Cannabinoid CB1 receptor calibrates excitatory synaptic balance in the mouse hippocampus

Journal of Neuroscience

Volumn 35, Issue 9, 2015, Pages 3842-3850

  Monory, Krisztina ^a   Polack, Martin ^b   Remus, Anita ^b,c   Lutz, Beat ^a   Korte, Martin ^b,c  

^a UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

^b TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

^c HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

Author keywords

Cannabinoids; CB1 receptor; Dendritic morphology; LTP; Spines; Synaptic plasticity

Indexed keywords

4 AMINOBUTYRIC ACID; CANNABINOID 1 RECEPTOR;

ADULT; ANIMAL TISSUE; ARTICLE; BRAIN DEPTH STIMULATION; CELL STRUCTURE; CONTROLLED STUDY; DENDRITE; ELECTROPHYSIOLOGICAL PROCEDURES; GENE DELETION; GENOTYPE; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; HIPPOCAMPUS; HISTOCHEMISTRY; LONG TERM POTENTIATION; MALE; MOUSE; MYELINATION; NERVE CELL PLASTICITY; NERVE FUNCTION; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; SYNAPSE; ANIMAL; C57BL MOUSE; EXCITATORY POSTSYNAPTIC POTENTIAL; GENETICS; KNOCKOUT MOUSE; PHYSIOLOGY; SYNAPTIC TRANSMISSION;

ANIMALS; EXCITATORY POSTSYNAPTIC POTENTIALS; HIPPOCAMPUS; LONG-TERM POTENTIATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURONAL PLASTICITY; RECEPTOR, CANNABINOID, CB1; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 84924777567     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3167-14.2015     Document Type: Article

References (49)

