Cannabinoid transmission in the prefrontal cortex Bi-phasically controls emotional memory formation via functional interactions with the ventral tegmental area

Journal of Neuroscience

Volumn 34, Issue 39, 2014, Pages 13096-13109

  Draycott, Brittany ^a   Loureiro, Michael ^a   Ahmad, Tasha ^a   Tan, Huibing ^a   Zunder, Jordan ^a   Laviolette, Steven R ^a  

^a WESTERN UNIVERSITY   (Canada)

Author keywords

Cannabinoids; Dopamine; Fear memory; Prefrontal cortex; Ventral tegmental area

Indexed keywords

2, 3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL) PYRROLO [1, 2, 3 DE] [1, 4] BENZOXAZINE; 4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID B RECEPTOR; 4 AMINOBUTYRIC ACID B RECEPTOR BLOCKING AGENT; CANNABINOID; CANNABINOID 1 RECEPTOR; DOPAMINE; UNCLASSIFIED DRUG; 4 AMINOBUTYRIC ACID RECEPTOR;

ANIMAL EXPERIMENT; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; FEAR MEMORY; FOOTSHOCK; IN VIVO STUDY; MALE; MEMORY; NEUROMODULATION; NEUROTRANSMISSION; NONHUMAN; OLFACTORY MEMORY; PERCEPTIVE THRESHOLD; PREFRONTAL CORTEX; RAT; SIGNAL TRANSDUCTION; SPIKE WAVE; VENTRAL TEGMENTUM; ACTION POTENTIAL; ANIMAL; CYTOLOGY; FEAR; METABOLISM; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ACTION POTENTIALS; ANIMALS; DOPAMINERGIC NEURONS; FEAR; GABAERGIC NEURONS; MALE; MEMORY; PREFRONTAL CORTEX; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, CANNABINOID, CB1; VENTRAL TEGMENTAL AREA;

EID: 84907294899     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1297-14.2014     Document Type: Article

References (62)

