Top-Down Beta Enhances Bottom-Up Gamma.

Craig G Richter, William H Thompson, Conrado A Bosman, Pascal Fries
Author Information
  1. Craig G Richter: Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society, 60528 Frankfurt, Germany, craig.richter@esi-frankfurt.de pascal.fries@esi-frankfurt.de. ORCID
  2. William H Thompson: Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society, 60528 Frankfurt, Germany.
  3. Conrado A Bosman: Donders Institute for Brain, Cognition and Behaviour, Radboud University, 6525 EN Nijmegen, The Netherlands, and. ORCID
  4. Pascal Fries: Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society, 60528 Frankfurt, Germany, craig.richter@esi-frankfurt.de pascal.fries@esi-frankfurt.de. ORCID

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. 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.

Keywords

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Grants

  1. U54 MH091657/NIMH NIH HHS

MeSH Term

Animals
Attention
Beta Rhythm
Cortical Synchronization
Gamma Rhythm
Macaca mulatta
Male
Nerve Net
Parietal Lobe
Photic Stimulation
Visual Cortex
Visual Fields
Visual Perception

Word Cloud

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