Tempering aversive/traumatic memories with cannabinoids: A review of evidence from animal and human studies
Abstract
Rationale Aversive learning and memory are essential to cope with dangerous and stressful stimuli present in an ever-changing environment. When this process is dysfunctional, however, it is associated with posttraumatic stress disorder (PTSD). The endocannabinoid (eCB) system has been implicated in synaptic plasticity associated with physiological and pathological aversive learning and memory.Objective and methods The objective of this study was to review and discuss evidence on how and where in the brain genetic or pharmacological interventions targeting the eCB system would attenuate aversive/traumatic memories through extinction facilitation in laboratory animals and humans. The effect size of the experimental intervention under investigation was also calculated.Results Currently available data indicate that direct or indirect activation of cannabinoid type-1 (CB1) receptor facilitates the extinction of aversive/traumatic memories. Activating CB1 receptors around the formation of aversive/traumatic memories or their reminders can potentiate their subsequent extinction. In most cases, the effect size has been large (Cohen's d ≥ 1.0). The brain areas responsible for the abovementioned effects include the medial prefrontal cortex, amygdala, and/or hippocampus. The potential role of cannabinoid type-2 (CB2) receptors in extinction learning is now under investigation.Conclusion Drugs augmenting the brain eCB activity can temper the impact of aversive/traumatic experiences by diverse mechanisms depending on the moment of their administration. Considering the pivotal role the extinction process plays in PTSD, the therapeutic potential of these drugs is evident. The sparse number of clinical trials testing these compounds in stress-related disorders is a gap in the literature that needs to be addressed.
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Enhanced eCB signalling, for example induced by blocking FAAH, reduces stress and anxiety responses and promotes fear-extinction learning.
“Enhanced eCB signallingfor example, induced by blocking the serine hydrolase enzyme FAAHreduces stress and anxiety responses and promotes fear-extinction learning (Gunduz-Cinar, Hill, McEwen, & Holmes, 2013;Lisboa et al., 2019;Mayo et al., 2019;Patel et al., 2017).”
From Novel pharmacological targets in drug development for the treatment of anxiety and anxiety-related disorders (2019) · cites this paper as Lisboa et al., 2019
Cites
Statistical Power Analysis for the Behavioral Sciences
Muller, K. E., & Cohen, J. (1989) · Technometrics · doi:10.2307/1270020 · Cited by 99,588 · see citing works
Statistical power analysis for the behavioral sciences
Cohen, J. (1990) · Computers Environment and Urban Systems · doi:10.1016/0198-9715(90)90050-4 · Cited by 65,406 · see citing works
LeDoux, J. E. (2000) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.23.1.155 · Cited by 8,444 · see citing works
da Luz, A. C. D. D. S., Dias, G. P., Bevilaqua, M. C. D. N., Cocks, G. D., Gardino, P. F., Thuret, S., & Nardi, A. E. (2013) · Neuropsychobiology · doi:10.1159/000353269 · Cited by 4,012 · see citing works
Etkin, A., & Wager, T. D. (2007) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2007.07030504 · Cited by 3,391 · see citing works
The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review.
Prut, L., & Belzung, C. (2003) · European Journal of Pharmacology · doi:10.1016/s0014-2999(03)01272-x · Cited by 3,190 · see citing works
Fear memories require protein synthesis in the amygdala for reconsolidation after retrieval
Nader, K., Schafe, G. E., & Le Doux, J. E. (2000) · Nature · doi:10.1038/35021052 · Cited by 2,706 · 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
Vanilloid receptors on sensory nerves mediate the vasodilator action of anandamide
Zygmunt, P. M., Petersson, J., Andersson, D. A., Chuang, H.-H., Sørgård, M., Di Marzo, V., Julius, D., & Högestätt, E. D. (1999) · Nature · doi:10.1038/22761 · Cited by 2,142 · see citing works
STRESS AND HIPPOCAMPAL PLASTICITY
McEwen, B. S. (1999) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.22.1.105 · Cited by 2,087 · 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 molecular logic of endocannabinoid signalling
Piomelli, D. (2003) · Nature Reviews Neuroscience · doi:10.1038/nrn1247 · Cited by 1,957 · see citing works
Effects of an expanding-spaced vs massed exposure schedule on fear reduction and return of fear
Rowe, M. K., & Craske, M. G. (1998) · Behaviour Research and Therapy · doi:10.1016/s0005-7967(97)10016-x · Cited by 1,778 · see citing works
Stress, memory and the amygdala
Roozendaal, B., McEwen, B. S., & Chattarji, S. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2651 · Cited by 1,760 · see citing works
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
Neural Mechanisms of Extinction Learning and Retrieval
Quirk, G. J., & Mueller, D. (2008) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301555 · Cited by 1,645 · see citing works
Smaller hippocampal volume predicts pathologic vulnerability to psychological trauma
Gilbertson, M. W., Shenton, M. E., Ciszewski, A., Kasai, K., Lasko, N. B., Orr, S. P., & Pitman, R. K. (2002) · Nature Neuroscience · doi:10.1038/nn958 · Cited by 1,635 · see citing works
Pattern Separation in the Dentate Gyrus and CA3 of the Hippocampus
Leutgeb, J. K., Leutgeb, S., Moser, M.-B., & Moser, E. I. (2007) · Science · doi:10.1126/science.1135801 · Cited by 1,601 · see citing works
Immunohistochemical distribution of cannabinoid CB1 receptors in the rat central nervous system
Tsou, K., Brown, S., Sañudo-Peña, M. C., Mackie, K., & Walker, J. M. (1998) · Neuroscience · doi:10.1016/s0306-4522(97)00436-3 · Cited by 1,586 · see citing works
Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation
Sahay, A., Scobie, K. N., Hill, A. S., O'Carroll, C. M., Kheirbek, M. A., Burghardt, N. S., Fenton, A. A., Dranovsky, A., & Hen, R. (2011) · Nature · doi:10.1038/nature09817 · Cited by 1,567 · see citing works
The contextual brain: implications for fear conditioning, extinction and psychopathology
Maren, S., Phan, K. L., & Liberzon, I. (2013) · Nature Reviews Neuroscience · doi:10.1038/nrn3492 · Cited by 1,547 · see citing works
Pattern separation in the hippocampus
Yassa, M. A., & Stark, C. E. L. (2011) · Trends in Neurosciences · doi:10.1016/j.tins.2011.06.006 · Cited by 1,544 · see citing works
Biological studies of post-traumatic stress disorder
Pitman, R. K., Rasmusson, A. M., Koenen, K. C., Shin, L. M., Orr, S. P., Gilbertson, M. W., Milad, M. R., & Liberzon, I. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3339 · Cited by 1,529 · see citing works
