The Role of Orbitofrontal-Amygdala Interactions in Updating Action-Outcome Valuations in Macaques

Abstract

A previous study revealed that, although monkeys with bilateral lesions of either the orbitofrontal cortex (OFC) or the amygdala could learn an action-outcome task, they could not adapt their choices in response to devalued outcomes. Specifically, they could not adjust their choice between two actions after the value of the outcome associated with one of the actions had decreased. Here, we investigated whether OFC needs to interact functionally with the amygdala in mediating such choices. Rhesus monkeys were trained to make two mutually exclusive actions on a touch-sensitive screen: "tap" and "hold." Taps led to the availability of one kind of food outcome; holds produced a different food. On each trial, monkeys could choose either a tap or a hold to earn the corresponding food reward. After consuming one of the two foods to satiety, monkeys were then tested on their ability to adapt their choices in response to the updated relative valuation of the two predicted outcomes. Whereas intact (control) monkeys shifted their choices toward the action associated with the higher value (nonsated) food, monkeys with crossed surgical disconnection of the amygdala and OFC did not. These findings demonstrate that amygdala-OFC interactions are necessary for choices among actions based on the updated value of predicted outcomes and they also have a bearing on the idea that OFC specializes in stimulus- or object-based choices in contrast to action- or response-based choices.SIGNIFICANCE STATEMENT Dysfunctional interactions between orbitofrontal cortex (OFC) and the amygdala underlie several mental health disorders, often related to value-based decision making. Understanding the underlying neural circuitry may help to develop therapies for those suffering from mood and anxiety disorders and provide insight into addiction. Here, we investigated whether the amygdala must interact with OFC to make adaptive choices. Monkeys learned to perform two different actions, "tap" for one kind of food reward and "hold" for another, and then one of the two foods was devalued temporarily. Intact monkeys shifted their choice to whichever action produced the higher-value food; monkeys with crossed surgical disconnection of OFC and the amygdala did not. Therefore, OFC and the amygdala must interact functionally to mediate adaptive choices.

Keywords: action value; decision making; medial frontal cortex; orbital frontal cortex; reward value.

Figure 1.

Crossed surgical disconnection of the amygdala and OFC: cases 1 and 3. Intended lesion (gray-shaded region) are shown on standard sections of a rhesus monkey brain (left column), together with postoperative T2-weighted MR images from two monkeys with crossed lesions (central and right columns). The MR images are selected to match the anteroposterior levels shown for the intended lesion. The white areas are regions of hypersignal due to edema resulting from injection of excitotoxins and are taken as a reflection of the extent of the lesion. Numerals indicate distance in millimeters from the interaural plane (0). Compare and contrast line drawings of the intended lesion (left column) with MR sections of the cases illustrated (center and right columns).

Figure 2.

Crossed surgical disconnection of the amygdala and OFC: cases 2 and 4. Intended lesion (gray-shaded region) are shown on standard sections of a rhesus monkey brain (left column), together with postoperative T2-weighted MR images from two monkeys with crossed lesions (central and right columns). Conventions are as in Figure 1. Note that case 4 sustained inadvertent damage to parts of the caudate nucleus and putamen (black arrows), presumably as a result of infarction associated with the amygdala injections.

Figure 3.

Mean number of actions (±SEM) made under extinction conditions averaged across the four devaluation tests. There were 15 trials per session and, on each trial, there were two action options available to the monkey: a tap or hold associated with the devalued reward (devalued action) and a tap or hold associated with the nondevalued reward (nondevalued action). CON, Unoperated control monkeys. *Significant difference between the number of devalued and nondevalued actions performed during the devaluation tests. Horizontal lines show scores of individual monkeys.