Disruption of fatty acid amide hydrolase activity prevents the effects of chronic stress on anxiety and amygdalar microstructure
Open accessAbstract
Hyperactivation of the amygdala following chronic stress is believed to be one of the primary mechanisms underlying the increased propensity for anxiety-like behaviors and pathological states; however, the mechanisms by which chronic stress modulates amygdalar function are not well characterized. The aim of the current study was to determine the extent to which the endocannabinoid (eCB) system, which is known to regulate emotional behavior and neuroplasticity, contributes to changes in amygdalar structure and function following chronic stress. To examine the hypothesis, we have exposed C57/Bl6 mice to chronic restraint stress, which results in an increase in fatty acid amide hydrolase (FAAH) activity and a reduction in the concentration of the eCB N-arachidonylethanolamine (AEA) within the amygdala. Chronic restraint stress also increased dendritic arborization, complexity and spine density of pyramidal neurons in the basolateral nucleus of the amygdala (BLA) and increased anxiety-like behavior in wild-type mice. All of the stress-induced changes in amygdalar structure and function were absent in mice deficient in FAAH. Further, the anti-anxiety effect of FAAH deletion was recapitulated in rats treated orally with a novel pharmacological inhibitor of FAAH, JNJ5003 (50 mg per kg per day), during exposure to chronic stress. These studies suggest that FAAH is required for chronic stress to induce hyperactivity and structural remodeling of the amygdala. Collectively, these studies indicate that FAAH-mediated decreases in AEA occur following chronic stress and that this loss of AEA signaling is functionally relevant to the effects of chronic stress. These data support the hypothesis that inhibition of FAAH has therapeutic potential in the treatment of anxiety disorders, possibly by maintaining normal amygdalar function in the face of chronic stress.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Gene deletion or pharmacological inhibition of FAAH prevents stress-induced reductions in AEA and associated increases in BLA dendritic hypertrophy and anxiety-like behavior.
“Gene deletion or pharmacological inhibition of FAAH prevents stress-induced reductions in AEA and associated increases in BLA dendritic hypertrophy and anxiety-like behavior.”
From Amygdala FAAH and anandamide: mediating protection and recovery from stress (2013) · cites this paper as [68]
The chronic stress-induced morphological changes in BLA pyramidal neurons are absent in mutant mice lacking FAAH.
“These morphological changes are absent in mutant mice lacking FAAH [68]”
From Amygdala FAAH and anandamide: mediating protection and recovery from stress (2013) · cites this paper as [68]
Rodents exposed to chronic stress show sustained enhancement of FAAH activity and prolonged reductions in tissue levels of BLA AEA that persist beyond exposure.
“Rodents exposed to chronic stress show sustained enhancement of FAAH activity and prolonged reductions in tissue levels of BLA AEA that persist beyond exposure [59,68,69].”
From Amygdala FAAH and anandamide: mediating protection and recovery from stress (2013) · cites this paper as [68]
Genetic loss or repeated, pre-stress pharmacological inhibition of FAAH prevents stress-induced reductions in AEA and increases in HPA activity and anxiety-like behavior.
