Involvement of the prelimbic prefrontal cortex on cannabidiol-induced attenuation of contextual conditioned fear in rats
Abstract
Rationale Systemic administration of cannabidiol (CBD), a non-psychotomimetic component of Cannabis sativa, is able to attenuate cardiovascular and behavioral (freezing) changes induced by re-exposure to a context that had been previously paired with footshocks. The brain sites mediating this effect, however, remain unknown. The medial prefrontal cortex (mPFC) has been related to contextual fear conditioning.Objectives (1) To verify, using c-Fos immunocytochemistry, if the mPFC is involved in the attenuation of contextual fear induced by systemic administration of CBD; (2) to investigate if direct microinjections of CBD into mPFC regions would also attenuate contextual fear.Results Confirming previous results systemic administration of CBD (10mg/kg) decreased contextual fear and associated c-Fos expression in the prefrontal cortex (prelimbic and infralimbic regions). The drug also attenuated c-Fos expression in the bed nucleus of the stria terminalis (BNST). Direct CBD (30 nmol) microinjection into the PL prefrontal cortex reduced freezing induced by re-exposure to the aversively conditioned context. In the infralimbic (IL) prefrontal cortex, however, CBD (30 nmol) produced an opposite result, increasing the expression of contextual fear conditioning. This result was confirmed by an additional experiment where the conditioning session was performed under a less aversive protocol.Conclusion These results suggest that the PL prefrontal cortex may be involved in the attenuation of contextual fear induced by systemic injection of CBD. They also support the proposition that the IL and PL play opposite roles in fear conditioning. A possible involvement of the BNST in CBD effects needs to be further investigated.
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CBD induced acute anxiolytic effects when injected into the dPAG and BNST.
“As shown in Figure 2, CBD induced acute anxiolytic effects when injected into the dPAG and BNST (21, 37–41).”
From Translational investigation of the therapeutic potential of Cannabidiol (CBD): Toward a new age (2018) · cites this paper as [41]
CBD modified anxiety-like behaviors in the mPFC, preventing the expression of contextual fear conditioning.
“CBD also modified anxiety-like behaviors in the mPFC, preventing the expression of contextual fear conditioning (41).”
From Translational investigation of the therapeutic potential of Cannabidiol (CBD): Toward a new age (2018) · cites this paper as [41]
Cites
The rat brain in stereotaxic coordinates
Palkovits, M. (1983) · Neuropeptides · doi:10.1016/0143-4179(83)90049-5 · Cited by 28,959 · see citing works
The Rat Brain in Stereotaxic Coordinates
Paxinos, G., & Watson, C. (1983) · Elsevier eBooks · doi:10.1016/c2009-0-63235-9 · Cited by 28,585 · see citing works
Isolation and Structure of a Brain Constituent That Binds to the Cannabinoid Receptor
Devane, W. A., Hanuš, L., Breuer, A., Pertwee, R. G., Stevenson, L. A., Griffin, G., Gibson, D., Mandelbaum, A., Etinger, A., & Mechoulam, R. (1992) · Science · doi:10.1126/science.1470919 · Cited by 5,633 · see citing works
Structure of a cannabinoid receptor and functional expression of the cloned cDNA
Matsuda, L. A., Lolait, S. J., Brownstein, M. J., Young, A. C., & Bonner, T. I. (1990) · Nature · doi:10.1038/346561a0 · Cited by 5,011 · see citing works
Determination and characterization of a cannabinoid receptor in rat brain
Devane, W. A., Dysarz, F. A., Johnson, M. R., Melvin, L. S., & Howlett, A. C. (1988) · Molecular Pharmacology · doi:10.1016/s0026-895x(25)09876-1 · Cited by 2,443 · 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
Neurobiology of Pavlovian Fear Conditioning
