Dynamic Changes in Phase-Amplitude Coupling Facilitate Spatial Attention Control in Fronto-Parietal Cortex

Abstract

Electrocorticography reveals how coupling between two frequencies of neuronal oscillation allows the frontal and parietal areas of the cortex to control visual attention from moment to moment in the human brain.

Abstract

Attention is a core cognitive mechanism that allows the brain to allocate limited resources depending on current task demands. A number of frontal and posterior parietal cortical areas, referred to collectively as the fronto-parietal attentional control network, are engaged during attentional allocation in both humans and non-human primates. Numerous studies have examined this network in the human brain using various neuroimaging and scalp electrophysiological techniques. However, little is known about how these frontal and parietal areas interact dynamically to produce behavior on a fine temporal (sub-second) and spatial (sub-centimeter) scale. We addressed how human fronto-parietal regions control visuospatial attention on a fine spatiotemporal scale by recording electrocorticography (ECoG) signals measured directly from subdural electrode arrays that were implanted in patients undergoing intracranial monitoring for localization of epileptic foci. Subjects ( n = 8) performed a spatial-cuing task, in which they allocated visuospatial attention to either the right or left visual field and detected the appearance of a target. We found increases in high gamma (HG) power (70–250 Hz) time-locked to trial onset that remained elevated throughout the attentional allocation period over frontal, parietal, and visual areas. These HG power increases were modulated by the phase of the ongoing delta/theta (2–5 Hz) oscillation during attentional allocation. Critically, we found that the strength of this delta/theta phase-HG amplitude coupling predicted reaction times to detected targets on a trial-by-trial basis. These results highlight the role of delta/theta phase-HG amplitude coupling as a mechanism for sub-second facilitation and coordination within human fronto-parietal cortex that is guided by momentary attentional demands.

Author Summary

The frontal and parietal areas of the cortex control the ability to focus visuospatial attention, and damage to these areas results in profound attentional disturbances. Although much research has concentrated on where these areas are located, little is known about how these areas may function in humans. Previous studies have demonstrated that neuronal spiking is more likely to occur in specific time windows based upon the phase of lower frequency neural oscillations – rhythmic or repetitive neuronal activity. These low-frequency rhythms are hypothesized to coordinate the timing of neuronal firing within local and across network regions. Here, we investigated how human frontal and parietal cortices use neural oscillations to control visuospatial attention. We identified a high-frequency component of electrical brain activity, broadband high gamma (70–250 Hz) amplitude, that became phase-locked to a slower rhythm, delta/theta (2–5 Hz), over frontal, parietal, and visual areas while the study subjects paid attention to the peripheral visual field. Changes in the strength of the coupling between delta/theta phase and high gamma amplitude predicted the attentional behavior of the subjects across single trials. From these results, we conclude that coupling between delta/theta phase and high gamma amplitude serves to coordinate information within – and perhaps between – frontal and parietal areas during allocation of visuospatial attention.