Adaptations in endocannabinoid signaling in response to repeated homotypic stress: a novel mechanism for stress habituation
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Daily life stressors are a major environmental factor contributing to precipitation and exacerbation of mental illness. Animal models using repeated homotypic stress induce anxious and depressive phenotypes and are used to study the pathophysiology of affective disorders. Here we discuss data demonstrating that repeated homotypic stress produces temporally and anatomically distinct changes in endocannabinoid signaling components within stress‐responsive brain regions. We also present evidence describing the neural and behavioral correlates of these adaptations in endocannabinoid signaling. These data support a role for endocannabinoid signaling in the central nervous system response to chronic, homotypic stress, and specifically in the process of stress–response habituation. The clinical implications of these findings for the pathophysiology and treatment of affective disorders are discussed.
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Recent preclinical evidence indicates that stress mobilizes the eCB system in both the brain and the periphery, and that the eCB system can modulate behavioral and endocrine responses to both acute and chronic stress.
“Recent preclinical evidence indicates that stress also mobilizes the endocannabinoid (eCB) system in both the brain and the periphery, and that the eCB system can modulate behavioral and endocrine responses to both acute and chronic stress (Hill et al, 2010;Patel and Hillard, 2008).”
From Acute stress increases circulating anandamide and other N-acylethanolamines in healthy humans (2012) · cites this paper as Patel and Hillard, 2008
Recent studies in animals and humans point to a major role of EC signaling in both the periphery and central nervous system in controlling adaptive processes to aversive situations and regulating and limiting stress reactions.
“Despite the abovementioned diversity in central and peripheral functions, recent studies in animals [9] and humans [10] point to a major role of EC signaling in both the periphery [10] and central nervous system [11] in controlling adaptive processes to aversive situations and regulating and limiting stress reactions.”
From Plasma concentrations of endocannabinoids and related primary fatty acid amides in patients with post-traumatic stress disorder (2013) · cites this paper as [9]
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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
Self-citationUncertainty and stress: Why it causes diseases and how it is mastered by the brain
Peters, A., McEwen, B. S., & Friston, K. (2017) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2017.05.004 · Cited by 652 · see citing works
Endogenous cannabinoid signaling is essential for stress adaptation
Hill, M. N., McLaughlin, R. J., Bingham, B., Shrestha, L., Lee, T. T. Y., Gray, J. M., Hillard, C. J., Gorzalka, B. B., & Viau, V. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0914661107 · Cited by 349 · see citing works
Self-citationCampos, A. C., Ortega, Z., Palazuelos, J., Fogaça, M. V., Aguiar, D. C., Díaz-Alonso, J., Ortega-Gutiérrez, S., Vázquez-Villa, H., Moreira, F. A., Guzmán, M., et al. (2013) · International Journal of Neuropsychopharmacology · doi:10.1017/s1461145712001502 · Cited by 313 · see citing works
Best Practice & Research Clinical Endocrinology & Metabolism
Grieb, M. (2009) · Cited by 276 · see citing works
Moreira, F. A., Grieb, M., & Lutz, B. (2009) · Best Practice & Research Clinical Endocrinology & Metabolism · doi:10.1016/j.beem.2008.09.003 · Cited by 272 · see citing works
Acute stress increases circulating anandamide and other N-acylethanolamines in healthy humans
Dlugos, A., Childs, E., Stuhr, K. L., Hillard, C. J., & de Wit, H. (2012) · Neuropsychopharmacology · doi:10.1038/npp.2012.100 · Cited by 248 · see citing works
Self-citationThe endocannabinoid system in anxiety, fear memory and habituation
Ruehle, S., Rey, A. A., Remmers, F., & Lutz, B. (2011) · Journal of Psychopharmacology · doi:10.1177/0269881111408958 · Cited by 236 · 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
2-Arachidonoylglycerol: A signaling lipid with manifold actions in the brain
Baggelaar, M. P., Maccarrone, M., & van der Stelt, M. (2018) · Progress in Lipid Research · doi:10.1016/j.plipres.2018.05.002 · Cited by 224 · see citing works
Stress and visceral pain: From animal models to clinical therapies
Larauche, M. H., Mulak, A., & Taché, Y. (2011) · Experimental Neurology · doi:10.1016/j.expneurol.2011.04.020 · Cited by 212 · see citing works
Hauer, 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
Moreira, F. A., & Wotjak, C. T. (2009) · Current topics in behavioral neurosciences · doi:10.1007/7854_2009_16 · Cited by 177 · see citing works