Maren, S. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.897 · Cited by 1,805 · 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
Formation and inactivation of endogenous cannabinoid anandamide in central neurons
Marzo, V. D., Fontana, A., Cadas, H., Schinelli, S., Cimino, G., Schwartz, J.-C., & Piomelli, D. (1994) · Nature · doi:10.1038/372686a0 · Cited by 1,585 · see citing works
LeDoux, J., Iwata, J., Cicchetti, P., & Reis, D. (1988) · The Journal of Neuroscience · doi:10.1523/jneurosci.08-07-02517.1988 · Cited by 1,580 · see citing works
Differential projections of the infralimbic and prelimbic cortex in the rat
Vertes, R. P. (2004) · Synapse · doi:10.1002/syn.10279 · Cited by 1,550 · see citing works
Neuronal signalling of fear memory
Maren, S., & Quirk, G. J. (2004) · Nature Reviews Neuroscience · doi:10.1038/nrn1535 · Cited by 1,428 · see citing works
Bisogno, T., Hanuš, L., PETROCELLIS, L. D., Tchilibon, S., Ponde, D. E., Brandi, I., Moriello, A. S., Davis, J. B., Mechoulam, R., & Marzo, V. D. (2001) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0704327 · Cited by 1,315 · 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
Conditional and unconditional components of post-shock freezing
Fanselow, M. S. (1980) · Pavlovian Journal of Biological Science · doi:10.1007/bf03001163 · Cited by 1,153 · see citing works
The neuroanatomical and neurochemical basis of conditioned fear
Fendt, M., & Fanselow, M. S. (1999) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(99)00016-0 · Cited by 1,092 · see citing works
The Involvement of the Anterior Cingulate Cortex in Remote Contextual Fear Memory
Frankland, P., Bontempi, B., Talton, L., Kaczmarek, L., & Silva, A. J. (2004) · Science · doi:10.1126/science.1094804 · Cited by 952 · see citing works
Quirk, G. J., Likhtik, E., Pelletier, J. G., & Paré, D. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-25-08800.2003 · Cited by 927 · see citing works
Agonistic properties of cannabidiol at 5-HT1a receptors
Russo, E. B., Burnett, A., Hall, B., & Parker, K. K. (2005) · Neurochemical Research · doi:10.1007/s11064-005-6978-1 · Cited by 878 · see citing works
Efferent projections of the infralimbic cortex of the rat
Hurley, K. M., Herbert, H., Moga, M. M., & Saper, C. B. (1991) · Journal of Comparative Neurology · doi:10.1002/cne.903080210 · Cited by 777 · see citing works
Thomas, A., Baillie, G. L., Phillips, A. M., Razdan, R. K., Ross, R. A., & Pertwee, R. G. (2007) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0707133 · Cited by 763 · see citing works
Innate and conditioned reactions to threat in rats with amygdaloid lesions.
Blanchard, D. C., & Blanchard, R. J. (1972) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0033521 · Cited by 753 · see citing works
Invited review c-Fos as a transcription factor: a stressful (re)view from a functional map
Kovács, K. J. (1998) · Neurochemistry International · doi:10.1016/s0197-0186(98)00023-0 · Cited by 740 · see citing works
Vidal-Gonzalez, I., Vidal-Gonzalez, B., Rauch, S. L., & Quirk, G. J. (2006) · Learning & Memory · doi:10.1101/lm.306106 · Cited by 705 · see citing works
Endocannabinoids: endogenous cannabinoid receptor ligands with neuromodulatory action
Marzo, V. D., Melck, D. J., Bisogno, T., & PETROCELLIS, L. D. (1998) · Trends in Neurosciences · doi:10.1016/s0166-2236(98)01283-1 · Cited by 704 · see citing works
Action of cannabidiol on the anxiety and other effects produced by ?9-THC in normal subjects
Zuardi, A. W., Shirakawa, I., Finkelfarb, E., & Karniol, I. G. (1982) · Psychopharmacology · doi:10.1007/bf00432554 · Cited by 608 · see citing works
Activity in Prelimbic Cortex Is Necessary for the Expression of Learned, But Not Innate, Fears
