Bilateral Orbital Prefrontal Cortex Lesions in Rhesus Monkeys Disrupt Choices Guided by Both Reward Value and Reward Contingency

Abstract

The orbital prefrontal cortex (PFo) operates as part of a network involved in reward-based learning and goal-directed behavior. To test whether the PFo is necessary for guiding behavior based on the value of expected reward outcomes, we compared four rhesus monkeys with two-stage bilateral PFo removals and six unoperated controls for their responses to reinforcer devaluation, a task that assesses the monkeys' abilities to alter choices of objects when the value of the underlying food has changed. For comparison, the same monkeys were tested on a standard test of flexible stimulus-reward learning, namely object reversal learning. Relative to controls, monkeys with bilateral PFo removals showed a significant attenuation of reinforcer devaluation effects on each of two separate assessments, one performed shortly after surgery and the other ϳ19 months after surgery; the operated monkeys were also impaired on object reversal learning. The same monkeys, however, were unimpaired in acquisition of object discrimination learning problems and responded like controls when allowed to choose foods alone, either on a food preference test among six different foods or after selective satiation. Thus, satiety mechanisms and the ability to assign value to familiar foods appear to be intact in monkeys with PFo lesions. The pattern of results suggests that the PFo is critical for response selection based on predicted reward outcomes, regardless of whether the value of the outcome is predicted by affective signals (reinforcer devaluation) or by visual signals conveying reward contingency (object reversal learning).

A comparison of discrimination and reversal learning for olfactory and visual stimuli in aged rats.

“…Lesions or temporary inactivations of the rodent prelimbic area do not impair reversal learning of a two-choice discrimination (Birrell & Brown, 2000;Boulougouris, Dalley, & Robbins, 2007;Ragozzino, Detrick, & Kesner, 1999;Ragozzino, Kim, Hassert, Minniti, & Kiang, 2003). However, lesions or pharmacological manipulations of the orbitofrontal region impair reversal learning for olfactory, tactile, or visual cues (Bohn, Giertler, & Hauber, 2003;Boulougouris et al, 2007;Chudasama & Robbins, 2003;Ferry, Lu, & Price, 2000;Izquierdo, Suda, & Murray, 2004;Kim & Ragozzino, 2005;McAlonan & Brown, 2003;Meunier, Bachevalier, & Mishkin, 1997;Rolls, Hornak, Wade, & McGrath, 1994;Schoenbaum et al, 2002aSchoenbaum et al, , 2002b. The orbitofrontal cortex may support reversal learning by governing goal-directed behavior or behavior guided by incentive values associated with a stimulus (Saddoris, Gallagher, & Schoenbaum, 2005;Schoenbaum & Roesch, 2005;Schoenbaum & Setlow, 2001;Schoenbaum, Setlow, Nugent, Saddoris, & Gallagher, 2003a;Schoenbaum, Setlow, & Ramus, 2003b;Schoenbaum, Setlow, Saddoris, & Gallagher, 2003c).…”

Anatomy of a decision: Striato-orbitofrontal interactions in reinforcement learning, decision making, and reversal.

“…First, rats and monkeys with OFC lesions are not sensitive to devaluation (Gallagher, McMahan, & Schoenbaum, 1999;Izquierdo, Suda, & Murray, 2004;Pickens, Saddoris, Gallagher, & Holland, 2005). In contrast, rats with dorsolateral striatal lesions are more sensitive than control rats (Yin, Knowlton, & Balleine, 2004).…”

Affective neuroscience of pleasure: reward in humans and animals

“…Although apathy and lack of affect is sometimes reported after to the dorsomedial prefrontal cortex, the nearly opposite symptoms of euphoria, impulsiveness, and general emotional disinhibition may be reported after damage to the ventromedial prefrontal and orbitofrontal cortex (Tucker et al 1995). Similarly, monkeys or rats with damage to orbitofrontal cortex (OFC) still respond robustly for rewards but are disrupted in subtle ways on the cognitive use of reward information to guide behavioral decisions (Burke et al 2008;Izquierdo et al 2004;Pears et al 2003;Pickens et al 2003;Rudebeck et al 2006;Schoenbaum et al 2006;Wallis 2007). As Schoenbaum and Shaham concluded, "the OFC does not appear to play an important role in the acute rewarding effect of cocaine or in relapse induced by acute exposure to the drug.…”