Integrated cannabinoid CB1 receptor transmission within the amygdala-prefrontal cortical pathway modulates neuronal plasticity and emotional memory encoding

Cerebral Cortex

Volumn 20, Issue 6, 2010, Pages 1486-1496

  Tan, Huibing ^a   Lauzon, Nicole M ^a   Bishop, Stephanie F ^a   Bechard, Melanie A ^a   Laviolette, Steven R ^a  

^a WESTERN UNIVERSITY   (Canada)

Author keywords

Amygdala; Cannabinoids; Emotional learning; Long term potentiation; Memory; Prefrontal cortex

Indexed keywords

1 (2,4 DICHLOROPHENYL) 5 (4 IODOPHENYL) 4 METHYL N (1 PIPERIDYL) 1H PYRAZOLE 3 CARBOXAMIDE; CANNABINOID 1 RECEPTOR;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; CONTROLLED STUDY; EMOTION; FEAR; IN VIVO STUDY; LIMBIC CORTEX; LONG TERM POTENTIATION; MALE; MEMORY; MODULATION; NERVE CELL PLASTICITY; NEUROTRANSMISSION; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT; STIMULATION;

AMYGDALA; ANIMALS; BRAIN MAPPING; ELECTRIC STIMULATION; EMOTIONS; LONG-TERM POTENTIATION; MALE; MEMORY; NEURAL PATHWAYS; NEURONAL PLASTICITY; PIPERIDINES; PREFRONTAL CORTEX; PYRAZOLES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, CANNABINOID, CB1; SYNAPTIC TRANSMISSION;

EID: 77952802123     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhp210     Document Type: Article

References (44)

