The CB1 cannabinoid receptor mediates glutamatergic synaptic suppression in the hippocampus

被引:112
作者
Takahashi, K. A. [1 ]
Castillo, P. E. [1 ]
机构
[1] Yeshiva Univ Albert Einstein Coll Med, Dept Neurosci, Kennedy Ctr, Bronx, NY 10461 USA
关键词
cannabinoid; CA1; CB3; CB1; knockout; excitatory synaptic transmission; glutamate;
D O I
10.1016/j.neuroscience.2006.01.024
中图分类号
Q189 [神经科学];
学科分类号
071006 ;
摘要
Cannabinoids have profound effects on synaptic function and behavior. Of the two cloned cannabinoid receptors, cannabinoid receptor 1 (CB1) is widely distributed in the CNS and accounts for most of the neurological effects of cannabinoids, while cannabinoid receptor 2 (CB2) expression in the CNS is very limited. The presence of additional receptors [i.e. cannabinoid receptor 3 (CB3)] is suggested by growing evidence of cannabinoid effects that are not mediated by CB1 or CB2. The most direct functional evidence for a CB3 comes from a study in hippocampus where deletion of CB1 was shown to have no effect on cannabinoid-mediated suppression of the excitatory synapse between Schaffer collateral/commissural fibers and CA1 pyramidal cells [Hajos N, Ledent C, Freund TF (2001) Novel cannabinoid-sensitive receptor mediates inhibition of glutamatergic synaptic transmission in the hippocampus. Neuroscience 106:1-4]. In contrast, we report here that in extracellular field recordings, the cannabinoid agonist WIN 55,212-2 (5 mu M) had no effect on Schaffer collateral/commissural fiber-CA1 pyramidal cell (Sch-CA1) synaptic transmission in slices from two independently made cannabinoid receptor 1(-/-) lines [Zimmer et al., 1999; Ledent et al., 1999] while strongly suppressing Sch-CA1 synaptic transmission in CB1(+/+) mice of the background strains. Also, we observed robust cannabinold-mediated suppression of the Sch-CA1 synapse in pure C57BL/6 mice, contradicting a recent report that cannabinoid suppression of this synapse is absent in this strain [Hoffman AF, Macgill AM, Smith D, Oz M, Lupica CR (2005) Species and strain differences in the expression of a novel glutamate-modulating cannabinoid receptor in the rodent hippocampus. Eur J Neurosci 22:2387-2391]. Our results strongly suggest that cannabinoid-induced suppression of the Sch-CA1 synapse is mediated by CB1. Non-canonical cannabinoid receptors do not seem to play a major role in inhibiting transmitter release at this synapse. (c) 2006 IBRO. Published by Elsevier Ltd. All rights reserved.
引用
收藏
页码:795 / 802
页数:8
相关论文
共 30 条
[1]   Cannabinoid receptor mediated inhibition of excitatory synaptic transmission in the rat hippocampal slice is developmentally regulated [J].
Al-Hayani, A ;
Davies, SN .
BRITISH JOURNAL OF PHARMACOLOGY, 2000, 131 (04) :663-665
[2]   Effects of the endogeneous cannabinoid, anandamide, on neuronal activity in rat hippocampal slices [J].
Ameri, A ;
Wilhelm, A ;
Simmet, T .
BRITISH JOURNAL OF PHARMACOLOGY, 1999, 126 (08) :1831-1839
[3]   Evidence for novel cannabinoid receptors [J].
Begg, M ;
Pacher, P ;
Bátkai, S ;
Osei-Hyiaman, D ;
Offertáler, L ;
Mo, FM ;
Liu, H ;
Kunos, G .
PHARMACOLOGY & THERAPEUTICS, 2005, 106 (02) :133-145
[4]   Endocannabinoids inhibit transmission at granule cell to Purkinje cell synapses by modulating three types of presynaptic calcium channels [J].
Brown, SP ;
Safo, PK ;
Regehr, WG .
JOURNAL OF NEUROSCIENCE, 2004, 24 (24) :5623-5631
[5]   Endocannabinoid-mediated synaptic plasticity in the CNS [J].
Chevaleyre, Vivien ;
Takahashi, Kanji A. ;
Castillo, Pablo E. .
ANNUAL REVIEW OF NEUROSCIENCE, 2006, 29 :37-76
[6]   Role of endogenous cannabinoids in synaptic signaling [J].
Freund, TF ;
Katona, I ;
Piomelli, D .
PHYSIOLOGICAL REVIEWS, 2003, 83 (03) :1017-1066
[7]   Cannabinoids inhibit hippocampal GABAergic transmission and network oscillations [J].
Hájos, N ;
Katona, I ;
Naiem, SS ;
Mackie, K ;
Ledent, C ;
Mody, I ;
Freund, TF .
EUROPEAN JOURNAL OF NEUROSCIENCE, 2000, 12 (09) :3239-3249
[8]   Novel cannabinoid-sensitive receptor mediates inhibition of glutamatergic synaptic transmission in the hippocampus [J].
Hájos, N ;
Ledent, C ;
Freund, TF .
NEUROSCIENCE, 2001, 106 (01) :1-4
[9]   Pharmacological separation of cannabinoid sensitive receptors on hippocampal excitatory and inhibitory fibers [J].
Hájos, N ;
Freund, TF .
NEUROPHARMACOLOGY, 2002, 43 (04) :503-510
[10]   Species and strain differences in the expression of a novel glutamate-modulating cannabinoid receptor in the rodent hippocampus [J].
Hoffman, AF ;
Macgill, AM ;
Smith, D ;
Oz, M ;
Lupica, CR .
EUROPEAN JOURNAL OF NEUROSCIENCE, 2005, 22 (09) :2387-2391