Corcoran, K., & Quirk, G. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.5327-06.2007 · Cited by 580 · see citing works
Beck, C., & Fibiger, H. (1995) · The Journal of Neuroscience · doi:10.1523/jneurosci.15-01-00709.1995 · Cited by 547 · see citing works
Cannabidiol: An Overview of Some Pharmacological Aspects
Mechoulam, R., Parker, L. A., & Gallily, R. (2002) · The Journal of Clinical Pharmacology · doi:10.1002/j.1552-4604.2002.tb05998.x · Cited by 511 · see citing works
Carrier, E. J., Auchampach, J. A., & Hillard, C. J. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0511232103 · Cited by 497 · see citing works
Afferent connections of the medial frontal cortex of the rat. II. Cortical and subcortical afferents
Condé, F., Maire-Lepoivre, E., Audinat, É., & Crépel, F. (1995) · The Journal of Comparative Neurology · doi:10.1002/cne.903520407 · Cited by 494 · see citing works
Endocannabinoid system and stress and anxiety responses
VIVEROS, M., MARCO, E., & FILE, S. (2005) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2005.01.029 · Cited by 485 · see citing works
Blanchard, R. J., Blanchard, D. C., Agullana, R., & Weiss, S. M. (1991) · Physiology & Behavior · doi:10.1016/0031-9384(91)90423-l · Cited by 461 · see citing works
Antianxiety effect of cannabidiol in the elevated plus-maze
Guimarães, F. S., Chiaretti, T. M., Graeff, F. G., & Zuardi, A. W. (1990) · Psychopharmacology · doi:10.1007/bf02244012 · Cited by 379 · see citing works
Cannabidiol is an allosteric modulator at mu- and delta-opioid receptors
Kathmann, M., Flau, K., Redmer, A., Tränkle, C., & Schlicker, E. (2006) · Naunyn-Schmiedeberg s Archives of Pharmacology · doi:10.1007/s00210-006-0033-x · Cited by 379 · see citing works
Chapter 26 Emotional networks and motor control: a fearful view
(1996) · Progress in brain research · doi:10.1016/s0079-6123(08)61880-4 · Cited by 364 · see citing works
Effects of ipsapirone and cannabidiol on human experimental anxiety
Zuardi, A. W., Cosme, R. A., Graeff, F. G., & Guimarães, F. S. (1993) · Journal of Psychopharmacology · doi:10.1177/026988119300700112 · Cited by 364 · see citing works
Campos, A. C., & Guimarães, F. S. (2008) · Psychopharmacology · doi:10.1007/s00213-008-1168-x · Cited by 364 · see citing works
Self-citationMarsch, 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
Sullivan, G. M., Apergis, J., Bush, D. E. A., Johnson, L. R., Hou, M., & Ledoux, J. E. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2004.06.015 · Cited by 327 · see citing works
Effects of cannabidiol (CBD) on regional cerebral blood flow
Crippa, J. A. D. S., Zuardi, A. W., Garrido, G. E. J., Wichert-Ana, L., Guarnieri, R., Ferrari, L., Azevedo-Marques, P. M., Hallak, J. E. C., McGuire, P. K., & Busatto, G. F. (2004) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300340 · Cited by 307 · see citing works
Costa, B., Giagnoni, G., Franke, C., Trovato, A. E., & Colleoni, M. (2004) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0705920 · Cited by 291 · see citing works
Resstel, L. B. M., Tavares, R. F., Lisboa, S. F. S., Joca, S. R. L., Corrêa, F. M. A., & Guimarães, F. S. (2009) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2008.00046.x · Cited by 283 · see citing works
Self-citationRole in Anxiety Behavior of the Endocannabinoid System in the Prefrontal Cortex
Rubino, T., Realini, N., Castiglioni, C., Guidali, C., Viganò, D., Marras, E., Petrosino, S., Perletti, G., Maccarrone, M., Marzo, V. D., et al. (2007) · Cerebral Cortex · doi:10.1093/cercor/bhm161 · Cited by 283 · see citing works
Hypnotic and Antiepileptic Effects of Cannabidiol
Carlini, E. A., & Cunha, J. M. (1981) · The Journal of Clinical Pharmacology · doi:10.1002/j.1552-4604.1981.tb02622.x · Cited by 278 · 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
Antipsychotic effect of cannabidiol.