Endocannabinoid-Mediated Control of Synaptic Transmission
Kano, M., Ohno‐Shosaku, T., Hashimotodani, Y., Uchigashima, M., & Watanabe, M. (2009) · Physiological Reviews · doi:10.1152/physrev.00019.2008 · Cited by 1,529 · see citing works
Fear Extinction as a Model for Translational Neuroscience: Ten Years of Progress
Milad, M. R., & Quirk, G. J. (2012) · Annual Review of Psychology · doi:10.1146/annurev.psych.121208.131631 · Cited by 1,466 · see citing works
Rauch, S. L., Shin, L. M., & Phelps, E. A. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.06.004 · Cited by 1,397 · see citing works
Brain monoglyceride lipase participating in endocannabinoid inactivation
Dinh, T. P., Carpenter, D., Leslie, F. M., Freund, T. F., Katona, I., Sensi, S. L., Kathuria, S., & Piomelli, D. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.152334899 · Cited by 1,373 · see citing works
Neurobiological Basis of Failure to Recall Extinction Memory in Posttraumatic Stress Disorder
Milad, M. R., Pitman, R. K., Ellis, C. B., Gold, A. L., Shin, L. M., Lasko, N. B., Zeidan, M. A., Handwerger, K., Orr, S. P., & Rauch, S. L. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2009.06.026 · Cited by 1,339 · see citing works
Endocannabinoid Signaling in the Brain
Wilson, R. I., & Nicoll, R. A. (2002) · Science · doi:10.1126/science.1063545 · Cited by 1,260 · see citing works
Preventing the return of fear in humans using reconsolidation update mechanisms
Schiller, D., Monfils, M.-H., Raio, C. M., Johnson, D. C., LeDoux, J. E., & Phelps, E. A. (2010) · Nature · doi:10.1038/nature08637 · Cited by 1,248 · see citing works
Sierra-Mercado, D., Padilla-Coreano, N., & Quirk, G. J. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2010.184 · Cited by 1,190 · see citing works
Memory Reconsolidation and Extinction Have Distinct Temporal and Biochemical Signatures
Suzuki, A., Josselyn, S. A., Frankland, P. W., Masushige, S., Silva, A. J., & Kida, S. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.5491-03.2004 · Cited by 1,127 · see citing works
Ethological and temporal analyses of anxiety-like behavior: The elevated plus-maze model 20 years on
Carobrez, A. P., & Bertoglio, L. J. (2005) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.04.017 · Cited by 993 · see citing works
Self-citationDentate gyrus NMDA receptors mediate rapid pattern separation in the hippocampal network
McHugh, T. J., Jones, M. W., Quinn, J. J., Balthasar, N., Coppari, R., Elmquist, J. K., Lowell, B. B., Fanselow, M. S., Wilson, M. A., & Tonegawa, S. (2007) · Science · doi:10.1126/science.1140263 · Cited by 958 · see citing works
Gurvits, T. V., Shenton, M. E., Hokama, H., Ohta, H., Lasko, N. B., Gilbertson, M. W., Orr, S. P., Kikinis, R., Jolesz, F. A., McCarley, R. W., et al. (1996) · Biological Psychiatry · doi:10.1016/s0006-3223(96)00229-6 · Cited by 899 · see citing works
Post-traumatic stress disorder.
Yehuda, R., Hoge, C. W., McFarlane, A. C., Vermetten, E., Lanius, R. A., Nievergelt, C. M., Hobfoll, S. E., Koenen, K. C., Neylan, T. C., & Hyman, S. E. (2015) · Nature Reviews Disease Primers · doi:10.1038/nrdp.2015.57 · Cited by 870 · see citing works
Role of adrenal stress hormones in forming lasting memories in the brain
McGaugh, J. L., & Roozendaal, B. (2002) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(02)00306-9 · Cited by 818 · see citing works
Bremner, J. D., Vythilingam, M., Vermetten, E. H. G. J. M., Southwick, S. M., McGlashan, T. H., Nazeer, A., Khan, S., Vaccarino, V., Soufer, R., Garg, P. K., et al. (2003) · American Journal of Psychiatry · doi:10.1176/appi.ajp.160.5.924 · Cited by 721 · see citing works
Synaptic and Behavioral Profile of Multiple Glutamatergic Inputs to the Nucleus Accumbens
Britt, J. P., Benaliouad, F., McDevitt, R. A., Stuber, G. D., Wise, R. A., & Bonci, A. (2012) · Neuron · doi:10.1016/j.neuron.2012.09.040 · Cited by 716 · see citing works
De novo conditioning in trauma-exposed individuals with and without posttraumatic stress disorder.
Orr, S. P., Metzger, L. J., Lasko, N. B., Macklin, M. L., Peri, T., & Pitman, R. K. (2000) · Journal of Abnormal Psychology · doi:10.1037/0021-843x.109.2.290 · Cited by 653 · see citing works
Shin, L. M., McNally, R. J., Kosslyn, S. M., Thompson, W. L., Rauch, S. L., Alpert, N. M., Metzger, L. J., Lasko, N. B., Orr, S. P., & Pitman, R. K. (1999) · American Journal of Psychiatry · doi:10.1176/ajp.156.4.575 · Cited by 647 · see citing works
Brain activation in PTSD in response to trauma-related stimuli
Liberzon, I., Taylor, S. F., Amdur, R., Jung, T. D., Chamberlain, K. R., Minoshima, S., Koeppe, R. A., & Fig, L. M. (1999) · Biological Psychiatry · doi:10.1016/s0006-3223(98)00246-7 · Cited by 635 · see citing works
Mahan, A. L., & Ressler, K. J. (2011) · Trends in Neurosciences · doi:10.1016/j.tins.2011.06.007 · Cited by 616 · see citing works
Fear extinction in rats: Implications for human brain imaging and anxiety disorders
Milad, M. R., Rauch, S. L., Pitman, R. K., & Quirk, G. J. (2006) · Biological Psychology · doi:10.1016/j.biopsycho.2006.01.008 · Cited by 597 · see citing works
Hippocampal Memory Traces Are Differentially Modulated by Experience, Time, and Adult Neurogenesis
Denny, C. A., Kheirbek, M. A., Alba, E. L., Tanaka, K. F., Brachman, R. A., Laughman, K. B., Tomm, N. K., Turi, G. F., Losonczy, A., & Hen, R. (2014) · Neuron · doi:10.1016/j.neuron.2014.05.018 · Cited by 558 · see citing works
Stress-restress: Effects on ACTH and fast feedback
Liberzon, I., Krstov, M., & Young, E. A. (1997) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(97)00044-9 · Cited by 556 · see citing works
Brunet, A., Orr, S. P., Tremblay, J., Robertson, K., Nader, K., & Pitman, R. K. (2008) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2007.05.006 · Cited by 548 · see citing works
Neurogenesis and generalization: a new approach to stratify and treat anxiety disorders
Kheirbek, M., Klemenhagen, K. C., Sahay, A., & Hen, R. (2012) · Nature Neuroscience · doi:10.1038/nn.3262 · Cited by 543 · see citing works
Hou, L., & Klann, E. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.0995-04.2004 · Cited by 527 · see citing works
Presence and acquired origin of reduced recall for fear extinction in PTSD: Results of a twin study
Milad, M. R., Orr, S. P., Lasko, N. B., Chang, Y., Rauch, S. L., & Pitman, R. K. (2008) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2008.01.017 · Cited by 512 · see citing works
A Role for the Human Dorsal Anterior Cingulate Cortex in Fear Expression
Milad, M. R., Quirk, G. J., Pitman, R. K., Orr, S. P., Fischl, B., & Rauch, S. L. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2007.04.032 · Cited by 485 · see citing works
