Coordination of high gamma activity in anterior cingulate and lateral prefrontal cortical areas during adaptation

Abstract

The anterior cingulate cortex (ACC) and the lateral prefrontal cortex (LPFC) process complementary information for planning and evaluating behavior. This suggests at least that processes in these two areas are coordinated during behavioral adaptation. We analyzed local field potentials recorded in both regions in two monkeys performing a problem-solving task that alternated exploration and repetitive behaviors with the specific prediction that neural activity should reveal interareal coordination mainly during exploration. Both areas showed increased high gamma power after errors in exploration and after rewards in exploitation. We found that high gamma (60-140 Hz) power increases in ACC were followed by a later increase in LPFC only after negative feedback (errors) or first positive feedback (correct) during the exploration period. The difference in latencies between the two structures disappeared in repetition period. Simultaneous recordings revealed correlations between high gamma power in the two areas around feedback; however, correlations were observed in both exploration and repetition. In contrast, postfeedback beta (10-20 Hz) power in ACC and LPFC correlated more frequently during repetition. Together, our data suggest that the coordination between ACC and LPFC activity is expressed during adaptive as well as stable behavioral periods but with different modes depending on the behavioral period.

Figure 1.

Behavioral task and recording sites. The animal has to search by trial and error for the correct target. A, Description of trial events. A trial starts with a touch on the lever and onset of central fixation spot. After a delay period with eye fixation on the central spot, all four targets switch on and the animal makes a saccade toward and touches one of them. All targets switch off, and the feedback is given (no reward: negative; reward: positive). The following trial starts after an intertrial interval (ITI). B, Example of successive problems. In the first problem, the monkey discovers the solution in two trials (search period). After discovery, the animal is allowed to repeat the response (repetition period) (INC, incorrect; CO1, first correct; COR, correct in repetition). A signal to change (SCS) indicates a new problem. C, Location of recording sites for the two monkeys M and P. The diagrams on the left represent the locations of penetrating sites to target LPFC (gray disks) and ACC (in black disks) in a common stereotaxic space. In the center, a histological section showing electrode tracks (indicated by arrows) targeting LPFC and ACC. On the right, MRI slice and 3D reconstruction for monkey P. Reconstruction of penetration sites are shown on the surface of the 3D volume.

Figure 2.

General description of high gamma oscillations. A, Average normalized power from 20 to 140 Hz from pairs of ACC and LPFC sites simultaneously recorded during incorrect trials. ACC, n = 14; LPFC, n = 7. B, Example of time frequency graph showing statistical change in activity compared with the baseline period (−500/−300 ms) before feedback (Wilcoxon and FDR). C, Boxplot of the frequency at peaks (left) and of the duration (right) of high gamma activations for recorded sites in ACC and LPFC after errors. The boxplots present the median (in red), the comparison intervals (notches), outliers (red crosses), box limits represent 25th and 75th percentiles, and whiskers give the +/−2.7σ interval. D, Proportion of sites with significant gamma power increase after feedback per frequency band. ACC: monkey M, n = 183 sites; monkey P, n = 61 sites; LPFC: monkey M, n = 76 sites; monkey P, n = 26 sites. Data are presented for two gamma bands: 60–100 Hz and 100–140 Hz. We observed more active sites in the repetition period than in the search period for the ACC and the same tendency in the LPFC for the INC and COR comparison. Activity linked to the CO1 was significantly less present in both regions for both frequency bands. The asterisks indicates the significance level: *p < 0.05, **p < 0.01, ***p < 0.001. E, Average raw activity (μV²) smoothed (rloess, 0.1) in the 100–140 Hz frequency band for the ACC (top, n = 244) and LPFC (bottom, n = 102) aligned on the three types of feedback (INC, red; CO1, light blue; COR, dark blue).

Figure 3.

High gamma latencies after negative feedback (FB). A, Averaged significant 100–140 Hz gamma per sites aligned on feedback delivery. The graph shows the normalized change in power of high gamma oscillations for INC feedback for the ACC (top) and the LPFC (bottom) compared with the baseline period. B, Kernel density estimates of latency distributions. Populations of high gamma activation latencies for both regions revealed an overall advance of ACC over LPFC in search periods.

Figure 4.

High gamma and beta power correlations after feedback. A, Temporal distribution of significant power correlations for search trials. For 60–100 Hz, we observed in the search period only a tendency for early ACC power to correlate with later LPFC power. B, Percentage of ACC/LPFC simultaneous recordings with gamma power correlation after INC, CO1, and COR in at least one 300 ms interval from −300 ms to 1100 ms (see Materials and Methods for details). C, Percentage of ACC/LPFC simultaneous recordings with beta power correlation after INC, CO1, and COR in at least one 500 ms interval from −500 ms to 1000 ms (see Materials and Methods for details). We observed more frequent correlations in the repetition period than in the search period.

Figure 5.

Beta band analyses. A, Percentage of sites with beta power desynchronization in the ACC (left) and LPFC (right). We observed more activity during the repetition period compared with the search period. B, Average of significant beta per sites aligned on feedback delivery. The graph shows the normalized averaged change in power of high beta oscillations for INC feedback for the ACC (top) and the LPFC (bottom) compared with the baseline period. C, Kernel density estimate. Cumulative proportions of beta deactivation latencies for both regions revealed an overall advance of LPFC over ACC for search trials only.