Enhanced Behavioral Performance through Interareal Gamma and Beta Synchronization

SUMMARY Cognitive functioning requires coordination between brain areas. Between visual areas, feedforward gamma synchronization improves behavioral performance. Here, we investigate whether similar principles hold across brain regions and frequency bands, using simultaneous local field potential recordings from 15 areas during performance of a selective attention task. Short behavioral reaction times (RTs), an index of efficient interareal communication, occurred when occipital areas V1, V2, V4, DP showed gamma synchronization, and fronto-central areas S1, 5, F1, F2, F4 showed beta synchronization. For both area clusters and corresponding frequency bands, deviations from the typically observed phase relations increased RTs. Across clusters and frequency bands, good phase relations occurred in a correlated manner specifically when they processed the behaviorally relevant stimulus. Furthermore, the fronto-central cluster exerted a beta-band influence onto the occipital cluster whose strength predicted short RTs. These results suggest that local gamma and beta synchronization and their inter-regional coordination jointly improve behavioral performance.

(A, B) PPC averaged over selected site pairs of both monkeys in each area pair, aligned to the individual gamma (A) or beta (B) peak frequency. Areas were ordered according to hierarchical level. We selected area pairs with PPC values exceeding a threshold (mean+2SD of all averaged PPC values across all frequencies and all area pairs). Dashed squares show the occipital gamma cluster (A) and the fronto-central beta cluster (B). The area pair DP-7A showed high beta PPC, but was not a direct neighbor of the beta cluster. (A, B) Across-trial correlation between power spectra and RTs for IN (red) and OUT (black) conditions, aligned to the gamma peak frequency in the occipital cluster (A) and the beta peak frequency in the fronto-central cluster (B). Correlations were first calculated per site and then averaged over sites.  . CC-BY 4.0 International license made available under a (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is The copyright holder for this preprint this version posted March 6, 2023. ; https://doi.org/10.1101/2023.03.06.531093 doi: bioRxiv preprint (C) GC between frontal and occipital clusters aligned to beta peak GC, for IN (red) and OUT (black) conditions, and in bottom-up (BU, tick lines) and top-down (TD, narrow lines) directions, separately. Colored horizontal lines indicate significant frequency bands for the indicated comparisons.
(D) Correlation between GPRs and RTs, as a function of frequency for IN (red) and OUT (black) conditions. Black horizontal dashed lines indicate significance thresholds, corrected for multiple comparisons.  (A) GC between the area pairs in the fronto-central cluster for bottom-up (BU, tick line) and top-down (TD, narrow line) directions, aligned to the beta peak. Areas were ordered according to hierarchical level. The area pairs highlighted in gray are between areas of different brain systems, namely the somatosensory (S1, 5) and frontal (F1, F2, F4) system.
(B) Strength of beta GC between somatosensory and between frontal areas. Between the recorded somatosensory areas, S1 and area 5, beta-band GC was stronger in the top-down direction. Between the recorded frontal areas, F1, F2, F4, beta-band GC was stronger in the bottom-up direction. The strength of GC is indicated by the thickness of the connecting lines.
. CC-BY 4.0 International license made available under a (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is  V2 V4 DP TEO 8L 8M 7A Tpt 7B S1 5 F1 F2 F4 V2 V4 DP TEO 8L 8M 7A Tpt 7B S1 5 F1 F2

Supplementary figure 2
. CC-BY 4.0 International license made available under a (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is The copyright holder for this preprint this version posted March 6, 2023. (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is The copyright holder for this preprint this version posted March 6, 2023.  . CC-BY 4.0 International license made available under a (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is The copyright holder for this preprint this version posted March 6, 2023. . CC-BY 4.0 International license made available under a (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is The copyright holder for this preprint this version posted March 6, 2023. ; https://doi.org/10.1101/2023.03.06.531093 doi: bioRxiv preprint