From Pavlov to PTSD: The extinction of conditioned fear in rodents, humans, and anxiety disorders
VanElzakker, M. B., Kathryn Dahlgren, M., Caroline Davis, F., Dubois, S., & Shin, L. M. (2014) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2013.11.014 · Cited by 482 · see citing works
Blechert, J., Michael, T., Vriends, N., Margraf, J., & Wilhelm, F. H. (2007) · Behaviour Research and Therapy · doi:10.1016/j.brat.2007.02.012 · Cited by 479 · see citing works
Consolidation of Fear Extinction Requires Protein Synthesis in the Medial Prefrontal Cortex
Santini, E., Ge, H., Ren, K., de Ortiz, S. P., & Quirk, G. J. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.0786-04.2004 · Cited by 479 · see citing works
Implications of memory modulation for post-traumatic stress and fear disorders
Parsons, R. G., & Ressler, K. J. (2013) · Nature Neuroscience · doi:10.1038/nn.3296 · Cited by 476 · see citing works
Impaired safety signal learning may be a biomarker of PTSD
Jovanovic, T., Kazama, A., Bachevalier, J., & Davis, M. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.02.023 · Cited by 473 · see citing works
Elzinga, B. (2002) · Journal of Affective Disorders · doi:10.1016/s0165-0327(01)00351-2 · Cited by 473 · see citing works
Izquierdo, A., Wellman, C. L., & Holmes, A. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.0474-06.2006 · Cited by 459 · see citing works
Hippocampal Inactivation Disrupts Contextual Retrieval of Fear Memory after Extinction
Corcoran, K. A., & Maren, S. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-05-01720.2001 · Cited by 455 · see citing works
Izquierdo, I., Furini, C. R. G., & Myskiw, J. C. (2016) · Physiological Reviews · doi:10.1152/physrev.00018.2015 · Cited by 453 · see citing works
Expression and distribution of vanilloid receptor 1 (TRPV1) in the adult rat brain
Tóth, A., Boczán, J., Kedei, N., Lizanecz, E., Bagi, Z. A., Papp, Z., Edes, I. F., Csiba, L., & Blumberg, P. M. (2005) · Molecular Brain Research · doi:10.1016/j.molbrainres.2004.12.003 · Cited by 452 · see citing works
Quantitative meta-analysis of neural activity in posttraumatic stress disorder
Hayes, J. P., Hayes, S. M., & Mikedis, A. M. (2012) · Biology of Mood & Anxiety Disorders · doi:10.1186/2045-5380-2-9 · Cited by 452 · see citing works
Understanding memory through hippocampal remapping
Colgin, L. L., Moser, E. I., & Moser, M.-B. (2008) · Trends in Neurosciences · doi:10.1016/j.tins.2008.06.008 · Cited by 450 · see citing works
Impaired fear inhibition is a biomarker of PTSD but not depression
Jovanovic, T., Norrholm, S. D., Blanding, N. Q., Davis, M., Duncan, E., Bradley, B., & Ressler, K. J. (2010) · Depression and Anxiety · doi:10.1002/da.20663 · Cited by 444 · see citing works
How the Neurocircuitry and Genetics of Fear Inhibition May Inform Our Understanding of PTSD
Jovanović, T., & Ressler, K. J. (2010) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2009.09071074 · Cited by 441 · see citing works
Neural and cellular mechanisms of fear and extinction memory formation
Orsini, C. A., & Maren, S. (2012) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2011.12.014 · Cited by 429 · see citing works
Kitayama, N., Vaccarino, V., Kutner, M., Weiss, P., & Bremner, J. D. (2005) · Journal of Affective Disorders · doi:10.1016/j.jad.2005.05.014 · Cited by 423 · see citing works
Estrous cycle phase and gonadal hormones influence conditioned fear extinction
Milad, M. R., Igoe, S. A., Lebron-Milad, K., & Novales, J. E. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.09.011 · Cited by 417 · see citing works
Maren, S., & Holmes, A. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2015.180 · Cited by 412 · see citing works
Attenuation of frontal asymmetry in pediatric posttraumatic stress disorder
Carrion, V. G., Weems, C. F., Eliez, S., Patwardhan, A., Brown, W., Ray, R. D., & Reiss, A. L. (2001) · Biological Psychiatry · doi:10.1016/s0006-3223(01)01218-5 · Cited by 400 · see citing works
Norrholm, S. D., Jovanovic, T., Olin, I. W., Sands, L. A., Karapanou, I., Bradley, B., & Ressler, K. J. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.09.013 · Cited by 397 · see citing works
Singewald, N., Schmuckermair, C., Whittle, N., Holmes, A., & Ressler, K. J. (2015) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2014.12.004 · Cited by 390 · 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
Enhancing Cannabinoid Neurotransmission Augments the Extinction of Conditioned Fear
Chhatwal, J. P., Davis, M., Maguschak, K. A., & Ressler, K. J. (2005) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300655 · Cited by 376 · see citing works
BREMNER, J. D., VERMETTEN, E., SCHMAHL, C., VACCARINO, V., VYTHILINGAM, M., AFZAL, N., GRILLON, C., & CHARNEY, D. S. (2005) · Psychological Medicine · doi:10.1017/s0033291704003290 · Cited by 370 · see citing works
Garfinkel, S. N., Abelson, J. L., King, A. P. J., Sripada, R. K., Wang, X., Gaines, L. M., & Liberzon, I. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.4287-13.2014 · Cited by 361 · see citing works
Marsch, R., Foeller, E., Rammes, G., Bunck, M., Kössl, M., Holsboer, F., Zieglgänsberger, W., Landgraf, R., Lutz, B., & Wotjak, C. T. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.3303-06.2007 · Cited by 359 · see citing works
Psychophysiologic assessment of aversive conditioning in posttraumatic stress disorder
Peri, T., Ben‐Shakhar, G., Orr, S. P., & Shalev, A. Y. (2000) · Biological Psychiatry · doi:10.1016/s0006-3223(99)00144-4 · Cited by 349 · see citing works
Egertová, M., Giang, D. K., Cravatt, B. F., & Elphick, M. R. (1998) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1998.0543 · Cited by 333 · see citing works
Grillon, C., & Morgan, C. A. (1999) · Journal of Abnormal Psychology · doi:10.1037/0021-843x.108.1.134 · Cited by 331 · see citing works
Wessa, M., & Flor, H. (2007) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2007.07030525 · Cited by 323 · see citing works
The influence of gonadal hormones on conditioned fear extinction in healthy humans
Milad, M. R., Zeidan, M. A., Contero, A., Pitman, R. K., Klibanski, A., Rauch, S. L., & Goldstein, J. M. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.04.030 · Cited by 320 · see citing works
Sim, L. J., Hampson, R. E., Deadwyler, S. A., & Childers, S. R. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-24-08057.1996 · Cited by 311 · see citing works
Stress-Induced Facilitation of Classical Conditioning
Shors, T. J., Weiss, C., & Thompson, R. F. (1992) · Science · doi:10.1126/science.1636089 · Cited by 310 · see citing works
Gunduz-Cinar, O., MacPherson, K. P., Cinar, R., Gamble-George, J., Sugden, K., Williams, B., Godlewski, G., Ramikie, T. S., Gorka, A. X., Alapafuja, S. O., et al. (2013) · Molecular Psychiatry · doi:10.1038/mp.2012.72 · Cited by 307 · see citing works
