Task-related coupling from high- to low-frequency signals among visual cortical areas in human subdural recordings

Cortical cooperativity during cognitive demands includes high- and low-frequency activities, which raises the question whether there are interdependencies between fast and slow processes and how they are reflected in electrical brain signals. We had the opportunity to record signals intracranially from occipital visual areas in an epileptic patient and quantified inter-areal signal coupling while the patient performed a visual delayed-match-to-sample task. We computed coherence, phase consistency and amplitude envelope correlation and we also determined inter-frequency coupling through correlation between low-frequency signal components and amplitude envelopes of high-frequency components. There was a pronounced task-related increase of correlation between gamma-band (28-70 Hz) signal envelopes from a superior (occipital) and low-frequency (0-3.5 Hz) signals from an inferior (occipital) visual area, lasting for approximately 1 s and possibly reflecting a short-term memory encoding process. The correlational delay between envelopes and low-frequency components was 40 ms. In contrast, coherence, phase consistency and envelope correlation showed event-, but no task-related changes of intra-areal and no changes of inter-areal coupling. Our data suggest a specific effect of gamma-activity in the superior onto low-frequency activity in the inferior area. We argue that temporal dispersion of conduction delays might prevent coherent transmission of high-frequency signals and thus account for the absence of gamma-coherence. As such dispersion is a general property of long-range projections, envelope-to-signal correlation possibly reflects a general neuronal mechanism. Hence, our method provides a powerful tool for detecting such inter-areal interactions not visible with conventional linear coupling measures.