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

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.

Neural Mechanisms of Feeding Behavior and Its Disorders

“…After training, it was observed that rats in the glucose group were more vigorous in licking the spout in the absence of intragastric infusion. The inter-spike interval variability of MSNs, which reflects dopamine release in the striatum, was higher in the glucose group than in the water group [23]. These findings suggest that dopamine release in the nucleus accumbens plays a crucial role in motivation.…”

“…A positive correlation between reward-seeking behavior and dopamine levels was also reported [21]. Another study analyzed the activity of medium spiny neurons (MSNs), the major output neurons in the nucleus accumbens that receive dopaminergic projections [22] in the rat nucleus accumbens [23]. In this study, water-deprived rats were trained with an operant conditioning task in which the licking of a spout was associated with intragastric glucose (glucose group) or water (water group) infusion.…”

Neural Representation of Overlapping Path Segments and Reward Acquisitions in the Monkey Hippocampus

“…The data were then transferred to the analysis software NeuroExplorer (Nex Technologies, Littleton, MA, United States). Recorded waveforms were projected to a principal component subspace using NDManager (Hazan et al, 2006) 1 and semi-automatically sorted into single units using KlustaKwik (Harris et al, 2000) 2 and Kluster (Hazan et al, 2006; see text footnote 1) as outlined by previous studies (e.g., Maingret et al, 2016; Patrono et al, 2017). Each cluster of neuronal spikes was then assessed manually to ensure that the cluster boundaries were well separated and that the waveform shapes were consistent with action potentials.…”

Schizophrenia, the gut microbiota, and new opportunities from optogenetic manipulations of the gut-brain axis

“…Over the past few years, the neuroscience field has started to pay more attention to how the central nervous system (CNS) connects with other physiological systems such as the enteric nervous system (ENS) and the neuroendocrine system (NES) [ 80 ]. Some have reviewed papers taken advantage of suggestive preclinical studies enlightening the pivotal role of the gut microbiota in a wide range of CNS pathologies, from mood disorders to Alzheimer's disease, from addiction to SCZ [ 19 , 27 , 81 ]. Here, we evaluate the current research lines investigating interconnections between the gut microbiota and SCZ, especially concerning how an altered microbiota may cause cognitive alterations inducing schizophrenia-like symptoms.…”

“…Recent findings highlighting the role of a gut-brain axis have shown that the gut microbiota plays a crucial role in many psychopathologies. For instance, depression and anxiety [ 25 ]; addiction [ 26 ]; eating disorders [ 27 ]; neurodegenerative disorders such as Alzheimer’s disease (AD) [ 28 ]; psychiatric disorders such as SCZ and autism [ 22 , 29 – 31 ] can involve changes in the gut-brain axis. In humans, the gut microbiota has many more bacteria and other organisms than other body areas [ 32 ].…”