Theta and beta synchrony coordinate frontal eye fields and anterior cingulate cortex during sensorimotor mapping

The frontal eye fields (FEFs) and the anterior cingulate cortex (ACC) are commonly coactivated for cognitive saccade tasks, but whether this joined activation indexes coordinated activity underlying successful guidance of sensorimotor mapping is unknown. Here we test whether ACC and FEF circuits coordinate through phase synchronization of local field potential and neural spiking activity in macaque monkeys performing memory-guided and pro- and anti-saccades. We find that FEF and ACC showed prominent synchronization at a 3–9 Hz theta and a 12–30 Hz beta frequency band during the delay and preparation periods with a strong Granger-causal influence from ACC to FEF. The strength of theta- and beta-band coherence between ACC and FEF but not variations in power predict correct task performance. Taken together, the results support a role of ACC in cognitive control of frontoparietal networks and suggest that narrow-band theta and to some extent beta rhythmic activity indexes the coordination of relevant information during periods of enhanced control demands.


Supplementary Figure 2. WPLI-debiased spectrum. (A)
The phase synchronization spectrum between ACC and FEF in memory-guided saccades is depicted across all recording pairs (n=674). The panel shows larger ACC-FEF phase synchronization across theta and beta bands in the delay period (400-1100 ms following the stimulus onset, blue) compared to the baseline (700 ms prior to the fixation onset, black). (B) The phase synchronization spectrum between ACC and FEF in pro-/anti-saccades is depicted across all recording pairs (n=674). The panel shows larger ACC-FEF phase synchronization across theta and beta bands in the preparatory period (400-1100 ms following the fixation onset, blue) compared to the baseline (700 ms prior to the fixation onset, black). The shading shows +/-SEM. Figure 3. Increased theta-and beta-coherence between ACC and FEF after event-related signal subtraction. (A) Time-Frequency spectra of the wplidebiased coherence between the FEF and ACC in memory-guided saccade task after subtraction of the averaged event-related potentials from the raw signal. The white contour shows the area in which the subsequent analyses were performed (see Methods). The dashed lines demarcate the time of the onset and offset of the target stimulus. (B) WPLI-debiased FEF-ACC coherence spectrum of the individual monkeys in the delay period across all recording pairs (n=674) after the subtraction of evoked response. (C) Theta band (3-9 Hz) time course of the ACC/FEF WPLI-debiased phase synchronization after subtraction of evoked response. (D) Beta band (12-30 Hz) time course of the ACC/FEF WPLI-debiased phase synchronization after subtraction of evoked response. (E) Theta band (3-9 Hz) time course of the ACC/FEF WPLI-debiased phase synchronization after subtraction of evoked response using a method described by Truccolo et al. 2 (F) Beta band (12-30 Hz) time course of the ACC/FEF WPLI-debiased phase synchronization after subtraction of evoked response using a method described by Truccolo et al. 2 .

Supplementary Figure 4. Granger causality spectrum between ACC and FEF. (A)
Influence of ACC over FEF in the delay period (400-1100 ms following the stimulus onset, blue) and the baseline (700 ms prior to fixation onset, black). The influence of ACC over FEF is larger in the delay period across theta and beta frequency range. (B) Influence of FEF over ACC in the delay period (red) and the baseline (black). The influence of FEF over ACC is larger in the delay period across theta and beta frequency range. (C) Influence of ACC over FEF (blue) is higher than the influence of FEF over ACC (red) in the delay period across theta and beta frequency range. The shading depicts +/-SEM. The ACC-FEF channel pairs (n=275) that displayed reversed Granger causality following the reversal of time series are included in this figure.

Supplementary Figure 5. Pairwise phase consistencies (PPCs) across alpha band.
(A) PPC spike-field coherence spectrum of the population of the ACC units with the LFP's recorded in the FEF across the alpha frequency range. Comparison between baseline and delay of contra-versive saccades (left), comparison between baseline and delay of ipsi-versive saccades (middle) and comparison between the contra-and ipsiversive saccades in the delay period (right). (B) PPC spike-field coherence spectrum of the population of the FEF units with the LFP's recorded in the ACC across the alpha frequency range. Comparison between baseline and delay of contra-versive saccades (left), comparison between baseline and delay of ipsi-versive saccades (middle) and comparison between the contra-and ipsi-versive saccades in the delay period (right). Error bars denote SEM in all panels. *: p < 0.05, paired t-test.

Supplementary Figure 6. Pairwise phase consistencies (PPCs) across gamma band.
(A) PPC spike-field coherence spectrum of the population of the ACC units with the LFP's recorded in the FEF across the gamma frequency range. Comparison between baseline and delay of contra-versive saccades (left), comparison between baseline and delay of ipsi-versive saccades (middle) and comparison between the contra-and ipsiversive saccades in the delay period (right). (B) PPC spike-field coherence spectrum of the population of the FEF units with the LFP's recorded in the ACC across the gamma frequency range. Comparison between baseline and delay of contra-versive saccades (left), comparison between baseline and delay of ipsi-versive saccades (middle) and comparison between the contra-and ipsi-versive saccades in the delay period (right). Error bars denote SEM in all panels.

Supplementary Figure 7. Pairwise phase consistencies (PPCs) spectrum. (A) PPC
spike-field coherence spectrum of the population of the ACC units with the LFP's recorded in the FEF across the frequency range of 1.5-100 Hz in the delay period of memory-guided saccade task. (B) PPC spike-field coherence spectrum of the population of the FEF units with the LFP's recorded in the ACC across the frequency range of 1.5-100 Hz in the delay period of memory-guided saccade task. In both panels, the peak spike-field coupling is observed in theta frequency range. Shades denote +/-SEM.