, D. C., Goichman, R., Reshef, A., Blanaru, M., & Cohen, T. (2002) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145702003061 · Cited by 134 · cited 1× · see citing works
“…stress disorder and depression, are characterized by problems with forgetting and behavioral flexibility that are manifested as pathological tendencies to ruminate or perseverate on negative information (Bagby et al, 1999; Gold and Chrousos, 2002; Heresco-Levy et al, 2002; King, 2002).”
Background
Down-regulation of cannabinoid-1 (CB-1) receptors in specific extrahypothalamic regions of rats with dietary obesity: a role for endogenous cannabinoids in driving appetite for palatable food?
Harrold, J. A., Elliott, J. C., King, P., Widdowson, P. S., & Williams, G. (2002) · Brain Research · doi:10.1016/s0006-8993(02)03245-6 · Cited by 130 · see citing works
Effect of Chronic Administration of R-(+)-[2,3-Dihydro-5-methyl-3-[(morpholinyl)methyl]pyrrolo[1,2,3-de]-1,4-benzoxazinyl]-(1-naphthalenyl)methanone Mesylate (WIN55,212-2) or Δ9-Tetrahydrocannabinol on Cannabinoid Receptor Adaptation in Mice
Sim‐Selley, L. J., & Martin, B. R. (2002) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.102.035618 · Cited by 125 · see citing works
Neurochemical and Behavioral Alterations in Glucocorticoid Receptor-Impaired Transgenic Mice after Chronic Mild Stress
Froger, N., Palazzo, E., Boni, C., Hanoun, N., Saurini, F., Joubert, C., Dutriez-Casteloot, I., Enache, M., Maccari, S., Barden, N., et al. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.4132-03.2004 · Cited by 122 · see citing works
Role of Cannabinoid Receptors in Memory Storage
Hampson, R. E., & Deadwyler, S. A. (1998) · Neurobiology of Disease · doi:10.1006/nbdi.1998.0223 · Cited by 119 · see citing works
Enhancement of anxiety-like responsiveness to the cannabinoid CB1 receptor agonist HU-210 following chronic stress
Hill, M. N., & Gorzalka, B. B. (2004) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2004.06.069 · Cited by 114 · see citing works
Self-citation
Alcohol‐Induced Changes in Pituitary‐Adrenal Activity during Pregnancy
Weinberg, J., & Bezio, S. (1987) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.1987.tb01307.x · Cited by 102 · see citing works
Changes in rat brain cannabinoid binding sites after acute or chronic exposure to their endogenous agonist, anandamide, or to δ9-tetrahydrocannabinol
Romero, J., García‐García, L., Fernández‐Ruíz, J., Cebeira, M., & Ramos, J. A. (1995) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(95)00023-p · Cited by 101 · see citing works
Functional expression of cell surface cannabinoid CB1 receptors on presynaptic inhibitory terminals in cultured rat hippocampal neurons
Irving, A. J., Coutts, A. A., Harvey, J., Rae, M. G., Mackie, K., Bewick, G. S., & Pertwee, R. G. (2000) · Neuroscience · doi:10.1016/s0306-4522(00)00120-2 · Cited by 96 · see citing works
SHORT COMMUNICATION Selective enhancement of spatial learning under chronic psychosocial stress
Bartolomucci, A., de Biurrun, G., Czéh, B., van Kampen, M., & Fuchs, E. (2002) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2002.02043.x · Cited by 95 · see citing works
Spatial learning impairment induced by chronic stress is related to individual differences in novelty reactivity: search for neurobiological correlates
Touyarot, K., Venero, C., & Sandi, C. (2003) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(03)00031-3 · Cited by 94 · see citing works
Brain monoamine receptors in a chronic unpredictable stress model in rats
Ossowska, G., Nowak, G., Kata, R., Klenk-Majewska, B., Danilczuk, Z., & Żebrowska-Łupina, I. (2001) · Journal of Neural Transmission · doi:10.1007/s007020170077 · Cited by 76 · see citing works
Effect of chronic stress on spatial memory in rats is attenuated by lithium treatment
de Vasconcellos, A. P. S., Tabajara, Â. S., Ferrari, C., Rocha, E., & Dalmaz, C. (2003) · Physiology & Behavior · doi:10.1016/s0031-9384(03)00113-6 · Cited by 75 · see citing works
