Abstract

The ventral striatum (VS) is a central node within a distributed network that controls appetitive behavior, and neuromodulation of the VS has demonstrated therapeutic potential for appetitive disorders. Local field potential (LFP) oscillations recorded from deep brain stimulation (DBS) electrodes within the VS are a pragmatic source of neural systems-level information about appetitive behavior that could be used in responsive neuromodulation systems. Here, we recorded LFPs from the bilateral nucleus accumbens core and shell (subregions of the VS) during limited access to palatable food across varying conditions of hunger and food palatability in male rats. We used standard statistical methods (logistic regression) as well as the machine learning algorithm lasso to predict aspects of feeding behavior using VS LFPs. We were able to predict the amount of food eaten, the increase in consumption following food deprivation, and the type of food eaten. Further, we were able to predict whether the initiation of feeding was imminent up to 42.5 seconds before feeding began and classify current behavior as either feeding or not-feeding. In classifying feeding behavior, we found an optimal balance between model complexity and performance with models using 3 LFP features primarily from the alpha and high gamma frequencies. As shown here, unbiased methods can identify systems-level neural activity linked to domains of mental illness with potential application to the development and personalization of novel treatments.

Highlights

  • The ventral striatum (VS) is a central node in the brain circuits influencing goal-directed and habitual behaviors with subregions like the nucleus accumbens (NAc) core and shell that mediate information between cognitive control regions of the prefrontal cortex and regions of learning and memory in the amygdala, hippocampus, and the ventral tegmental area [1,2,3]

  • Animals were deprived of food for 24 hours before recording a 2-hour house chow session (Chow) to ensure that the animals consumed enough food to provide a comparable amount of Local field potential (LFP) data during feeding to the three sessions with access to the high-fat/highsugar diet (See General methods: Surgery and binge eating)

  • There was a bimodal pattern of feeding behavior during the baseline conditions that was not maintained across the food deprived conditions (Fig 1A) in which more animals were feeding during the beginning of the recording

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Summary

Introduction

The VS is a central node in the brain circuits influencing goal-directed and habitual behaviors with subregions like the nucleus accumbens (NAc) core and shell that mediate information between cognitive control regions of the prefrontal cortex and regions of learning and memory in the amygdala, hippocampus, and the ventral tegmental area [1,2,3]. Targeting the VS for eating disorders and obesity is supported by the known connectivity of the NAc with energy homeostasis circuits within the hypothalamus and brain stem [7,8] and the role of an-/orexigenic states modulating VS activity through central and peripheral ligands [9,10,11,12] In both preclinical and clinical investigations DBS targeting these subregions has altered appetitive behavior [13,14,15,16], but variable treatment outcomes combined with the known risks of DBS have limited more widespread use. A source of neural activity that contains information relevant to appetitive behaviors is needed to apply these advanced DBS approaches to appetitive disorders

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