Ganon-Elazar, E., & Akirav, I. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.1223-09.2009 · Cited by 173 · see citing works
Anxiety, stress, and fear response in mice with reduced endocannabinoid levels
Jenniches, I., Ternes, S., Albayram, O., Otte, D. M., Bach, K., Bindila, L., Michel, K., Lutz, B., Bilkei-Gorzo, A., & Zimmer, A. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.03.033 · Cited by 169 · see citing works
Moloney, R. D., O’Mahony, S. M., Dinan, T. G., & Cryan, J. F. (2015) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2015.00015 · Cited by 167 · see citing works
Shonesy, B. C., Bluett, R. J., Ramikie, T. S., Báldi, R., Hermanson, D. J., Kingsley, P. J., Marnett, L. J., Winder, D. G., Colbran, R. J., & Patel, S. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.11.001 · Cited by 155 · see citing works
Self-citationPatel, S., Kingsley, P. J., Mackie, K., Marnett, L. J., & Winder, D. G. (2009) · Neuropsychopharmacology · doi:10.1038/npp.2009.101 · Cited by 153 · see citing works
Self-citationDissociation of within- and between-Session Extinction of Conditioned Fear
Plendl, W., & Wotjak, C. T. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.6038-09.2010 · Cited by 148 · see citing works
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
Repeated Stress Impairs Endocannabinoid Signaling in the Paraventricular Nucleus of the Hypothalamus
Cusulin, J. I. W., Kuzmiski, J. B., & Bains, J. S. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.1046-10.2010 · Cited by 145 · see citing works
Riebe, C. J. N., & Wotjak, C. T. (2011) · Stress · doi:10.3109/10253890.2011.586753 · Cited by 144 · see citing works
Motion Sickness, Stress and the Endocannabinoid System
Choukèr, A., Kaufmann, I., Kreth, S., Hauer, D., Feuerecker, M., Thieme, D., Vogeser, M., Thiel, M., & Schelling, G. (2010) · PLoS ONE · doi:10.1371/journal.pone.0010752 · Cited by 140 · see citing works
Atsak, P., Hauer, D., Campolongo, P., Schelling, G., McGaugh, J. L., & Roozendaal, B. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1200742109 · Cited by 140 · 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-citationEndocannabinoid signalling modulates susceptibility to traumatic stress exposure
Bluett, R. J., Báldi, R., Haymer, A., Gaulden, A. D., Hartley, N. D., Parrish, W. P., Baechle, J. J., Marcus, D. J., Bey, R. M., Shonesy, B. C., et al. (2017) · Nature Communications · doi:10.1038/ncomms14782 · Cited by 136 · see citing works
Self-citationSubstrate-selective COX-2 inhibition decreases anxiety via endocannabinoid activation
Hermanson, D. J., Hartley, N. D., Gamble-George, J., Brown, N., Shonesy, B. C., Kingsley, P. J., Colbran, R. J., Reese, J., Marnett, L. J., & Patel, S. (2013) · Nature Neuroscience · doi:10.1038/nn.3480 · Cited by 126 · see citing works
Sumislawski, J. J., Ramikie, T. S., & Patel, S. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2011.166 · Cited by 124 · see citing works
Self-citationEndocannabinoid signals in the control of emotion
Lutz, B. (2009) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2008.12.001 · Cited by 124 · see citing works
McLaughlin, R. J., Hill, M. N., Bambico, F. R., Stuhr, K. L., Gobbi, G., Hillard, C. J., & Gorzalka, B. B. (2012) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2012.01.004 · Cited by 113 · see citing works
Self-citationAbush, H., & Akirav, I. (2012) · PLoS ONE · doi:10.1371/journal.pone.0031731 · Cited by 114 · see citing works
Vinod, K. Y., Kassir, S. A., Hungund, B. L., Cooper, T. B., Mann, J. J., & Arango, V. (2009) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2009.11.013 · Cited by 114 · see citing works
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-citationBedse, G., Hartley, N. D., Neale, E., Gaulden, A. D., Patrick, T. A., Kingsley, P. J., Uddin, M. J., Plath, N., Marnett, L. J., & Patel, S. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2017.03.002 · Cited by 104 · see citing works
Self-citationKamprath, K., Plendl, W., Marsicano, G., Deussing, J. M., Wurst, W., Lutz, B., & Wotjak, C. T. (2008) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2008.00463.x · Cited by 104 · see citing works
Ulrich‐Lai, Y. M., & Ryan, K. K. (2014) · Cell Metabolism · doi:10.1016/j.cmet.2014.01.020 · Cited by 108 · 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
Marco, E. M., Echeverry‐Alzate, V., López‐Moreno, J. A., Giné, E., Peñasco, S., & Viveros, M. (2014) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000068 · Cited by 96 · see citing works
Jacob, W., Yassouridis, A., Marsicano, G., Monory, K., Lutz, B., & Wotjak, C. T. (2009) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2009.00512.x · Cited by 95 · see citing works
CB1 receptor signaling regulates social anxiety and memory
Litvin, Y., Phan, A., Hill, M. N., Pfaff, D. W., & McEwen, B. S. (2013) · Genes Brain & Behavior · doi:10.1111/gbb.12045 · Cited by 93 · see citing works
Stress-Related Alterations of Visceral Sensation: Animal Models for Irritable Bowel Syndrome Study