Rumination and distraction in major depression: assessing response to pharmacological treatment
Bagby, R. M., Rector, N. A., Segal, Z. V., Joffe, R. T., LEVITT, A. J., Kennedy, S. H., & Levitan, R. D. (1999) · Journal of Affective Disorders · doi:10.1016/s0165-0327(99)00015-4 · Cited by 58 · see citing works
Melatonin protects against the effects of chronic stress on sexual behaviour in male rats
Brotto, L. A., Gorzalka, B. B., & LaMarre, A. K. (2001) · Neuroreport · doi:10.1097/00001756-200111160-00018 · Cited by 56 · see citing works
Self-citation
Glucocorticoid regulation of cannabinoid receptor messenger RNA levels in the rat caudate-putamen. An in situ hybridization study
Mailleux, P., & Vanderhaeghen, J. (1993) · Neuroscience Letters · doi:10.1016/0304-3940(93)90437-p · Cited by 48 · see citing works
Perseveration of traumatic re-experiencing in PTSD; a cautionary note regarding exposure based psychological treatments for PTSD when head injury and dysexecutive impairment are also present
King, N. S. (2002) · Brain Injury · doi:10.1080/02699050110088263 · Cited by 20 · see citing works
Interaction between estradiol replacement and chronic stress on feeding behavior and on serum leptin
Gamaro, G. D., Prediger, M. E., Lopes, J. B., & Dalmaz, C. (2003) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2003.08.002 · Cited by 18 · see citing works
Untitled work
(1996) · doi:10.1002/(sici)1096-9861(19960520)369:1
Stress induces Fos expression in neurons of the thalamic paraventricular nucleus that innervate limbic forebrain sites
Bubser, M., & Deutch, A. Y. (1999) · Synapse · doi:10.1002/(sici)1098-2396(199904)32:1

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Pacher, P., Bátkai, S., & Kunos, G. (2006) · Pharmacological Reviews · doi:10.1124/pr.58.3.2 · Cited by 2,077 · see citing works
Chronic Mild Stress (CMS) Revisited: Consistency and Behavioural-Neurobiological Concordance in the Effects of CMS
Willner, P. (2005) · Neuropsychobiology · doi:10.1159/000087097 · Cited by 1,605 · see citing works
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McEwen, B. S., Bowles, N. P., Gray, J. D., Hill, M. N., Hunter, R. G., Karatsoreos, I. N., & Nasca, C. (2015) · Nature Neuroscience · doi:10.1038/nn.4086 · Cited by 1,386 · see citing works
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Onaivi, E. S., Ishiguro, H., GONG, J., Sejal, P., Perchuk, A., Meozzi, P. A., MYERS, L., Mora, Z., Tagliaferro, P. A., Gardner, E., et al. (2006) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1369.052 · Cited by 546 · see citing works
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Lutz, B., Marsicano, G., Maldonado, R., & Hillard, C. J. (2015) · Nature reviews. Neuroscience · doi:10.1038/nrn4036 · Cited by 506 · see citing works
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Moreira, F. A., & Lutz, B. (2008) · Addiction Biology · doi:10.1111/j.1369-1600.2008.00104.x · Cited by 222 · see citing works
Understanding resilience: New approaches for preventing and treating PTSD
Horn, S. R. G.-V., Charney, D. S., & Feder, A. (2016) · Experimental Neurology · doi:10.1016/j.expneurol.2016.07.002 · Cited by 223 · see citing works
The impact of chronic stress on the rat brain lipidome
Oliveira, T. G., Chan, R., Bravo, F. V., Miranda, A. M., Caridade-Silva, R., Zhou, B., Marques, F., Pinto, V., Cerqueira, J., Paolo, G. D., et al. (2015) · Molecular Psychiatry · doi:10.1038/mp.2015.14 · Cited by 219 · see citing works
Regulation of endocannabinoid signaling by stress: Implications for stress-related affective disorders
Gorzalka, B. B., Hill, M. N., & Hillard, C. J. (2008) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.03.004 · Cited by 211 · see citing works
Self-citation
The therapeutic potential of drugs that target cannabinoid receptors or modulate the tissue levels or actions of endocannabinoids
Pertwee, R. G. (2005) · The AAPS Journal · doi:10.1208/aapsj070364 · Cited by 204 · see citing works
Cannabis and cognitive dysfunction: Parallels with endophenotypes of schizophrenia?
