Finding the balance between model complexity and performance: Using ventral striatal oscillations to classify feeding behavior in rats

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.

[1]  R. Christopher Pierce,et al.  Deep brain stimulation for the treatment of addiction: basic and clinical studies and potential mechanisms of action , 2013, Psychopharmacology.

[2]  Matthijs A. A. van der Meer,et al.  Gamma Oscillations in the Rat Ventral Striatum Originate in the Piriform Cortex , 2017, The Journal of Neuroscience.

[3]  Stanislas Dehaene,et al.  Cortical activity is more stable when sensory stimuli are consciously perceived , 2015, Proceedings of the National Academy of Sciences.

[4]  M. Fox,et al.  Connectivity Predicts deep brain stimulation outcome in Parkinson disease , 2017, Annals of neurology.

[5]  A. Green,et al.  Machine Learning Based Classification of Deep Brain Stimulation Outcomes in a Rat Model of Binge Eating Using Ventral Striatal Oscillations , 2018, bioRxiv.

[6]  C. Kornetsky,et al.  Deep brain stimulation of the nucleus accumbens reduces ethanol consumption in rats , 2009, Pharmacology Biochemistry and Behavior.

[7]  Reuben R. Shamir,et al.  Machine Learning Approach to Optimizing Combined Stimulation and Medication Therapies for Parkinson's Disease , 2015, Brain Stimulation.

[8]  K. Berridge,et al.  The tempted brain eats: Pleasure and desire circuits in obesity and eating disorders , 2010, Brain Research.

[9]  K. Deisseroth,et al.  Gamma oscillations organize top-down signalling to hypothalamus and enable food seeking , 2017, Nature.

[10]  Jonathan D. Cohen,et al.  Reproducibility Distinguishes Conscious from Nonconscious Neural Representations , 2010, Science.

[11]  A. Graybiel,et al.  Habit learning is associated with major shifts in frequencies of oscillatory activity and synchronized spike firing in striatum , 2011, Proceedings of the National Academy of Sciences.

[12]  R. Corwin,et al.  Behavioral models of binge-type eating , 2004, Physiology & Behavior.

[13]  Nitzan Censor,et al.  Neural Variability Quenching Predicts Individual Perceptual Abilities , 2017, The Journal of Neuroscience.

[14]  Alberto J Espay,et al.  Computer‐Guided Deep Brain Stimulation Programming for Parkinson's Disease , 2016, Neuromodulation : journal of the International Neuromodulation Society.

[15]  K. Berridge,et al.  Lateral hypothalamus, nucleus accumbens, and ventral pallidum roles in eating and hunger: interactions between homeostatic and reward circuitry , 2015, Front. Syst. Neurosci..

[16]  Edward H. Nieh,et al.  Homeostasis Meets Motivation in the Battle to Control Food Intake , 2016, The Journal of Neuroscience.

[17]  N. Volkow,et al.  Food and drug reward: overlapping circuits in human obesity and addiction. , 2012, Current topics in behavioral neurosciences.

[18]  Sidney A. Simon,et al.  Food Reward in the Absence of Taste Receptor Signaling , 2008, Neuron.

[19]  Simone Ferrari-Toniolo,et al.  Modulation of Neural Variability in Premotor, Motor, and Posterior Parietal Cortex during Change of Motor Intention , 2016, The Journal of Neuroscience.

[20]  Matthijs A. A. van der Meer,et al.  Frontiers in Integrative Neuroscience Integrative Neuroscience Low and High Gamma Oscillations in Rat Ventral Striatum Have Distinct Relationships to Behavior, Reward, and Spiking Activity on a Learned Spatial Decision Task , 2022 .

[21]  Fair M. Vassoler,et al.  Deep Brain Stimulation of the Nucleus Accumbens Shell Attenuates Cocaine Priming-Induced Reinstatement of Drug Seeking in Rats , 2008, The Journal of Neuroscience.

[22]  H. Schmidt,et al.  GLP-1 influences food and drug reward , 2016, Current Opinion in Behavioral Sciences.

