A Neural Mechanism of Cue-Outcome Expectancy Generated by the Interaction Between Orbitofrontal Cortex and Amygdala

Taste perception is important for animals to take adequate nutrients and avoid toxins for their survival. Appetitive and aversive behaviors are produced by value evaluation of taste and taste expectation caused by other sensations. The value evaluation, coupled with a cue presentation, produces outcome expectation and guides flexible behaviors when the environment is changed. Experimental studies demonstrated distinct functional roles of basolateral amygdala (ABL) and orbitofrontal cortex (OFC) in value evaluation and adaptive behavior. ABL is involved in generating a cue-outcome association, whereas OFC makes a contribution of generating a cue-triggered expectation to guide adaptive behavior. However, it remains unclear how ABL and OFC form their functional roles, with the learning of adaptive behavior. To address this issue, we focus on an odor discrimination task of rats and develop a computational model that consists of OFC and ABL, interacting with reward and decision systems. We present the neural mechanisms underlying the rapid formation of cue-outcome association in ABL and late behavioral adaptation mediated by OFC. Moreover, we offer 2 functions of cue-selective neurons in OFC: one is that the activation of cue-selective neurons transmits value information to decision area to guide behavior and another is that persistent activity of cue-selective neurons evokes a weak activity of taste-sensitive OFC neurons, leading to cue-outcome expectation. Our model further accounts for ABL and OFC responses caused by lesions of these areas. The results provide a computational framework of how ABL and OFC are functionally linked through their interactions with the reward and decision systems.