Solowij, N., & Michie, P. T. (2007) · Journal of Psychiatry and Neuroscience · doi:10.1139/jpn.0705 · Cited by 201 · see citing works
Is there a role for the endocannabinoid system in the etiology and treatment of melancholic depression?
Hill, M. N., & Gorzalka, B. B. (2005) · Behavioural Pharmacology · doi:10.1097/00008877-200509000-00006 · Cited by 193 · see citing works
Self-citation
Neuropsychobiological Evidence for the Functional Presence and Expression of Cannabinoid CB2 Receptors in the Brain
Onaivi, E. S. (2006) · Neuropsychobiology · doi:10.1159/000100778 · Cited by 187 · see citing works
Contributions of endocannabinoid signaling to psychiatric disorders in humans: genetic and biochemical evidence
Hillard, C. J., Weinlander, K. M., & Stuhr, K. L. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.11.020 · Cited by 186 · see citing works
Self-citation
Endocannabinoid signalling: has it got rhythm?
Vaughn, L. K., Denning, G., Stuhr, K. L., de Wit, H., Hill, M. N., & Hillard, C. J. (2010) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2010.00790.x · Cited by 176 · see citing works
Self-citation
Enhancement of endocannabinoid signaling with JZL184, an inhibitor of the 2-arachidonoylglycerol hydrolyzing enzyme monoacylglycerol lipase, produces anxiolytic effects under conditions of high environmental aversiveness in rats
Sciolino, N. R., Zhou, W., & Hohmann, A. G. (2011) · Pharmacological Research · doi:10.1016/j.phrs.2011.04.010 · Cited by 179 · see citing works
Prefrontal cortex executive processes affected by stress in health and disease
Girotti, M., Adler, S. M., Bulin, S. E., Fucich, E. A., Paredes, D., & Morilak, D. A. (2018) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2017.07.004 · Cited by 176 · see citing works
The Therapeutic Potential of the Endocannabinoid System for the Development of a Novel Class of Antidepressants
Hill, M. N., Hillard, C. J., Bambico, F. R., Patel, S., Gorzalka, B. B., & Gobbi, G. (2009) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2009.06.006 · Cited by 172 · see citing works
Self-citation
Endocannabinoid system, stress and HPA axis
Micale, V., & Drago, F. (2018) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2018.07.039 · Cited by 189 · see citing works
Role of the endocannabinoid system in regulation of the hypothalamic-pituitary-adrenocortical axis
Steiner, M. S., & Wotjak, C. T. (2008) · Progress in brain research · doi:10.1016/s0079-6123(08)00433-0 · Cited by 167 · see citing works
Adaptations in endocannabinoid signaling in response to repeated homotypic stress: a novel mechanism for stress habituation
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
Self-citation
Antistress Effect of TRPV1 Channel on Synaptic Plasticity and Spatial Memory
Li, H.-B., Mao, R., Zhang, J., Yang, Y., Cao, J., & Xu, L. (2008) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.02.020 · Cited by 160 · see citing works
Care and Feeding of the Endocannabinoid System: A Systematic Review of Potential Clinical Interventions that Upregulate the Endocannabinoid System
McPartland, J. M., Guy, G. W., & Marzo, V. D. (2014) · PLoS ONE · doi:10.1371/journal.pone.0089566 · Cited by 161 · see citing works
Central anandamide deficiency predicts stress-induced anxiety: behavioral reversal through endocannabinoid augmentation
Bluett, R. J., Gamble-George, J. C., Hermanson, D. J., Hartley, N. D., Marnett, L. J., & Patel, S. (2014) · Translational Psychiatry · doi:10.1038/tp.2014.53 · Cited by 157 · see citing works
Self-citation