[23]  Byron M. Yu,et al.  Neural Variability in Premotor Cortex Provides a Signature of Motor Preparation , 2006, The Journal of Neuroscience.

[24]  M. Morrell Responsive cortical stimulation for the treatment of medically intractable partial epilepsy , 2011, Neurology.

[25]  Trevor Hastie,et al.  Regularization Paths for Generalized Linear Models via Coordinate Descent. , 2010, Journal of statistical software.

[26]  Hoon-Ki Min,et al.  A neurochemical closed-loop controller for deep brain stimulation: toward individualized smart neuromodulation therapies , 2014, Front. Neurosci..

[27]  Richard Coppola,et al.  Reduced Variability of Ongoing and Evoked Cortical Activity Leads to Improved Behavioral Performance , 2012, PloS one.

[28]  M. Morris,et al.  The role of reward circuitry and food addiction in the obesity epidemic: An update , 2018, Biological Psychology.

[29]  Alexander W. Johnson,et al.  The antagonism of ghrelin alters the appetitive response to learned cues associated with food , 2016, Behavioural Brain Research.

[30]  P. Chandler-Laney,et al.  High intake of palatable food predicts binge-eating independent of susceptibility to obesity: an animal model of lean vs obese binge-eating and obesity with and without binge-eating , 2007, International Journal of Obesity.

[31]  Arshad M. Khan,et al.  Direct hypothalamic and indirect trans-pallidal, trans-thalamic, or trans-septal control of accumbens signaling and their roles in food intake , 2015, Front. Syst. Neurosci..

[32]  K. Berridge,et al.  Opioid site in nucleus accumbens shell mediates eating and hedonic ‘liking’ for food: map based on microinjection Fos plumes , 2000, Brain Research.

[33]  Adriano B. L. Tort,et al.  Theta–gamma coupling increases during the learning of item–context associations , 2009, Proceedings of the National Academy of Sciences.

[34]  Martin A. Riedmiller,et al.  Autonomous Optimization of Targeted Stimulation of Neuronal Networks , 2016, PLoS Comput. Biol..

[35]  Paul Witkovsky,et al.  Insulin enhances striatal dopamine release by activating cholinergic interneurons and thereby signals reward , 2015, Nature Communications.

[36]  R. Malenka,et al.  Closing the loop on impulsivity via nucleus accumbens delta-band activity in mice and man , 2017, Proceedings of the National Academy of Sciences.

[37]  B. Hoebel,et al.  Bingeing, Self‐restriction, and Increased Body Weight in Rats With Limited Access to a Sweet‐fat Diet , 2008, Obesity.

[38]  A. Green,et al.  Nucleus accumbens deep brain stimulation in a rat model of binge eating , 2015, Translational Psychiatry.

[39]  Karl A. Sillay,et al.  Obesity and deep brain stimulation: an overview , 2015, Annals of neurosciences.

[40]  Andrew M. Clark,et al.  Stimulus onset quenches neural variability: a widespread cortical phenomenon , 2010, Nature Neuroscience.

[41]  P. Brown,et al.  Adaptive Deep Brain Stimulation In Advanced Parkinson Disease , 2013, Annals of neurology.

[42]  M. Gnegy,et al.  Leptin promotes dopamine transporter and tyrosine hydroxylase activity in the nucleus accumbens of Sprague‐Dawley rats , 2010, Journal of neurochemistry.

[43]  H. Berthoud,et al.  Reversible suppression of food reward behavior by chronic mu-opioid receptor antagonism in the nucleus accumbens , 2010, Neuroscience.

[44]  Hans-Jochen Heinze,et al.  Deep brain stimulation of the nucleus accumbens for the treatment of addiction , 2013, Annals of the New York Academy of Sciences.

[45]  Ying Liu,et al.  High frequency deep brain stimulation: What are the therapeutic mechanisms? , 2008, Neuroscience & Biobehavioral Reviews.

[46]  S. Haber,et al.  Closed-Loop Deep Brain Stimulation Is Superior in Ameliorating Parkinsonism , 2011, Neuron.

[47]  R. Corwin Binge-type eating induced by limited access in rats does not require energy restriction on the previous day , 2004, Appetite.