Magnetic Resonance Imaging of Hippocampal Subfields in Posttraumatic Stress Disorder
Wang, Z., Neylan, T. C., Mueller, S. G., Lenoci, M., Truran, D., Marmar, C. R., Weiner, M. W., & Schuff, N. W. (2010) · Archives of General Psychiatry · doi:10.1001/archgenpsychiatry.2009.205 · Cited by 300 · see citing works
Mechanisms for memory types differ
Izquierdo, I., Barros, D. M., Souza, T. M. E., de Souza, M. M., Izquierdo, L. A., & Medina, J. H. (1998) · Nature · doi:10.1038/31371 · Cited by 294 · see citing works
Auclair, N., Otani, S., Soubrié, P., & Crépel, F. (2000) · Journal of Neurophysiology · doi:10.1152/jn.2000.83.6.3287 · Cited by 293 · see citing works
Altered Processing of Contextual Information during Fear Extinction in PTSD: An fMRI Study
Rougemont-Bücking, A., Linnman, C., Zeffiro, T. A., Zeidan, M. A., Lebron-Milad, K., Rodriguez-Romaguera, J., Rauch, S. L., Pitman, R. K., & Milad, M. R. (2011) · CNS Neuroscience & Therapeutics · doi:10.1111/j.1755-5949.2010.00152.x · Cited by 292 · see citing works
FAAH genetic variation enhances fronto-amygdala function in mouse and human
Dincheva, I., Drysdale, A. T., Hartley, C. A., Johnson, D. C., Jing, D., King, E. C., Ra, S., Gray, J. M., Yang, R., DeGruccio, A. M., et al. (2015) · Nature Communications · doi:10.1038/ncomms7395 · Cited by 289 · see citing works
Chronic 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
Chiang, K. P. (2004) · Human Molecular Genetics · doi:10.1093/hmg/ddh216 · Cited by 278 · see citing works
Akirav, I., & Maroun, M. (2007) · Neural Plasticity · doi:10.1155/2007/30873 · Cited by 277 · see citing works
The effect of predictive cues on freezing in rats
Bolles, R. C., & Collier, A. C. (1976) · Animal Learning & Behavior · doi:10.3758/bf03211975 · Cited by 266 · see citing works
de Bitencourt, R. M., Pamplona, F. A., & Takahashi, R. N. (2008) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2008.07.001 · Cited by 264 · see citing works
Decreased anterior cingulate volume in combat-related PTSD
Woodward, S. H., Kaloupek, D. G., Streeter, C. C., Martinez, C., Schaer, M., & Eliez, S. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.07.033 · Cited by 259 · 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
Vaughan, C. W., Connor, M. A., Bagley, E. E., & Christie, M. J. (2000) · Molecular Pharmacology · doi:10.1016/s0026-895x(24)23200-4 · Cited by 241 · see citing works
Synaptic functions of endocannabinoid signaling in health and disease
Araque, A., Castillo, P. E., Manzoni, O. J., & Tonini, R. (2017) · Neuropharmacology · doi:10.1016/j.neuropharm.2017.06.017 · Cited by 239 · see citing works
Hill, M. N., Campolongo, P., Yehuda, R., & Patel, S. (2017) · Neuropsychopharmacology · doi:10.1038/npp.2017.162 · Cited by 239 · see citing works
The 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
Fonzo, G. A., Simmons, A. N., Thorp, S. R., Norman, S. B., Paulus, M. P., & Stein, M. B. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.04.028 · Cited by 235 · see citing works
The 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
Adult Hippocampal Neurogenesis, Fear Generalization, and Stress
Besnard, A., & Sahay, A. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.167 · Cited by 226 · see citing works
Yamamoto, S., Morinobu, S., Fuchikami, M., Kurata, A., Kozuru, T., & Yamawaki, S. (2008) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301605 · Cited by 224 · see citing works
Cannabinoid CB1 Receptor Mediates Fear Extinction via Habituation-Like Processes
Kamprath, K., Marsicano, G., Tang, J., Monory, K., Bisogno, T., Marzo, V. D., Lutz, B., & Wotjak, C. T. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.0153-06.2006 · Cited by 217 · see citing works
Chronic stress impairs recall of extinction of conditioned fear
Miracle, A. D., BRACE, M., HUYCK, K., SINGLER, S., & Wellman, C. L. (2005) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2005.10.005 · Cited by 217 · see citing works
Bryant, R. A., Felmingham, K. L., Kemp, A. H., Barton, M., Peduto, A. S., Rennie, C., Gordon, E., & Williams, L. M. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.03.021 · Cited by 211 · see citing works
Pamplona, F. A., Prediger, R. D. S., Pandolfo, P., & Takahashi, R. N. (2006) · Psychopharmacology · doi:10.1007/s00213-006-0514-0 · Cited by 211 · see citing works
Single prolonged stress disrupts retention of extinguished fear in rats.Preprint
Knox, D., George, S. A., Fitzpatrick, C. J., Rabinak, C. A., Maren, S., & Liberzon, I. (2012) · Learning & memory (Cold Spring Harbor, N.Y.) · doi:10.1101/lm.024356.111 · Cited by 202 · see citing works
Extinction Learning Before Trauma and Subsequent Posttraumatic Stress
Guthrie, R. M., & Bryant, R. A. (2006) · Psychosomatic Medicine · doi:10.1097/01.psy.0000208629.67653.cc · Cited by 198 · see citing works
How important are sex differences in cannabinoid action?
Fattore, L., & Fratta, W. (2010) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2010.00776.x · Cited by 196 · see citing works
The role of the ventromedial prefrontal cortex in memory consolidation
Nieuwenhuis, I. L. C., & Takashima, A. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.12.009 · Cited by 195 · see citing works
Simmons, A. N., Paulus, M. P., Thorp, S. R., Matthews, S. C., Norman, S. B., & Stein, M. B. (2008) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.05.027 · Cited by 191 · see citing works
Cannabidiol enhances consolidation of explicit fear extinction in humans
Das, R., Kamboj, S. K., Ramadas, M., Yogan, K., Gupta, V., Redman, E., Curran, H. V., & Morgan, C. J. A. (2013) · Psychopharmacology · doi:10.1007/s00213-012-2955-y · Cited by 191 · see citing works
Deng, W., Mayford, M. R., & Gage, F. H. (2013) · eLife · doi:10.7554/elife.00312 · Cited by 182 · see citing works
Acute Stress Rapidly and Persistently Enhances Memory Formation in the Male Rat
Shors, T. J. (2001) · Neurobiology of Learning and Memory · doi:10.1006/nlme.1999.3956 · Cited by 182 · see citing works
Stress Differentially Modulates Fear Conditioning in Healthy Men and Women
Jackson, E. D., Payne, J. D., Nadel, L., & Jacobs, W. J. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.08.002 · Cited by 181 · see citing works
An electroconvulsive therapy procedure impairs reconsolidation of episodic memories in humans
Kroes, M. C. W., Tendolkar, I., van Wingen, G. A., van Waarde, J. A., Strange, B. A., & Fernández, G. (2013) · Nature Neuroscience · doi:10.1038/nn.3609 · Cited by 177 · see citing works
The contribution of pharmacology to research on the mechanisms of memory formation
McGaugh, J. L., & Izquierdo, I. (2000) · Trends in Pharmacological Sciences · doi:10.1016/s0165-6147(00)01473-5 · Cited by 176 · 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
