Involvement of the endocannabinoid system in the neurobehavioural effects of stress and glucocorticoids
Open accessAbstract
The endocannabinoid system is a neuroactive lipid signaling system that functions to gate synaptic transmitter release. Accumulating evidence has demonstrated that this system is responsive to modulation by both stress and glucocorticoids within the hypothalamus and limbic structures; however, the nature of this regulation is more complex than initially assumed. The aim of the current review is to summarize the research to date which examines the effects of acute stress and glucocorticoid administration on endocannabinoid signaling in limbic-hypothalamic-pituitary-adrenal (LHPA) axis, and in turn the role endocannabinoid signaling plays in the neurobehavioural responses to acute stress and glucocorticoid administration. The majority of research suggests that acute stress produces a mobilization of the endocannabinoid 2-arachidonoylglycerol (2-AG) while concurrently reducing the tissue content of the other endocannabinoid ligand anandamide. Genetic and pharmacological studies demonstrate that the reduction in anandamide signaling may be involved in the initiation of HPA axis activation and the generation of changes in emotional behaviour, while the increase in 2-AG signaling may be involved in terminating the stress response, limiting neuronal activation and contributing to changes in motivated behaviours. Collectively, these studies reveal a complex interplay between endocannabinoids and the HPA axis, and further identify endocannabinoid signaling as a critical regulator of the stress response.
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The endocannabinoid system is implicated in the regulation of the HPA axis and play behavior.
“The endocannabinoid system has been implicated in a myriad of functions, including the regulation of the HPA axis21,22 and play behavior.”
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Cites
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
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
An endocannabinoid mechanism for stress-induced analgesia
Hohmann, A. G., Suplita, R. L., Bolton, N. M., Neely, M. H., Fegley, D., Mangieri, R., Krey, J. F., Michael Walker, J., Holmes, P. V., Crystal, J. D., et al. (2005) · Nature · doi:10.1038/nature03658 · Cited by 778 · see citing works
A corticosteroid receptor in neuronal membranes
Orchinik, M., Murray, T. F., & Moore, F. L. (1991) · Science · doi:10.1126/science.2063198 · Cited by 523 · see citing works
Hill, M. N., Miller, G. E., Carrier, E. J., Gorzalka, B. B., & Hillard, C. J. (2009) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2009.03.013 · Cited by 328 · see citing works
McGregor, I. S., Hargreaves, G. A., Apfelbach, R., & Hunt, G. E. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.0187-04.2004 · Cited by 231 · cited 1× · see citing works
“Specifically, exposure to predator odor stress is known to produce a behavioural phenotype of defensive burying that is believed to represent an anxiety-like behaviour (McGregor et al., 2004).”
BackgroundImpaired action of anxiolytic drugs in mice deficient in cannabinoid CB1 receptors
Urigüen, L., Pérez-Rial, S., Ledent, C., Palomo, T., & Manzanares, J. (2004) · Neuropharmacology · doi:10.1016/j.neuropharm.2004.01.003 · Cited by 218 · 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
Barna, I., Zelena, D., Arszovszki, A. C., & Ledent, C. (2004) · Life Sciences · doi:10.1016/j.lfs.2004.06.006 · Cited by 136 · see citing works
Flagged first, then by citations
Research works printed but not linked: 62
- Aguado T Monory K Palazuelos J Stella N Cravatt B Lutz B Marsicano G Kokaia Z Guzman M Galve-Roperh I The endocannabinoid system drives neural progenitor proliferation FASEB J 2005 19 1704 1706 16037095
- Ahn K McKinney MK Cravatt BF Enzymatic pathways that regulate endocannabinoid signaling in the nervous system Chem Rev 2008 108 1687 1707 18429637 PMC3150828
- Aso E Ozaita A Valdizan EM Ledent C Pazos A Maldonado R Valverde O BDNF impairment in the hippocampus is related to enhanced despair behavior in CB1 knockout mice J Neurochem 2008 105 565 572 18047561
- Benito C Tolon RM Pazos MR Nunez E Castillo AI Romero J Cannabinoid CB2 receptors in human brain inflammation Br J Pharmacol 2008 153 277 285 17934510 PMC2219537