1. Abel T, Martin KC, Bartsch D, Kandel ER (1998) Memory suppressor genes: inhibitory constraints on the storage of long-term memory. Science 279: 338-341.
2. Auclair N, Otani S, Soubrie P, Crepel F (2000) Cannabinoids modulate synaptic strength and plasticity at glutamatergic synapses of rat pre-frontal cortex pyramidal neurons. J Neurophysiol 83:3287-3293.
3. Ballesteros-Yáñez I, Valverde O, Ledent C, Maldonado R, DeFelipe J (2007) Chronic cocaine treatment alters dendritic arborization in the adult motor cortex through a CB1 cannabinoid receptor-dependent mechanism. Neuroscience 146:1536-1545.
4. Bellocchio L, Lafenêtre P, Cannich A, Cota D, Puente N, Grandes P, Chaou-loff F, Piazza PV, Marsicano G (2010) Bimodal control of stimulated food intake by the endocannabinoid system. Nat Neurosci 13:281-283.
5. Berghuis P, Rajnicek AM, Morozov YM, Ross RA, Mulder J, Urbán GM, Monory K, Marsicano G, Matteoli M, Canty A, Irving AJ, Katona I, Yana-gawa Y, Rakic P, Lutz B, Mackie K, Harkany T (2007) Hardwiring the brain: endocannabinoids shape neuronal connectivity. Science 316:1212-1216.
6. Bliss TV, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31-39.
7. Bohme GA, Laville M, Ledent C, Parmentier M, Imperato A (2000) Enhanced long-term potentiation in mice lacking cannabinoid CB1 receptors. Neuroscience 95:5-7.
8. Bojnik E, Turunc¸ E, Armağan G, Kanıt L, Benyhe S, Yalçın A, Borsodi A (2012) Changes in the cannabinoid (CB1) receptor expression level and G-protein activation in kainic acid induced seizures. Epilepsy Res 99:64-68.
9. Buhl E, Whittington M (2007) Local circuits. In: The hippocampus book (Amaral D, Andersen P, Morris R, Bliss T, O’Keefe J, eds). New York: Oxford UP.
10. Carlson G, Wang Y, Alger BE (2002) Endocannabinoids facilitate the induction of LTP in the hippocampus. Nat Neurosci 5:723-724.
11. Castillo PE, Younts TJ, Chávez AE, Hashimotodani Y (2012) Endocannabi-noid signaling and synaptic function. Neuron 76:70-81.
12. Chevaleyre V, Castillo PE (2004) Endocannabinoid-mediated metaplastic-ity in the hippocampus. Neuron 43:871-881.
13. Citri A, Malenka RC (2008) Synaptic plasticity: multiple forms, functions, and mechanisms. Neuropsychopharmacology 33:18-41.
14. Fan N, Yang H, Zhang J, Chen C (2010) Reduced expression of glutamate receptors and phosphorylation of CREB are responsible for in vivo Delta9-THC exposure-impaired hippocampal synaptic plasticity. J Neu-rochem 112:691-702.
15. 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.
16. 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.
17. Hensch TK, Fagiolini M (2005) Excitatory-inhibitory balance and critical period plasticity in developing visual cortex. Prog Brain Res 147:115-124.
18. Hill MN, Hillard CJ, McEwen BS (2011) Alterations in corticolimbic dendritic morphology and emotional behavior in cannabinoid CB1 receptor-deficient mice parallel the effects of chronic stress. Cereb Cortex 21:2056-2064.
19. Hoffman AF, Oz M, Yang R, Lichtman AH, Lupica CR (2007) Opposing actions of chronic Delta9-tetrahydrocannabinol and cannabinoid antagonists on hippocampal long-term potentiation. Learn Mem 14:63-74.
20. Jacob W, Marsch R, Marsicano G, Lutz B, Wotjak CT (2012) Cannabinoid CB1 receptor deficiency increases contextual fear memory under highly aversive conditions and long-term potentiation in vivo. Neurobiol Learn Mem 98:47-55.
21. Kamprath K, Plendl W, Marsicano G, Deussing JM, Wurst W, Lutz B, Wotjak CT (2009) Endocannabinoids mediate acute fear adaptation via gluta-matergic neurons independently of corticotropin-releasing hormone signaling. Genes Brain Behav 8:203-211.
22. Kano M, Ohno-Shosaku T, Hashimotodani Y, Uchigashima M, Watanabe M (2009) Endocannabinoid-mediated control of synaptic transmission. Physiol Rev 89:309-380.
23. Kim J, Alger BE (2010) Reductioninendocannabinoid toneisahomeostatic mechanism for specific inhibitory synapses. Nat Neurosci 13:592-600.
24. Kleppisch T, Wolfsgruber W, Feil S, Allmann R, Wotjak CT, Goebbels S, Nave KA, Hofmann F, Feil R (2003) Hippocampal cGMP-dependent protein kinase I supports an age-and protein synthesis-dependent component of long-term potentiation but is not essential for spatial reference and contextual memory. J Neurosci 23:6005-6012.