1. Abush H, Akirav I (2012) Short- and long-term cognitive effects of chronic cannabinoids administration in late-adolescence rats. PLoS One 7:e31731. CrossRef Medline
2. Ahmad T, Lauzon NM, de Jaeger X, Laviolette SR (2013) Cannabinoid transmission in the prelimbic cortex bidirectionally controls opiate reward and aversion signaling through dissociable kappa versus μ-opiate receptor dependent mechanisms. J Neurosci 33:15642-15651. CrossRef Medline
3. Albrecht DS, Skosnik PD, Vollmer JM, Brumbaugh MS, Perry KM, Mock BH, Zheng QH, Federici LA, Patton EA, Herring CM, Yoder KK (2013) Striatal D(2)/D(3) receptor availability is inversely correlated with cannabis consumption in chronic marijuana users. Drug Alcohol Depend 128:52-57. CrossRef Medline
4. Andréasson S, Allebeck P, Engström A, Rydberg U (1987) Cannabis and schizophrenia. A longitudinal study of Swedish conscripts. Lancet 2:1483-1486. Medline
5. Andréasson S, Allebeck P, Rydberg U (1989) Schizophrenia in users and nonusers of cannabis. A longitudinal study in Stockholm County. Acta Psychiatr Scand 79:505-510. CrossRef Medline
6. Antoniadis EA, McDonald RJ (1999) Discriminative fear conditioning to context expressed by multiple measures of fear in the rat. Behav Brain Res 101:1-13. CrossRef Medline
7. Auclair N, Otani S, Soubrie P, Crepel F (2000) Cannabinoids modulate synaptic strength and plasticity at glutamatergic synapses of rat prefrontal cortex pyramidal neurons. J Neurophysiol 83:3287-3293. Medline
8. Bellocchio L, Lafenêtre P, Cannich A, Cota D, Puente N, Grandes P, Chaouloff F, Piazza PV, Marsicano G (2010) Bimodal control of stimulated food intake by the endocannabinoid system. Nat Neurosci 13:281-283. CrossRef Medline
9. Bloomfield MA, Morgan CJ, Egerton A, Kapur S, Curran HV, Howes OD (2014) Dopaminergic function in cannabis users and its relationship to cannabis-induced psychotic symptoms. Biol Psychiatry 75:470-478. CrossRef Medline
10. Bossert JM, Stern AL, Theberge FR, Marchant NJ, Wang HL, Morales M, Shaham Y (2012) Role of projections from ventral medial prefrontal cortex to nucleus accumbens shell in context-induced reinstatement of heroin seeking. J Neurosci 32:4982- 4991. CrossRef Medline
11. Carr DB, Sesack SR (2000a) GABA-containing neurons in the rat ventral tegmental area project to the prefrontal cortex. Synapse 38:114 -123. CrossRef Medline
12. Carr DB, Sesack SR (2000b) Projections from the rat prefrontal cortex to the ventral tegmental area: target specificity in the synaptic associations with mesoaccumbens and mesocortical neurons. J Neurosci 20:3864 -38673. Medline
13. Chiu CQ, Puente N, Grandes P, Castillo PE (2010) Dopaminergic modulation of endocannabinoid-mediated plasticity at GABAergic synapses in the prefrontal cortex. J Neurosci 30:7236 -7248. CrossRef Medline
14. Churchill L, Dilts RP, Kalivas PW (1992) Autoradiographic localization of gamma-aminobutyric acid-A receptors within the ventral tegmental area. Neurochem Res 17:101-106. CrossRef Medline
15. Dalton VS, Long LE, Weickert CS, Zavitsanou K (2011) Paranoid schizophrenia is characterized by increased CB1 receptor binding in the dorsolateral prefrontal cortex. Neuropsychopharmacology 36:1620 -1630. CrossRef Medline
16. Dean B, Sundram S, Bradbury R, Scarr E, Copolov D (2001) Studies on [3H]CP-55940 binding in the human central nervous system: regional specific changes in density of cannabinoid-1 receptors associated with schizophrenia and cannabis use. Neuroscience 103:9 -15. CrossRef Medline
17. Degenhardt L, Hall W, LynskeyM (2003) Exploring the association between cannabis use and depression. Addiction 98:1493-1504. CrossRef Medline
18. Fitzgerald ML, Mackie K, PickelVM (2013) The impact of adolescent social isolation on dopamine D2 and cannabinoid CB1 receptors in the adult rat prefrontal cortex. Neuroscience 235:40 -50. CrossRef Medline
19. French ED, Dillon K, Wu X (1997) Cannabinoids excite dopamine neurons in the ventral tegmentum and substantia nigra. Neuroreport 8:649-652. CrossRef Medline
20. Gessa GL, Melis M, Muntoni AL, Diana M (1998) Cannabinoids activate mesolimbic dopamine neurons by an action on cannabinoid CB1 receptors. Eur J Pharmacol 341:39-44. CrossRef Medline
21. Grace AA, Bunney BS (1983) Intracellular and extracellular electrophysiology of nigral dopaminergic neurons-1. Identification and characterization. Neuroscience 10:301-315. CrossRef Medline
