Role of Striatal Direct Pathway 2-Arachidonoylglycerol Signaling in Sociability and Repetitive Behavior

Biol Psychiatry. 2018 Aug 15;84(4):304-315. doi: 10.1016/j.biopsych.2017.11.036. Epub 2017 Dec 28.

Abstract

Background: Endocannabinoid signaling plays an important role in regulating synaptic transmission in the striatum, a brain region implicated as a central node of dysfunction in autism spectrum disorder. Deficits in signaling mediated by the endocannabinoid 2-arachidonoylglycerol (2-AG) have been reported in mouse models of autism spectrum disorder, but a causal role for striatal 2-AG deficiency in phenotypes relevant to autism spectrum disorder has not been explored.

Methods: Using conditional knockout mice, we examined the electrophysiological, biochemical, and behavioral effects of 2-AG deficiency by deleting its primary synthetic enzyme, diacylglycerol lipase α (DGLα), from dopamine D1 receptor-expressing or adenosine A2a receptor-expressing medium spiny neurons (MSNs) to determine the role of 2-AG signaling in striatal direct or indirect pathways, respectively. We then used viral-mediated deletion of DGLα to study the effects of 2-AG deficiency in the ventral and dorsal striatum.

Results: Targeted deletion of DGLα from direct-pathway MSNs caused deficits in social interaction, excessive grooming, and decreased exploration of a novel environment. In contrast, deletion from indirect-pathway MSNs had no effect on any measure of behavior examined. Loss of 2-AG in direct-pathway MSNs also led to increased glutamatergic drive, which is consistent with a loss of retrograde feedback inhibition. Subregional DGLα deletion from the dorsal striatum produced deficits in social interaction, whereas deletion from the ventral striatum resulted in repetitive grooming.

Conclusions: These data suggest a role for 2-AG deficiency in social deficits and repetitive behavior, and they demonstrate a key role for 2-AG in regulating striatal direct-pathway MSNs.

Keywords: 2-Arachindonoylglycerol; Autism spectrum disorder; Diacylglycerol lipase; Endocannabinoid; Nucleus accumbens; Striatum.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Arachidonic Acids / deficiency
  • Arachidonic Acids / metabolism*
  • Autism Spectrum Disorder / metabolism
  • Corpus Striatum / metabolism*
  • Endocannabinoids / deficiency
  • Endocannabinoids / metabolism*
  • Glycerides / deficiency
  • Glycerides / metabolism*
  • Mice
  • Mice, Knockout
  • Receptor, Adenosine A2A / metabolism*
  • Receptors, Dopamine D1 / metabolism*
  • Signal Transduction
  • Social Behavior*
  • Synaptic Transmission

Substances

  • Arachidonic Acids
  • Endocannabinoids
  • Glycerides
  • Receptor, Adenosine A2A
  • Receptors, Dopamine D1
  • glyceryl 2-arachidonate