Abstract
Anandamide (AEA) and N-oleoylethanolamine (OEA) are produced in the intestine and brain during fasting and satiety, respectively. Subsequently, AEA facilitates food intake via activation of cannabinoid type-1 receptors (CB1Rs) while OEA decreases food intake via activation of peroxisome proliferator-activated receptor-α (PPARα) and/or G-protein-coupled receptor 119 (GPR119). Neuronal activity in the gastrointestinal region of the autonomic insula (GI-Au-I) that rostrally adjoins the gustatory insula (Gu-I) increases during fasting, enhancing appetite while umami and sweet taste sensations in Gu-I enhances appetite in GI-Au-I, strongly suggesting the presence of a neural interaction between the Gu-I and GI-Au-I which changes depending on the concentrations of AEA and OEA. However, this possibility has never been investigated. In rat slice preparations, we demonstrate with voltage-sensitive dye imaging that activation of CB1Rs by AEA induces θ-rhythm oscillatory synchronization in the Gu-I which propagates into the GI-Au-I but stops at its caudal end, displaying an oscillatory coordination. The AEA-induced oscillation was abolished by a CB1R antagonist or OEA through activation of GPR119. Our results demonstrate that the neural coordination between the Gu-I and GI-Au-I is generated or suppressed by the opposing activities between CB1R and GPR119. This mechanism may be involved in the feeding behavior based on taste recognition.
Highlights
The concentration of anandamide (AEA) and that of N-oleoylethanolamine (OEA) in the small intestine rises and falls, respectively, during fasting and vice versa upon refeeding[1,2]
The line profile clearly showed that the excitatory response emerged periodically at 5 Hz at ROIs1–2 (Gu-I), each of which propagated along L3 caudally into ROIs4–5 (GI-Au-I) through ROI3 with a progressive delay, and stopped around the caudal end of gastrointestinal autonomic insula (GI-Au-I) but did not invade into the cardiovascular region of autonomic insula (CV-Au-I) including ROI6 (Fig. 1d)
The power spectral analysis of optical responses at ROI2 and ROI4 revealed that the geometric mean (GM)-F5-normalized power densities (NPDs) and GM-F10-NPDs obtained following application of AEA were significantly (†p < 0.01, †p < 0.01, respectively) decreased by addition of AM251 (Fig. 4d,e, n = 5) and OEA (Fig. 4i,j, n = 5), and thereafter significantly (†p < 0.01, †p < 0.01, respectively) increased following washout of AM251 (Fig. 4d,e, n = 5) or OEA (Fig. 4i,j, n = 5). These results suggest that the oscillation in the gustatory insula (Gu-I) was induced through activation of the cannabinoid type 1 receptors (CB1Rs) while it was abolished through activation of either the G-protein-coupled receptor 119 (GPR119) or PPARα.Subsequently, the AEA-induced oscillatory coordination between the Gu-I and granular insula (GI)-Au-I was abolished by AM251 or OEA as reflected in significant decreases in the coherence of F5 component between ROI2 and ROI4 from 0.989 ± 0.007 to 0.456 ± 0.427 following application of AM251 (**p < 0.05; n = 5) and from 0.999 ± 0.001 to 0.549 ± 0.100 following application of OEA (**p < 0.01; n = 5)
Summary
The concentration of anandamide (AEA) and that of N-oleoylethanolamine (OEA) in the small intestine rises and falls, respectively, during fasting and vice versa upon refeeding[1,2]. The neuronal activity in the GI-Au-I increases in the hunger state[8], enhancing appetite while it decreases in response to feeding[9]. Neuronal activity induced in the Gu-I in response to tastant stimulation increases during fasting[10] or decreases during satiety[11]. The enhancement of appetite would be brought about by the modulation of the neural activity in the GI-Au-I through the recognition of umami or sweet taste in the Gu-I, suggesting the presence of a neural interaction between the Gu-I and GI-Au-I that changes www.nature.com/scientificreports/. (c) Sample pseudocolor images of optical responses following AEA application. The AEA-induced oscillation was abolished by a CB1R antagonist and OEA. A GPR119 agonist but not a PPARαagonist abolished the AEA-induced oscillation, and a GPR119 antagonist but not a PPARαantagonist blocked the inhibitory effects of OEA. The θ-rhythm neural coordination between the Gu-I and GI-Au-I modulated by the opposing activities between the CB1R and GPR119 may mediate the neural activities in the Gu-I and GI-Au-I during satiety or hunger
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