Shin, L. M., Bush, G., Milad, M. R., Lasko, N. B., Brohawn, K. H., Hughes, K. C., Macklin, M. L., Gold, A. L., Karpf, R. D., Orr, S. P., et al. (2011) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2011.09121812 · Cited by 170 · 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
Starowicz, K., Maione, S., Cristino, L., Palazzo, E., Marabese, I., Rossi, F., de Novellis, V., & Marzo, V. D. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.3258-07.2007 · Cited by 168 · see citing works
Mayo, L. M., Asratian, A., Lindé, J., Holm, L., Nätt, D., Augier, G., Stensson, N., Vecchiarelli, H. A., Balsevich, G., Aukema, R. J., et al. (2018) · Molecular Psychiatry · doi:10.1038/s41380-018-0215-1 · Cited by 166 · see citing works
Ross, D. A., Arbuckle, M. R., Travis, M. J., Dwyer, J. B., van Schalkwyk, G. I., & Ressler, K. J. (2017) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2016.3325 · Cited by 165 · see citing works
Cannabinoid facilitation of fear extinction memory recall in humans
Rabinak, C. A., Angstadt, M., Sripada, C. S., Abelson, J. L., Liberzon, I., Milad, M. R., & Phan, K. L. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2012.06.063 · Cited by 163 · see citing works
Role of cyclic AMP in the actions of cannabinoid receptors
Childers, S. R., & Deadwyler, S. A. (1996) · Biochemical Pharmacology · doi:10.1016/0006-2952(96)00419-4 · Cited by 159 · see citing works
Sartim, A. G., Guimarães, F. S., & Joca, S. R. L. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.01.033 · Cited by 156 · see citing works
Can fear extinction be enhanced? A review of pharmacological and behavioral findings
Fitzgerald, P. J., Seemann, J. R., & Maren, S. (2013) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2013.12.007 · Cited by 152 · see citing works
Shin, L. M., Lasko, N. B., Macklin, M. L., Karpf, R. D., Milad, M. R., Orr, S. P., Goetz, J. M., Fischman, A. J., Rauch, S. L., & Pitman, R. K. (2009) · Archives of General Psychiatry · doi:10.1001/archgenpsychiatry.2009.138 · Cited by 151 · see citing works
Genetics of PTSD: fear conditioning as a model for future research
Amstadter, A. B., Nugent, N. R., & Koenen, K. C. (2009) · Psychiatric Annals · doi:10.3928/00485713-20090526-01 · Cited by 150 · see citing works
Reduction in endocannabinoid tone is a homeostatic mechanism for specific inhibitory synapses
Kim, J., & Alger, B. E. (2010) · Nature Neuroscience · doi:10.1038/nn.2517 · Cited by 149 · see citing works
PTSD Symptom Reports of Patients Evaluated for the New Mexico Medical Cannabis Program
Greer, G. R., Grob, C. S., & Halberstadt, A. L. (2014) · Journal of Psychoactive Drugs · doi:10.1080/02791072.2013.873843 · Cited by 149 · see citing works
Dissociation 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
Rabinak, C. A., Angstadt, M., Lyons, M., Mori, S., Milad, M. R., Liberzon, I., & Phan, K. L. (2013) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2013.09.009 · Cited by 148 · see citing works
Bowers, M. E., & Ressler, K. J. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.06.008 · Cited by 147 · 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
Wilkinson, S. T., Stefanovics, E., & Rosenheck, R. A. (2015) · The Journal of Clinical Psychiatry · doi:10.4088/jcp.14m09475 · Cited by 145 · see citing works
Opposite action of hippocampal CB1 receptors in memory reconsolidation and extinction
de Oliveira Alvares, L., Pasqualini Genro, B., Diehl, F., Molina, V. A., & Quillfeldt, J. A. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.05.005 · Cited by 143 · see citing works
Individual differences in recovery from traumatic fear
Holmes, A., & Singewald, N. (2012) · Trends in Neurosciences · doi:10.1016/j.tins.2012.11.003 · Cited by 141 · see citing works
Campos, A. C., Ferreira, F. R., & Guimarães, F. S. (2012) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2012.08.012 · Cited by 139 · see citing works
Endocannabinoid 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
Knox, D., Perrine, S. A., George, S. A., Galloway, M. P., & Liberzon, I. (2010) · Neuroscience Letters · doi:10.1016/j.neulet.2010.05.052 · Cited by 132 · see citing works
Ruehle, S., Remmers, F., Romo-Parra, H., Massa, F., Wickert, M., Wortge, S., Haring, M., Kaiser, N., Marsicano, G., Pape, H.-C., et al. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.4171-12.2013 · Cited by 132 · see citing works
Xing, J., & Li, J. (2006) · Journal of Neurophysiology · doi:10.1152/jn.01023.2006 · Cited by 132 · see citing works
Glover, E. M., Phifer, J. E., Crain, D. F., Norrholm, S. D., Davis, M., Bradley, B., Ressler, K. J., & Jovanovic, T. (2011) · Depression and Anxiety · doi:10.1002/da.20880 · Cited by 130 · see citing works
Cannich, A., Wotjak, C. T., Kamprath, K., Hermann, H., Lutz, B., & Marsicano, G. (2004) · Learning & Memory · doi:10.1101/lm.77904 · Cited by 130 · see citing works
Modulation of the extinction of two different fear-motivated tasks in three distinct brain areas
Fiorenza, N. G., Rosa, J., Izquierdo, I., & Myskiw, J. D. C. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.04.015 · Cited by 129 · see citing works
Self-citationInduction and Expression of Fear Sensitization Caused by Acute Traumatic Stress
Perusini, J. N., Meyer, E. M., Long, V., Rau, V., Nocera, N. A., Avershal, J., Maksymetz, J., Spigelman, I., & Fanselow, M. S. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.224 · Cited by 128 · see citing works
Abnormal Fear Memory as a Model for Posttraumatic Stress Disorder
Desmedt, A., Marighetto, A., & Piazza, P. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.06.017 · Cited by 127 · see citing works
Terzian, A. L. B., Drago, F., Wotjak, C. T., & Micale, V. (2011) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2011.00049 · Cited by 127 · see citing works
Garcia, R., Spennato, G., Nilsson-Todd, L., Moreau, J., & Deschaux, O. (2008) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2007.10.005 · Cited by 126 · see citing works
Schacht, J. P., Hutchison, K. E., & Filbey, F. M. (2012) · Neuropsychopharmacology · doi:10.1038/npp.2012.92 · Cited by 126 · see citing works
Green, M. K., Rani, C. S. S., Joshi, A., Soto-Piña, A. E., Martinez, P. A., Frazer, A., Strong, R., & Morilak, D. A. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.06.041 · Cited by 124 · see citing works
Short- and long-term effects of cannabinoids on the extinction of contextual fear memory in rats
Pamplona, F. A., Bitencourt, R. M., & Takahashi, R. N. (2008) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2008.04.003 · Cited by 123 · see citing works
Association of the Cannabinoid Receptor Gene (CNR1) With ADHD and Post-Traumatic Stress Disorder
