Ventrolateral prefrontal cortex is required for performance of a strategy implementation task but not reinforcer devaluation effects in rhesus monkeys

Abstract

The ability to apply behavioral strategies to obtain rewards efficiently and make choices based on changes in the value of rewards is fundamental to the adaptive control of behavior. The extent to which different regions of the prefrontal cortex are required for specific kinds of decisions is not well understood. We tested rhesus monkeys with bilateral ablations of the ventrolateral prefrontal cortex on tasks that required the use of behavioral strategies to optimize the rate with which rewards were accumulated, or to modify choice behavior in response to changes in the value of particular rewards. Monkeys with ventrolateral prefrontal lesions were impaired in performing the strategy-based task, but not on value-based decision-making. In contrast, orbital prefrontal ablations produced the opposite impairments in the same tasks. These findings support the conclusion that independent neural systems within the prefrontal cortex are necessary for control of choice behavior based on strategies or on stimulus value.

Fig. 1

Lesions of VLPFC in cases VL1–VL4. The intended lesion is shown in red on coronal sections of a normal rhesus monkey in the leftmost column, at five stereotaxic levels through the prefrontal cortex, moving from rostral to caudal from the top to the bottom of the figure. Photomicrographs of brain sections from cases VL1–VL4 at corresponding stereotaxic levels are shown in the other columns.

Fig. 2

The extent of VLPFC damage is shown on coronal sections from a standard rhesus monkey brain atlas (Szwarcbart, 2005) at five stereotaxic levels through the frontal lobes (numerals represent mm anterior to the interaural plane) for cases VL1–VL4. Areas of lesion overlap are illustrated in shades of gray, the darkest indicating damage present in all four cases, the lightest indicating damage present in only one of the four cases.

Fig. 3

Lesions of orbital prefrontal cortex in cases ORB1–ORB3. The intended lesion is shown in red on coronal sections of a normal rhesus monkey in the leftmost column, at four stereotaxic levels through the prefrontal cortex, moving from rostral to caudal from the top to the bottom of the figure. These correspond to the approximate stereotaxic levels illustrated in Fig. 1 for the cases with VLPFC lesions. Photomicrographs of brain sections from cases ORB1–ORB3 at corresponding stereotaxic levels are shown in the other columns.

Fig. 4

The extent of orbital prefrontal cortex damage is shown on coronal sections from a standard rhesus monkey brain atlas (Szwarcbart, 2005) at four stereotaxic levels through the frontal lobes (numerals represent mm anterior to the interaural plane). Areas of lesion overlap are illustrated in shades of gray, the darkest indicating damage present in all three cases, the lightest indicating damage present in only one of the three cases.

Fig. 5

VLPFC lesions impair strategy implementation performance. The critical measure of strategy implementation performance (trials/reward ratio) is illustrated; a ratio of 2.5 represents perfect performance, and higher ratios reflect progressively worse performance. Open bars represent mean preoperative performance, gray bars represent mean postoperative performance, and the labels CON1–CON5, ORB1–ORB3 and VL1–VL4 represent scores of individual monkeys.

Fig. 6

Probability of a sporadic choice after one, two, three or four persistent choices in control, VLPFC and orbital groups. Preoperatively in all groups, and postoperatively in control monkeys and monkeys with orbital prefrontal lesions, the probability of a sporadic choice after one, two or three persistent choices is extremely low, and it is very high after four consecutive persistent choices. This is consistent with correct and efficient application of the behavioral strategies associated with the different categories of objects. Postoperatively in the VLPFC group, the probability of making an inappropriate sporadic response after fewer than four persistent responses is increased, but the probability of making an appropriate sporadic response after four persistent responses is reduced. Thus, they are impaired in the overall implementation of behavioral strategies, and are not simply more likely to commit an impulsive sporadic response overall. Error bars indicate mean ± SEM.

Fig. 7

Performance in the reinforcer devaluation task is unimpaired in monkeys with ventrolateral prefrontal lesions, but it is impaired in monkeys with bilateral ablation of the orbital prefrontal cortex with identical testing histories (Baxter et al., 2007) and tested in precisely the same procedures.