Involvement of the prelimbic prefrontal cortex on cannabidiol-induced attenuation of contextual conditioned fear in rats

Behavioural Brain Research

Volumn 207, Issue 1, 2010, Pages 105-111

  Lemos, José Inácio ^a   Resstel, Leonardo Barbosa ^a   Guimarães, Francisco Silveira ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Anxiety; Anxiolytic; Cannabinoid; Conditioning; Fos; Infralimbic

Indexed keywords

CANNABIDIOL; CYTOKINE; PROTEIN C FOS;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY DISORDER; ARTICLE; BEHAVIOR CHANGE; BRAIN FUNCTION; BRAIN REGION; CARDIOVASCULAR RESPONSE; CONDITIONING; CONTROLLED STUDY; FEAR; FOOTSHOCK; IMMUNOCYTOCHEMISTRY; LIMBIC SYSTEM; MALE; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; STRIA TERMINALIS;

ANIMALS; BEHAVIOR, ANIMAL; CANNABIDIOL; CONDITIONING, CLASSICAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTROSHOCK; EXPLORATORY BEHAVIOR; FEAR; HYPOTHALAMUS; IMMUNOHISTOCHEMISTRY; MALE; NEURONS; PREFRONTAL CORTEX; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, WISTAR; SPATIAL BEHAVIOR;

EID: 70849116349     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2009.09.045     Document Type: Article

References (79)