Zuardi, A. W., Morais, S. L., Guimarães, F. S., & Mechoulam, R. (1995) · PubMed · Cited by 264 · see citing works
Self-citationMishima, K., Hayakawa, K., Abe, K., Ikeda, T., Egashira, N., Iwasaki, K., & Fujiwara, M. (2005) · Stroke · doi:10.1161/01.str.0000163083.59201.34 · Cited by 225 · see citing works
Infralimbic cortex activation increases c-fos expression in intercalated neurons of the amygdala
Berretta, S., Pantazopoulos, H., Caldera, M., Pantazopoulos, P., & Paré, D. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.01.020 · Cited by 223 · see citing works
The endocannabinoid system: emotion, learning and addiction
Moreira, F. A., & Lutz, B. (2008) · Addiction Biology · doi:10.1111/j.1369-1600.2008.00104.x · Cited by 222 · see citing works
Anxiolytic-like effect of cannabidiol in the rat Vogel conflict test
Moreira, F. A., Aguiar, D. C., & Guimarães, F. S. (2006) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2006.06.004 · Cited by 207 · see citing works
Self-citationCannabidiol inhibits the hyperlocomotion induced by psychotomimetic drugs in mice
Moreira, F. A., & Guimarães, F. S. (2005) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2005.02.040 · Cited by 206 · see citing works
Self-citationAmygdalar NMDA Receptors Are Critical for the Expression of Multiple Conditioned Fear Responses
Lee, H. J., Choi, J.-S., Brown, T. H., & Kim, J. J. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-11-04116.2001 · Cited by 195 · see citing works
Herry, C., & Mons, N. E. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03542.x · Cited by 192 · see citing works
Effects of cannabidiol in animal models predictive of antipsychotic activity
Zuardi, A. W., Antunes Rodrigues, J., & Cunha, J. M. (1991) · Psychopharmacology · doi:10.1007/bf02244189 · Cited by 191 · see citing works
Laviolette, S. R., & Grace, A. A. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.0707-06.2006 · Cited by 189 · see citing works
Resstel, L. B. M., Joca, S. R. L., Moreira, F. A., Corrêa, F. M. A., & Guimarães, F. S. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.05.016 · Cited by 182 · see citing works
Self-citationPetitet, F., Jeantaud, B., Reibaud, M., Impérato, A., & Dubroeucq, M. C. (1998) · Life Sciences · doi:10.1016/s0024-3205(98)00238-0 · Cited by 180 · see citing works
Kim‐Mitsuyama, S., Yamamoto, E., Tanaka, T., Zhan, Y., Izumi, Y., Izumiya, Y., Ioroi, T., Wanibuchi, H., & Iwao, H. (2005) · Stroke · doi:10.1161/01.str.0000163084.16505.e3 · Cited by 173 · see citing works
Discriminative fear conditioning to context expressed by multiple measures of fear in the rat
Antoniadis, E. A., & McDonald, R. J. (1999) · Behavioural Brain Research · doi:10.1016/s0166-4328(98)00056-4 · Cited by 151 · see citing works
Effects of conditioned fear stress on serotonin neurotransmission and freezing behavior in rats
Hashimoto, S., Inoue, T., & Koyama, T. (1999) · European Journal of Pharmacology · doi:10.1016/s0014-2999(99)00441-0 · Cited by 135 · see citing works
Differential effects of THC- or CBD-rich cannabis extracts on working memory in rats.
Fadda, P., Robinson, L., Fratta, W., Pertwee, R., & Riedel, G. (2004) · Neuropharmacology · doi:10.1016/j.neuropharm.2004.08.009 · Cited by 122 · see citing works
Conditioned fear to environmental context: cardiovascular and behavioral components in the rat
Carrive, P. (2000) · Brain Research · doi:10.1016/s0006-8993(00)02029-1 · Cited by 119 · 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
Morrow, B. A., Elsworth, J. D., Inglis, F. M., & Roth, R. H. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-13-05666.1999 · Cited by 114 · see citing works
Effect of tone-dependent fear conditioning on heart rate and behavior of C57BL/6N mice.
