Monkey orbitofrontal cortex encodes response choices near feedback time

Abstract

The primate prefrontal cortex contributes to stimulus-guided behavior, but the functional specializations among its areas remain uncertain. To better understand such specializations, we contrasted neuronal activity in the dorsolateral prefrontal cortex (PFdl) and the orbital prefrontal cortex (PFo). The task required rhesus monkeys to use a visual cue to choose a saccade target. Some cues instructed the monkeys to repeat their most recent response; others instructed them to change it. Responses were followed by feedback: fluid reward if correct, visual feedback if incorrect. Previous studies, using different tasks, have reported that PFo neurons did not encode responses. We found PFo did encode responses in this task, but only near feedback time, after the response had been completed. PFdl differed from PFo in several respects. As reported previously, some PFdl neurons encoded responses from the previous trial and others encoded planned responses. PFo neurons did not have these properties. After feedback, PFdl encoded rewarded responses better than unrewarded ones and thus combined response and outcome information. PFo, in contrast, encoded the responses chosen, rewarded or not. These findings suggest that PFdl and PFo contribute differently to response knowledge, with PFo using an outcome-independent signal to monitor current responses at feedback time.

Figure 1.

Behavioral task, recording locations, and representative eye-position records. A, Sequence of task events. Each gray rectangle represents the video screen. A central white circle (the fixation point) and two white squares appeared on each trial. The dashed lines show the monkey's gaze angle and fixation target. Next, the cue appeared, followed by a delay period. Offset of the fixation point triggered a saccade (red arrow). Feedback was delivered after the saccade. Fix, Fixation period; ITI, intertrial interval. B, Cues and the response strategies each instructed. The vertical, gray bar and yellow square instructed the monkeys to stay with their previous response; the horizontal bar and purple square instructed a shift to the alternative response. C, Coronal section based on MRI. Angle of penetration (black lines) allowed sampling of neuronal activity in both PFdl (blue) and PFo (pink). LO, Lateral orbital; MO, medial orbital; P, principal sulcus. D, Coronal MRI from monkey 1, ∼35 mm rostral to the interaural plane. Arrow, Electrode location at the center of the recording chamber. Cg, Cingulate sulcus; L, monkey's left; R, monkey's right; otherwise as in C. E, Representative horizontal (x) and vertical (y) eye-position records, collected from monkey 1 while recording the activity illustrated in Figure 2B. In 96% of the trials, eye position was within ±1° of the fixation point when the cue appeared, and in 91% of the trials, it was within ±1° of the center of the target when reward was delivered. Background shading: feedback period.

Figure 2.

Two response-selective PFo neurons. A, Neuron from monkey 2. Activity aligned on reward (Rw), sorted chronologically from top to bottom, with saccade onset (sac) and the go cue indicated by marks on each raster line. Raster displays show spike times with spike-density averages above each display. Left and right responses shown separately. Correct trials only are shown. Background shading: feedback period. B, Neuron from monkey 1, in format of A. C, From the cell in B, for error trials, in format of A. Note that on error trials, feedback was visual, in contrast to reward feedback on correct trials. Trials are sorted by responses made (not by correct responses).

Figure 3.

A, Of task-related neurons (n = 393 and 278 for PFdl and PFo, respectively), percentage showing significant response-dependent activity. Dashed horizontal line: percentage expected by chance. B, Response-selectivity for all task-related neurons estimated as the difference in ROC values between observed and shuffled data. Error bars indicate SEM. Fb, Feedback period; Fix, the fixation period of the next trial.

Figure 4.

Response-selective activity in PFdl and PFo. A, Average population activity (shaded area = SEM), for PFdl neurons with significant response-selective activity during the feedback period (n = 144), computed separately for each neuron's preferred (black) and antipreferred (red) response. Dashed and solid vertical lines show the time of target acquisition (acq) and reward (rw), respectively. B, Population activity as in A, for PFo neurons (n = 79). C, Difference in activity between the preferred and antipreferred responses from A (brown) and B (green). D, Sliding ROC plots for PFdl neurons with response-selective feedback-period activity (as in A), with the area under the ROC curve color coded for each cell, ranked according to the mean ROC value during the feedback period. E, ROC values as in D, for PFo. F, Means, with SEM, for the data in D (brown) and E (green).