Neural Coding of Appetitive Food Experiences in the Amygdala

Abstract

Real-life experiences involve the consumption of various foods, yet it is unclear how the brain distinguishes and categorizes such food experiences. Despite the crucial roles of the basolateral amygdala (BLA) in appetitive behavior and emotion, how BLA pyramidal cells and interneurons encode food experiences has not yet been well characterized. Here we employ large-scale tetrode recording techniques to investigate the coding properties of pyramidal neurons vs. fast-spiking interneurons in the BLA as mice freely consumed a variety of foods, such as biscuits, rice, milk and water. We found that putative pyramidal cells conformed to the power-of-two-based permutation logic, as postulated by the Theory of Connectivity, to generate specific-to-general neural clique-coding patterns. Many pyramidal cells exhibited firing increases specific to a given food type, while some other pyramidal cells increased firings to various combinations of multiple foods. In contrast, fast-spiking interneurons can increase or decrease firings to given food types, and were more broadly tuned to various food experiences. We further show that a subset of pyramidal cells exhibited rapid desensitization to repeated eating of the same food, correlated with rapid behavioral habituation. Finally, we provide the intuitive visualization of BLA ensemble activation patterns using the dimensionality-reduction classification method to decode real-time appetitive stimulus identity on a moment-to-moment, single trial basis. Elucidation of the neural coding patterns in the BLA provides a key insight into how the brain's emotion and memory circuits performs the computational operation of pattern discrimination and categorization of natural food experiences.

Keywords: Amygdala; Cell assemblies; Emotion; Food experiences; Pattern-discrimination and categorization.