22. Gysling K, Wang RY (1983) Morphine-induced activation of A10 dopamine neurons in the rat. Brain Res 277:119 -127. Medline
23. Hall W, Degenhardt L (2011) Cannabis and the increased incidence and persistence of psychosis. BMJ 342:d719. CrossRef Medline
24. Hill MN, McLaughlin RJ, Pan B, Fitzgerald ML, Roberts CJ, Lee TT, Karatsoreos IN, Mackie K, Viau V, Pickel VM, McEwen BS, Liu QS, Gorzalka BB, Hillard CJ (2011) Recruitment of prefrontal cortical endocannabinoid signaling by glucocorticoids contributes to termination of the stress response. J Neurosci 31:10506 -10515. CrossRef Medline
25. Jensen J, Willeit M, Zipursky RB, Savina I, Smith AJ, Menon M, Crawley AP, Kapur S (2008) The formation of abnormal associations in schizophrenia: neural and behavioral evidence. Neuropsychopharmacology 33:473- 479. CrossRef Medline
26. Kalivas PW (1993) Neurotransmitter regulation of dopamine neurons in the ventral tegmental area. Brain Res Brain Res Rev 18:75-113. CrossRef Medline
27. Kalivas PW, Duffy P, Eberhardt H (1990) Modulation of A10 dopamine neurons by gamma-aminobutyric acid agonists. J Pharmacol Exp Ther 253:858-866. Medline
28. Kalivas PW, Churchill L, Klitenick MA (1993) GABA and enkephalin projection from the nucleus accumbens and ventral pallidum to the ventral tegmental area Neuroscience 57:1047-1060. CrossRef
29. Katsidoni V, Kastellakis A, Panagis G (2013) Biphasic effects of Δ9- tetrahydrocannabinol on brain stimulation reward and motor activity. Int J Neuropsychopharmacol 16:2273-2284. CrossRef Medline
30. Kiritoshi T, Sun H, Ren W, Stauffer SR, Lindsley CW, Conn PJ, Neugebauer V (2013) Modulation of pyramidal cell output in the medial prefrontal cortex by mGluR5 interacting with CB1. Neuropharmacology 66:170- 178. CrossRef Medline
31. Klitenick MA, DeWitte P, Kalivas PW (1992) Regulation of somatodendritic dopamine release in the ventral tegmental area by opioids and GABA: an in vivo microdialysis study. J Neurosci 12:2623-2632. Medline
32. Kuepper R, van Os J, Lieb R, Wittchen HU, Höfler M, Henquet C (2011) Continued cannabis use and risk of incidence and persistence of psychotic symptoms: 10 year follow-up cohort study. BMJ 342:d738, 2011 Mar 1. CrossRef Medline
33. Kuepper R, Ceccarini J, Lataster J, van Os J, van Kroonenburgh M, van Gerven JM, Marcelis M, Van Laere K, Henquet C (2013) Delta-9- tetrahydrocannabinol-induced dopamine release as a function of psychosis risk: 18F-fallypride positron emission tomography study. PLoS One 8:e70378. CrossRef Medline
34. Lacey MG (1993) Neurotransmitter receptors and ionic conductances regulating the activity of neurones in substantia nigra pars compacta and ventral tegmental area. Prog Brain Res 99:251-276. CrossRef Medline
35. Lafourcade M, Elezgarai I, Mato S, Bakiri Y, Grandes P, Manzoni OJ (2007) Molecular components and functions of the endocannabinoid system in mouse prefrontal cortex. PLoS One 2:e709. CrossRef Medline
36. Lauzon NM, Bishop SF, Laviolette SR (2009) Dopamine D1 versus D4 receptors differentially modulate the encoding of salient versus nonsalient emotional information in the medial prefrontal cortex. J Neurosci 29: 4836-4845. CrossRef Medline
37. Laviolette SR, Grace AA (2006) Cannabinoids potentiate emotional learning plasticity in neurons of the medial prefrontal cortex through basolateral amygdala inputs. J Neurosci 26:6458-6468. CrossRef Medline
38. A receptors in the ventral tegmental area control bidirectional reward signalling between dopaminergic and non-dopaminergic neural motivational systems. Eur J Neurosci 13:1009 -1015. CrossRef Medline
39. Laviolette SR, Gallegos RA, Henriksen SJ, van der Kooy D (2004) Opiate state controls bi-directional reward signaling via GABAA receptors in the ventral tegmental area. Nat Neurosci 7:160 -169. CrossRef Medline
40. Laviolette SR, Lipski WJ, Grace AA (2005) A subpopulation of neurons in the medial prefrontal cortex encodes emotional learning with burst and frequency codes through a dopamine D4 receptor-dependent basolateral amygdala input. J Neurosci 25:6066-6075. CrossRef Medline
41. B receptor activation in the ventral tegmental area inhibits the acquisition and expression of opiate-induced motor sensitization. J Pharmacol Exp Ther 308:667- 678. Medline