“whereas genetic loss or repeated, pre-stress pharmacological inhibition (JNJ5003) of FAAH prevents stress-induced reductions in AEA and increases in HPA activity and anxiety-like behavior [68,73,74]”
From Amygdala FAAH and anandamide: mediating protection and recovery from stress (2013) · cites this paper as [68]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Physiology and neurobiology of stress and adaptation: central role of the brain
McEwen, B. S. (2007) · Physiological Reviews · doi:10.1152/physrev.00041.2006 · Cited by 4,981 · see citing works
Self-citationStress and the brain: from adaptation to disease
de Kloet, E. R., Joëls, M., & Holsboer, F. (2005) · Nature Reviews Neuroscience · doi:10.1038/nrn1683 · Cited by 4,621 · see citing works
Contributions of the Amygdala to Emotion Processing: From Animal Models to Human Behavior
Phelps, E. A., & LeDoux, J. E. (2005) · Neuron · doi:10.1016/j.neuron.2005.09.025 · Cited by 3,203 · see citing works
The Neurocircuitry of Fear, Stress, and Anxiety Disorders
Shin, L. M., & Liberzon, I. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2009.83 · Cited by 2,083 · 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
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
Self-citationMCEWEN, B. S. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1314.001 · Cited by 1,638 · see citing works
Self-citationNeurocircuitry of Mood Disorders
Price, J. L., & Drevets, W. C. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2009.104 · Cited by 1,606 · see citing works
Role 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
Joëls, M., & Baram, T. Z. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2632 · Cited by 1,521 · see citing works
Cravatt, B. F., Demarest, K., Patricelli, M. P., Bracey, M. H., Giang, D. K., Martin, B. R., & Lichtman, A. H. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.161191698 · Cited by 1,310 · see citing works
Self-citationCortical pathways to the mammalian amygdala
McDonald, A. J. (1998) · Progress in Neurobiology · doi:10.1016/s0301-0082(98)00003-3 · Cited by 1,303 · see citing works
Pitkänen, A., Savander, V., & LeDoux, J. E. (1997) · Trends in Neurosciences · doi:10.1016/s0166-2236(97)01125-9 · Cited by 980 · see citing works
Postsynaptic endocannabinoid release is critical to long-term depression in the striatum
Gerdeman, G. L., Ronesi, J. A., & Lovinger, D. M. (2002) · Nature Neuroscience · doi:10.1038/nn832 · Cited by 767 · see citing works
Stress duration modulates the spatiotemporal patterns of spine formation in the basolateral amygdala
Mitra, R., Jadhav, S., McEwen, B. S., Vyas, A., & Chattarji, S. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0504011102 · Cited by 663 · see citing works
Self-citationGulyas, A. I., Cravatt, B. F., Bracey, M. H., Dinh, T. P., Piomelli, D., Boscia, F., & Freund, T. F. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03428.x · Cited by 561 · see citing works
Self-citationVyas, A., Pillai, A. G., & Chattarji, S. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2004.07.013 · Cited by 445 · see citing works
Self-citationAcute corticosterone treatment is sufficient to induce anxiety and amygdaloid dendritic hypertrophy
Mitra, R., & Sapolsky, R. M. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0705615105 · Cited by 409 · see citing works
Patel, S., & Hillard, C. J. (2006) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.106.101287 · Cited by 390 · see citing works
Self-citationWellman, C. L., Izquierdo, A., Garrett, J. E., Martin, K. P., Carroll, J., Millstein, R., Lesch, K.-P., Murphy, D. L., & Holmes, A. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.4595-06.2007 · Cited by 366 · 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-citationMetaplasticity of amygdalar responses to the stress hormone corticosterone
Karst, H., Berger, S., Erdmann, G., Schütz, G., & Joëls, M. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0914381107 · Cited by 342 · see citing works
Govindarajan, A., Rao, B. S. S., Nair, D., Trinh, M. A., Mawjee, N., Tonegawa, S., & Chattarji, S. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0605180103 · Cited by 332 · see citing works
Self-citationGubellini, P., Picconi, B., Bari, M., Battista, N., Calabresi, P., Centonze, D., Bernardi, G., Finazzi‐Agrò, A., & Maccarrone, M. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-16-06900.2002 · Cited by 321 · see citing works
Regulation of anxiety by GABAA receptors in the rat amygdala
Sanders, S., & Shekhar, A. (1995) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(95)00153-n · Cited by 319 · see citing works
van Marle, H. J. F., Hermans, E. J., Qin, S., & Fernández, G. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2009.05.014 · Cited by 317 · see citing works
Hill, M. N., McLaughlin, R. J., Morrish, A. C., Viau, V., Floresco, S. B., Hillard, C. J., & Gorzalka, B. B. (2009) · Neuropsychopharmacology · doi:10.1038/npp.2009.114 · Cited by 304 · see citing works
