Cannabinoid CB1 receptor in dorsal telencephalic glutamatergic neurons: Distinctive sufficiency for hippocampus-dependent and amygdala-dependent synaptic and behavioral functions

Journal of Neuroscience

Volumn 33, Issue 25, 2013, Pages 10264-10277

  Ruehle, Sabine ^a   Remmers, Floor ^a   Romo Parra, Hector ^b   Massa, Federico ^c   Wickert, Melanie ^a   Wörtge, Simone ^a   Häring, Martin ^a   Kaiser, Nadine ^a   Marsicano, Giovanni ^c   Pape, Hans Christian ^b   Lutz, Beat ^a  

^a UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

^b UNIVERSITY OF MÜNSTER   (Germany)

^c INSTITUT FRANÇOIS MAGENDIE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CANNABINOID 1 RECEPTOR;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY; ARTICLE; AUTORADIOGRAPHY; BEHAVIOR; BRAIN ELECTROPHYSIOLOGY; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; DEPOLARIZATION; FEAR; FEMALE; GLUTAMATERGIC NERVE CELL; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; LIGHT DARK CYCLE; MALE; MAZE TEST; MOUSE; NERVE CELL; NERVE CELL INHIBITION; NERVE CELL PLASTICITY; NERVE CELL STIMULATION; NEUROPROTECTION; NONHUMAN; PAIN THRESHOLD; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RNA ISOLATION; TELENCEPHALON; WESTERN BLOTTING;

AMYGDALA; ANIMALS; ANXIETY; BEHAVIOR, ANIMAL; BLOTTING, WESTERN; ELECTROPHYSIOLOGICAL PHENOMENA; EXCITATORY AMINO ACID AGONISTS; GLUTAMIC ACID; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; KAINIC ACID; LIGHT; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURONAL PLASTICITY; NEURONS; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTOR, CANNABINOID, CB1; RNA; SYNAPSES; TELENCEPHALON;

EID: 84879135358     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4171-12.2013     Document Type: Article

References (53)