25. Lafenêtre P, Chaouloff F, Marsicano G (2009) Bidirectional regulation of novelty-induced behavioral inhibition by the endocannabinoid system. Neuropharmacology 57:715-721.
26. Malenka RC, Bear MF (2004) LTP and LTD: an embarrassment of riches. Neuron 44:5-21.
27. Marsicano G, Lafenêtre P (2009) Roles of the endocannabinoid system in learning and memory. Curr Top Behav Neurosci 1:201-230.
28. 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.
29. 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 aver-sive memories. Nature 418:530-534.
30. 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, Schütz G, Zieglgänsberger W, Di Marzo V, Behl C, Lutz B (2003) CB1 cannabinoid receptors and on-demand defense against excitotoxicity. Science 302:84-88.
31. Massa F, Mancini G, Schmidt H, Steindel F, Mackie K, Angioni C, Oliet SH, Geisslinger G, Lutz B (2010) Alterations in the hippocampal endocan-nabinoid system in diet-induced obese mice. J Neurosci 30:6273-6281.
32. Metna-Laurent M, Soria-Gómez E, Verrier D, Conforzi M, Jégo P, Lafenêtre P, Marsicano G (2012) Bimodal control of fear-coping strategies by CB(1) cannabinoid receptors. J Neurosci 32:7109-7118.
33. Monory K, Massa F, Egertova´ 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, Zieglgäns-berger W, Wotjak CT, et al. (2006) The endocannabinoid system controls key epileptogenic circuits in the hippocampus. Neuron 51:455-466.
34. Monory K, Blaudzun H, Massa F, Kaiser N, Lemberger T, Schütz G, Wotjak CT, Lutz B, Marsicano G (2007) Genetic dissection of behavioural and autonomic effects of delta(9)-tetrahydrocannabinol in mice. PLoS Biol 5:e269.
35. Mulder J, Aguado T, Keimpema E, Barabás K, Ballester Rosado CJ, Nguyen L, Monory K, Marsicano G, Di Marzo V, Hurd YL, Guillemot F, Mackie K, Lutz B, Guzmán M, Lu HC, Galve-Roperh I, Harkany T (2008) Endo-cannabinoid signaling controls pyramidal cell specification and long-range axon patterning. Proc Natl Acad Sci U S A 105:8760-8765.
36. Navakkode S, Korte M (2014) Pharmacological activation of CB1 receptor modulates long term potentiation by interfering with protein synthesis. Neuropharmacology 79:525-533.
37. Paton GS, Pertwee RG, Davies SN (1998) Correlation between cannabinoid-mediated effects on paired pulse depression and induction of long term po-tentiation in the rat hippocampal slice. Neuropharmacology 37:1123-1130.
38. Puighermanal E, Marsicano G, Busquets-Garcia A, Lutz B, Maldonado R, Ozaita A (2009) Cannabinoid modulation of hippocampal long-term memory is mediated by mTOR signaling. Nat Neurosci 12:1152-1158.
39. Puighermanal E, Busquets-Garcia A, Gomis-González M, Marsicano G, Mal-donado R, Ozaita A (2013) Dissociation of the pharmacological effects of THC by mTOR blockade. Neuropsychopharmacology 38:1334-1343.
40. Riedel G, Davies SN (2005) Cannabinoid function in learning, memory and plasticity. Handb Exp Pharmacol 168:445-477.
41. Rösch H, Schweigreiter R, Bonhoeffer T, Barde YA, Korte M (2005) The neurotrophin receptor p75NTR modulates long-term depression and regulates the expression of AMPA receptor subunits in the hippocampus. Proc Natl Acad Sci USA 102:7362-7367.
42. Roth-Alpermann C, Morris RG, Korte M, Bonhoeffer T (2006) Homeo-static shutdown of long-term potentiation in the adult hippocampus. Proc Natl Acad Sci USA 103:11039-11044.
43. Ruehle S, Rey AA, Remmers F, Lutz B (2012) The endocannabinoid system in anxiety, fear memory and habituation. J Psychopharmacol 26:23-39.
44. Sholl DA (1953) Dendritic organization in the neurons of the visual and motor cortices of the cat. J Anat 87:387-406.
45. Steindel F, Lerner R, Häring M, Ruehle S, Marsicano G, Lutz B, Monory K (2013) Neuron-type specific cannabinoid-mediated G protein signalling in mouse hippocampus. J Neurochem 124:795-807.
46. Stella N, Schweitzer P, Piomelli D (1997) A second endogenous cannabi-noid that modulates long-term potentiation. Nature 388:773-778.
47. Turrigiano G (2011) Too many cooks? Intrinsic and synaptic homeostatic mechanisms in cortical circuit refinement. Annu Rev Neurosci 34:89-103.
48. Varvel SA, Lichtman AH (2002) Evaluation of CB1 receptor knock-out mice in the Morris water maze. J Pharmacol Exp Ther 301:915-924.
49. Zagrebelsky M, Korte M (2014) Maintaining stable memory engrams: new roles for Nogo-A in the CNS. Neuroscience 283C:17-25.