1. Antoniadis E.A., and McDonald R.J. Discriminative fear conditioning to context expressed by multiple measures of fear in the rat. Behav Brain Res 101 (1999) 1-13
2. Beck C.H., and Fibiger H.C. Conditioned fear-induced changes in behavior and in the expression of the immediate early gene c-fos: with and without diazepam pretreatment. J Neurosci 15 (1995) 709-720
3. Berretta S., Pantazopoulos H., Caldera M., Pantazopoulos P., and Pare D. Infralimbic cortex activation increases c-Fos expression in intercalated neurons of the amygdala. Neuroscience 132 (2005) 943-953
4. Bisogno T., Hanus L., De Petrocellis L., Tchilibon S., Ponde D.E., Brandi I., et al. Molecular targets for cannabidiol and its synthetic analogues: effect on vanilloid VR1 receptors and on the cellular uptake and enzymatic hydrolysis of anandamide. Br J Pharmacol 134 (2001) 845-852
5. Bitencourt R.M., Pamplona F.A., and Takahashi R.N. Facilitation of contextual fear memory extinction and anti-anxiogenic effects of AM404 and cannabidiol in conditioned rats. Eur Neuropsychopharmacol 18 (2008) 849-859
6. Blanchard D.C., and Blanchard R.J. Innate and conditioned reactions to threat in rats with amygdaloid lesions. J Comp Physiol Psychol 81 (1972) 281-290
7. Blanchard R.J., Blanchard D.C., Agullana R., and Weiss S.M. Twenty-two kHz alarm cries to presentation of a predator, by laboratory rats living in visible burrow systems. Physiol Behav 50 (1991) 967-972
8. Campos A.C., and Guimarães F.S. Involvement of 5HT1A receptors in the anxiolytic-like effects of cannabidiol injected into the dorsolateral periaqueductal gray of rats. Psychopharmacology [Berl] 199 (2008) 223-230
9. Carlini E.A., and Cunha J.M. Hypnotic and antiepileptic effects of cannabidiol. J Clin Pharmacol 21 (1981) 417S-427S
10. Carrier E.J., Auchampach J.A., and Hillard C.J. Inhibition of an equilibrative nucleoside transporter by cannabidiol: a mechanism of cannabinoid immunosuppression. Proc Natl Acad Sci USA 103 (2006) 7895-7900
11. Carrive P. Conditioned fear to environmental context: cardiovascular and behavioral components in the rat. Brain Res 858 (2000) 440-445
12. Conde F., Maire-Lepoivre E., Audinat E., and Crepel F. Afferent connections of the medial frontal cortex of the rat. II. Cortical and subcortical afferents. J Comp Neurol 352 (1995) 567-593
13. Corcoran K.A., and Quirk G.J. Activity in prelimbic cortex is necessary for the expression of learned, but not innate, fears. J Neurosci 27 (2007) 840-844
14. Costa B., Giagnoni G., Franke C., Trovato A.E., and Colleoni M. Vanilloid TRPV1 receptor mediates the antihyperalgesic effect of the nonpsychoactive cannabinoid, cannabidiol, in a rat model of acute inflammation. Br J Pharmacol 43 (2004) 247-250
15. Crippa J.A., Zuardi A.W., Garrido G.E., Wichert-Ana L., Guarnieri R., Ferrari L., et al. Effects of cannabidiol [CBD] on regional cerebral blood flow. Neuropsychopharmacology 29 (2004) 417-426
16. Devane W.A., Dysarz III F.A., Johnson M.R., Melvin L.S., and Howlett A.C. Determination and characterization of a cannabinoid receptor in rat brain. Mol Pharmacol 34 (1988) 605-613
17. Devane W.A., Hanus L., Breuer A., Pertwee R.G., Stevenson L.A., Griffin G., et al. Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science 258 (1992) 1946-1949
18. Di Marzo V., Fontana A., Cadas H., Schinelli S., Cimino G., Schwartz J.C., et al. Formation and inactivation of endogenous cannabinoid anandamide in central neurons. Nature 372 (1994) 686-691
19. Di Marzo V., Melck D., Bisogno T., and De Petrocellis L. Endocannabinoids: endogenous cannabinoid receptor ligands with neuromodulatory action. Trends Neurosci 21 (1998) 521-528
20. Dunn J.D., and Williams T.J. Cardiovascular responses to electrical stimulation of the bed nucleus of the stria terminalis. J Comp Neurol 352 (1995) 227-234
21. Fadda P., Robinson L., Fratta W., Pertwee R.G., and Riedel G. Differential effects of THC- or CBD-rich cannabis extracts on working memory in rats. Neuropharmacology 47 (2004) 1170-1179
22. Fanselow M.S. Conditioned and unconditional components of post-shock freezing. Pavlov J Biol Sci 15 (1980) 177-182
23. Fendt M., and Fanselow M.S. The neuroanatomical and neurochemical basis of conditioned fear. Neurosci Biobehav Rev 23 (1999) 743-760
24. Frankland P.W., Bontempi B., Talton L.E., Kaczmarek L., and Silva A.J. The involvement of the anterior cingulate cortex in remote contextual fear memory. Science 304 (2004) 881-883
25. Guimarães F.S., Chiaretti T.M., Graeff F.G., and Zuardi A.W. Antianxiety effect of cannabidiol in the elevated plus-maze. Psychopharmacology [Berl] 100 (1990) 558-559
26. Guimarães V.M., Zuardi A.W., Del Bel E.A., and Guimarães F.S. Cannabidiol increases Fos expression in the nucleus accumbens but not in the dorsal striatum. Life Sci 75 (2004) 633-638