1. Balthasar N, Dalgaard LT, Lee CE, Yu J, Funahashi H, Williams T, Ferreira M, Tang V, McGovern RA, Kenny CD, Christiansen LM, Edelstein E, Choi B, Boss O, Aschkenasi C, Zhang CY, Mountjoy K, Kishi T, Elmquist JK, Lowell BB (2005) Divergence of melanocortin pathways in the control of food intake and energy expenditure. Cell 123:493-505. CrossRef Medline
2. 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
3. Ben-Ari Y, Cossart R (2000) Kainate, a double agent that generates seizures: two decades of progress. Trends Neurosci 23:580-587. CrossRef Medline
4. Chiu CQ, Castillo PE (2008) Input-specific plasticity at excitatory synapses mediated by endocannabinoids in the dentate gyrus. Neuropharmacology 54:68-78. CrossRef Medline
5. Cota D, Steiner MA, Marsicano G, Cervino C, Herman JP, Grubler Y, Stalla J, Pasquali R, Lutz B, Stalla GK, Pagotto U (2007) Requirement of cannabinoid receptor type 1 for the basal modulation of hypothalamicpituitary-adrenal axis function. Endocrinology 148:1574-1581. Medline
6. Dubreucq S, Kambire S, Conforzi M, Metna-Laurent M, Cannich A, Soria-Gomez E, Richard E, Marsicano G, Chaouloff F (2012a) Cannabinoid type 1 receptors located on single-minded 1-expressing neurons control emotional behaviors. Neuroscience 204:230-244. CrossRef Medline
7. Dubreucq S, Matias I, Cardinal P, Häring M, Lutz B, Marsicano G, Chaouloff F (2012b) Genetic dissection of the role of cannabinoid type-1 receptors in the emotional consequences of repeated social stress in mice. Neuropsychopharmacology 37:1885-1900. CrossRef Medline
8. Goebbels S, Bormuth I, Bode U, Hermanson O, Schwab MH, Nave KA (2006) Genetic targeting of principal neurons in neocortex and hippocampus of NEX-Cre mice. Genesis 44:611-621. CrossRef Medline
9. Gross C, Zhuang X, Stark K, Ramboz S, Oosting R, Kirby L, Santarelli L, Beck S, Hen R (2002) Serotonin 1A receptor acts during development to establish normal anxiety-like behaviour in the adult. Nature 416:396-400. CrossRef Medline
10. Guggenhuber S, Monory K, Lutz B, Klugmann M (2010) AAV vectormediated overexpression of CB1 cannabinoid receptor in pyramidal neurons of the hippocampus protects against seizure-induced excitoxicity. PLoS One 5:e15707. CrossRef Medline
11. Haller J, Varga B, Ledent C, Barna I, Freund TF (2004) Context-dependent effects of CB1 cannabinoid gene disruption on anxiety-like and social behaviour in mice. Eur J Neurosci 19:1906-1912. CrossRef Medline
12. Han J, Kesner P, Metna-Laurent M, Duan T, Xu L, Georges F, Koehl M, Abrous DN, Mendizabal-Zubiaga J, Grandes P, Liu Q, Bai G, Wang W, Xiong L, Ren W, Marsicano G, Zhang X (2012) Acute cannabinoids impair working memory through astroglial CB1 receptor modulation of hippocampal LTD. Cell 148:1039-1050. CrossRef Medline
13. Häring M, Kaiser N, Monory K, Lutz B (2011) Circuit specific functions of cannabinoid CB1 receptor in the balance of investigatory drive and exploration. PLoS One 6:e26617. CrossRef Medline
14. Herkenham M, Lynn AB, de Costa BR, Richfield EK (1991) Neuronal localization of cannabinoid receptors in the basal ganglia of the rat. Brain Res 547:267-274. CrossRef Medline
15. Kamprath K, Wotjak CT (2004) Nonassociative learning processes determine expression and extinction of conditioned fear in mice. Learn Mem 11:770-786. CrossRef Medline
16. Kamprath K, Plendl W, Marsicano G, Deussing JM, Wurst W, Lutz B, Wotjak CT (2009) Endocannabinoids mediate acute fear adaptation via glutamatergic neurons independently of corticotropin-releasing hormone signaling. Genes Brain Behav 8:203-211. CrossRef Medline
17. Kamprath K, Romo-Parra H, Häring M, Gaburro S, Doengi M, Lutz B, Pape HC (2011) Short-term adaptation of conditioned fear responses through endocannabinoid signaling in the central amygdala. Neuropsychopharmacology 36:652-663. CrossRef Medline