A role for cannabinoid CB1 receptors in mood and anxiety disorders
Witkin, J. M., Tzavara, E. T., & Nomikos, G. G. (2005) · Behavioural Pharmacology · doi:10.1097/00008877-200509000-00005 · Cited by 156 · see citing works
The endocannabinoid system and psychiatric disorders
Parolaro, D., Realini, N., Viganò, D., Guidali, C., & Rubino, T. (2010) · Experimental Neurology · doi:10.1016/j.expneurol.2010.03.018 · Cited by 150 · see citing works
Genetic Dissection of the Role of Cannabinoid Type-1 Receptors in the Emotional Consequences of Repeated Social Stress in Mice
Dubreucq, S., Matias, I., Cardinal, P., Häring, M., Lutz, B., Marsicano, G., & Chaouloff, F. (2012) · Neuropsychopharmacology · doi:10.1038/npp.2012.36 · Cited by 147 · see citing works
Chronic mild stress paradigm as a rat model of depression: facts, artifacts, and future perspectives
Strekalova, T. V., Liu, Y., Kiselev, D., Khairuddin, S., Chiu, J. L. Y., Lam, J., Chan, Y., Pavlov, D., Proshin, A. T., Lesch, K., et al. (2022) · Psychopharmacology · doi:10.1007/s00213-021-05982-w · Cited by 146 · see citing works
A review of the interactions between alcohol and the endocannabinoid system: Implications for alcohol dependence and future directions for research
Pava, M. J., & Woodward, J. J. (2012) · Alcohol · doi:10.1016/j.alcohol.2012.01.002 · Cited by 145 · see citing works
Therapeutic Potential of Inhibitors of Endocannabinoid Degradation for the Treatment of Stress-Related Hyperalgesia in an Animal Model of Chronic Pain
Lomazzo, E., Bîndilă, L., Remmers, F., Lerner, R., Schwitter, C., Hoheisel, U., & Lutz, B. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.198 · Cited by 141 · see citing works
Endocannabinoids and stress
Riebe, C. J. N., & Wotjak, C. T. (2011) · Stress · doi:10.3109/10253890.2011.586753 · Cited by 144 · see citing works
Endocannabinoid System and Synaptic Plasticity: Implications for Emotional Responses
Viveros, M., Marco, E. M., Llorente, R., & López‐Gallardo, M. (2007) · Neural Plasticity · doi:10.1155/2007/52908 · Cited by 144 · see citing works
Acute restraint stress enhances hippocampal endocannabinoid function via glucocorticoid receptor activation
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
Self-citation
Monoacylglycerol Lipase Inhibition Blocks Chronic Stress-Induced Depressive-Like Behaviors via Activation of mTOR Signaling
Zhong, P., Wang, W., Pan, B., Liu, X., Zhang, Z., Long, J. Z., Zhang, H., Cravatt, B. F., & Liu, Q.-S. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.24 · Cited by 137 · see citing works
Stress regulates endocannabinoid-CB1 receptor signaling
Hillard, C. J. (2014) · Seminars in Immunology · doi:10.1016/j.smim.2014.04.001 · Cited by 136 · see citing works
Self-citation
Endocannabinoid system and psychiatry: in search of a neurobiological basis for detrimental and potential therapeutic effects
Marco, E. M. (2011) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2011.00063 · Cited by 136 · see citing works
Role of the endocannabinoid system in depression and suicide
Vinod, K. Y., & Hungund, B. L. (2006) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2006.08.006 · Cited by 132 · see citing works
A critical role for prefrontocortical endocannabinoid signaling in the regulation of stress and emotional behavior
McLaughlin, R. J., Hill, M. N., & Gorzalka, B. B. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.02.006 · Cited by 130 · see citing works
Self-citation
Endogenous cannabinoid signaling is required for voluntary exercise‐induced enhancement of progenitor cell proliferation in the hippocampus