Larauche, M. H., Mulak, A., & Taché, Y. (2011) · Journal of Neurogastroenterology and Motility · doi:10.5056/jnm.2011.17.3.213 · Cited by 92 · 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
Schneider, P., Bindila, L., Schmahl, C., Bohus, M., Meyer-Lindenberg, A., Lutz, B., Spanagel, R., & Schneider, M. (2016) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2016.00203 · Cited by 89 · see citing works
Segev, A., Rubin, A. S., Abush, H., Richter‐Levin, G., & Akirav, I. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2013.292 · Cited by 88 · see citing works
Finn, D. P. (2009) · Immunobiology · doi:10.1016/j.imbio.2009.05.011 · Cited by 88 · see citing works
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
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-citationLaricchiuta, D., & Petrosini, L. (2014) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2014.00238 · Cited by 80 · see citing works
Harris, B. N. (2019) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2019.113355 · Cited by 76 · see citing works
Larauche, M. H., Gourcerol, G., Million, M., Adelson, D. W., & Taché, Y. (2010) · Stress · doi:10.3109/10253891003664166 · Cited by 77 · see citing works
Abush, H., & Akirav, I. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2013.51 · Cited by 77 · see citing works
The endocannabinoid system modulates stress, emotionality, and inflammation
Crowe, M. S., Nass, S. R., Gabella, K. M., & Kinsey, S. G. (2014) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2014.06.007 · Cited by 72 · see citing works
D’Asti, E., Long, H., Tremblay‐Mercier, J., Grajzer, M., Cunnane, S. C., Marzo, V. D., & Walker, C. (2010) · Endocrinology · doi:10.1210/en.2009-1092 · Cited by 71 · see citing works
Morena, 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
Meet Your Stress Management Professionals: The Endocannabinoids
deRoon‐Cassini, T. A., Stollenwerk, T. M., Beatka, M. J., & Hillard, C. J. (2020) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2020.07.002 · Cited by 66 · see citing works
Self-citation2-arachidonoylglycerol signaling impairs short-term fear extinction
Hartley, N. D., Gunduz‐Cinar, O., Halladay, L. R., Bukalo, O., Holmes, A., & Patel, S. (2016) · Translational Psychiatry · doi:10.1038/tp.2016.26 · Cited by 65 · see citing works
Self-citationNey, L. J., Matthews, A. J., Bruno, R., & Felmingham, K. L. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.07.006 · Cited by 65 · see citing works
Marco, E. M., & Giovanni Laviola, A. (2011) · Journal of Psychopharmacology · doi:10.1177/0269881111408459 · Cited by 65 · see citing works
Cannabinoids and glucocorticoids modulate emotional memory after stress
Akirav, I. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.08.002 · Cited by 64 · see citing works
Ramikie, T. S., & Patel, S. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2011.08.037 · Cited by 62 · see citing works
Rimonabant Precipitates Anxiety in Rats Withdrawn from Palatable Food: Role of the Central Amygdala
Blasio, A., Iemolo, A., Sabino, V., Petrosino, S., Steardo, L., Rice, K. C., Orlando, P., Iannotti, F. A., Marzo, V. D., Zorrilla, E. P., et al. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2013.153 · Cited by 62 · see citing works
Interleukin-1 (IL-1) in stress-induced activation of limbic-hypothalamic-pituitary adrenal axis
Gądek-Michalska, A., & Bugajski, J. (2010) · Pharmacological Reports · doi:10.1016/s1734-1140(10)70359-5 · Cited by 56 · see citing works
Endocannabinoid Modulation of Predator Stress-Induced Long-Term Anxiety in Rats
Lim, J., Igarashi, M., Jung, K., Butini, S., Campiani, G., & Piomelli, D. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.284 · Cited by 53 · 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
Ratano, P., Petrella, C., Forti, F., Passeri, P. P., Morena, M., Palmery, M., Trezza, V., Severini, C., & Campolongo, P. (2018) · Neuropharmacology · doi:10.1016/j.neuropharm.2018.05.030 · Cited by 51 · see citing works
Hauer, 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
Marco, E. M., Rapino, C., Caprioli, A., Borsini, F., Maccarrone, M., & Giovanni Laviola, A. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.01.044 · Cited by 45 · see citing works
Stress modulation of reconsolidation
Akirav, I., & Maroun, M. (2012) · Psychopharmacology · doi:10.1007/s00213-012-2887-6 · Cited by 45 · see citing works
Cannabinoid Actions on Neural Stem Cells: Implications for Pathophysiology
Rodrigues, R. S., Lourenço, D. M., Paulo, S. L., Mateus, J. M., Ferreira, M. F., Mouro, F. M., Moreira, J. B., Ribeiro, F. F., Sebastião, A. M., & Xapelli, S. (2019) · Molecules · doi:10.3390/molecules24071350 · Cited by 45 · see citing works
Dubreucq, S., Kambiré, S. J., Conforzi, M., Metna‐Laurent, M., Cannich, A., Gómez, E. S., Richard, É. M., Marsicano, G., & Chaouloff, F. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.08.049 · Cited by 44 · see citing works
Slow to warm up: the role of habituation in social fear.
