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 approximately 19 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).

Figure 1.

Top, Ventral view of a standard rhesus monkey brain showing the location and extent of the PFo lesion for monkey PFo-1 (left; shaded region) and the extent of the intended PFo lesion (right; shaded region). Bottom, Representative T1-weighted MR images from PFo-1 (left) and coronal sections at matching levels from a standard rhesus monkey brain (right) showing the extent of the intended removal. The numerals indicate the distance in millimeters from the interaural plane (0).

Figure 2.

Photomicrographs of Nissl-stained coronal sections through the lesion in PFo-3. The black arrows mark the boundaries of the bilateral PFo lesion. Top to bottom, The levels shown are approximately +36, +32, and +28 mm anterior to the interaural plane (0). Compare and contrast with Figure 1.

Figure 3.

Difference scores of monkeys with PFo lesions (filled symbols) relative to unoperated controls (open symbols). The higher the bar, the greater the response to changes in reinforcer value (solid bars, test 1; hatched bars, test 2). The symbols represent scores for individual monkeys: filled diamond, PFo-1; filled square, PFo-2; filled circle, PFo-3; filled triangle, PFo-4; open circle, Con-1; open right-angled triangle, Con-2; open square, Con-3; open equilateral triangle, Con-4; open plus sign, Con-5; open diamond, Con-6.

Figure 4.

Mean difference scores of monkeys with bilateral PFo lesions (shaded bars) and unoperated controls (open bars) on two tests of re inforcer devaluation: a test administered with objects overlying food rewards (test 3) and a test with food rewards presented alone (test 4). Monkeys with bilateral PFo removals were only impaired when required to choose objects. The symbols represent scores for individual monkeys: filled diamond, PFo-1; filled square, PFo-2; filled circle, PFo-3; filled triangle, PFo-4; open circle, Con-1; open right-angled triangle, Con-2; open square, Con-3; open equilateral triangle, Con-4; open plus sign, Con-5; open diamond, Con-6.

Figure 5.

Group mean scores on the PR task. Baseline data are the mean number of responses emitted during 20 baseline sessions (solid bars) compared with the mean responses emitted during a single session after satiation (hatched bars). All monkeys decreased responding after the food reinforcer was devalued by selective satiation. The symbols represent scores for individual monkeys: filled diamond, PFo-1; filled square, PFo-2; filled circle, PFo-3; open circle, Con-1; open right-angled triangle, Con-2; open square, Con-3; open equilateral triangle, Con-4; open plus sign, Con-5; open diamond, Con-6.

Figure 6.

Group mean errors to criterion for initial learning (Initial) and nine serial reversals in object reversal learning. Filled diamonds, Monkeys with bilateral PFo lesions; open diamonds, unoperated controls. Error bars indicate ± SEM.