The DOI matches its Crossref record; 267 of the 268 references it cites were found in a registry or an index.
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.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
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?
In the citing paper
“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
Citations
Cites
Statistical Power Analysis for the Behavioral Sciences
Muller, K. E., & Cohen, J. (1989) · Technometrics · doi:10.2307/1270020 · Cited by 99,603
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 65,417
LeDoux, J. E. (2000) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.23.1.155 · Cited by 8,444
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 4,015
Etkin, A., & Wager, T. D. (2007) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2007.07030504 · Cited by 3,391
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
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
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
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
STRESS AND HIPPOCAMPAL PLASTICITY
McEwen, B. S. (1999) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.22.1.105 · Cited by 2,087
Research works printed but not linked: 1
- Egertová M, Giang DK, Cravatt BF, Elphick MR (1998) A new perspective on cannabinoid signalling: complementary localization of fatty acid amide hydrolase and the CB1 receptor in rat brain. Proc Biol Sci 265:2081–2085 · DOI
Cited by
Sorted by citations
Sartori, S. B., & Singewald, N. (2019) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2019.107402 · Cited by 236
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 180
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 94
Calpe-López, C., García-Pardo, M. P., & Aguilar, M. A. (2019) · Molecules · doi:10.3390/molecules24142583 · Cited by 79
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 67
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 51
Cannabinoids as therapeutics for PTSD
Sbarski, B., & Akirav, I. (2020) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2020.107551 · Cited by 47
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 44
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
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
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 32
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 29
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
Self-citationGasparyan, A., Navarrete, F., & Manzanares, J. (2021) · Frontiers in Pharmacology · doi:10.3389/fphar.2021.694510 · Cited by 25
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
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
Hahnefeld, L., Vogel, A., Gurke, R., Geißlinger, G., Schäfer, M. K. E., & Tegeder, I. (2022) · Biomedicines · doi:10.3390/biomedicines10040914 · Cited by 23
de Bitencourt, R. M., Takahashi, R. N., & Carlini, E. A. (2021) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2021.638032 · Cited by 23
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
Self-citationCoelho, A. A., Bastos, S., Gobira, P. H., & Lisboa, S. F. D. S. (2023) · Neuronal Signaling · doi:10.1042/ns20220034 · Cited by 22
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
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 18
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 18
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 16
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
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
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
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 12
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
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
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
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
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
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
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
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
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
Obi, T., & Ressler, K. J. (2026) · Neuropsychopharmacology · doi:10.1038/s41386-026-02371-9 · Cited by 5
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
Nightmares and the Cannabinoids
Mamelak, M. (2020) · Current Neuropharmacology · doi:10.2174/1570159x18666200114142321 · Cited by 4
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
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 3
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
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
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-citationde Souza, F. J. C. (2023) · Digital Library of Theses and Dissertations (Universidade de São Paulo) · doi:10.11606/d.17.2023.tde-10112023-160939
Coelho, 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., 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
Metadata
- 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 (medical) › 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
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