Avery, S., & Blackford, J. (2016) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsw095 · Cited by 42 · see citing works
Almeida-Santos, A. F., Gobira, P. H., Rosa, L. C., Guimaraes, F. S., Moreira, F. A., & Aguiar, D. C. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.05.027 · Cited by 41 · see citing works
Vaughn, L. K., Mantsch, J. R., Vranjkovic, O., Stroh, G., LaCourt, M., Kreutter, M., & Hillard, C. J. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.08.021 · Cited by 41 · see citing works
Self-citationEndocannabinoid signaling in neurotoxicity and neuroprotection
Pope, C., Mechoulam, R., & Parsons, L. H. (2009) · NeuroToxicology · doi:10.1016/j.neuro.2009.12.002 · Cited by 40 · see citing works
Frisardi, V., Panza, F., & Farooqui, A. A. (2011) · Brain Research Reviews · doi:10.1016/j.brainresrev.2011.04.003 · Cited by 40 · see citing works
Gamble‐George, J., Conger, J. R., Hartley, N. D., Gupta, P., Sumislawski, J. J., & Patel, S. (2013) · Psychopharmacology · doi:10.1007/s00213-013-3042-8 · Cited by 39 · see citing works
Self-citationGonda, X., Petschner, P., Eszlari, N., Sutori, S., Gal, Z., Koncz, S., Anderson, I. M., Deakin, B., Juhasz, G., & Bagdy, G. (2019) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2019.00138 · Cited by 37 · see citing works
Radahmadi, M., Hosseini, N., & Nasimi, A. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.09.005 · Cited by 38 · see citing works
Haj‐Dahmane, S., & Shen, R. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.1310-14.2014 · Cited by 38 · see citing works
Batista, L. A., Gobira, P. H., Viana, T. G., de Aguiar, D. C., & Moreira, F. A. (2014) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000073 · Cited by 38 · see citing works
A synaptocentric view of the neuroendocrine response to stress
Cusulin, J. I. W., & Bains, J. S. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07513.x · Cited by 37 · see citing works
The Management of Cancer Symptoms and Treatment-Induced Side Effects With Cannabis or Cannabinoids
Sexton, M., Garcia, J. M., Jatoi, A., Clark, C. S., & Wallace, M. S. (2021) · JNCI Monographs · doi:10.1093/jncimonographs/lgab011 · Cited by 36 · see citing works
Kondev, V., Najeed, M., Yasmin, F., Morgan, A., Loomba, N., Johnson, K., Adank, D. N., Dong, A., Delpire, E. J., Li, Y., et al. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.113027 · Cited by 35 · see citing works
Self-citationHauer, 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
Sánchez-Marín, L., Flores-López, M., Pastor, A., Gavito, A. L., Suárez, J., de la Torre, R., Pavón, F. J., Rodríguez de Fonseca, F., & Serrano, A. (2022) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2021.110460 · Cited by 33 · see citing works
Cannabinoids and Reproduction: A Lasting and Intriguing History
Cacciola, G., Chianese, R., Chioccarelli, T., Ciaramella, V., Fasano, S., Pierantoni, R., Meccariello, R., & Cobellis, G. (2010) · Pharmaceuticals · doi:10.3390/ph3103275 · Cited by 33 · see citing works
Dono, L. M., & Currie, P. J. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.06.019 · Cited by 32 · 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
Naef, L., Gratton, A. P., & Walker, C. (2013) · Stress · doi:10.3109/10253890.2013.805321 · Cited by 30 · see citing works
Emotional, endocrine and brain anandamide response to social challenge in infant male rats
Marco, E. M., Scattoni, M. L., Rapino, C., Ceci, C., Chaves, N., Macrı̀, S., Maccarrone, M., & Giovanni Laviola, A. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.04.004 · Cited by 27 · see citing works