- Bisogno T Endogenous cannabinoids: structure and metabolism J Neuroendocrinol 2008 20 1 1 9 18426492
- Blednov YA Cravatt BF Boehm SL 2nd Walker D Harris RA Role of endocannabinoids in alcohol consumption and intoxication: studies of mice lacking fatty acid amide hydrolase Neuropsychopharmacology 2007 32 1570 1582 17164820
- Campolongo P Roozendaal B Trezza V Hauer D Schelling G McGaugh JL Cuomo V Endocannabinoids in the rat basolateral amygdala enhance memory consolidation and enable glucocorticoid modulation of memory Proc Natl Acad Sci U S A 2009 106 4888 4893 19255436 PMC2660732
- Coddington E Lewis C Rose JD Moore FL Endocannabinoids mediate the effects of acute stress and corticosterone on sex behavior Endocrinology 2007 148 493 500 17095597
- Cota D Marsicano G Tschop M Grubler Y Flachskamm C Schubert M Auer D Yassouridis A Thone-Reineke C Ortmann S Tomassoni F Cervino C Nisoli E Linthorst AC Pasquali R Lutz B Stalla GK Pagotto U The endogenous cannabinoid system affects energy balance via central orexigenic drive and peripheral lipogenesis J Clin Invest 2003 112 423 431 12897210 PMC166293
- Degroot A Kofalvi A Wade MR Davis RJ Rodrigues RJ Rebola N Cunha RA Nomikos GG CB1 receptor antagonism increases hippocampal acetylcholine release: site and mechanism of action Mol Pharmacol 2006 70 1236 1245 16855179
- Deutsch DG Ueda N Yamamoto S The fatty acid amide hydrolase (FAAH) Prostaglandins Leukot Essent Fatty Acids 2002 66 201 210 12052036
- Devane WA Hanus L Breuer A Pertwee RG Stevenson LA Griffin G Gibson D Mandelbaum A Etinger A Mechoulam R Isolation and structure of a brain constituent that binds to the cannabinoid receptor Science 1992 258 1946 1949 1470919
- Di S Boudaba C Popescu IR Weng FJ Harris C Marcheselli VL Bazan NG Tasker JG Activity-dependent release and actions of endocannabinoids in the rat hypothalamic supraoptic nucleus J Physiol 2005a 569 751 760 16239276 PMC1464259
- Di S Malcher-Lopes R Halmos KC Tasker JG Nongenomic glucocorticoid inhibition via endocannabinoid release in the hypothalamus: a fast feedback mechanism J Neurosci 2003 23 4850 4857 12832507 PMC6741208
- Di S Malcher-Lopes R Marcheselli VL Bazan NG Tasker JG Rapid glucocorticoid-mediated endocannabinoid release and opposing regulation of glutamate and gamma-aminobutyric acid inputs to hypothalamic magnocellular neurons Endocrinology 2005b 146 4292 4301 15994343
- Di S Maxson MM Franco A Tasker JG Glucocorticoids regulate glutamate and GABA synapse-specific retrograde transmission via divergent nongenomic signaling pathways J Neurosci 2009 29 393 401 19144839 PMC2775558
- Dinh TP Carpenter D Leslie FM Freund TF Katona I Sensi SL Kathuria S Piomelli D Brain monoglyceride lipase participating in endocannabinoid inactivation Proc Natl Acad Sci U S A 2002 99 10819 10824 12136125 PMC125056
- Freund TF Katona I Piomelli D Role of endogenous cannabinoids in synaptic signaling Physiol Rev 2003 83 1017 1066 12843414
- Gorzalka BB Hill MN Chang SC Male-female differences in the effects of cannabinoids on sexual behavior and gonadal hormone function Horm Behav 2009 19733173
- Gorzalka BB Hill MN Hillard CJ Regulation of endocannabinoid signaling by stress: implications for stress-related affective disorders Neurosci Biobehav Rev 2008 32 1152 1160 18433869
- Haller J Barna I Barsvari B Gyimesi Pelczer K Yasar S Panlilio LV Goldberg S Interactions between environmental aversiveness and the anxiolytic effects of enhanced cannabinoid signaling by FAAH inhibition in rats Psychopharmacology (Berl) 2009 PMC2719980 19259645
- Haller J Varga B Ledent C Barna I Freund TF Context-dependent effects of CB1 cannabinoid gene disruption on anxiety-like and social behaviour in mice Eur J Neurosci 2004 19 1906 1912 15078564
- Hansson AC Bermudez-Silva FJ Malinen H Hyytia P Sanchez-Vera I Rimondini R Rodriguez de Fonseca F Kunos G Sommer WH Heilig M Genetic impairment of frontocortical endocannabinoid degradation and high alcohol preference Neuropsychopharmacology 2007 32 117 126 16482090
- Herman JP Figueiredo H Mueller NK Ulrich-Lai Y Ostrander MM Choi DC Cullinan WE Central mechanisms of stress integration: hierarchical circuitry controlling hypothalamo-pituitary-adrenocortical responsiveness Front Neuroendocrinol 2003 24 151 180 14596810