Hill, M. N., Titterness, A. K., Morrish, A. C., Carrier, E. J., Lee, T. T. ‐., Gil‐Mohapel, J., Gorzalka, B. B., Hillard, C. J., & Christie, B. R. (2009) · Hippocampus · doi:10.1002/hipo.20647 · Cited by 129 · see citing works
Self-citation
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Hill, M. N., Hillard, C. J., & McEwen, B. S. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhq280 · Cited by 127 · see citing works
Self-citation
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Self-citation
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Jowf, G. I. A., Ahmed, Z. T., Reijnders, R. A., de Nijs, L., & Eijssen, L. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24065238 · Cited by 129 · see citing works
Reciprocal changes in vanilloid (TRPV1) and endocannabinoid (CB1) receptors contribute to visceral hyperalgesia in the water avoidance stressed rat
Hong, S. K., Fan, J., Kemmerer, E. S., Evans, S. J., Li, Y., & Wiley, J. W. (2008) · Gut · doi:10.1136/gut.2008.157594 · Cited by 120 · see citing works
Putative role of endocannabinoid signaling in the etiology of depression and actions of antidepressants
Gorzalka, B. B., & Hill, M. N. (2010) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2010.11.021 · Cited by 118 · see citing works
Self-citation
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Hill, M. N., Ho, W. ‐. V., Sinopoli, K. J., Viau, V., Hillard, C. J., & Gorzalka, B. B. (2006) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301092 · Cited by 116 · see citing works
Self-citation
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Mizrahi, R. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.274 · Cited by 115 · see citing works
Effects of chronic stress on cognitive function – From neurobiology to intervention
Girotti, M., Bulin, S. E., & Carreno, F. R. (2024) · Neurobiology of Stress · doi:10.1016/j.ynstr.2024.100670 · Cited by 142 · see citing works
Translational evidence for the involvement of the endocannabinoid system in stress-related psychiatric illnesses
Hill, M. N., & Patel, S. (2013) · Biology of Mood & Anxiety Disorders · doi:10.1186/2045-5380-3-19 · Cited by 117 · see citing works
Self-citation
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Rossi, S., Chiara, V. D., Musella, A., Kusayanagi, H., Mataluni, G., Bernardi, G., Usiello, A., & Centonze, D. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.5346-07.2008 · Cited by 112 · see citing works
An endocannabinoid mechanism in relapse to drug seeking: A review of animal studies and clinical perspectives
Fattore, L., Spano, M. S., Deiana, S., Melis, V., Cossu, G., Fadda, P., & Fratta, W. (2006) · Brain Research Reviews · doi:10.1016/j.brainresrev.2006.05.003 · Cited by 109 · see citing works
Cannabinoids and the Brain
Köfalvi, A. (2007) · Springer eBooks · doi:10.1007/978-0-387-74349-3 · Cited by 110 · see citing works
Neuroendocrine Circuits Governing Energy Balance and Stress Regulation: Functional Overlap and Therapeutic Implications
Ulrich‐Lai, Y. M., & Ryan, K. K. (2014) · Cell Metabolism · doi:10.1016/j.cmet.2014.01.020 · Cited by 108 · see citing works
Endocannabinoid Signaling Collapse Mediates Stress-Induced Amygdalo-Cortical Strengthening
Marcus, D. J., Bedse, G., Gaulden, A. D., Ryan, J. D., Kondev, V., Winters, N. D., Rosas-Vidal, L. E., Altemus, M., Mackie, K., Lee, F. S., et al. (2020) · Neuron · doi:10.1016/j.neuron.2019.12.024 · Cited by 104 · see citing works
Self-citation
