Top-down and bottom-up interactions rely on nested brain oscillations to shape rhythmic visual attention sampling

PLoS Biol. 2025 Apr 10;23(4):e3002688. doi: 10.1371/journal.pbio.3002688. eCollection 2025 Apr.

Abstract

Adaptive visual processing is enabled through the dynamic interplay between top-down and bottom-up (feedback/feedforward) information exchange, presumably propagated through brain oscillations. Here, we causally tested for the oscillatory mechanisms governing this interaction in the human visual system. Using concurrent transcranial magnetic stimulation-electroencephalography (TMS-EEG), we emulated top-down signals by a single TMS pulse over the frontal eye field (right FEF), while manipulating the strength of sensory input through the presentation of moving concentric gratings (compared to a control-TMS site). FEF-TMS without sensory input led to a top-down modulated occipital phase realignment, alongside higher fronto-occipital phase connectivity, in the alpha/beta band. Sensory input in the absence of FEF-TMS increased occipital gamma activity. Crucially, testing the interaction between top-down and bottom-up processes (FEF-TMS during sensory input) revealed an increased nesting of the bottom-up gamma activity in the alpha/beta-band cycles. This establishes a causal link between phase-to-power coupling and top-down modulation of feedforward signals, providing novel mechanistic insights into how attention interacts with sensory input at the neural level, shaping rhythmic sampling.

MeSH terms

  • Adult
  • Attention* / physiology
  • Brain* / physiology
  • Electroencephalography
  • Female
  • Humans
  • Male
  • Photic Stimulation
  • Transcranial Magnetic Stimulation
  • Visual Perception* / physiology
  • Young Adult