27. Hashimoto S., Inoue T., and Koyama T. Effects of conditioned fear stress on serotonin neurotransmission and freezing behavior in rats. Eur J Pharmacol 378 (1999) 23-30
28. Herry C., and Mons N. Resistance to extinction is associated with impaired immediate early gene induction in medial prefrontal cortex and amygdala. Eur J Neurosci 20 (2004) 781-790
29. Hurley K.M., Herbert H., Moga M.M., and Saper C.B. Efferent projections of the infralimbic cortex of the rat. J Comp Neurol 308 (1991) 249-276
30. Inoue T., Tsuchiya K., and Koyama T. Serotonergic activation reduces defensive freezing in the conditioned fear paradigm. Pharmacol Biochem Behav 53 (1996) 825-831
31. Iwata J., LeDoux J.E., and Reis D.J. Destruction of intrinsic neurons in the lateral hypothalamus disrupts the classical conditioning of autonomic but not behavioral emotional responses in the rat. Brain Res 368 (1986) 161-166
32. Izumi T., Inoue T., Kitaichi Y., Nakagawa S., and Koyama T. Target brain sites of the anxiolytic effect of citalopram, a selective serotonin reuptake inhibitor. Eur J Pharmacol 534 (2006) 129-132
33. Kasckow J.W., Mulchahey J.J., and Geracioti Jr. T.D. Effects of the vanilloid agonist olvanil and antagonist capsazepine on rat behaviors. Prog Neuropsychopharmacol Biol Psychiatry 28 (2004) 291-295
34. Kathmann M., Flau K., Redmer A., Trankle C., and Schlicker E. Cannabidiol is an allosteric modulator at mu- and delta-opioid receptors. Naunyn Schmiedebergs Arch Pharmacol 372 (2006) 354-361
35. Kovacs K.J. c-Fos as a transcription factor: a stressful [re]view from a functional map. Neurochem Int 33 (1998) 287-297
36. Kujtan P.W., Carlen P.L., and Kapur B.M. delta 9-Tetrahydrocannabinol and cannabidiol: dose-dependent effects on evoked potentials in the hippocampal slice. Can J Physiol Pharmacol 61 (1983) 420-426
37. Laviolette S.R., and Grace A.A. Cannabinoids potentiate emotional learning plasticity in neurons of the medial prefrontal cortex through basolateral amygdala inputs. J Neurosci 26 (2006) 6458-6468
38. LeDoux J. Emotional networks and motor control: a fearful view. Prog Brain Res 107 (1996) 437-446
39. LeDoux J.E., Iwata J., Cicchetti P., and Reis D.J. Different projections of the central amygdaloid nucleus mediate autonomic and behavioral correlates of conditioned fear. J Neurosci 8 (1998) 2517-2529
40. Lee H.J., Choi J.S., Brown T.H., and Kim J.J. Amygdalar NMDA receptors are critical for the expression of multiple conditioned fear responses. J Neurosci 21 (2001) 4116-4124
41. Li X., Inoue T., Abekawa T., Weng S., Nakagawa S., Izumi T., et al. 5-HT1A receptor agonist affects fear conditioning through stimulations of the postsynaptic 5-HT1A receptors in the hippocampus and amygdala. Eur J Pharmacol 532 (2006) 74-80
42. Lin H.C., Mao S.C., Su C.L., and Gean P.W. The role of prefrontal cortex CB1 receptors in the modulation of fear memory. Cereb Cortex 19 1 (2009) 165-175
43. Lino-de-Oliveira C., Sales A.J., Del Bel E.A., Silveira M.C., and Guimarães F.S. Effects of acute and chronic fluoxetine treatments on restraint stress-induced Fos expression. Brain Res Bull 55 (2001) 747-754
44. Maren S., and Quirk G.J. Neuronal signalling of fear memory. Nat Rev Neurosci 5 (2004) 844-852
45. Maren S. Neurobiology of Pavlovian fear conditioning. Annu Rev Neurosci 24 (2001) 897-931
46. Marsch R., Foeller E., Rammes G., Bunck M., Kossl M., Holsboer F., et al. Reduced anxiety, conditioned fear, and hippocampal long-term potentiation in transient receptor potential vanilloid type 1 receptor-deficient mice. J Neurosci 27 (2007) 832-839
47. Matsuda L.A., Lolait S.J., Brownstein M.J., Young A.C., and Bonner T.I. Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature 346 (1990) 561-564
48. Mechoulam R., Parker L.A., and Gallily R. Cannabidiol: an overview of some pharmacological aspects. J Clin Pharmacol 42 (2002) 11S-19S
49. Mishima K., Hayakawa K., Abe K., Ikeda T., Egashira N., Iwasaki K., et al. Cannabidiol prevents cerebral infarction via a serotonergic 5-hydroxytryptamine1A receptor-dependent mechanism. Stroke 36 (2005) 1077-1082
50. Moreira F.A., Aguiar D.C., and Guimarães F.S. Anxiolytic-like effect of cannabidiol in the rat Vogel conflict test. Prog Neuropsychopharmacol Biol Psychiatry 30 (2006) 1466-1471
51. Moreira F.A., and Guimarães F.S. Cannabidiol inhibits the hyperlocomotion induced by psychotomimetic drugs in mice. Eur J Pharmacol 512 (2005) 199-205
52. Moreira F.A., and Lutz B. The endocannabinoid system: emotion, learning and addiction. Addict Biol 3 (2008) 196-212
53. Morrow B.A., Elsworth J.D., Inglis F.M., and Roth R.H. An antisense oligonucleotide reverses the footshock-induced expression of fos in the rat medial prefrontal cortex and the subsequent expression of conditioned fear-induced immobility. J Neurosci 19 (1999) 5666-5673
