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Abstract:
We show that (1) gamma-rhythmic neuronal inputs are most effective in causing spike output, (2) local neuronal gamma-band activity modulates input gain, (3) gamma-band synchronization between visual areas partly predicts behavioral reaction times, and (4) the same holds for beta synchronization between frontal areas and the top-down fronto-occipital beta-band Granger causality. (1) We use optogenetics to emulate synaptic input, while simultaneously recording spike output. We find that the input-output transmission prefers gamma-rhythmic input. Computational modeling reveals that inputs preferentially cause spike outputs when they are coherent with ongoing gamma-rhythmic fluctuations of excitation and thereby avoiding the lagging inhibition. (2) We show that gamma-band activity rhythmically modulates neuronal and behavioral responses to unpredictable changes of the visual stimulus. Gamma phases leading to strong spike responses and to short behavioral reaction times are very similar. Thus, gamma-band activity rhythmically modulates input gain. (3) We show that visually induced interareal gamma entrainment between visual areas occurs at the phase relation that optimally subserves stimulus transmission. Deviations from the phase relation of gamma synchronization increase behavioral reaction times. (4) We show that also interareal beta synchronization between frontal areas occurs at the phase relation leading to shortest reaction times. Furthermore, fronto-occipital beta-band Granger causality is positively predictive of short reaction times. Together, these results strongly suggest that local and interareal rhythmic neuronal synchronization has a causal functional role for neuronal communication and behavior.