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Mizrahi, R., Kenk, M., Suridjan, I., Boileau, I., George, T. P., McKenzie, K., Wilson, A. A., Houle, S., & Rusjan, P. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2013.347 · Cited by 101 · see citing works
The association between cannabis use and anxiety disorders: Results from a population-based representative sample
Feingold, D., Weiser, M., Rehm, J. T., & Lev‐Ran, S. (2015) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2015.12.037 · Cited by 101 · see citing works
Endocannabinoid-Mediated plasticity in nucleus accumbens controls vulnerability to anxiety after social defeat stress
Bosch-Bouju, C., Larrieu, T., Linders, L., Manzoni, O. J., & Layé, S. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.06.082 · Cited by 100 · see citing works
Brain Type 1 Cannabinoid Receptor Availability in Patients with Anorexia and Bulimia Nervosa
Gérard, N., Pieters, G., Goffin, K. E., Bormans, G. M., & Laere, K. V. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.05.010 · Cited by 97 · see citing works
Prolonged glucocorticoid treatment decreases cannabinoid CB 1 receptor density in the hippocampus
Hill, M. N., Carrier, E. J., Ho, W. ‐. V., Shi, L., Patel, S., Gorzalka, B. B., & Hillard, C. J. (2007) · Hippocampus · doi:10.1002/hipo.20386 · Cited by 96 · see citing works
Self-citation
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Goeldner, C., Ballard, T. M., Knoflach, F., Wichmann, J., Gatti, S., & Umbricht, D. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2012.08.001 · Cited by 96 · see citing works
Antidepressant‐like effects of fenofibrate in mice via the hippocampal brain‐derived neurotrophic factor signalling pathway
Jiang, B., Wang, Y., Wang, H., Song, L., Huang, C., Zhu, Q., Wu, F., & Zhang, W. (2016) · British Journal of Pharmacology · doi:10.1111/bph.13668 · Cited by 96 · see citing works
Endocannabinoids in the Treatment of Mood Disorders: Evidence from Animal Models
Bambico, F. R., Duranti, A., Tontini, A., Tarzia, G., & Gobbi, G. (2009) · Current Pharmaceutical Design · doi:10.2174/138161209788168029 · Cited by 91 · see citing works
The endocannabinoid system as a target for the treatment of cannabis dependence
Clapper, J. R., Mangieri, R. A., & Piomelli, D. (2008) · Neuropharmacology · doi:10.1016/j.neuropharm.2008.07.018 · Cited by 92 · see citing works
Recent Progress in Understanding the Pathophysiology of Post-Traumatic Stress Disorder: Implications for Targeted Pharmacological Treatment
Bailey, C. R., Cordell, E., Sobin, S. M., & Neumeister, A. (2013) · CNS Drugs · doi:10.1007/s40263-013-0051-4 · Cited by 89 · see citing works
Sex differences in the chronic mild stress model of depression
Franceschelli, A., Herchick, S., Thelen, C., Papadopoulou‐Daifoti, Z., & Pitychoutis, P. M. (2014) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000062 · Cited by 89 · see citing works
Altered Brain Activation During Visuomotor Integration in Chronic Active Cannabis Users: Relationship to Cortisol Levels
King, G., Ernst, T., Deng, W., Stenger, V. A., Gonzales, R. M. K., Nakama, H., & Chang, L. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.4148-11.2011 · Cited by 89 · see citing works
Beneficial effects of desipramine on cognitive function of chronically stressed rats are mediated by α1-adrenergic receptors in medial prefrontal cortex
Bondi, C. O., Jett, J. D., & Morilak, D. A. (2010) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2010.04.016 · Cited by 88 · see citing works