Self-citationProlonged behavioral stress enhances synaptic connectivity in the basolateral amygdala
Vyas, A., Jadhav, S., & Chattarji, S. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.08.003 · Cited by 299 · see citing works
Self-citationPatel, S., Roelke, C. T., Rademacher, D. J., & Hillard, C. J. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.03916.x · Cited by 297 · see citing works
Self-citationRainnie, D. G., Bergeron, R., Sajdyk, T. J., Patil, M. M., Gehlert, D. R., & Shekhar, A. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.5740-03.2004 · Cited by 293 · see citing works
Serum Endocannabinoid Content is Altered in Females with Depressive Disorders: A Preliminary Report
Hill, M., Miller, G., Ho, W.-S., Gorzalka, B., & Hillard, C. (2008) · Pharmacopsychiatry · doi:10.1055/s-2007-993211 · Cited by 292 · see citing works
Self-citationChronic Stress Causes Amygdala Hyperexcitability in Rodents
Rosenkranz, J. A., Venheim, E. R., & Padival, M. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.02.008 · Cited by 284 · see citing works
Moreira, F. A., Kaiser, N., Monory, K., & Lutz, B. (2007) · Neuropharmacology · doi:10.1016/j.neuropharm.2007.07.005 · Cited by 282 · see citing works
Circuitry for associative plasticity in the amygdala involves endocannabinoid signaling
Azad, S. C., Monory, K., Marsicano, G., Cravatt, B. F., Lutz, B., Zieglgänsberger, W., & Rammes, G. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.2134-04.2004 · Cited by 263 · see citing works
Endocannabinoid-mediated long-term plasticity requires cAMP/PKA signaling and RIM1α
Chevaleyre, V., Heifets, B. D., Kaeser, P. S., Südhof, T. C., & Castillo, P. E. (2007) · Neuron · doi:10.1016/j.neuron.2007.05.020 · Cited by 261 · see citing works
Hariri, A. R., Gorka, A. X., Hyde, L. W., Kimak, M. A., Halder, I., Ducci, F., Ferrell, R. E., Goldman, D. A., & Manuck, S. B. (2008) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.10.047 · Cited by 250 · see citing works
Hill, M. N., Carrier, E. J., McLaughlin, R. J., Morrish, A. C., Meier, S. E., Hillard, C. J., & Gorzalka, B. B. (2008) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2008.05567.x · Cited by 246 · see citing works
Self-citationRole of stress, corticotrophin releasing factor (CRF) and amygdala plasticity in chronic anxiety
Shekhar, A., Truitt, W., Rainnie, D., & Sajdyk, T. (2005) · Stress · doi:10.1080/10253890500504557 · Cited by 237 · 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
Self-citationHillard, C. J., Wilkison, D. M., Edgemond, W. S., & Campbell, W. B. (1995) · Biochimica et Biophysica Acta (BBA) - Lipids and Lipid Metabolism · doi:10.1016/0005-2760(95)00087-s · Cited by 233 · see citing works
Self-citationRademacher, D. J., Meier, S. E., Shi, L., Vanessa Ho, W.-S., Jarrahian, A., & Hillard, C. J. (2008) · Neuropharmacology · doi:10.1016/j.neuropharm.2007.06.012 · Cited by 233 · see citing works
Self-citationMozhui, K., Karlsson, R.-M., Kash, T. L., Ihne, J., Norcross, M., Patel, S., Farrell, M. R., Hill, E. E., Graybeal, C., Martin, K. P., et al. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.5017-09.2010 · Cited by 226 · see citing works
Domenici, M. R., Azad, S. C., Marsicano, G., Schierloh, A., Wotjak, C. T., Dodt, H.-U., Zieglgänsberger, W., Lutz, B., & Rammes, G. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.0372-06.2006 · Cited by 224 · see citing works
Pesold, C., & Treit, D. (1995) · Brain Research · doi:10.1016/0006-8993(94)01318-c · Cited by 208 · see citing works
Marzo, V. D., & PETROCELLIS, L. D. (2010) · Current Medicinal Chemistry · doi:10.2174/092986710790980078 · Cited by 197 · see citing works
A technique for estimating total spine numbers on golgi‐impregnated dendrites
Feldman, M. L., & Peters, A. (1979) · The Journal of Comparative Neurology · doi:10.1002/cne.901880403 · Cited by 194 · see citing works
Evaluation of fatty acid amide hydrolase inhibition in murine models of emotionality
Naidu, P. S., Varvel, S. A., Ahn, K., Cravatt, B. F., Martin, B. R., & Lichtman, A. H. (2007) · Psychopharmacology · doi:10.1007/s00213-006-0689-4 · Cited by 184 · see citing works
Self-citationHill, 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-citationHaller, J., Barna, I., Barsvari, B., Gyimesi Pelczer, K., Yasar, S., Panlilio, L. V., & Goldberg, S. (2009) · Psychopharmacology · doi:10.1007/s00213-009-1494-7 · Cited by 159 · see citing works
Patel, 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
TRPV1 channels facilitate glutamate transmission in the striatum
Musella, A., Chiara, V. D., Rossi, S., Prosperetti, C., Bernardi, G., Maccarrone, M., & Centonze, D. (2008) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2008.09.001 · Cited by 146 · see citing works
Estrogen recruits the endocannabinoid system to modulate emotionality.