- Hill MN Hillard CJ Bambico FR Patel S Gorzalka BB Gobbi G The therapeutic potential of the endocannabinoid system for the development of a novel class of antidepressants Trends Pharmacol Sci 2009a 30 484 493 19732971
- Hill MN Kambo JS Sun JC Gorzalka BB Galea LA Endocannabinoids modulate stress-induced suppression of hippocampal cell proliferation and activation of defensive behaviours Eur J Neurosci 2006 24 1845 1849 17067290
- Hill MN Karatsoreos IN Hillard CJ McEwen BS Rapid induction of limbic endocannabinoid signaling in vivo by glucocorticoid hormones Psychoneuroendocrinology 2009b Under review PMC2914801 20399021
- Hill MN McLaughlin RJ Morrish AC Viau V Floresco SB Hillard CJ Gorzalka BB Suppression of amygdalar endocannabinoid signaling by stress contributes to activation of the hypothalamic-pituitary-adrenal axis Neuropsychopharmacology 2009c in press PMC3197779 19710634
- Hill MN McLaughlin RJ Viau V Gorzalka BB Hillard CJ Stress-induced alterations in limbic endocannabinoid content in the rat: Correlations to HPA axis activation 17th Annual Symposium of the International Cannabinoid Research Society 2007 23
- Hillard CJ Biochemistry and pharmacology of the endocannabinoids arachidonylethanolamide and 2-arachidonylglycerol Prostaglandins Other Lipid Mediat 2000 61 3 18 10785538
- Howlett AC The cannabinoid receptors Prostaglandins Other Lipid Mediat 2002 68-69 619 631 12432948
- Karst H Berger S Turiault M Tronche F Schutz G Joels M Mineralocorticoid receptors are indispensable for nongenomic modulation of hippocampal glutamate transmission by corticosterone Proc Natl Acad Sci U S A 2005 102 19204 19207 16361444 PMC1323174
- Keller-Wood ME Dallman MF Corticosteroid inhibition of ACTH secretion Endocr Rev 1984 5 1 24 6323158
- Laugero KD Bell ME Bhatnagar S Soriano L Dallman MF Sucrose ingestion normalizes central expression of corticotropin-releasing-factor messenger ribonucleic acid and energy balance in adrenalectomized rats: a glucocorticoid-metabolic-brain axis? Endocrinology 2001 142 2796 2804 11415998
- Liu J Wang L Harvey-White J Osei-Hyiaman D Razdan R Gong Q Chan AC Zhou Z Huang BX Kim HY Kunos G A biosynthetic pathway for anandamide Proc Natl Acad Sci U S A 2006 103 13345 13350 16938887 PMC1557387
- Malcher-Lopes R Di S Marcheselli VS Weng FJ Stuart CT Bazan NG Tasker JG Opposing crosstalk between leptin and glucocorticoids rapidly modulates synaptic excitation via endocannabinoid release J Neurosci 2006 26 6643 6650 16775153 PMC6674033
- Mikics E Barsy B Barsvari B Haller J Behavioral specificity of non-genomic glucocorticoid effects in rats: effects on risk assessment in the elevated plus-maze and the open-field Horm Behav 2005 48 152 162 16042965
- Mikics E Kruk MR Haller J Genomic and non-genomic effects of glucocorticoids on aggressive behavior in male rats Psychoneuroendocrinology 2004 29 618 635 15041085
- Moldrich G Wenger T Localization of the CB1 cannabinoid receptor in the rat brain An immunohistochemical study Peptides 2000 21 1735 1742 11090929
- Munro S Thomas KL Abu-Shaar M Molecular characterization of a peripheral receptor for cannabinoids Nature 1993 365 61 65 7689702
- Naidu PS Varvel SA Ahn K Cravatt BF Martin BR Lichtman AH Evaluation of fatty acid amide hydrolase inhibition in murine models of emotionality Psychopharmacology (Berl) 2007 192 61 70 17279376
- Ohno-Shosaku T Maejima T Kano M Endogenous cannabinoids mediate retrograde signals from depolarized postsynaptic neurons to presynaptic terminals Neuron 2001 29 729 738 11301031
- Okamoto Y Morishita J Tsuboi K Tonai T Ueda N Molecular characterization of a phospholipase D generating anandamide and its congeners J Biol Chem 2004 279 5298 5305 14634025
- Orchinik M Murray TF Franklin PH Moore FL Guanyl nucleotides modulate binding to steroid receptors in neuronal membranes Proc Natl Acad Sci U S A 1992 89 3830 3834 1570300 PMC525584
- Palazuelos J Aguado T Egia A Mechoulam R Guzman M Galve-Roperh I Non-psychoactive CB2 cannabinoid agonists stimulate neural progenitor proliferation FASEB J 2006 20 2405 2407 17015409
- Parolaro D Presence and functional regulation of cannabinoid receptors in immune cells Life Sci 1999 65 637 644 10462064
