Unique inhibitory synapse with particularly rich endocannabinoid signaling machinery on pyramidal neurons in basal amygdaloid nucleus

Proceedings of the National Academy of Sciences of the United States of America

Volumn 108, Issue 7, 2011, Pages 3059-3064

  Yoshida, Takayuki ^a,b   Uchigashima, Motokazu ^a   Yamasaki, Miwako ^a   Katona, Istvan ^c   Yamazaki, Maya ^d   Sakimura, Kenji ^d,e   Kano, Masanobu ^b,f   Yoshioka, Mitsuhiro ^a   Watanabe, Masahiko ^a,e  

^a HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^d NIIGATA UNIVERSITY   (Japan)

^e JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^f UNIVERSITY OF TOKYO   (Japan)

Author keywords

Depolarization induced suppression of excitation; Depolarization induced suppression of inhibition; Metabotropic glutamate receptor; Muscarinic acetylcholine receptor; Retrograde signaling

Indexed keywords

2 ARACHIDONOYLGLYCEROL; ACYLGLYCEROL LIPASE; CANNABINOID 1 RECEPTOR; CHOLECYSTOKININ; DIACYLGLYCEROL LIPASE ALPHA; LIPOPROTEIN LIPASE; PARVALBUMIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BASAL AMYGDALA; DEPOLARIZATION; INTERNEURON; MOUSE; NONHUMAN; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION;

AMYGDALA; ANIMALS; ARACHIDONIC ACIDS; CHOLECYSTOKININ; ELECTROPHYSIOLOGY; ENDOCANNABINOIDS; GLYCERIDES; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION, FLUORESCENCE; LIPOPROTEIN LIPASE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON; MICROSCOPY, IMMUNOELECTRON; MONOACYLGLYCEROL LIPASES; NEURAL INHIBITION; PYRAMIDAL TRACTS; SIGNAL TRANSDUCTION; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 79952602237     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1012875108     Document Type: Article

References (44)