Lu, A., Ogdie, M. N., Järvelin, M., Moilanen, I., Loo, S., McCracken, J. T., McGough, J. J., Yang, M. H., Peltonen, L., Nelson, S. F., et al. (2008) · American Journal of Medical Genetics Part B: Neuropsychiatric Genetics · doi:10.1002/ajmg.b.30693 · Cited by 123 · see citing works
van Rooij, S. J. H., Kennis, M., Vink, M., & Geuze, E. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2015.257 · Cited by 122 · see citing works
The influence of acute stress on the regulation of conditioned fear
Raio, C. M., & Phelps, E. A. (2015) · Neurobiology of Stress · doi:10.1016/j.ynstr.2014.11.004 · Cited by 121 · see citing works
Ganon-Elazar, E., & Akirav, I. (2012) · Neuropsychopharmacology · doi:10.1038/npp.2011.204 · Cited by 120 · see citing works
The role of prefrontal cortex CB1 receptors in the modulation of fear memory
Lin, H.-C., Mao, S.-C., Su, C.-L., & Gean, P.-W. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhn075 · Cited by 119 · see citing works
Bedse, G., Bluett, R. J., Patrick, T. A., Romness, N. K., Gaulden, A. D., Kingsley, P. J., Plath, N., Marnett, L. J., & Patel, S. (2018) · Translational Psychiatry · doi:10.1038/s41398-018-0141-7 · Cited by 118 · see citing works
Passie, T., Emrich, H. M., Karst, M., Brandt, S. D., & Halpern, J. H. (2012) · Drug Testing and Analysis · doi:10.1002/dta.1377 · Cited by 117 · see citing works
Lopresto, D., Schipper, P., & Homberg, J. R. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.10.009 · Cited by 117 · see citing works
Bush, D. E. A., Caparosa, E. M., Gekker, A., & LeDoux, J. E. (2010) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2010.00154 · Cited by 117 · see citing works
Brain sites involved in fear memory reconsolidation and extinction of rodents
Baldi, E., & Bucherelli, C. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.04.003 · Cited by 116 · see citing works
Lopez, J., Gamache, K., Schneider, R. E., & Nader, K. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.0735-14.2015 · Cited by 114 · see citing works
Vouimba, R., Yaniv, D., Diamond, D., & Richter‐Levin, G. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03294.x · Cited by 114 · see citing works
Nguyen, P., Schmid, C. L., Raehal, K. M., Selley, D. E., Bohn, L., & Sim‐Selley, L. J. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.11.027 · Cited by 113 · see citing works
Learning not to Fear: Neural Correlates of Learned Safety
Kong, E., Monje, F. J., Hirsch, J., & Pollak, D. D. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2013.191 · Cited by 113 · see citing works
Czerniawski, J. L., & Guzowski, J. F. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.0542-14.2014 · Cited by 113 · see citing works
Stressor controllability modulates fear extinction in humans
Hartley, C. A., Gorun, A., Reddan, M. C., Ramirez, F., & Phelps, E. A. (2014) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2013.12.003 · Cited by 110 · see citing works
Niyuhire, F., Varvel, S. A., Thorpe, A. J., Stokes, R. J., Wiley, J. L., & Lichtman, A. H. (2007) · Psychopharmacology · doi:10.1007/s00213-006-0650-6 · Cited by 110 · see citing works
Suvrathan, A., Bennur, S., Ghosh, S., Tomar, A., Anilkumar, S., & Chattarji, S. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2013.0151 · Cited by 110 · see citing works
Animal models of post-traumatic stress disorder and recent neurobiological insights
Whitaker, A. M., Gilpin, N. W., & Edwards, S. (2014) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000069 · Cited by 110 · see citing works
Resstel, L. B. M., Joca, S. R. L., Guimarães, F. G. E., & Corrêa, F. M. D. A. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.08.002 · Cited by 109 · see citing works
Self-citationAnandamide: an endogenous activator of the vanilloid receptor
Smart, D., & Jerman, J. C. (2000) · Trends in Pharmacological Sciences · doi:10.1016/s0165-6147(00)01459-0 · Cited by 107 · see citing works
Llorente‐Berzal, A., Terzian, A. L. B., Marzo, V. D., Micale, V., Viveros, M., & Wotjak, C. T. (2015) · Psychopharmacology · doi:10.1007/s00213-015-3917-y · Cited by 107 · see citing works
Kamprath, 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
Spagnolo, P. A., Ramchandani, V. A., Schwandt, M. L., Kwako, L. E., George, D. T., Mayo, L. M., Hillard, C. J., & Heilig, M. A. (2016) · Alcoholism Clinical and Experimental Research · doi:10.1111/acer.13210 · Cited by 104 · see citing works
Bedse, 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
Dubreucq, S., Koehl, M., Abrous, D. N., Marsicano, G., & Chaouloff, F. (2010) · Experimental Neurology · doi:10.1016/j.expneurol.2010.01.017 · Cited by 103 · see citing works
Is posttraumatic stress disorder a stress‐induced fear circuitry disorder?
Shin, L. M., & Handwerger, K. (2009) · Journal of Traumatic Stress · doi:10.1002/jts.20442 · Cited by 102 · see citing works
Ganon-Elazar, E., & Akirav, I. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.01.014 · Cited by 98 · see citing works
Vouimba, R.-M., Muñoz, C., & Diamond, D. M. (2006) · Stress · doi:10.1080/10253890600610973 · Cited by 96 · see citing works
Wilson, C., Vazdarjanova, A. I., & Terry, A. V. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.10.003 · Cited by 96 · see citing works
Morena, M., Berardi, A., Colucci, P., Palmery, M., Trezza, V., Hill, M. N., & Campolongo, P. (2017) · Neuropsychopharmacology · doi:10.1038/npp.2017.305 · Cited by 94 · see citing works
Lisboa, S. F. D. S., dos Reis, D. G., da Silva, A. L., Corrêa, F. M. D. A., Guimarães, F. S., & Resstel, L. B. M. (2010) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145710000684 · Cited by 91 · see citing works
Self-citationAcute stress impairs the retrieval of extinction memory in humans
Raio, C. M., Brignoni-Perez, E., Goldman, R., & Phelps, E. A. (2014) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2014.01.015 · Cited by 90 · see citing works
Effects of the vanilloid agonist olvanil and antagonist capsazepine on rat behaviors
Kasckow, J., Mulchahey, J. J., & Geracioti, T. D. (2003) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2003.10.007 · Cited by 89 · see citing works
Frontal lobe dysfunction in long-term cannabis users
Lundqvist, T., Jönsson, S., & Warkentin, S. (2001) · Neurotoxicology and Teratology · doi:10.1016/s0892-0362(01)00165-9 · Cited by 88 · 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
Infusion of cannabidiol into infralimbic cortex facilitates fear extinction via CB1 receptors
Monte, F. H. D., de Souza, R. R., de Bitencourt, R. M., Kroon, J. A. V., & Takahashi, R. N. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.04.045 · Cited by 88 · see citing works
Roche, M., O'Connor, E., Diskin, C., & Finn, D. P. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05861.x · Cited by 83 · see citing works
