Rewarding Effects of Operant Dry-Licking Behavior on Neuronal Firing in the Nucleus Accumbens Core.

Taketoshi Ono,Ikhruud C Chinzorig,Hiroshi Nishimaru,Yusaku Takamura,Enrico Patrono,Jumpei Matsumoto,Hisao Nishijo

doi:10.3389/fphar.2017.00536

Abstract

Certain eating behaviors are characterized by a trend of elevated food consumption. However, neural mechanisms mediating the motivation for food consumption are not fully understood. Food impacts the brain-rewarding-system via both oral-sensory and post-ingestive information. Recent studies have reported an important role of visceral gut information in mediating dopamine (DA) release in the brain rewarding system. This is independent of oral sensation, suggesting a role of the gut-brain-DA-axis in feeding behavior. In this study, we investigated the effects of intra-gastric (IG) self-administration of glucose on neuronal firings in the nucleus accumbens (NA) of water-deprived rats. Rats were trained in an operant-licking paradigm. During training, when the light was on for 2 min (light-period), rats were required to lick a spout to acquire the water oral-intake learning, and either an IG self-infusion of 0.4 M glucose (GLU group) or water (H2O group). Rats rested in the dark-period (3 min) following the light-period. Four cycles of the operant-licking paradigm consisting of the light–dark periods were performed per day, for 4 consecutive days. In the test session, the same rats licked the same spout to acquire the IG self-administration of the corresponding solutions, without oral water ingestion (dry licking). Behavioral results indicated IG self-administration of glucose elicits more dry-licking behavior than that of water. Neurophysiological results indicated in the dark period, coefficient of variance (CV) measuring the inter-spike interval variability of putative medial spiny neurons (pMSNs) in the NA was reduced in the H2O group compared to the GLU group, while there was no significant difference in physical behaviors in the dark period between the two groups. Since previous studies reported that DA release increases CV of MSNs, the present results suggest that greater CV of pMSNs in the GLU group reflects greater DA release in the NA and elevated motivation in the GLU group, which might increase lickings in the test session in the GLU group compared to the H2O group.

Highlights

Eating behaviors are occasionally characterized by a trend of elevated food consumption
These results indicate that the firing variability of putative medial spiny neurons (pMSNs) in the dark period was maintained in the test session without oral water intake in the GLU group, while the firing variability of pMSNs was reduced in the test session in the H2O group
Post hoc analysis revealed that coefficient of variance (CV) during test session in the H2O group was significantly smaller than the CV during the training session in the same group (p = 0.020, simple main effect test) and the CV during test in the GLU group (p = 0.0024, simple main effect test)

Summary

Introduction

Eating behaviors are occasionally characterized by a trend of elevated food consumption. Studies have shown that a low availability of dopamine D2 receptors (DA D2Rs) in the nucleus accumbens (NA) is a genetic risk factor for chocolate compulsive-seeking behavior, which is mediated by stressful environments (Hoebel et al, 2009; Campbell et al, 2010; Kenny, 2011; Di Segni et al, 2014) This supports the idea that a complex gene–environment interaction plays a key role in the development of maladaptive compulsive eating behavior (Campbell et al, 2010; Patrono et al, 2015). A functional magnetic resonance imaging (fMRI) study using rats reported that IG infusion of glucose activated the NA in less than 10 min (Tsurugizawa and Uneyama, 2014) This suggests a potential role for autonomic afferents innervating the hepato-portal system, in peripheral-glucose-sensing and communication with brainreward-circuits (Delaere et al, 2013). Nutrient-related DA efflux is induced directly by gastrointestinal tract stimulation, suggesting a gutbrain-DA-axis involved in feeding behavior (de Araujo et al, 2012)

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