- Patel S Roelke CT Rademacher DJ Cullinan WE Hillard CJ Endocannabinoid signaling negatively modulates stress-induced activation of the hypothalamic-pituitary-adrenal axis Endocrinology 2004 145 5431 5438 15331569
- Patel S Roelke CT Rademacher DJ Hillard CJ Inhibition of restraint stress-induced neural and behavioural activation by endogenous cannabinoid signalling Eur J Neurosci 2005 21 1057 1069 15787710
- Pecoraro N Dallman MF Warne JP Ginsberg AB Laugero KD la Fleur SE Houshyar H Gomez F Bhargava A Akana SF From Malthus to motive: how the HPA axis engineers the phenotype, yoking needs to wants Prog Neurobiol 2006 79 247 340 16982128
- Racz I Bilkei-Gorzo A Toth ZE Michel K Palkovits M Zimmer A A critical role for the cannabinoid CB1 receptors in alcohol dependence and stress-stimulated ethanol drinking J Neurosci 2003 23 2453 2458 12657705 PMC6742040
- Rademacher DJ Meier SE Shi L Ho WS Jarrahian A Hillard CJ Effects of acute and repeated restraint stress on endocannabinoid content in the amygdala, ventral striatum, and medial prefrontal cortex in mice Neuropharmacology 2008 54 108 116 17675104
- Roozendaal B McEwen BS Chattarji S Stress, memory and the amygdala Nat Rev Neurosci 2009 10 423 433 19469026
- Rose JD Moore FL A neurobehavioral model for rapid actions of corticosterone on sensorimotor integration Steroids 1999 64 92 99 10323677
- Schlicker E Kathmann M Modulation of transmitter release via presynaptic cannabinoid receptors Trends Pharmacol Sci 2001 22 565 572 11698100
- Simon GM Cravatt BF Endocannabinoid biosynthesis proceeding through glycerophospho-N-acyl ethanolamine and a role for alpha/beta-hydrolase 4 in this pathway J Biol Chem 2006 281 26465 26472 16818490
- Steiner MA Marsicano G Nestler EJ Holsboer F Lutz B Wotjak CT Antidepressant-like behavioral effects of impaired cannabinoid receptor type 1 signaling coincide with exaggerated corticosterone secretion in mice Psychoneuroendocrinology 2008 33 54 67 17976922 PMC2267923
- Sugiura T Waku K Cannabinoid receptors and their endogenous ligands J Biochem 2002 132 7 12 12097154
- Tsou K Brown S Sanudo-Pena MC Mackie K Walker JM Immunohistochemical distribution of cannabinoid CB1 receptors in the rat central nervous system Neuroscience 1998 83 393 411 9460749
- Ueda N Endocannabinoid hydrolases Prostaglandins Other Lipid Mediat 2002 68-69 521 534 12432941
- Ulrich-Lai YM Herman JP Neural regulation of endocrine and autonomic stress responses Nat Rev Neurosci 2009 PMC4240627 19469025
- Van Sickle MD Duncan M Kingsley PJ Mouihate A Urbani P Mackie K Stella N Makriyannis A Piomelli D Davison JS Marnett LJ Di Marzo V Pittman QJ Patel KD Sharkey KA Identification and functional characterization of brainstem cannabinoid CB2 receptors Science 2005 310 329 332 16224028
- Wilson RI Kunos G Nicoll RA Presynaptic specificity of endocannabinoid signaling in the hippocampus Neuron 2001 31 453 462 11516401
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- Authors
- Hill, M. N., & McEwen, B. S.
- Affiliations
- Rockefeller University (US)
- Corresponding author
- Hill, Matthew N.
- Venue
- Progress in Neuro-Psychopharmacology and Biological Psychiatry
- Publisher
- Elsevier BV
- Published
- 2010-06
- Volume
- 34
- Issue
- 5
- Pages
- 791-797
- ISSN
- 0278-5846 (ISSN-L)
- PMC
- PMC2945244
- OpenAlex
- W1977774953
- Cited by
- 235
- References
- 9
- Citations by year
- 2026: 7 · 2025: 11 · 2024: 10 · 2023: 11 · 2022: 10 · 2021: 14 · 2020: 12 · 2019: 11 · 2018: 16 · 2017: 12 · 2016: 12 · 2015: 22 · 2014: 24 · 2013: 14 · 2012: 23
- FWCI
- 1.68
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Progress in Neuro-Psychopharmacology and Biological Psychiatry (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Mental Health (R01MH041256)
- Topics
- Health Sciences › Medicine › Pharmacology › Cannabis and Cannabinoid Research
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Keywords
- endocannabinoid system, acute stress, glucocorticoids, hypothalamic-pituitary-adrenal axis, 2-arachidonoylglycerol, anandamide, emotional behavior, motivated behavior, hypothalamus, limbic structures
- MeSH terms
- Animals, Behavior, Behavior, Animal, Glucocorticoids, Humans, Hypothalamo-Hypophyseal System, Male, Pituitary-Adrenal System, Stress, Psychological, Signal Transduction, Mice, Rats, Cannabinoid Receptor Modulators, Endocannabinoids
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