Abstract

Several recent studies have demonstrated that the bottom-up signaling of a visual stimulus is subserved by interareal gamma-band synchronization, whereas top-down influences are mediated by alpha-beta band synchronization. These processes may implement top-down control of stimulus processing if top-down and bottom-up mediating rhythms are coupled via cross-frequency interaction. To test this possibility, we investigated Granger-causal influences among awake macaque primary visual area V1, higher visual area V4, and parietal control area 7a during attentional task performance. Top-down 7a-to-V1 beta-band influences enhanced visually driven V1-to-V4 gamma-band influences. This enhancement was spatially specific and largest when beta-band activity preceded gamma-band activity by ∼0.1 s, suggesting a causal effect of top-down processes on bottom-up processes. We propose that this cross-frequency interaction mechanistically subserves the attentional control of stimulus selection.SIGNIFICANCE STATEMENT Contemporary research indicates that the alpha-beta frequency band underlies top-down control, whereas the gamma-band mediates bottom-up stimulus processing. This arrangement inspires an attractive hypothesis, which posits that top-down beta-band influences directly modulate bottom-up gamma band influences via cross-frequency interaction. We evaluate this hypothesis determining that beta-band top-down influences from parietal area 7a to visual area V1 are correlated with bottom-up gamma frequency influences from V1 to area V4, in a spatially specific manner, and that this correlation is maximal when top-down activity precedes bottom-up activity. These results show that for top-down processes such as spatial attention, elevated top-down beta-band influences directly enhance feedforward stimulus-induced gamma-band processing, leading to enhancement of the selected stimulus.

Highlights

  • Many cognitive effects in vision can only be explained by invoking the concept of top-down influences (Gilbert and Sigman, 2007)

  • This arrangement inspires an attractive hypothesis, which posits that top-down betaband influences directly modulate bottom-up gamma band influences via cross-frequency interaction. We evaluate this hypothesis determining that beta-band top-down influences from parietal area 7a to visual area V1 are correlated with bottom-up gamma frequency influences from V1 to area V4, in a spatially specific manner, and that this correlation is maximal when top-down activity precedes bottom-up activity

  • Influences mediated by bottom-up projections are primarily carried by gamma-band synchronization; influences mediated by top-down projections are primarily carried by alpha-beta-band synchronization (Bastos et al, 2012; Bosman et al, 2012; Grothe et al, 2012; Jia et al, 2013; van Kerkoerle et al, 2014; Bastos et al, 2015a,b; Michalareas et al, 2016)

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Summary

Introduction

Many cognitive effects in vision can only be explained by invoking the concept of top-down influences (Gilbert and Sigman, 2007). Neurons in higher visual areas show enhanced firing when processing attended stimuli These neurophysiological consequences of top-down control must be mediated by corresponding anatomical projections. Bottom-up and top-down projections show different characteristic laminar patterns of origin and termination, and the pattern of interareal pairwise projections abides by a global hierarchy (Felleman and Van Essen, 1991; Hilgetag et al, 1996; Markov et al, 2014). It has been shown in both macaque and human visual cortex, that the pattern of anatomical projections is closely correlated to a pattern of frequency-specific directed interareal influences. A similar association of higher frequency bands with bottom-up

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