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Open AccessArticle

Hippocampal Stratum Oriens Somatostatin-Positive Cells Undergo CB1-Dependent Long-Term Potentiation and Express Endocannabinoid Biosynthetic Enzymes

1
Neuroscience Center, Brigham Young University, Provo, UT 84602, USA
2
Department of Physiology and Developmental Biology, Brigham Young University, Provo, UT 84602, USA
*
Author to whom correspondence should be addressed.
Academic Editor: Mauro Maccarrone
Molecules 2019, 24(7), 1306; https://doi.org/10.3390/molecules24071306
Received: 12 December 2018 / Revised: 29 March 2019 / Accepted: 30 March 2019 / Published: 3 April 2019
(This article belongs to the Special Issue Emerging Topics in (Endo)Cannabinoid Signalling)
The hippocampus is thought to encode information by altering synaptic strength via synaptic plasticity. Some forms of synaptic plasticity are induced by lipid-based endocannabinoid signaling molecules that act on cannabinoid receptors (CB1). Endocannabinoids modulate synaptic plasticity of hippocampal pyramidal cells and stratum radiatum interneurons; however, the role of endocannabinoids in mediating synaptic plasticity of stratum oriens interneurons is unclear. These feedback inhibitory interneurons exhibit presynaptic long-term potentiation (LTP), but the exact mechanism is not entirely understood. We examined whether oriens interneurons produce endocannabinoids, and whether endocannabinoids are involved in presynaptic LTP. Using patch-clamp electrodes to extract single cells, we analyzed the expression of endocannabinoid biosynthetic enzyme mRNA by reverse transcription and then real-time PCR (RT-PCR). The cellular expression of calcium-binding proteins and neuropeptides were used to identify interneuron subtype. RT-PCR results demonstrate that stratum oriens interneurons express mRNA for both endocannabinoid biosynthetic enzymes and the type I metabotropic glutamate receptors (mGluRs), necessary for endocannabinoid production. Immunohistochemical staining further confirmed the presence of diacylglycerol lipase alpha, an endocannabinoid-synthesizing enzyme, in oriens interneurons. To test the role of endocannabinoids in synaptic plasticity, we performed whole-cell experiments using high-frequency stimulation to induce long-term potentiation in somatostatin-positive cells. This plasticity was blocked by AM-251, demonstrating CB1-dependence. In addition, in the presence of a fatty acid amide hydrolase inhibitor (URB597; 1 µM) and MAG lipase inhibitor (JZL184; 1 µM) that increase endogenous anandamide and 2-arachidonyl glycerol, respectively, excitatory current responses were potentiated. URB597-induced potentiation was blocked by CB1 antagonist AM-251 (2 µM). Collectively, this suggests somatostatin-positive oriens interneuron LTP is CB1-dependent. View Full-Text
Keywords: anandamide; LTP; eCB; mGluR5; mGluR1; hippocampus; DAGLα; 12-lipoxygenase anandamide; LTP; eCB; mGluR5; mGluR1; hippocampus; DAGLα; 12-lipoxygenase
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MDPI and ACS Style

Friend, L.N.; Williamson, R.C.; Merrill, C.B.; Newton, S.T.; Christensen, M.T.; Petersen, J.; Wu, B.; Ostlund, I.; Edwards, J.G. Hippocampal Stratum Oriens Somatostatin-Positive Cells Undergo CB1-Dependent Long-Term Potentiation and Express Endocannabinoid Biosynthetic Enzymes. Molecules 2019, 24, 1306. https://doi.org/10.3390/molecules24071306

AMA Style

Friend LN, Williamson RC, Merrill CB, Newton ST, Christensen MT, Petersen J, Wu B, Ostlund I, Edwards JG. Hippocampal Stratum Oriens Somatostatin-Positive Cells Undergo CB1-Dependent Long-Term Potentiation and Express Endocannabinoid Biosynthetic Enzymes. Molecules. 2019; 24(7):1306. https://doi.org/10.3390/molecules24071306

Chicago/Turabian Style

Friend, Lindsey N.; Williamson, Ryan C.; Merrill, Collin B.; Newton, Scott T.; Christensen, Michael T.; Petersen, Jake; Wu, Bridget; Ostlund, Isaac; Edwards, Jeffrey G. 2019. "Hippocampal Stratum Oriens Somatostatin-Positive Cells Undergo CB1-Dependent Long-Term Potentiation and Express Endocannabinoid Biosynthetic Enzymes" Molecules 24, no. 7: 1306. https://doi.org/10.3390/molecules24071306

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