Top-Down Beta Oscillatory Signaling Conveys Behavioral Context to Primary Visual Cortex

Abstract

Top-down modulation of sensory processing is a critical neural mechanism subserving a number of important cognitive roles. Principally, top-down influences appear to inform lower-order sensory systems of the current task at hand, and thus may convey behavioral context to these systems. Accumulating evidence indicates that top-down cortical influences are carried by directed interareal synchronization of oscillatory neuronal populations. An important question currently under investigation by a number of laboratories is whether the information conveyed by directed interareal synchronization depends on the frequency band in which it is conveyed. Recent results point to the beta frequency band as being particularly important for conveying task-related information. However, little is known about the nature of the information conveyed by top-down directed influences. To investigate the information content of top-down directed beta-frequency influences, we measured spectral Granger Causality using local field potentials recorded from microelectrodes chronically implanted in visual cortical areas V1, V4, and TEO, and then applied multivariate pattern analysis to the spatial patterns of top-down spectral Granger Causality in the visual cortex. We decoded behavioral context by discriminating patterns of top-down (V4/TEO [->] V1) beta-peak spectral Granger Causality for two different task rules governing the correct responses to visual stimuli. The results indicate that top-down directed influences in visual cortex are carried by beta oscillations, and differentiate current task demands even before visual stimulus processing. They suggest that top-down beta-frequency oscillatory processes may coordinate the processing of sensory information by conveying global knowledge states to early levels of the sensory cortical hierarchy independently of bottom-up stimulus-driven processing.