The endocannabinoid 2-arachidonoylglycerol negatively regulates habituation by suppressing excitatory recurrent network activity and reducing long-term potentiation in the dentate gyrus

Endocannabinoids are known to mediate retrograde suppression of synaptic transmission, modulate synaptic plasticity, and influence learning and memory. The 2-arachidonoylglycerol (2-AG) produced by diacylglycerol lipase α (DGLα) is regarded as the major endocannabinoid that causes retrograde synapti...

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Veröffentlicht in:The Journal of neuroscience 2013-02, Vol.33 (8), p.3588-3601
Hauptverfasser: Sugaya, Yuki, Cagniard, Barbara, Yamazaki, Maya, Sakimura, Kenji, Kano, Masanobu
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container_issue 8
container_start_page 3588
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creator Sugaya, Yuki
Cagniard, Barbara
Yamazaki, Maya
Sakimura, Kenji
Kano, Masanobu
description Endocannabinoids are known to mediate retrograde suppression of synaptic transmission, modulate synaptic plasticity, and influence learning and memory. The 2-arachidonoylglycerol (2-AG) produced by diacylglycerol lipase α (DGLα) is regarded as the major endocannabinoid that causes retrograde synaptic suppression. To determine how 2-AG signaling influences learning and memory, we subjected DGLα knock-out mice to two learning tasks. We tested the mice using habituation and odor-guided transverse patterning tasks that are known to involve the dentate gyrus and the CA1, respectively, of the hippocampus. We found that DGLα knock-out mice showed significantly faster habituation to an odor and a new environment than wild-type littermates with normal performance in the transverse patterning task. In freely moving animals, long-term potentiation (LTP) induced by theta burst stimulation was significantly larger at perforant path-granule cell synapses in the dentate gyrus of DGLα knock-out mice. Importantly, prior induction of synaptic potentiation at this synapse caused a significant retardation of habituation in DGLα knock-out but not in wild-type littermates. The excitability of granule cells became higher in DGLα knock-out mice after they generated action potentials. Since no differences were found in intrinsic membrane properties and responses to odor stimuli in granule cells, the elevated excitability is considered to result from enhanced activity of an excitatory recurrent network composed of granule cells and mossy cells. These results suggest that retrograde 2-AG signaling negatively regulates habituation by suppressing excitatory recurrent network activity and reducing LTP in the dentate gyrus.
doi_str_mv 10.1523/JNEUROSCI.3141-12.2013
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source MEDLINE; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central
subjects Animals
Arachidonic Acids - physiology
Association Learning - physiology
Dentate Gyrus - physiology
Endocannabinoids - physiology
Excitatory Postsynaptic Potentials - physiology
Female
Glycerides - physiology
Habituation, Psychophysiologic - physiology
Long-Term Potentiation - physiology
Male
Mice
Mice, Inbred C57BL
Mice, Knockout
Nerve Net - physiology
Neural Inhibition - physiology
Reaction Time - physiology
Secondary Prevention
title The endocannabinoid 2-arachidonoylglycerol negatively regulates habituation by suppressing excitatory recurrent network activity and reducing long-term potentiation in the dentate gyrus
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