Orbital prefrontal cortex is required for object-in-place scene memory but not performance of a strategy implementation task

Abstract

The orbital prefrontal cortex is thought to be involved in behavioral flexibility in primates, and human neuroimaging studies have identified orbital prefrontal activation during episodic memory encoding. The goal of the present study was to ascertain whether deficits in strategy implementation and episodic memory that occur after ablation of the entire prefrontal cortex can be ascribed to damage to the orbital prefrontal cortex. Rhesus monkeys were preoperatively trained on two behavioral tasks, the performance of both of which is severely impaired by the disconnection of frontal cortex from inferotemporal cortex. In the strategy implementation task, monkeys were required to learn about two categories of objects, each associated with a different strategy that had to be performed to obtain food reward. The different strategies had to be applied flexibly to optimize the rate of reward delivery. In the scene memory task, monkeys learned 20 new object-in-place discrimination problems in each session. Monkeys were tested on both tasks before and after bilateral ablation of orbital prefrontal cortex. These lesions impaired new scene learning but had no effect on strategy implementation. This finding supports a role for the orbital prefrontal cortex in memory but places limits on the involvement of orbital prefrontal cortex in the representation and implementation of behavioral goals and strategies.

Figure 1.

Lesions of orbital prefrontal cortex. The first column shows the extent of intended damage (red) on sections from the brain of a monkey without damage to orbital prefrontal cortex. The three remaining columns show histological sections from each of the three cases with orbital prefrontal lesions. Each row represents one approximate stereotaxic level, in millimeters anterior to the interaural plane, from anterior to posterior.

Figure 2.

Individual subject performance in strategy implementation. Both control monkeys and monkeys with orbital prefrontal lesions perform comparably on preoperative and postoperative tests of strategy implementation performance.

Figure 3.

Performance on scene learning. Mean data for each group are shown in preoperative and postoperative performance, in errors per list of 20 scenes (on the vertical axis) on each of eight repetitions of each list of problems (horizontal axis). Performance is identical in control monkeys in preoperative and postoperative performance tests, but monkeys with orbital prefrontal lesions show a learning deficit postoperatively.

Figure 4.

Individual subject data in scene learning. The dependent measure is the mean percentage error on trials 2–8 of each list of new scenes (performance in trial 1 is at chance for each list, because it is the first time monkeys have encountered the scenes, and they must discover the rewarded object by trial and error). The four control monkeys show stable performance between preoperative and postoperative performance tests; each monkey with an orbital prefrontal lesion is impaired relative to its preoperative performance.

Figure 5.

Performance on scene learning divided by whether the initial response to each scene was correct (1C) or incorrect (1W). Monkeys make more errors throughout learning on 1W scenes compared with 1C scenes. Monkeys with orbital prefrontal lesions, importantly, make more errors on both 1C scenes and 1W scenes postoperatively (compare open symbols with shaded symbols). Thus, their impairment is not limited to problems in which they must adjust their responding after an error.