Impact of commitment on performance evaluation in the rostral cingulate motor area

Abstract

Performance evaluation is a prerequisite for behavioral adaptation. Although the anterior cingulate cortex (ACC) is thought to play a central role in error detection, little is known about the electrophysiological activity of this structure during the performance-monitoring process. We directly addressed this issue by training monkeys to perform a Stroop-like task and then recorded neuronal activity in the rostral cingulate motor area (CMAr), a relatively unexplored region of the ACC known to be involved in motor processing. We found that most CMAr neurons responded during the evaluation period to both positive and negative feedback, but neuronal changes were more important after an error than after a successful trial. Interestingly, this performance-monitoring activity was not directly modulated by the degree of difficulty of the cognitive situation because changes in discharge frequency were similar whatever the level of attentional control imposed on the monkey. Firing activity during the evaluation period increased more, however, in erroneously completed than in incompleted trials and when the reward was delivered in an active rather than passive context, indicating that performance evaluation was conditioned by the degree of commitment of the animal to the task. It would thus seem that CMAr neurons could constitute a system for the evaluation of behavioral performance contingent on the subject's commitment to the task.

Figure 1.

Composition of our Stroop-like task. A, Monkeys were taught to associate each fruit shape with its normal color. B, Shapes and colors were then assembled to form different cognitive situations, of three different levels of difficulty.

Figure 2.

Description of the trial. A, Timescale: (1) a 3 s rest period, (2) presentation of a 500 ms warning stimulus, (3) waiting period of 500 to 1000 ms, (4) presentation of the Stroop-like task with maximum 4 s response period, and (5) 1–1.5 s after completion of response movement, either delivery of reward (after correct response) or negative feedback (after errors of type 1–4; type 5 errors were too rare to allow statistical analysis). B, Timelines of the different stages of the trial.

Figure 3.

Location of single neuron recording sites. Regions of the upper and lower banks of the cingulate sulcus (CgS) sampled. Individual electrode paths are indicated by red lines in a coronal histological section taken at level A28. Inset is a mediosagittal MRI scan showing recorded regions (in red).

Figure 4.

Mean behavioral performance for trials (correct responses or errors of type 4) during which there was significant neuronal activity during the evaluation period (n = 92). Mean reaction time increased with the level of difficulty, confirming that behavioral cost is a function of the level of cognitive control. Error rate (bars) increased significantly as the level of cognitive difficulty augmented.

Figure 5.

Typical examples of the mean activation of an individual CMAr neuron responding only to positive or only to negative feedback. A. Activation of a group 1 neuron that responded only to positive feedback (in red; n = 72) and not to negative (in black; n = 12). B, Activation of a group 2 neuron that responded only to negative (in black; n = 65) and not to positive (in red; n = 111) feedback.

Figure 6.

Neurons that responded to both positive and negative feedback (group 3) presented a more important activation after negative than after positive feedback. Example of an individual group 3 neuron. Firing rate increased more after negative (in black; n = 43) than after positive (in red; n = 104) feedback.

Figure 7.

Activity of a typical CMAr neuron during the evaluation period in the three cognitive situations. Raster display showing firing frequency after positive (top left) and after negative (top right) feedback. Response profiles (after positive feedback, bottom left; after negative feedback, bottom right) were similar, whatever the cognitive situation.

Figure 8.

CMAr neuronal activation during the evaluation period was contingent on animal's commitment to the task. A, Top represents raster display and frequency histogram comparing firing activity of an individual neuron during the initial 3 s rest period and during the evaluation period after positive feedback pooled for both correct response and out of the task reward. Bottom represents in two separate curves the mean activity for correct response and out of the task reward. B, Top represents raster display and histogram comparing firing activity of an individual neuron during the initial 3 s rest period and during the evaluation period after the negative feedback engendered by the pooled four types of error analyzed. Bottom represents in four separate curves the mean activity of each of the four error types. C, White bars, Mean firing activity during the evaluation period of all neurons that responded to positive feedback. Activation was more important after positive feedback (reward delivery) consecutive to a correct execution of the SLT than after a reward delivered out of the task context. Black bars, Mean firing activity during the evaluation period of all neurons that responded to negative feedback, according to error type. The degree of activation during the evaluation period after negative feedback varied according to the type of error. The greater the degree of commitment of the animal to the task, the more important the activation.