18. Kano M, Ohno-Shosaku T, Hashimotodani Y, Uchigashima M, Watanabe M (2009) Endocannabinoid-mediated control of synaptic transmission. Physiol Rev 89:309-380. CrossRef Medline
19. Katona I, Freund TF (2012) Multiple functions of endocannabinoid signaling in the brain. Annu Rev Neurosci 35:529-558. CrossRef Medline
20. Kawamura Y, Fukaya M, Maejima T, Yoshida T, Miura E, Watanabe M, Ohno-Shosaku T, Kano M (2006) The CB1 cannabinoid receptor is the major cannabinoid receptor at excitatory presynaptic sites in the hippocampus and cerebellum. J Neurosci 26:2991-3001. CrossRef Medline
21. Lafenêtre P, Chaouloff F, Marsicano G (2009) Bidirectional regulation of novelty-induced behavioral inhibition by the endocannabinoid system. Neuropharmacology 57:715-721. CrossRef Medline
22. Lakso M, Pichel JG, Gorman JR, Sauer B, Okamoto Y, Lee E, Alt FW, Westphal H (1996) Efficient in vivo manipulation of mouse genomic sequences at the zygote stage. Proc Natl Acad Sci U S A 93:5860-5865. CrossRef Medline
23. Lee S, Ahmed T, Lee S, Kim H, Choi S, Kim DS, Kim SJ, Cho J, Shin HS (2012) Bidirectional modulation of fear extinction by mediodorsal thalamic firing in mice. Nat Neurosci 15:308-314. CrossRef Medline
24. Lourenco J, Cannich A, Carta M, Coussen F, Mulle C, Marsicano G (2010) Synaptic activation of kainate receptors gates presynaptic CB1 signaling at GABAergic synapses. Nat Neurosci 13:197-204. CrossRef Medline
25. Ludányi A, Eross L, Czirják S, Vajda J, Halász P, Watanabe M, Palkovits M, Maglóczky Z, Freund TF, Katona I (2008) Downregulation of the CB1 cannabinoid receptor and related molecular elements of the endocannabinoid system in epileptic human hippocampus. J Neurosci 28:2976-2990. CrossRef Medline
26. Marsicano G, Kuner R (2008) Anatomical distribution of receptors, ligands and enzymes in the brain and in the spinal cord: circuitries and neuro-chemistry. In: Cannabinoids and the brain (Köfalvi A, ed), pp 161-201. Boston: Springer US.
27. Marsicano G, Lutz B (1999) Expression of the cannabinoid receptor CB1 in distinct neuronal subpopulations in the adult mouse forebrain. Eur J Neurosci 11:4213-4225. CrossRef Medline
28. Marsicano G, Wotjak CT, Azad SC, Bisogno T, Rammes G, Cascio MG, Hermann H, Tang J, Hofmann C, Zieglgänsberger W, Di Marzo V, Lutz B (2002) The endogenous cannabinoid system controls extinction of aversive memories. Nature 418:530-534. CrossRef Medline
29. Marsicano G, Goodenough S, Monory K, Hermann H, Eder M, Cannich A, Azad SC, Cascio MG, Gutiérrez SO, van der Stelt M, López-Rodriguez ML, Casanova E, Schutz G, Zieglgänsberger W, Di Marzo V, Behl C, Lutz B (2003) CB1 cannabinoid receptors and on-demand defense against excitotoxicity. Science 302:84-88. CrossRef Medline
30. Metna-Laurent M, Soria-Gómez E, Verrier D, Conforzi M, Jégo P, Lafenêtre P, Marsicano G (2012) Bimodal control of fear-coping strategies by CB1 cannabinoid receptors. J Neurosci 32:7109-7118. CrossRef Medline
31. Monory K, Massa F, Egertová M, Eder M, Blaudzun H, Westenbroek R, Kelsch W, Jacob W, Marsch R, Ekker M, Long J, Rubenstein JL, Goebbels S, Nave KA, During M, Klugmann M, Wölfel B, Dodt HU, Zieglgänsberger W, Wotjak CT et al. (2006) The endocannabinoid system controls key epileptogenic circuits in the hippocampus. Neuron 51:455-466. CrossRef Medline
32. Nagy A (2000) Cre recombinase: the universal reagent for genome tailoring. Genesis 26:99-109. CrossRef Medline
33. Ohno-Shosaku T, Tsubokawa H, Mizushima I, Yoneda N, Zimmer A, Kano M (2002) Presynaptic cannabinoid sensitivity is a major determinant of depolarization-induced retrograde suppression at hippocampal synapses. J Neurosci 22:3864-3872. Medline