Hill, M., Karacabeyli, E., & Gorzalka, B. (2007) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2007.02.003 · Cited by 141 · see citing works
Self-citationBambico, F. R., Cassano, T., Domínguez-López, S., Katz, N., Walker, C. D., Piomelli, D., & Gobbi, G. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2010.80 · Cited by 139 · see citing works
Fat-induced satiety factor oleoylethanolamide enhances memory consolidation
Campolongo, P., Roozendaal, B., Trezza, V., Cuomo, V., Astarita, G., Fu, J., McGaugh, J. L., & Piomelli, D. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0903038106 · Cited by 133 · see citing works
Hill, M. N., Hillard, C. J., & McEwen, B. S. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhq280 · Cited by 127 · see citing works
Self-citationSumislawski, J. J., Ramikie, T. S., & Patel, S. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2011.166 · Cited by 124 · see citing works
Patel, S., Carrier, E. J., Ho, W. ‐. V., Rademacher, D. J., Cunningham, S., Reddy, D. S., Falck, J. R., Cravatt, B. F., & Hillard, C. J. (2004) · Journal of Lipid Research · doi:10.1194/jlr.m400377-jlr200 · Cited by 123 · see citing works
Self-citationBiomarkers of Endocannabinoid System Activation in Severe Obesity
Sipe, J. C., Scott, T. M., Murray, S., Harismendy, O., Simon, G. M., Cravatt, B. F., & Waalen, J. (2010) · PLoS ONE · doi:10.1371/journal.pone.0008792 · Cited by 119 · see citing works
Self-citationSajdyk, T. J., & Shekhar, A. (1997) · Brain Research · doi:10.1016/s0006-8993(97)00594-5 · Cited by 107 · see citing works
Trommald, M., Jensen, V., & Andersen, P. N. (1995) · The Journal of Comparative Neurology · doi:10.1002/cne.903530208 · Cited by 106 · see citing works
Chronic Cold Stress Alters Prefrontal Cortical Modulation of Amygdala Neuronal Activity in Rats
Correll, C. M., Rosenkranz, J. A., & Grace, A. A. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.04.009 · Cited by 106 · see citing works
Development of microglia in the prenatal rat hippocampus
Dalmau, I., Finsen, B. R., T�nder, N., Zimmer, J., Gonz�lez, B., & Castellano, B. (1997) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19970106)377:1 · Cited by 99 · see citing works
Arachidonoyl ethanolamide-[1,2-14C] as a substrate for anandamide amidase
Omeir, R. L., Chin, S. A., Hong, Y. H., Ahern, D. G., & Deutsch, D. G. (1995) · Life Sciences · doi:10.1016/0024-3205(95)00181-5 · Cited by 99 · see citing works
Horner, C. H., & Arbuthnott, E. R. (1991) · Europe PMC (PubMed Central) · Cited by 90 · see citing works
Sanders, S., & Shekhar, A. (1995) · Biological Psychiatry · doi:10.1016/0006-3223(94)00183-4 · Cited by 88 · 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
Rossi, S., De Chiara, V., Musella, A., Sacchetti, L., Cantarella, C., Castelli, M., Cavasinni, F., Motta, C., Studer, V., Bernardi, G., et al. (2010) · Molecular Pharmacology · doi:10.1124/mol.110.064196 · Cited by 82 · see citing works
Self-citationPetersen, E. N., Bræstrup, C., & Scheel‐Krüger, J. (1985) · Neuroscience Letters · doi:10.1016/0304-3940(85)90552-x · Cited by 71 · see citing works
Huang, Y.-C., Wang, S., Chiou, L., & Gean, P. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-32-10311.2003 · Cited by 70 · see citing works
Mitra, R., Ferguson, D., & Sapolsky, R. M. (2009) · Molecular Psychiatry · doi:10.1038/mp.2009.9 · Cited by 70 · see citing works
Shin, R.-M., Tully, K., Li, Y., Cho, J.-H., Higuchi, M., Suhara, T., & Bolshakov, V. Y. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1009803107 · Cited by 67 · see citing works
Sajdyk, T. J., & Shekhar, A. (2000) · European Journal of Pharmacology · doi:10.1016/s0014-2999(00)00128-x · Cited by 63 · see citing works