Fear relief—toward a new conceptual frame work and what endocannabinoids gotta do with it
Riebe, C. J. N., Pamplona, F. A., Kamprath, K., & Wotjak, C. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.11.057 · Cited by 82 · see citing works
Hoffman, A. N., Lorson, N. G., Sanabria, F., Olive, M. F., & Conrad, C. D. (2014) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2014.01.018 · Cited by 82 · see citing works
Emotional Modulation of Learning and Memory: Pharmacological Implications
LaLumiere, R., McGaugh, J. D., & McIntyre, C. K. (2017) · Pharmacological Reviews · doi:10.1124/pr.116.013474 · Cited by 82 · see citing works
Lisboa, S. F. D. S., Niraula, A., Resstel, L. B. M., Guimarães, F. S., Godbout, J. P., & Sheridan, J. F. (2018) · Neuropsychopharmacology · doi:10.1038/s41386-018-0064-2 · Cited by 81 · see citing works
Self-citationChhatwal, J. P., Gutman, A. R., Maguschak, K. A., Bowser, M. E., Yang, Y., Davis, M., & Ressler, K. J. (2008) · Neuropsychopharmacology · doi:10.1038/npp.2008.97 · Cited by 80 · see citing works
An fMRI study of unconditioned responses in post-traumatic stress disorder
Linnman, C., Zeffiro, T. A., Pitman, R. K., & Milad, M. R. (2011) · Biology of Mood & Anxiety Disorders · doi:10.1186/2045-5380-1-8 · Cited by 80 · see citing works
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Sartori, S. B., & Singewald, N. (2019) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2019.107402 · Cited by 236 · see citing works
Cannabidiol (CBD) use in psychiatric disorders: A systematic review
Bonaccorso, S., Ricciardi, A., Zangani, C., Chiappini, S., & Schifano, F. (2019) · NeuroToxicology · doi:10.1016/j.neuro.2019.08.002 · Cited by 170 · see citing works
Evidence for Use of Cannabinoids in Mood Disorders, Anxiety Disorders, and PTSD: A Systematic Review
Stanciu, C. N., Brunette, M. F., Teja, N., & Budney, A. J. (2021) · Psychiatric Services · doi:10.1176/appi.ps.202000189 · Cited by 86 · see citing works
Calpe-López, C., García-Pardo, M. P., & Aguilar, M. A. (2019) · Molecules · doi:10.3390/molecules24142583 · Cited by 76 · 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
Understanding the dynamic and destiny of memories
Alvares, L. D. O., & Monte, F. H. D. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.03.009 · Cited by 47 · see citing works
Cannabinoids as therapeutics for PTSD
Sbarski, B., & Akirav, I. (2020) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2020.107551 · Cited by 47 · see citing works
Vogel, A., Wilken‐Schmitz, A., Hummel, R., Lang, M., Gurke, R., Schreiber, Y., Schäfer, M. K. E., & Tegeder, I. (2020) · Scientific Reports · doi:10.1038/s41598-020-71879-x · Cited by 43 · see citing works
Salviato, B. Z., Raymundi, A. M., da Silva, T. R., Salemme, B. W., Sohn, J. M. B., de Araujo, F. S., Guimarães, F. S., Bertoglio, L. J., & Stern, C. A. J. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2021.108684 · Cited by 35 · see citing works
Self-citationGenes associated with cognitive performance in the Morris water maze: an RNA-seq study
Reshetnikov, V. V., Kisaretova, P. E., Ershov, N., Shulyupova, A. S., Oshchepkov, D. Y., Klimova, N. V., Ivanchikhina, A. V., Merkulova, T. I., & Bondar, N. P. (2020) · Scientific Reports · doi:10.1038/s41598-020-78997-6 · Cited by 32 · see citing works
FAAH polymorphism (rs324420) modulates extinction recall in healthy humans: an fMRI study
Spohrs, J., Martin, U., Grön, G., Plener, P. L., & Abler, B. (2021) · European Archives of Psychiatry and Clinical Neuroscience · doi:10.1007/s00406-021-01367-4 · Cited by 30 · see citing works
Bayer, H., Stern, C. A. J., Troyner, F., Gazarini, L., Guimarães, F. S., & Bertoglio, L. J. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2021.108913 · Cited by 27 · see citing works
Self-citationFranzen, J. M., Werle, I., Vanz, F., de Oliveira, B. B., Nascimento, L. M. M., Guimarães, F. S., & Bertoglio, L. J. (2022) · Neuropharmacology · doi:10.1016/j.neuropharm.2022.109316 · Cited by 27 · see citing works
Self-citationGasparyan, A., Navarrete, F., & Manzanares, J. (2021) · Frontiers in Pharmacology · doi:10.3389/fphar.2021.694510 · Cited by 25 · see citing works
Sohn, J. M. B., de Souza, S. T. F., Raymundi, A. M., Bonato, J. M., de Oliveira, R. M. W., Prickaerts, J., & Stern, C. A. J. (2020) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2020.107244 · Cited by 23 · see citing works
Self-citationSadaka, A. H., Ozuna, A. G., Ortiz, R. J., Kulkarni, P., Johnson, C. T., Bradshaw, H. B., Cushing, B. S., Li, A.-L., Hohmann, A. G., & Ferris, C. F. (2021) · Journal of Translational Medicine · doi:10.1186/s12967-021-02891-6 · Cited by 24 · see citing works
Hahnefeld, L., Vogel, A., Gurke, R., Geißlinger, G., Schäfer, M. K. E., & Tegeder, I. (2022) · Biomedicines · doi:10.3390/biomedicines10040914 · Cited by 23 · see citing works
de Bitencourt, R. M., Takahashi, R. N., & Carlini, E. A. (2021) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2021.638032 · Cited by 21 · see citing works
The NLRP3 Inflammasome in Stress Response: Another Target for the Promiscuous Cannabidiol
dos Santos, A. H., Vila-Verde, C., Guimarães, F. S., Joca, S. R. L., & Lisboa, S. F. D. S. (2022) · Current Neuropharmacology · doi:10.2174/1570159x20666220411101217 · Cited by 20 · see citing works
Self-citationCoelho, A. A., Bastos, S., Gobira, P. H., & Lisboa, S. F. D. S. (2023) · Neuronal Signaling · doi:10.1042/ns20220034 · Cited by 22 · see citing works
Self-citationda Silva, T. R., Sohn, J. M. B., Andreatini, R., & Stern, C. A. J. (2020) · Learning & Memory · doi:10.1101/lm.051615.120 · Cited by 19 · see citing works
Self-citationThe Endocannabinoid System as Modulator of Exercise Benefits in Mental Health
Amatriain‐Fernández, S., Budde, H., Gronwald, T., Quiroga, C., Carreón, C., Viana-Torre, G., Yamamoto, T., Imperatori, C., Machado, S. E. D. C., & Murillo‐Rodríguez, E. (2020) · Current Neuropharmacology · doi:10.2174/1570159x19666201218112748 · Cited by 17 · see citing works
Franzen, J. M., Vanz, F., Werle, I., Guimarães, F. S., & Bertoglio, L. J. (2022) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2022.08.002 · Cited by 16 · see citing works
Self-citationde Souza-Júnior, F. J. C., Cunha, L. C., & Lisboa, S. F. D. S. (2022) · Exploration of Neuroprotective Therapy · doi:10.37349/ent.2022.00028 · Cited by 14 · see citing works
Self-citationCannabinoids, Inner Ear, Hearing, and Tinnitus: A Neuroimmunological Perspective
Perin, P., Tagne, A. M., Enrico, P., Marino, F., Cosentino, M., Pizzala, R., & Boselli, C. (2020) · Frontiers in Neurology · doi:10.3389/fneur.2020.505995 · Cited by 15 · see citing works
Editorial: the psychopharmacology of extinction—from theory to therapy