34. Pan B, Wang W, Long JZ, Sun D, Hillard CJ, Cravatt BF, Liu QS (2009) Blockade of 2-arachidonoylglycerol hydrolysis by selective monoacylglycerol lipase inhibitor 4-nitrophenyl 4-(dibenzo[d][1,3]dioxol-5-yl(hydroxy)methyl)piperidine-1-carboxylate (JZL184) enhances retrograde endocannabinoid signaling. J Pharmacol Exp Ther 331:591-597. CrossRef Medline
35. Pan B, Wang W, Zhong P, Blankman JL, Cravatt BF, Liu QS (2011) Alterations of endocannabinoid signaling, synaptic plasticity, learning, and memory in monoacylglycerol lipase knock-out mice. J Neurosci 31:13420-13430. CrossRef Medline
36. Pape HC, Paré D (2010) Plastic synaptic networks of the amygdala for the acquisition, expression, and extinction of conditioned fear. Physiol Rev 90:419-463. CrossRef Medline
37. Paxinos G, Franklin KBJ (2008) The mouse brain in stereotaxic coordinates, third edition: the coronal plates and diagrams. New York: Academic.
38. ©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30:e36. CrossRef Medline
39. Quirk GJ, Mueller D (2008) Neural mechanisms of extinction learning and retrieval. Neuropsychopharmacology 33:56-72. CrossRef Medline
40. Rey AA, Purrio M, Viveros MP, Lutz B (2012) Biphasic effects of cannabinoids in anxiety responses: CB1 and GABAB receptors in the balance of GABAergic and glutamatergic neurotransmission. Neuropsychopharmacology 37:2624-2634. CrossRef Medline
41. Rideout WM 3rd, Wakayama T, Wutz A, Eggan K, Jackson-Grusby L, Dausman J, Yanagimachi R, Jaenisch R (2000) Generation of mice from wild-type and targeted ES cells by nuclear cloning. Nat Genet 24:109-110. CrossRef Medline
42. Ruehle S, Rey AA, Remmers F, Lutz B (2012) The endocannabinoid system in anxiety, fear memory and habituation. J Psychopharmacol 26:23-39. CrossRef Medline
43. Schauwecker PE, Steward O (1997) Genetic determinants of susceptibility to excitotoxic cell death: implications for gene targeting approaches. Proc Natl Acad Sci U S A 94:4103-4108. CrossRef Medline
44. Schwab MH, Bartholomae A, Heimrich B, Feldmeyer D, Druffel-Augustin S, Goebbels S, Naya FJ, Zhao S, Frotscher M, Tsai MJ, Nave KA (2000) Neuronal basic helix-loop-helix proteins (NEX and BETA2/Neuro D) regulate terminal granule cell differentiation in the hippocampus. J Neurosci 20:3714-3724. Medline
45. Self DW (2005) Molecular and genetic approaches for behavioral analysis of protein function. Biol Psychiatry 57:1479-1484. CrossRef Medline
46. 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
47. Steindel F, Lerner R, Häring M, Ruehle S, Marsicano G, Lutz B, Monory K (2013) Neuron-type specific cannabinoid-mediated G protein signaling in mouse hippocampus. J Neurochem 124:795-807. CrossRef Medline
48. Steiner MA, Marsicano G, Wotjak CT, Lutz B (2008) Conditional cannabinoid receptor type 1 mutants reveal neuron subpopulation-specific effects on behavioral and neuroendocrine stress responses. Psychoneuroendocrinology 33:1165-1170. CrossRef Medline
49. Terzian AL, Drago F, Wotjak CT, Micale V (2011) The dopamine and cannabinoid interaction in the modulation of emotions and cognition: assessing the role of cannabinoid CB1 receptor in neurons expressing dopamine D1 receptors. Front Behav Neurosci 5:49. Medline
50. Torres R, Kuhn R (1997) Laboratory protocols for conditional gene targeting. New York: Oxford UP.
51. Walf AA, Frye CA (2007) The use of the elevated plus maze as an assay of anxiety-related behavior in rodents. Nat Protoc 2:322-328. CrossRef Medline
52. Wilson RI, Nicoll RA (2001) Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature 410:588-592. CrossRef Medline
53. Yizhar O, Fenno LE, Prigge M, Schneider F, Davidson TJ, O'Shea DJ, Sohal VS, Goshen I, Finkelstein J, Paz JT, Stehfest K, Fudim R, Ramakrishnan C, Huguenard JR, Hegemann P, Deisseroth K (2011) Neocortical excitation/inhibition balance in information processing and social dysfunction. Nature 477:171-178. CrossRef Medline