1. Aggleton JP. 2000. The amygdala: a functional analysis. 2nd ed. New York: Oxford University Press.
2. 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.
3. Azad SC, Eder M, Marsicano G, Lutz B, Zieglgansberger W, Rammes G. 2003. Activation of the cannabinoid receptor type 1 decreases glutamatergic and GABAergic synaptic transmission in the lateral amygdala of the mouse. Learn Mem. 10:116-128.
4. Azad SC, Monory K, Marsicano G, Cravatt BF, Lutz B, Zieglgansberger W, Rammes G. 2004. Circuitry for associative plasticity in the amygdala involves endocannabinoid signaling. J Neurosci. 24:9953-9961.
5. Bacon SJ, Headlam AJ, Gabbott PL, Smith AD. 1996. Amygdala input to medial prefrontal cortex in the rat: a light and electron microscope study. Brain Res. 720:211-219.
6. Balleine BW, Dickenson A. 1998. Goal directed instrumental action: contingency and incentive learning and their cortical substrates. Neuropharmacology. 37:407-419.
7. Bangalore SS, Prasad KM, Montrose DM, Goradia DD, Diwadkar VA, Keshavan MS. 2008. Cannabis use and brain structural alterations in first episode schizophrenia: a region of interest, voxel based morphometric study. Schizophr Res. 99:1-6.
8. Cohen M, Solowij N, Carr V. 2008. Cannabis, cannabinoids and schizophrenia: integration of the evidence. Aust NZ J Psych. 42:357-368.
9. Corcoran KA, Quirk GJ. 2007. Activity in prelimbic cortex is necessary for the expression of learning, but not innate fears. J Neurosci. 27:840-844.
10. Finn DP, Beckett SR, Richardson D, Kendall DA, Marsden CA, Chapman V. 2004. Evidence for differential modulation of conditioned aversion and fear-conditioned analgesia by CB1 receptors. Eur J Neurosci. 20:848-852.
11. Finn DP, Jhaveri MD, Beckett SR, Madjd A, Kendall DA, Marsden CA, Chapman V. 2006. Behavioural, central monoaminergic and hypothalamo-pituitary-adrenal axis correlates of fear-conditioned analgesia. Neuroscience. 138:1309-1317.
12. Gatley SJ, Lan R, Pyatt B, Gifford AN, Volkow ND, Makriyannis A. 1997. Binding of the non-classical cannabinoid CP 55, 940, and the diarylpyrazole AM 251 to rodent brain cannabinoid receptors. Life Sci. 61:191-197.
13. Giuffrida A, Leweke FM, Gerth CW, Schreiber D, Koethe D, Faulhaber J, Klosterkotter J, Piomelli D. 2004. Cerebrospinal anandamide levels are elevated in acute schizophrenia and are inversely correlated with psychotic symptoms. Neuropsychopharmacology. 29:2108-2114.
14. Hasanein P, Parviz M, Keshavarz M, Javanmardi K. 2007. CB1 receptor activation in the basolateral amygdala produces antinociception in animal models of acute and tonic nociception. Clin Exp Pharmacol Physiol. 34:439-449.
15. Hodge J, Bow JP, Plyler KS, Vemuri VK, Wisniecki A, Salamone JD, Makriyannis A, Mclaughlin PJ. 2008. The cannabinoid CB1 receptor inverse agonist AM 251 and antagonist AM 4113 produce similar effects on the behavioural satiety sequence in rats. Behav Brain Res. 193:298-305.
16. Hoffman AF, Lupica CR. 2001. Direct actions of cannabinoids on synaptic transmission in the nucleus accumbens: a comparison with opioids. J Neurophysiol. 85:72-83.
17. Herkenham M, Lynn AB, Little MD, Johnson MR, Melvin LS, de Costa BR, Rice KC. 1990. Cannabinoid receptor localization in brain. Proc Natl Acad Sci USA. 87:1932-1936.
18. Katona I, Rancz EA, Acsady L, Ledent C, Mackie K, Hajos N, Freund TF. 2001. Distribution of CB1 receptors in the amygdala and their role in the control of GABAergic transmission. J Neurosci. 21:9506-9518.
19. Koethe D, Giuffrida A, Schreiber D, Hellmich M, Schultz-Lutter F, Ruhrmann S, Klosterkotter J, Piomelli D, Leweke FM. 2009. Anandamide elevation in cerebrospinal fluid in prodromal states of psychosis. Br J Psychiatry. 194:371-372.
20. 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. 8:e709.
21. Lan R, Liu Q, Fan P, Lin S, Fernando SR, McCallion D, Pertwee R, Makriyannis A. 1999. Structure-activity relationships of pyrazole derivatives as cannabinoid receptor antagonists. J Med Chem. 42:769-776.
22. Laviolette SR, Grace AA. 2006a. The roles of cannabinoid and dopamine receptor systems in neural emotional learning circuits: implications for schizophrenia and addiction. Cell Mol Life Sci. 63:1597-1613.
23. Laviolette SR, Grace AA. 2006b. Cannabinoids dramatically potentiate emotional learning plasticity in neurons of the medial prefrontal cortex through basolateral amygdala. J Neurosci. 26:6458-6468.
24. Laviolette SR, Lipski WJ, Grace AA. 2005. A subpopulation of neurons in the medial prefrontal cortex encodes emotional learning through burst and frequency codes through a dopamine D4 receptor-dependent basolateral amygdala input. J Neurosci. 25:6066-6075.
25. Manning BH, Martin WJ, Meng ID. 2003. The rodent amygdala contributes to the production of cannabinoid-induced antinocicep-tion. Neuroscience. 120:1157-1170.
26. Manzoni OJ, Bockaert J. 2001. Cannabinoids inhibit GABAergic synaptic transmission in mice nucleus accumbens. Eur J Pharmacol. 412:R3-R5.
27. Marsicano G, Wotjak CT, Azad SC, Bisogno T, Rammes G, Cascio MG, Hermann H, Tang J, Hoffman G, Zieglansberger W, et al. 2002. The endogenous cannabinoid systems controls extinction of aversive memories. Nature. 418:530-534.
28. Maroun M. 2006. Stress reverses plasticity in the pathway projecting from the ventromedial prefrontal cortex to the basolateral amygdala. Eur J Neurosci. 24:2917-2922.
29. Maroun M, Richter-Levin G. 2003. Exposure to acute stress blocks the induction of long-term potentiation in the amygdala-prefrontal cortex pathway in vivo. J Neurosci. 23:4406-4409.
30. McDonald AJ, Mascagni F. 2001. Localization of the CB1 type cannabinoid receptor in the rat basolateral amygdala: high concentrations in a subpopulation of cholecystokinin-containing inter-neurons. Neuroscience. 107:641-652.
31. McGinty V, Grace AA. 2008. Selective activation of medial prefrontal-to-accumbens projection neurons by amygdala stimulation and Pavlovian conditioned stimuli. Cereb Cortex. 18:1961-1972.
32. Milad MR, Quirk GJ. 2002. Neurons in the medial prefrontal cortex signal memory for fear extinction. Nature. 420:70-74.
33. Newell KA, Deng C, Huang XF. 2006. Increased cannabinoid receptor density in the posterior cingulate cortex in schizophrenia. Exp Brain Res. 172:556-560.
34. Orozco-Cabal L, Pollandt S, Liu J, Vergara L, Shinnick-Gallagher P, Gallagher JP. 2006. A novel rat medial prefrontal cortical slice preparation to investigate synaptic transmission from amygdala to layer V prelimbic pyramidal neurons. J Neurosci Methods. 151: 148-158.
35. Paxinos G, Watson C. 1997. The rat brain in stereotaxic coordinates. 3rd ed. San Diego (CA): Academic.
36. Pistis M, Perra S, Pillolla G, Melis M, Gessa GL, Muntoni AL. 2004. Cannabinoids modulate neuronal firing in the rat basolateral amygdala: evidence for CB1 and non-CB1-mediated actions. Neuropharmacology. 46:115-125.
37. Roche M, O'Connor E, Diskin C, Finn DP. 2007. The effects of CB1 receptor antagonism in the right basolateral amygdala on conditioned fear and associated analgesia in rats. Eur J Neurosci. 26:2643-2653.
38. Rosenkranz JA, Grace AA. 2002. Cellular mechanisms of infralimbic and prelimbic prefrontal cortical inhibition and dopaminergic modulation of basolateral amygdala neurons in vivo. J Neurosci. 22: 324-337.
39. Rosenkranz JA, Grace AA. 2003. The prefrontal cortex regulates lateral amygdala neuronal plasticity and responses to previously conditioned stimuli. J Neurosci. 23:11054-11064.
40. Schneider M. 2008. Puberty as a highly vulnerable developmental period for the consequences of cannabis exposure. Addict Biol. 13:253-263.
41. Thiemann G, Marzo V, Molleman A, Hasenohrl RU. 2008. The CB1 cannabinoid receptor antagonist AM 251 attenuates amphetamine-induced behavioural sensitization while causing monoamine changes in nucleus accumbens and hippocampus. Parmacol Biochem Behav. 89:384-391.
42. Tsou K, Brown S, Sanudo-Pena MC, Mackie K, Walker JM. 1998. Immunohistochemical distribution of cannabinoid CB1 receptors in the rat central nervous system. Neuroscience. 83:393-411.
43. Vertes RP. 2004. Differential projections of the infralimbic and prelimbic cortex in the rat. Synapse. 51:32-58.
44. Zavitsanou K, Garrick T, Huang XF. 2004. Selective antagonist [3H]SR141716A binding to cannabinoid CB1 receptors is increased in the anterior cingulate cortex in schizophrenia. Prog Neuro-psychopharmacol Biol Psychiatry. 28:355-360.