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Sciolino, N. R., Bortolato, M., Eisenstein, S. A., Fu, J., Oveisi, F., Hohmann, A. G., & Piomelli, D. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.04.007 · Cited by 89 · see citing works
Potential application of endocannabinoid system agents in neuropsychiatric and neurodegenerative diseases—focusing on FAAH/MAGL inhibitors
Ren, S., Wang, Z., Zhang, Y., & Chen, N. (2020) · Acta Pharmacologica Sinica · doi:10.1038/s41401-020-0385-7 · Cited by 88 · see citing works
Inhibition of monoamine oxidase activity by cannabinoids
Fišar, Z. (2010) · Naunyn-Schmiedeberg s Archives of Pharmacology · doi:10.1007/s00210-010-0517-6 · Cited by 88 · see citing works
The Endocannabinoid System in Peripheral Lymphocytes as a Mirror of Neuroinflammatory Diseases
Centonze, D., Battistini, L., & Maccarrone, M. (2008) · Current Pharmaceutical Design · doi:10.2174/138161208785740018 · Cited by 86 · see citing works
Endocannabinoid-mediated modulation of stress responses: Physiological and pathophysiological significance
Finn, D. P. (2009) · Immunobiology · doi:10.1016/j.imbio.2009.05.011 · Cited by 88 · see citing works
The Role of the Brain's Endocannabinoid System in Pain and Its Modulation by Stress
Corcoran, L., Roche, M., & Finn, D. P. (2015) · International review of neurobiology · doi:10.1016/bs.irn.2015.10.003 · Cited by 86 · see citing works
Possible antidepressant effects and mechanisms of memantine in behaviors and synaptic plasticity of a depression rat model
Quan, M., Zhang, N., Wang, Y.-Y., Zhang, T., & Yang, Z. R. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.03.026 · Cited by 86 · see citing works
Short-term adaptation of conditioned fear responses through endocannabinoid signaling in the central amygdala
Kamprath, K., Romo-Parra, H., Häring, M., Gaburro, S., Doengi, M., Lutz, B., & Pape, H.-C. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2010.196 · Cited by 86 · see citing works
Administration of cannabidiol and imipramine induces antidepressant-like effects in the forced swimming test and increases brain-derived neurotrophic factor levels in the rat amygdala
Réus, G. Z., Stringari, R. B., Ribeiro, K. F., Luft, T., Abelaira, H. M., Fries, G. R., Aguiar, B. W., Kapczinski, F., Hallak, J. E., Zuardi, A. W., et al. (2011) · Acta Neuropsychiatrica · doi:10.1111/j.1601-5215.2011.00579.x · Cited by 86 · see citing works
Genetically reduced FAAH activity may be a risk for the development of anxiety and depression in persons with repetitive childhood trauma
Lazáry, J., Eszlári, N., Juhász, G., & Bagdy, G. (2016) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2016.03.003 · Cited by 87 · see citing works
Brain CB2 Receptors: Implications for Neuropsychiatric Disorders
Roche, M., & Finn, D. P. (2010) · Pharmaceuticals · doi:10.3390/ph3082517 · Cited by 87 · see citing works
Chapter 5 The Endocannabinoid System as A Target for Novel Anxiolytic and Antidepressant Drugs
Gaetani, S., Dipasquale, P., Romano, A., Righetti, L., Cassano, T., Piomelli, D., & Cuomo, V. (2009) · International Review of Neurobiology · doi:10.1016/s0074-7742(09)85005-8 · Cited by 83 · see citing works
Role of Endocannabinoid Signaling in Anxiety and Depression
Patel, S., & Hillard, C. J. (2009) · Current topics in behavioral neurosciences · doi:10.1007/978-3-540-88955-7_14 · Cited by 85 · see citing works
Self-citation
Cannabinoid Receptor Genotype Moderation of the Effects of Childhood Physical Abuse on Anhedonia and Depression