Simone, J. J., Green, M. R., Hodges, T. E., & McCormick, C. M. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.11.012 · Cited by 28 · see citing works
Endocannabinoids: Stress, Anxiety, and Fear
Taber, K. H., & Hurley, R. A. (2009) · Journal of Neuropsychiatry · doi:10.1176/jnp.2009.21.2.iv · Cited by 27 · see citing works
A review of the effects of acute and chronic cannabinoid exposure on the stress response
Glodosky, N. C., Cuttler, C., & McLaughlin, R. J. (2021) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2021.100945 · Cited by 28 · see citing works
Clarke, D. J., Stuart, J. M., McGregor, I. S., & Arnold, J. C. (2016) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2016.08.006 · Cited by 26 · see citing works
Anxiolytic effects of endocannabinoid enhancing compounds: A systematic review and meta-analysis
Kwee, C., Leen, N. A., der Kamp, R. C. V., Lissa, C. J. V., Cath, D. C., Groenink, L., & Baas, J. M. P. (2023) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2023.04.001 · Cited by 23 · see citing works
Italia, M., Forastieri, C., Longaretti, A., Battaglioli, E., & Rusconi, F. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21207455 · Cited by 25 · see citing works
Kang, M., Bohorquez‐Montoya, L., McAuliffe, T. L., Claesges, S. A., Blair, N.-O. P., Sauber, G., Reynolds, C. F., Hillard, C. J., & Goveas, J. S. (2021) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2021.783187 · Cited by 22 · see citing works
Self-citationVariants in the CNR1 gene predispose to headache with nausea in the presence of life stress
Juhász, G., Csépány, É., Magyar, M., Édes, A. E., Eszlári, N., Hullám, G., Antal, P., Kökönyei, G., Anderson, I. M., Deakin, J. F. W., et al. (2016) · Genes Brain & Behavior · doi:10.1111/gbb.12352 · Cited by 22 · see citing works
Feedforward inhibition of stress by brainstem neuropeptide Y neurons
Zhang, Y., Shen, J., Xie, F., Liu, Z., Yin, F., Cheng, M., Wang, L., Cai, M., Herzog, H., Wu, P., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-51956-9 · Cited by 20 · see citing works
Endocannabinoids and the cardiovascular response to stress
O’Sullivan, S. E., Kendall, P. J., & Kendall, D. A. (2011) · Journal of Psychopharmacology · doi:10.1177/0269881111408457 · Cited by 20 · see citing works
- Authors
- Patel, S., & Hillard, C. J.
- Affiliations
- Vanderbilt University Medical Center (US)
- Medical College of Wisconsin (US)
- Corresponding author
- Patel, Sachin
- Venue
- European Journal of Neuroscience
- Publisher
- Wiley
- Published
- 2008-06
- Volume
- 27
- Issue
- 11
- Pages
- 2821-2829
- ISSN
- 0953-816X (ISSN-L)
- 1460-9568
- PMC
- PMC2593941
- OpenAlex
- W1981670902
- Cited by
- 162
- References
- 95
- Citations by year
- 2026: 1 · 2025: 4 · 2024: 6 · 2023: 4 · 2022: 8 · 2021: 8 · 2020: 6 · 2019: 8 · 2018: 6 · 2017: 4 · 2016: 7 · 2015: 13 · 2014: 12 · 2013: 18 · 2012: 15
- FWCI
- 1.51
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- European Journal of Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health
- National Institute on Drug Abuse (F30 DA15575, R01DA016967, F30DA015575, R21DA022439)
- 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 › Neurotransmitter Receptor Influence on Behavior
- Keywords
- endocannabinoid signaling, stress habituation, chronic stress, anxiety, depression, mood disorders
- MeSH terms
- Adaptation, Physiological, Animals, Anxiety Disorders, Brain, Depressive Disorder, Disease Models, Animal, Humans, Stress, Psychological, Mood Disorders, Cannabinoid Receptor Modulators, Endocannabinoids
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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