Stiedl, O., & Spiess, J. (1997) · Behavioral Neuroscience · doi:10.1037//0735-7044.111.4.703 · Cited by 109 · see citing works
Iwata, J., LeDoux, J. E., & Reis, D. J. (1986) · Brain Research · doi:10.1016/0006-8993(86)91055-3 · Cited by 108 · see citing works
Resstel, L. B. M., Alves, F. H. F., Reis, D. G., Crestani, C. C., Corrêa, F. M. A., & Guimarães, F. S. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.04.007 · Cited by 107 · see citing works
Self-citationSerotonergic activation reduces defensive freezing in the conditioned fear paradigm
Inoue, T. (1996) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(95)02084-5 · Cited by 106 · see citing works
Tavares, R. F., Corrêa, F. M. D. A., & Resstel, L. B. M. (2009) · Journal of Neuroscience Research · doi:10.1002/jnr.22070 · Cited by 98 · see citing works
Self-citationEffects of acute and chronic fluoxetine treatments on restraint stress-induced Fos expression
de Oliveira, C. L., Sales, A. J., Bel, E. A. D., Silveira, M. C. L., & Guimarães, F. S. (2001) · Brain Research Bulletin · doi:10.1016/s0361-9230(01)00566-4 · Cited by 95 · see citing works
Self-citationEffect of tone-dependent fear conditioning on heart rate and behavior of C57BL/6N mice.
Stiedl, O., & Spiess, J. (1997) · Behavioral Neuroscience · doi:10.1037/0735-7044.111.4.703 · Cited by 95 · 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
Li, X., Inoue, T., Abekawa, T., Weng, S.-M., Nakagawa, S., Izumi, T., & Koyama, T. (2006) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2005.12.008 · Cited by 81 · see citing works
Cardiovascular responses to electrical stimulation of the bed nucleus of the stria terminalis
Dunn, J. D., & Williams, T. J. (1995) · The Journal of Comparative Neurology · doi:10.1002/cne.903520206 · Cited by 79 · see citing works
Cannabidiol increases Fos expression in the nucleus accumbens but not in the dorsal striatum
Guimaraes, V. H. (2004) · Life Sciences · doi:10.1016/j.lfs.2004.01.015 · Cited by 75 · see citing works
Resstel, L. B. M., Lisboa, S. F. D. S., de Aguiar, D. C., Corrêa, F. M. D. A., & Guimarães, F. S. (2008) · Psychopharmacology · doi:10.1007/s00213-008-1156-1 · Cited by 75 · see citing works
Self-citationTarget brain sites of the anxiolytic effect of citalopram, a selective serotonin reuptake inhibitor
Izumi, T., Inoue, T., Kitaichi, Y., Nakagawa, S., & Koyama, T. (2006) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2005.12.073 · Cited by 42 · see citing works
Ghosh, D. K. (2019) · Natural Medicines · doi:10.1201/9781315187853-29 · Cited by 19 · see citing works
Cannabidiol-caused depression of spinal motoneuron responses in cats
Turkanis, S. A., & Karler, R. (1986) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(86)90235-2 · Cited by 17 · see citing works
Kujtan, P. W., Carlen, P. L., & Kapur, B. M. (1983) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/y83-063 · Cited by 17 · see citing works
Buspirone attenuates conditioned fear-induced c-Fos expression in the rat hippocampus
Wisłowska-Stanek, A., Zienowicz, M., Lehner, M., Taracha, E., Bidziński, A., Maciejak, P., Skórzewska, A., Szyndler, J., & Płaźnik, A. (2005) · Neuroscience Letters · doi:10.1016/j.neulet.2005.07.033 · Cited by 15 · see citing works
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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
Prefrontal control of fear: more than just extinction
Sotres-Bayon, F., & Quirk, G. J. (2010) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2010.02.005 · Cited by 625 · see citing works
“Current Opinion in Neurobiology 2010, 20:231–235 agents that reduce fear expression, such as propranolol [33] and cannabidiol [34].”