Milton, A. L., & Holmes, A. (2019) · Psychopharmacology · doi:10.1007/s00213-018-5152-9 · Cited by 14 · see citing works
Lisboa, S. F. D. S., Stern, C. A. J., Gazarini, L., & Bertoglio, L. J. (2024) · International review of neurobiology · doi:10.1016/bs.irn.2024.03.007 · Cited by 12 · see citing works
Self-citationJin, J., Fu, C.-L., Xia, J., Luo, H., Wang, X., Chen, S. X., Mao, H., Yuan, K., Lü, L., Xiong, W., et al. (2024) · Molecular Psychiatry · doi:10.1038/s41380-024-02789-x · Cited by 11 · see citing works
PTSD Perceptions in U.S. Military Members and Their Families: A Qualitative Study
Thomson, J. L. (2021) · SAGE Open · doi:10.1177/21582440211006393 · Cited by 10 · see citing works
Matias, M. E., Radulski, D. R., da Silva, T. R., Raymundi, A. M., Stern, C. A. J., & Zampronio, A. R. (2023) · International Immunopharmacology · doi:10.1016/j.intimp.2023.110745 · Cited by 9 · see citing works
Self-citationFischer, C., Thomas, D., Gurke, R., & Tegeder, I. (2024) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-024-03012-0 · Cited by 9 · see citing works
Raymundi, A. M., Sohn, J. M. B., Salemme, B. W., Cardoso, N. C., Guimarães, F. S., & Stern, C. A. J. (2022) · Neuropharmacology · doi:10.1016/j.neuropharm.2022.109386 · Cited by 8 · see citing works
Self-citationGe, Q., Zhang, J., Huo, Q., Yu, J., Zheng, Q., Qian, Z., Wei, C., Jiang, T., Liu, Y., Liu, Z., et al. (2025) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2423974122 · Cited by 7 · see citing works
Corrêa, M. S., de Freitas, B. S., Machado, G. D. B., Pires, V. N., Bromberg, E., Hallak, J. E. C., Zuardi, A. W., Crippa, J. A. S., & Schröder, N. (2021) · Behavioural Brain Research · doi:10.1016/j.bbr.2021.113555 · Cited by 7 · see citing works
Cannabis and Complex Posttraumatic Stress Disorder
Dagan, Y., & Yager, J. (2020) · The Journal of Nervous and Mental Disease · doi:10.1097/nmd.0000000000001172 · Cited by 7 · see citing works
Rosa, J., Myskiw, J. D. C., Fiorenza, N. G., Furini, C. R. G., Sapiras, G. G., & Izquierdo, I. (2022) · Behavioural Brain Research · doi:10.1016/j.bbr.2022.114129 · Cited by 7 · see citing works
Self-citationHippocampal Cb2 receptors: an untold story
Visvanathar, R., Papanikolaou, M., Nôga, D. A., Pádua-Reis, M., Tort, A. B. L., & Blunder, M. (2021) · Reviews in the Neurosciences · doi:10.1515/revneuro-2021-0109 · Cited by 6 · see citing works
Obi, T., & Ressler, K. J. (2026) · Neuropsychopharmacology · doi:10.1038/s41386-026-02371-9 · Cited by 5 · see citing works
Endocannabinoid system in trauma and psychosis: distant guardian of mental stability
Bielawski, T., Albrechet‐Souza, L., & Frydecka, D. (2021) · Reviews in the Neurosciences · doi:10.1515/revneuro-2020-0102 · Cited by 4 · see citing works
Nightmares and the Cannabinoids
Mamelak, M. (2020) · Current Neuropharmacology · doi:10.2174/1570159x18666200114142321 · Cited by 3 · see citing works
Warren, W. G., Papagianni, E. P., Hale, E., Brociek, R. A., Cassaday, H. J., & Stevenson, C. W. (2022) · Frontiers in Pharmacology · doi:10.3389/fphar.2022.1082760 · Cited by 2 · see citing works
Pharmacology of Drugs of Abuse: Pharmacokinetics and Pharmacodynamics of Psychotropic Compounds
Guimarães, M. Z. P., & Neves, G. A. (2021) · Springer eBooks · doi:10.1007/978-3-030-62855-0_8 · Cited by 2 · see citing works
Akirav, I., Portugalov, A., Sbarski, B., Nestler, E. J., Parise, E. M., Akirav, I., & Zer‐Aviv, T. M. (2023) · Progress in Neurobiology · doi:10.60124/j.pneuro.2023.10.05 · Cited by 1 · see citing works
Psychoactive Effects of Cannabinoid-Based Medicines: Exploration and Inquiry
Cyr, C. (2022) · Springer eBooks · doi:10.1007/978-3-030-89918-9_8 · Cited by 1 · see citing works
Hippocampal TRPV1 channels in the modulation of contextual fear conditioningPreprint
Iglesias, L. P., Fernandes, H. D. B., de Miranda, A. S., Sorgi, C. A., & Moreira, F. A. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.05.23.445340
Sadaka, A. H., Ozuna, A., Ortiz, R. J., Kulkarni, P., Johnson, C. T., Bradshaw, H. B., Cushing, B. S., Li, A.-L., Hohmann, A. G., & Ferris, C. F. (2021) · Research Square · doi:10.21203/rs.3.rs-253550/v1
Gazarini, L., Stern, C. A. J., & Bertoglio, L. J. (2023) · Neuromethods · doi:10.1007/978-1-0716-3218-5_13
Self-citationCoelho, A. A. (2024) · Digital Library of Theses and Dissertations (Universidade de São Paulo) · doi:10.11606/d.17.2024.tde-25072024-105142
Suprani, F., Paribello, P., Mancini, G. F., Morena, M., Pinna, M., Pinna, F., Contu, M., Visioli, C., Medas, F., Canu, G. L., et al. (2025) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2025.1584583
Gliksberg, O., Hulaihel, A., Sznitman, S. R., Brill, S., Amit, B. H., Lev‐Ran, S., Kushnir, T., & Feingold, D. (2025) · Qualitative Health Research · doi:10.1177/10497323251361328
de Pontes, L. R., & Ribeiro, S. T. G. (2025) · Progress in brain research · doi:10.1016/bs.pbr.2025.08.001
Sadaka, A. H., Ozuna, A. G., Ortiz, R. J., Kulkarni, P., Johnson, C. T., Bradshaw, H. B., Cushing, B. S., Li, A.-L., Hohmann, A. G., & Ferris, C. F. (2021) · Figshare · doi:10.6084/m9.figshare.14670466
- Authors
- Lisboa, S. F., Vila-Verde, C., Rosa, J., Uliana, D. L., Stern, C. A. J., Bertoglio, L. J., Resstel, L. B., & Guimaraes, F. S.
- Affiliations
- Universidade de São Paulo (BR)
- Universidade Federal do Paraná (BR)
- Universidade Federal de Santa Catarina (BR)
- Corresponding author
- Lisboa, Sabrina F.
- Venue
- Psychopharmacology
- Published
- 2019-01
- Volume
- 236
- Issue
- 1
- Pages
- 201-226
- ISSN
- 0033-3158 (ISSN-L)
- 1432-2072
- OpenAlex
- W2907417472
- Cited by
- 54
- References
- 268
- Citations by year
- 2026: 1 · 2025: 4 · 2024: 4 · 2023: 5 · 2022: 10 · 2021: 16 · 2020: 10 · 2019: 4
- FWCI
- 1.28
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Psychopharmacology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Fundação de Amparo à Pesquisa do Estado de São Paulo (2012/17626-7)
- Instituto Nacional de Ciência e Tecnologia Translacional em Medicina (465458/2014-9)
- Topics
- Health Sciences › Medicine › Pharmacology › Cannabis and Cannabinoid Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Social Sciences › Psychology › Clinical Psychology › Posttraumatic Stress Disorder Research
- Keywords
- endocannabinoid system, cannabinoid type 1 receptor, cannabinoid type 2 receptor, post-traumatic stress disorder, aversive memory, traumatic memory, memory extinction, medial prefrontal cortex, amygdala, hippocampus, synaptic plasticity, stress-related disorders, cannabinoid receptor agonists
- MeSH terms
- Amygdala, Animals, Avoidance Learning, Cannabinoids, Extinction, Psychological, Fear, Hippocampus, Humans, Neuronal Plasticity, Stress Disorders, Post-Traumatic, Prefrontal Cortex
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