42. Lynskey MT, Glowinski AL, Todorov AA, Bucholz KK, Madden PA, Nelson EC, Statham DJ, Martin NG, Heath AC (2004) Major depressive disorder, suicidal ideation, and suicide attempt in twins discordant for cannabis dependence and early-onset cannabis use. Arch Gen Psychiatry 61: 1026-1032. CrossRef Medline
43. B receptors in the rat central nervous system. J Comp Neurol 405:299 -321. CrossRef Medline
44. Margolis EB, Toy B, Himmels P, Morales M, FieldsHL (2012) Identification of rat ventral tegmental area GABAergic neurons. PLoS One 7:e42365. CrossRef Medline
45. Margulies JE, Hammer RP Jr (1991) Delta 9-tetrahydrocannabinol alters cerebral metabolism in a biphasic, dose-dependent manner in rat brain. Eur J Pharmacol 202:373-378. CrossRef Medline
46. Oropeza VC, Mackie K, Van Bockstaele EJ (2007) Cannabinoid receptors are localized to noradrenergic axon terminals in the rat frontal cortex. Brain Res 1127:36-44. CrossRef Medline
47. Paxinos G, Watson C (2005) The rat brain in stereotaxic coordinates. San Diego, CA: Academic.
48. Pistis M, Porcu G, Melis M, Diana M, Gessa GL (2001) Effects of cannabinoids on prefrontal neuronal responses to ventral tegmental area stimulation. Eur J Neurosci 14:96 -102. CrossRef Medline
49. Renard J, Krebs MO, Jay TM, Le Pen G (2013) Long-term cognitive impairments induced by chronic cannabinoid exposure during adolescence in rats: a strain comparison. Psychopharmacology 225:781-790. CrossRef Medline
50. B receptors in the balance of GABAergic and glutamatergic neurotransmission. Neuropsychopharmacology 37:2624 -2634. CrossRef Medline
51. Seutin V, Johnson SW, North RA (1994) Effect of dopamine and baclofen on N-methyl-D-aspartate-induced burst firing in rat ventral tegmental neurons. Neuroscience 58:201-206. CrossRef Medline
52. Sierra-Mercado D, Padilla-Coreano N, Quirk GJ (2011) Dissociable roles of prelimbic and infralimbic cortices, ventral hippocampus, and basolateral amygdala in the expression and extinction of conditioned fear. Neuropsychopharmacology 36:529 -538. CrossRef Medline
53. Smith MJ, Cobia DJ, Wang L, Alpert KI, Cronenwett WJ, Goldman MB, Mamah D, Barch DM, Breiter HC, Csernansky JG (2014) Cannabisrelated working memory deficits and associated subcortical morphological differences in healthy individuals and schizophrenia subjects. Schizophr Bull 40:287-299. CrossRef Medline
54. Sotres-Bayon F, Sierra-Mercado D, Pardilla-Delgado E, Quirk GJ (2012) Gating of fear in prelimbic cortex by hippocampal and amygdala inputs. Neuron 76:804-812. CrossRef Medline
55. Szutorisz H, DiNieri JA, Sweet E, Egervari G, Michaelides M, Carter JM, Ren Y, Miller ML, Blitzer RD, Hurd YL (2014) Parental THC exposure leads to compulsive heroin-seeking and altered striatal synaptic plasticity in the subsequent generation. Neuropsychopharmacology 39:1315-1323. CrossRef Medline
56. Tan H, Lauzon NM, Bishop SF, Bechard MA, Laviolette SR (2010) Integrated cannabinoid CB1 receptor transmission within the amygdalaprefrontal cortical pathway modulates neuronal plasticity and emotional memory encoding. Cereb Cortex 20:1486 -1496. CrossRef Medline
57. Tan H, Lauzon NM, Bishop SF, Chi N, Bechard M, Laviolette SR (2011) Cannabinoid transmission in the basolateral amygdala modulates fear memory formation via functional inputs to the prelimbic cortex. J Neurosci 31:5300 -5312. CrossRef Medline
58. Urban NB, Slifstein M, Thompson JL, Xu X, Girgis RR, Raheja S, Haney M, Abi-Dargham A (2012) Dopamine release in chronic cannabis users: a [11C]raclopride positron emission tomography study. Biol Psychiatry 71:677- 683. CrossRef Medline
59. Valjent E, Maldonado R (2000) A behavioral model to reveal place preference to delta 9-tetrahydrocannabinol in mice. Psychopharmacology 147: 436-448. CrossRef Medline
60. Westerink BH, Kwint HF, deVries JB (1996) The pharmacology of mesolimbic dopamine neurons: a dual-probe microdialysis study in the ventral tegmental area and nucleus accumbens of the rat brain. J Neurosci 16:2605-2611. Medline
61. B receptors in midbrain monoamine containing neurons in the rat. Brain Res Bull 56: 1-5. CrossRef Medline
62. Xi ZX, Stein EA (1999) Baclofen inhibits heroin self-administration behavior and mesolimbic dopamine release. J Pharmacol Exp Ther 290:1369- 1374. Medline