BackgroundCampos, A. C., Moreira, F. A., Gomes, F. V., Del Bel, E. A., & Guimarães, F. S. (2012) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2011.0389 · Cited by 475 · see citing works
Self-citationTranslational investigation of the therapeutic potential of Cannabidiol (CBD): Toward a new age
Crippa, J. A., Guimarães, F. S., Campos, A. C., & Zuardi, A. W. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.02009 · Cited by 308 · see citing works
Self-citationGarcía-Gutiérrez, M. S., Navarrete, F., Gasparyan, A., Austrich-Olivares, A., Sala, F., & Manzanares, J. (2020) · Biomolecules · doi:10.3390/biom10111575 · Cited by 306 · see citing works
Waldo Zuardi, A., Alexandre S. Crippa, J., E.C. Hallak, J., Bhattacharyya, S., Atakan, Z., Martin-Santos, R., K. McGuire, P., & Silveira Guimaraes, F. (2012) · Current Pharmaceutical Design · doi:10.2174/138161212802884681 · Cited by 222 · see citing works
Fogaça, M. V., Reis, F. M. C. V., Campos, A. C., & Guimarães, F. S. (2014) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2013.10.012 · Cited by 153 · see citing works
Self-citationCampos, 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
Self-citationSoares, V. D. P., Campos, A. C., Bortoli, V. C. D., Zangrossi, H., Guimarães, F. S., & Zuardi, A. W. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.05.004 · Cited by 112 · see citing works
Self-citationGomes, F. V., Reis, D. G., Alves, F. H., Corrêa, F. M., Guimarães, F. S., & Resstel, L. B. (2012) · Journal of Psychopharmacology · doi:10.1177/0269881110389095 · Cited by 97 · see citing works
Self-citationMarinho, A. L. Z., Vila-Verde, C., Fogaça, M. V., & Guimarães, F. S. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.02.023 · Cited by 68 · see citing works
Gomes, F. V., Alves, F. H. F., Guimarães, F. S., Correa, F. M. A., Resstel, L. B. M., & Crestani, C. C. (2013) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2012.09.007 · Cited by 27 · see citing works
- Authors
- Lemos, J. I., Resstel, L. B., & Guimarães, F. S.
- Affiliations
- Universidade de São Paulo (BR)
- Corresponding author
- Guimarães, Francisco Silveira
- Venue
- Behavioural Brain Research
- Publisher
- Elsevier BV
- Published
- 2010-02
- Volume
- 207
- Issue
- 1
- Pages
- 105-111
- ISSN
- 0166-4328 (ISSN-L)
- OpenAlex
- W2003968300
- Cited by
- 146
- References
- 82
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- FWCI
- 6.46
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Behavioural Brain Research (publishedVersion)
- PubMed (publishedVersion)
- Scientific Electronic Library Online (São Paulo Research Foundation, Latin American and Caribbean Center on Health Sciences Information, Conselho Nacional de Desenvolvimento Científico e Tecnológico) (publishedVersion)
- Funders
- Fundação de Amparo à Pesquisa do Estado de São Paulo
- Conselho Nacional de Desenvolvimento Científico e Tecnológico
- Topics
- Health Sciences › Medicine › Pharmacology › Cannabis and Cannabinoid Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- cannabidiol, contextual fear conditioning, fear extinction, prelimbic cortex, infralimbic cortex, bed nucleus of the stria terminalis, Fos expression, microinjection, freezing behavior, aversive conditioning, medial prefrontal cortex
- MeSH terms
- Animals, Behavior, Animal, Cannabidiol, Conditioning, Classical, Dose-Response Relationship, Drug, Electroshock, Exploratory Behavior, Fear, Hypothalamus, Immunohistochemistry, Male, Neurons, Spatial Behavior, Proto-Oncogene Proteins c-fos, Rats, Wistar, Prefrontal Cortex, Rats
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