Top-Down Beta Enhances Bottom-Up Gamma

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.

Gating by induced Α–Γ asynchrony in selective attention

“…Recent studies using Granger causality measures have shown similar frequency‐specific interactions in selective attention, in which slow‐wave activity (e.g., α and β) in higher order visual areas modulates lower order regions, while the reverse occurs for γ oscillations (Bastos et al, ; Bonnefond, Kastner, & Jensen, ; Van Kerkoerle et al, ; Michalareas et al, ; von Stein, Chiang, & König, ). Furthermore, feedback activity in the α–β range has been found to promote the feedforward propagation of visual γ‐band activity during attentional selection (Richter, Thompson, Bosman, & Fries, ), an evidence that corroborates the regulatory role of top–down α influences observed in our study. The critical interplay between top–down α and bottom–up γ in visual processing has been also investigated using microstimulation: the electrical stimulation of V1 causes increases of gamma activity at later stages of the visual hierarchy (V4), whereas the stimulation of V4 increases alpha power in V1 (Van Kerkoerle et al, ).…”

Beta band oscillatory deficits during working memory encoding in adolescents with attention‐deficit hyperactive disorder

“…At the cellular level, beta oscillations have been generated in both cortical and subcortical neurons, such as the intrinsic bursting neurons in cortical layer 5 (Roopun et al., ) and medium spiny neurons in the striatum (McCarthy et al., ), respectively, and may involve the interaction of various currents, such as the one between inhibitory GABA A currents and slow potassium currents (McCarthy et al., ). Circuitry mechanisms for beta generation have also been proposed in parallel and likely involve the recruitment of various supra‐ and infragranular cortical inhibitory and excitatory neural subtypes (Kramer et al., ; Lee, Whittington, & Kopppel, ; Richter, Thompson, Bosman, & Fries, ; Roopun et al., ). Through a combination of human magnetoencephalographic recordings, mice and monkey local field potentials, recently, Sherman et al.…”

Evaluating the neurophysiological evidence for predictive processing as a model of perception

“…A number of other studies have provided evidence consistent with the idea that gamma‐ and beta‐band activity constitute prediction error and expectation signals, respectively. For instance, analyses of Granger causality by Richter et al 179 . indicated that top‐down beta‐band activity targeting macaque V1 enhanced subsequent, spatially specific, stimulus‐driven ascending gamma‐band signals from V1 to V4 in a manner consistent with precision‐weighting mechanisms invoked by PP.…”