Arpana Agrawal, A., Nelson, E. C., Littlefield, A. K., Bucholz, K. K., Degenhardt, L. J., Henders, A. K., Madden, P. A. F., Martin, N. G., Montgomery, G. W., Pergadia, M. L., et al. (2012) · Archives of General Psychiatry · doi:10.1001/archgenpsychiatry.2011.2273 · Cited by 83 · see citing works

Cannabinoid Modulation of the Stressed Hippocampus
Scarante, F. F., Vila-Verde, C., Lopes, V. D., Ferreira‐Junior, N. C., Guimarães, F. S., & Campos, A. C. (2017) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2017.00411 · Cited by 64 · see citing works
Chronic restraint stress impairs endocannabinoid mediated suppression of GABAergic signaling in the hippocampus of adult male rats
Hu, W., Zhang, M., Czéh, B., Zhang, W., & Flügge, G. (2011) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2011.04.005 · Cited by 48 · see citing works
Deficiency in Endocannabinoid Signaling in the Nucleus Accumbens Induced by Chronic Unpredictable Stress
Wang, W., Sun, D., Pan, B., Roberts, C. J., Sun, X., Hillard, C. J., & Liu, Q.-S. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2010.99 · Cited by 124 · see citing works
Self-citation
Acute restraint stress enhances hippocampal endocannabinoid function via glucocorticoid receptor activation
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
Self-citation
Endocannabinoids and Stress Resilience: Is Deficiency Sufficient to Promote Vulnerability?
Hill, M. N., & Lee, F. S. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2016.03.2099 · Cited by 15 · see citing works
Self-citation

Authors: Hill, M. N., Patel, S., Carrier, E. J., Rademacher, D. J., Ormerod, B. K., Hillard, C. J., & Gorzalka, B. B.
Affiliations: University of British Columbia (CA)
Medical College of Wisconsin (US)
Corresponding author: Hillard, Cecilia J
Gorzalka, Boris B
ORCID: Hill, Matthew N
Patel, Sachin
Carrier, Erica J
Ormerod, Brandi K
Hillard, Cecilia J
Venue: Neuropsychopharmacology
Publisher: Springer Science and Business Media LLC
Published: 2004-11-03
Volume: 30
Issue: 3
Pages: 508-515
ISSN: 0893-133X (ISSN-L)
1740-634X
DOI: 10.1038/sj.npp.1300601
OpenAlex: W2124037107
Cited by: 363
References: 56
Citations by year: 2026: 8 · 2025: 12 · 2024: 16 · 2023: 7 · 2022: 12 · 2021: 29 · 2020: 15 · 2019: 15 · 2018: 11 · 2017: 14 · 2016: 20 · 2015: 21 · 2014: 21 · 2013: 18 · 2012: 20
FWCI: 8.15
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
Locations: Neuropsychopharmacology (publishedVersion)
PubMed (publishedVersion)
Funders: National Alliance for Research on Schizophrenia and Depression
Michael Smith Health Research BC
National Institutes of Health
Natural Sciences and Engineering Research Council of Canada
National Institute on Drug Abuse (F32 DA-16510, F30 DA15575, R01DA016967, F30DA015575, F32DA016510)
Topics: Health Sciences › Medicine › Pharmacology › Cannabis and Cannabinoid Research
Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Keywords: endocannabinoid signaling, chronic unpredictable mild stress, hippocampus, CB1 receptor, 2-arachidonoylglycerol, reversal learning, behavioral flexibility, perseveration, cognitive impairment, stress-related neuropsychiatric disorders
MeSH terms: Animals, Cannabinoids, Copulation, Female, Hippocampus, Male, Reference Values, Stress, Psychological, Signal Transduction, Maze Learning, Rats, Long-Evans, Receptor, Cannabinoid, CB1, Rats, Cannabinoid Receptor Modulators, Endocannabinoids

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Downregulation of Endocannabinoid Signaling in the Hippocampus Following Chronic Unpredictable Stress

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