1. Kano M, Ohno-Shosaku T, Hashimotodani Y, Uchigashima M, Watanabe M (2009) Endocannabinoid-mediated control of synaptic transmission. Physiol Rev 89:309-380.
2. Bisogno T, et al. (2003) Cloning of the first sn1-DAG lipases points to the spatial and temporal regulation of endocannabinoid signaling in the brain. J Cell Biol 163:463-468. (Pubitemid 37429860)
3. Karlsson M, Contreras JA, Hellman U, Tornqvist H, Holm C (1997) cDNA cloning, tissue distribution, and identification of the catalytic triad of monoglyceride lipase. Evolutionary relationship to esterases, lysophospholipases, and haloperoxidases. J Biol Chem 272:27218-27223. (Pubitemid 27452682)
4. Dinh TP, et al. (2002) Brain monoglyceride lipase participating in endocannabinoid inactivation. Proc Natl Acad Sci USA 99:10819-10824.
5. Katona I, Freund TF (2008) Endocannabinoid signaling as a synaptic circuit breaker in neurological disease. Nat Med 14:923-930.
6. Kawamura Y, et al. (2006) The CB1 cannabinoid receptor is the major cannabinoid receptor at excitatory presynaptic sites in the hippocampus and cerebellum. J Neurosci 26:2991-3001.
7. Yoshida T, et al. (2006) Localization of diacylglycerol lipase-alpha around postsynaptic spine suggests close proximity between production site of an endocannabinoid, 2-arachidonoylglycerol, and presynaptic cannabinoid CB1 receptor. J Neurosci 26:4740-4751. (Pubitemid 44315313)
8. Uchigashima M, et al. (2007) Subcellular arrangement of molecules for 2-arachidonoylglycerol-mediated retrograde signaling and its physiological contribution to synaptic modulation in the striatum. J Neurosci 27:3663-3676. (Pubitemid 46557660)
9. LeDoux J (2003) The emotional brain, fear, and the amygdala. Cell Mol Neurobiol 23:727-738.
10. Haller J, Varga B, Ledent C, Freund TF (2004) CB1 cannabinoid receptors mediate anxiolytic effects: Convergent genetic and pharmacological evidence with CB1-specific agents. Behav Pharmacol 15:299-304. (Pubitemid 39062560)
11. Viveros MP, Marco EM, Llorente R, Lamota L (2007) The role of the hippocampus in mediating emotional responses to nicotine and cannabinoids: A possible neural substrate for functional interactions. Behav Pharmacol 18:375-389. (Pubitemid 47356366)
12. Mailleux P, Vanderhaeghen JJ (1992) Distribution of neuronal cannabinoid receptor in the adult rat brain: A comparative receptor binding radioautography and in situ hybridization histochemistry. Neuroscience 48:655-668.
13. Matsuda LA, Bonner TI, Lolait SJ (1993) Localization of cannabinoid receptor mRNA in rat brain. J Comp Neurol 327:535-550. (Pubitemid 23033649)
14. 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. (Pubitemid 30009252)
15. Katona I, et al. (2001) Distribution of CB1 cannabinoid receptors in the amygdala and their role in the control of GABAergic transmission. J Neurosci 21:9506-9518. (Pubitemid 33096895)
16. Kamprath K, et al. (2011) Short-Term Adaptation of Conditioned Fear Responses Through Endocannabinoid Signaling in the Central Amygdala Neuropsychopharmacology 36:652-663.
17. Davis M, Whalen PJ (2001) The amygdala: Vigilance and emotion. Mol Psychiatry 6:13-34. (Pubitemid 32096061)
18. McGaugh JL (2004) The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annu Rev Neurosci 27:1-28.
19. Zhu PJ, Lovinger DM (2005) Retrograde endocannabinoid signaling in a postsynaptic neuron/synaptic bouton preparation from basolateral amygdala. J Neurosci 25:6199-6207. (Pubitemid 40923486)
20. Marsicano G, et al. (2002) The endogenous cannabinoid system controls extinction of aversive memories. Nature 418:530-534. (Pubitemid 34851398)
21. Campolongo P, et al. (2009) Endocannabinoids in the rat basolateral amygdala enhance memory consolidation and enable glucocorticoid modulation of memory. Proc Natl Acad Sci USA 106:4888-4893.
22. Ganon-Elazar E, Akirav I (2009) Cannabinoid receptor activation in the basolateral amygdala blocks the effects of stress on the conditioning and extinction of inhibitory avoidance. J Neurosci 29:11078-11088.
23. Ohno-Shosaku T, Maejima T, Kano M (2001) Endogenous cannabinoids mediate retrograde signals from depolarized postsynaptic neurons to presynaptic terminals. Neuron 29:729-738. (Pubitemid 32323945)
24. Yoshida T, et al. (2002) The cannabinoid CB1 receptor mediates retrograde signals for depolarization-induced suppression of inhibition in cerebellar Purkinje cells. J Neurosci 22:1690-1697. (Pubitemid 35386287)
25. Kreitzer AC, Regehr WG (2001) Retrograde inhibition of presynaptic calcium influx by endogenous cannabinoids at excitatory synapses onto Purkinje cells. Neuron 29:717-727. (Pubitemid 32323944)
26. Wilson RI, Nicoll RA (2001) Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature 410:588-592. (Pubitemid 32267203)
27. Azad SC, et al. (2004) Circuitry for associative plasticity in the amygdala involves endocannabinoid signaling. J Neurosci 24:9953-9961. (Pubitemid 39463576)
28. Patel S, Kingsley PJ, Mackie K, Marnett LJ, Winder DG (2009) Repeated homotypic stress elevates 2-arachidonoylglycerol levels and enhances short-term endocannabinoid signaling at inhibitory synapses in basolateral amygdala. Neuropsychopharmacology 34:2699-2709.
29. Kodirov SA, et al. (2010) Endogenous cannabinoids trigger the depolarization-induced suppression of excitation in the lateral amygdala. Learn Mem 17:43-49.
30. Leranth C, Frotscher M (1986) Synaptic connections of cholecystokinin-immunoreactive neurons and terminals in the rat fascia dentata: A combined light and electron microscopic study. J Comp Neurol 254:51-64. (Pubitemid 17194490)
31. Acsády L, Katona I, Martínez-Guijarro FJ, Buzsáki G, Freund TF (2000) Unusual target selectivity of perisomatic inhibitory cells in the hilar region of the rat hippocampus. J Neurosci 20:6907-6919.
32. Ehrlich I, et al. (2009) Amygdala inhibitory circuits and the control of fear memory. Neuron 62:757-771.
33. Pape HC, Pare D (2010) Plastic synaptic networks of the amygdala for the acquisition, expression, and extinction of conditioned fear. Physiol Rev 90:419-463.
34. Freund TF (2003) Interneuron Diversity series: Rhythm and mood in perisomatic inhibition. Trends Neurosci 26:489-495.
35. Amano T, Unal CT, Paré D (2010) Synaptic correlates of fear extinction in the amygdala. Nat Neurosci 13:489-494.
36. Ben-Ari Y, Zigmond RE, Shute CC, Lewis PR (1977) Regional distribution of choline acetyltransferase and acetylcholinesterase within the amygdaloid complex and stria terminalis system. Brain Res 120:435-444.
37. McDonald AJ (1998) Cortical pathways to the mammalian amygdala. Prog Neurobiol 55:257-332.
38. Muller JF, Mascagni F, McDonald AJ (2007) Serotonin-immunoreactive axon terminals innervate pyramidal cells and interneurons in the rat basolateral amygdala. J Comp Neurol 505:314-335. (Pubitemid 350134070)
39. Onishi BK, Xavier GF (2010) Contextual, but not auditory, fear conditioning is disrupted by neurotoxic selective lesion of the basal nucleus of amygdala in rats. Neurobiol Learn Mem 93:165-174.
40. Zimmer A, Zimmer AM, Hohmann AG, Herkenham M, Bonner TI (1999) Increased mortality, hypoactivity, and hypoalgesia in cannabinoid CB1 receptor knockout mice. Proc Natl Acad Sci USA 96:5780-5785. (Pubitemid 29234695)
41. Tanimura A, et al. (2010) The endocannabinoid 2-arachidonoylglycerol produced by diacylglycerol lipase alpha mediates retrograde suppression of synaptic transmission. Neuron 65:320-327.
42. Yamasaki M, Matsui M, Watanabe M (2010) Preferential localization of muscarinic M1 receptor on dendritic shaft and spine of cortical pyramidal cells and its anatomical evidence for volume transmission. J Neurosci 30:4408-4418.
43. Narushima M, et al. (2007) Tonic enhancement of endocannabinoid-mediated retrograde suppression of inhibition by cholinergic interneuron activity in the striatum. J Neurosci 27:496-506. (Pubitemid 46143754)
44. Narushima M, Uchigashima M, Hashimoto K, Watanabe M, Kano M (2006) Depolarization-induced suppression of inhibition mediated by endocannabinoids at synapses from fast-spiking interneurons to medium spiny neurons in the striatum. Eur J Neurosci 24:2246-2252. (Pubitemid 44622345)