54. Paxinos G., and Watson C. The rat brain in stereotaxic coordinates (1997), Academic Press, New York
55. Petitet F., Jeantaud B., Reibaud M., Imperato A., and Dubroeucq M.C. Complex pharmacology of natural cannabinoids: evidence for partial agonist activity of delta9-tetrahydrocannabinol and antagonist activity of cannabidiol on rat brain cannabinoid receptors. Life Sci 63 (1998) PL1-6
56. Piomelli D. The molecular logic of endocannabinoid signalling. Nat Rev Neurosci 4 (2003) 873-884
57. Quirk G.J., Likhtik E., Pelletier J.G., and Pare D. Stimulation of medial prefrontal cortex decreases the responsiveness of central amygdala output neurons. J Neurosci 23 (2003) 8800-8807
58. Quirk G.J., and Mueller D. Neural mechanisms of extinction learning and retrieval. Neuropsychopharmacology 33 (2008) 56-72
59. Resstel L.B., Alves F.H., Reis D.G., Crestani C.C., Correa F.M., and Guimarães F.S. Anxiolytic-like effects induced by acute reversible inactivation of the bed nucleus of stria terminalis. Neuroscience 154 (2008) 869-876
60. Resstel L.B., Joca S.R., Moreira F.A., Correa F.M., and Guimarães F.S. Effects of cannabidiol and diazepam on behavioral and cardiovascular responses induced by contextual conditioned fear in rats. Behav Brain Res 172 (2006) 294-298
61. Resstel L.B., Lisboa S.F., Aguiar D.C., Corrêa F.M., and Guimarães F.S. Activation of CB1 cannabinoid receptors in the dorsolateral periaqueductal gray reduces the expression of contextual fear conditioning in rats. Psychopharmacology [Berl] 198 (2008) 405-411
62. Resstel L.B., Tavares R.F., Lisboa S.F., Joca S.R., Corrêa F.M., and Guimarães F.S. 5-HT1A receptors are involved in the cannabidiol-induced attenuation of behavioural and cardiovascular responses to acute restraint stress in rats. Br J Pharmacol 156 (2009) 181-188
63. Rubino T., Realini N., Castiglioni C., Guidali C., Vigano D., Marras E., et al. Role in anxiety behavior of the endocannabinoid system in the prefrontal cortex. Cereb Cortex 18 (2008) 1292-1301
64. Russo E.B., Burnett A., Hall B., and Parker K.K. Agonistic properties of cannabidiol at 5-HT1a receptors. Neurochem Res 30 (2005) 1037-1043
65. Stiedl O., and Spiess J. Effect of tone-dependent fear conditioning on heart rate and behavior of C57BL/6N mice. Behav Neurosci 111 (1997) 703-711
66. Sullivan G.M., Apergis J., Bush D.E., Johnson L.R., Hou M., and Ledoux J.E. Lesions in the bed nucleus of the stria terminalis disrupt corticosterone and freezing responses elicited by a contextual but not by a specific cue-conditioned fear stimulus. Neuroscience 128 (2004) 7-14
67. Tavares R.F., Corrêa F.M., and Resstel L.B. Opposite role of infralimbic and prelimbic cortex in the tachycardiac response evoked by acute restraint stress in rats. J Neurosci Res 87 (2009) 2601-2607
68. Thomas A., Baillie G.L., Phillips A.M., Razdan R.K., Ross R.A., and Pertwee R.G. Cannabidiol displays unexpectedly high potency as an antagonist of CB1 and CB2 receptor agonists in vitro. Br J Pharmacol 150 (2007) 613-623
69. Turkanis S.A., and Karler R. Cannabidiol-caused depression of spinal motoneuron responses in cats. Pharmacol Biochem Behav 25 (1986) 89-94
70. Vertes R.P. Differential projections of the infralimbic and prelimbic cortex in the rat. Synapse 51 (2004) 32-58
71. Vidal-Gonzalez I., Vidal-Gonzalez B., Rauch S.L., and Quirk G.J. Microstimulation reveals opposing influences of prelimbic and infralimbic cortex on the expression of conditioned fear. Learn Mem 13 (2006) 728-733
72. Viveros M.P., Marco E.M., and File S.E. Endocannabinoid system and stress and anxiety responses. Pharmacol Biochem Behav 81 (2005) 331-342
73. Wilson R.I., and Nicoll R.A. Endocannabinoid signaling in the brain. Science 296 (2002) 678-682
74. Wislowska-Stanek A., Zienowicz M., Lehner M., Taracha E., Bidzinski A., Maciejak P., et al. Buspirone attenuates conditioned fear-induced c-Fos expression in the rat hippocampus. Neurosci Lett 389 (2005) 115-120
75. Zuardi A.W., Cosme R.A., Graeff F.G., and Guimarães F.S. Effects of ipsapirone and cannabidiol on human experimental anxiety. J Psychopharmacol 7 (1993) 82-88
76. Zuardi A.W., Guimarães F.S., Guimarães V.M.C., and Del Bel E.A. Cannabidiol: possible therapeutic applications. In: Grotenhermen F., and Russo E. (Eds). Cannabis and cannabinoids (2002), Howorth Int Healing Press, New York 359-369
77. Zuardi A.W., Morais S.L., Guimarães F.S., and Mechoulam R. Antipsychotic effect of cannabidiol. J Clin Psychiatry 56 (1995) 485-486
78. Zuardi A.W., Rodrigues J.A., and Cunha J.M. Effects of cannabidiol in animal models predictive of antipsychotic activity. Psychopharmacology [Berl] 104 (1991) 260-264
79. Zuardi A.W., Shirakawa I., Finkelfarb E., and Karniol I. Action of cannabidiol on the anxiety and other effects produced by Δ9-THC in normal subjects. Psychopharmacology 76 (1982) 245-250