Homeostatic Reinforcement Theory Accounts for Sodium Appetitive State- and Taste-Dependent Dopamine Responding

Abstract

Seeking and consuming nutrients is essential to survival and the maintenance of life. Dynamic and volatile environments require that animals learn complex behavioral strategies to obtain the necessary nutritive substances. While this has been classically viewed in terms of homeostatic regulation, recent theoretical work proposed that such strategies result from reinforcement learning processes. This theory proposed that phasic dopamine (DA) signals play a key role in signaling potentially need-fulfilling outcomes. To examine links between homeostatic and reinforcement learning processes, we focus on sodium appetite as sodium depletion triggers state- and taste-dependent changes in behavior and DA signaling evoked by sodium-related stimuli. We find that both the behavior and the dynamics of DA signaling underlying sodium appetite can be accounted for by a homeostatically regulated reinforcement learning framework (HRRL). We first optimized HRRL-based agents to sodium-seeking behavior measured in rodents. Agents successfully reproduced the state and the taste dependence of behavioral responding for sodium as well as for lithium and potassium salts. We then showed that these same agents account for the regulation of DA signals evoked by sodium tastants in a taste- and state-dependent manner. Our models quantitatively describe how DA signals evoked by sodium decrease with satiety and increase with deprivation. Lastly, our HRRL agents assigned equal preference for sodium versus the lithium containing salts, accounting for similar behavioral and neurophysiological observations in rodents. We propose that animals use orosensory signals as predictors of the internal impact of the consumed good and our results pose clear targets for future experiments. In sum, this work suggests that appetite-driven behavior may be driven by reinforcement learning mechanisms that are dynamically tuned by homeostatic need.

The Hunger for Salt: A Tribute to Derek Denton and Jay Schulkin with an Updated Collection of Papers on Salt Appetite

“…Additionally challenging the consensus, in ‘Homeostatic reinforcement theory accounts for sodium appetitive state- and taste-dependent dopamine responding’, Duriez, Bergero, Cone, Roitman, and Gutkin, in a carefully crafted hypothesis, deconstruct the mechanisms of homeostasis into remarkable hypotheses of adaptive learning to address the little-considered fundamental question of why salt is consumed beyond its necessity [ 6 ]. The authors use their model to reproduce behavioral data and the underlying brain dopamine signaling that plays a key role in signaling potentially need-fulfilling outcomes.…”