Ramikie, T. S., & Patel, S. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2011.08.037 · Cited by 62 · see citing works
Role of amygdaloid nuclei in the anxiolytic effects of benzodiazepines in rats
Green, S., & Vale, A. L. (1992) · Behavioural Pharmacology · doi:10.1097/00008877-199206000-00010 · Cited by 54 · see citing works
Lithium treatment prevents stress-induced dendritic remodeling in the rodent amygdala
Johnson, S. A., Wang, J., Sun, X., McEwen, B. S., Chattarji, S., & Young, L. T. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.06.005 · Cited by 54 · see citing works
Self-citationKodirov, S. A., Jasiewicz, J., Amirmahani, P., Psyrakis, D., Bonni, K., Wehrmeister, M., & Lutz, B. (2009) · Learning & Memory · doi:10.1101/lm.1663410 · Cited by 51 · see citing works
Buffalari, D. M., & Grace, A. A. (2008) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145708009140 · Cited by 51 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Stress Effects on Neuronal Structure: Hippocampus, Amygdala, and Prefrontal Cortex
McEwen, B. S., Nasca, C., & Gray, J. D. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2015.171 · Cited by 1,574 · see citing works
Self-citationMechanisms of stress in the brain
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
Self-citationRevisiting the Stress Concept: Implications for Affective Disorders
McEwen, B. S., & Akil, H. (2020) · The Journal of Neuroscience · doi:10.1523/jneurosci.0733-19.2019 · Cited by 686 · see citing works
Self-citationThe endocannabinoid system in guarding against fear, anxiety and stress
Lutz, B., Marsicano, G., Maldonado, R., & Hillard, C. J. (2015) · Nature reviews. Neuroscience · doi:10.1038/nrn4036 · Cited by 506 · see citing works
Self-citationNeumeister, A., Normandin, M. D., Pietrzak, R. H., Piomelli, D., Zheng, M. Q., Gujarro-Anton, A., Potenza, M. N., Bailey, C. R., Lin, S. F., Najafzadeh, S., et al. (2013) · Molecular Psychiatry · doi:10.1038/mp.2013.61 · Cited by 361 · see citing works
McEwen, B. S., Gray, J. D., & Nasca, C. (2015) · Journal of Endocrinology · doi:10.1530/joe-15-0121 · Cited by 253 · see citing works
Self-citationCorticotropin-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
Self-citationThe endocannabinoid system as a target for novel anxiolytic drugs
Patel, S., Hill, M. N., Cheer, J. F., Wotjak, C. T., & Holmes, A. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.12.033 · Cited by 233 · see citing works
Self-citationAmygdala FAAH and anandamide: mediating protection and recovery from stress
Gunduz-Cinar, O., Hill, M. N., McEwen, B. S., & Holmes, A. (2013) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2013.08.008 · Cited by 229 · see citing works
Self-citationStress and trauma: BDNF control of dendritic-spine formation and regression
Bennett, M. R., & Lagopoulos, J. (2014) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2013.10.005 · Cited by 199 · see citing works
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
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
Redefining neuroendocrinology: Epigenetics of brain-body communication over the life course
McEwen, B. S. (2018) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2017.11.001 · Cited by 129 · see citing works
Self-citationNatividad, L. A., Buczynski, M. W., Herman, M. A., Kirson, D., Oleata, C. S., Irimia, C., Polis, I., Ciccocioppo, R., Roberto, M., & Parsons, L. H. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2017.01.005 · Cited by 84 · see citing works
Serrano, A., Pavon, F. J., Buczynski, M. W., Schlosburg, J., Natividad, L. A., Polis, I. Y., Stouffer, D. G., Zorrilla, E. P., Roberto, M., Cravatt, B. F., et al. (2018) · Neuropsychopharmacology · doi:10.1038/s41386-018-0055-3 · Cited by 83 · see citing works
Self-citationEffects of repeated stress on excitatory drive of basal amygdala neurons in vivo
Padival, M., Quinette, D., & Rosenkranz, J. A. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2013.74 · Cited by 75 · see citing works
Qin, M., Zeidler, Z., Moulton, K., Krych, L., Xia, Z., & Smith, C. B. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.05.003 · Cited by 69 · see citing works
McLaughlin, R. J., Hill, M. N., Dang, S. S., Wainwright, S. R., Galea, L. A. M., Hillard, C. J., & Gorzalka, B. B. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.09.053 · Cited by 65 · see citing works
Self-citationStopponi, S., Fotio, Y., Domi, A., Borruto, A. M., Natividad, L., Roberto, M., Ciccocioppo, R., & Cannella, N. (2018) · Addiction Biology · doi:10.1111/adb.12573 · Cited by 48 · see citing works
Markey, L., Hooper, A., Melon, L. C., Baglot, S., Hill, M. N., Maguire, J., & Kumamoto, C. A. (2020) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2020.104808 · Cited by 45 · see citing works
Self-citationThe endocannabinoid system in social anxiety disorder: from pathophysiology to novel therapeutics
Ahmed, M., Boileau, I., Le Foll, B., Carvalho, A. F., & Kloiber, S. (2022) · Brazilian Journal of Psychiatry · doi:10.1590/1516-4446-2021-1926 · Cited by 11 · see citing works
A precision medicine approach to pharmacological adjuncts to extinction: A call to broaden research
King, G., Baker, K. D., Bisby, M. A., Chan, D., Cowan, C. S. M., Stylianakis, A. A., Zimmermann, K. S., & Richardson, R. (2019) · Psychopharmacology · doi:10.1007/s00213-018-4999-0 · Cited by 6 · see citing works
- Authors
- Hill, M. N., Kumar, S. A., Filipski, S. B., Iverson, M., Stuhr, K. L., Keith, J. M., Cravatt, B. F., Hillard, C. J., Chattarji, S., & McEwen, B. S.
- Affiliations
- University of Calgary (CA)
- National Centre for Biological Sciences (IN)
- Rockefeller University (US)
- Medical College of Wisconsin (US)
- Scripps Research Institute (US)
- Corresponding author
- Hill, M N
- Venue
- Molecular Psychiatry
- Published
- 2012-07-10
- Volume
- 18
- Issue
- 10
- Pages
- 1125-1135
- ISSN
- 1359-4184 (ISSN-L)
- 1476-5578
- PMC
- PMC4148304
- OpenAlex
- W2090774121
- Cited by
- 222
- References
- 77
- Citations by year
- 2026: 5 · 2025: 11 · 2024: 13 · 2023: 13 · 2022: 18 · 2021: 20 · 2020: 18 · 2019: 14 · 2018: 15 · 2017: 23 · 2016: 13 · 2015: 30 · 2014: 9 · 2013: 15 · 2012: 4
- FWCI
- 13.64
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Molecular Psychiatry (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health
- Johnson and Johnson
- Canadian Institutes of Health Research
- National Centre for Biological Sciences
- National Institute of Mental Health (MH-41256, R37MH041256, R01MH041256)
- National Institute on Drug Abuse (R01DA026996, R01DA009155, DA09155, DA026996)
- Janssen Research and Development
- 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 › Neuroscience and Neuropharmacology Research
- Keywords
- fatty acid amide hydrolase, FAAH inhibition, chronic stress, anxiety-like behavior, amygdala, endocannabinoid system, basolateral amygdala, dendritic spine density, pyramidal neurons, restraint stress, anxiety disorders, neuroplasticity
- MeSH terms
- Fatty Acid Amide Hydrolases, Amidohydrolases, Amygdala, Animals, Anxiety, Arachidonic Acids, Chronic Disease, Cyclohexanols, Dendrites, Drug Evaluation, Preclinical, Exploratory Behavior, Male, Mice, Inbred C57BL, Restraint, Physical, Stress, Psychological, Rats, Sprague-Dawley, Pyramidal Cells, Mice, Knockout, Maze Learning, Receptor, Cannabinoid, CB1, Mice, Rats, Polyunsaturated Alkamides, 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 ›
Are you an author, or do you see a problem with this page? Request a review
