Attention Drives Synchronization of Alpha and Beta Rhythms between Right Inferior Frontal and Primary Sensory Neocortex

Abstract

The right inferior frontal cortex (rIFC) is specifically associated with attentional control via the inhibition of behaviorally irrelevant stimuli and motor responses. Similarly, recent evidence has shown that alpha (7-14 Hz) and beta (15-29 Hz) oscillations in primary sensory neocortical areas are enhanced in the representation of non-attended stimuli, leading to the hypothesis that allocation of these rhythms plays an active role in optimal inattention. Here, we tested the hypothesis that selective synchronization between rIFC and primary sensory neocortex occurs in these frequency bands during inattention. We used magnetoencephalography to investigate phase synchrony between primary somatosensory (SI) and rIFC regions during a cued-attention tactile detection task that required suppression of response to uncertain distractor stimuli. Attentional modulation of synchrony between SI and rIFC was found in both the alpha and beta frequency bands. This synchrony manifested as an increase in the alpha-band early after cue between non-attended SI representations and rIFC, and as a subsequent increase in beta-band synchrony closer to stimulus processing. Differences in phase synchrony were not found in several proximal control regions. These results are the first to reveal distinct interactions between primary sensory cortex and rIFC in humans and suggest that synchrony between rIFC and primary sensory representations plays a role in the inhibition of irrelevant sensory stimuli and motor responses.

Neural mechanisms of transient neocortical beta rhythms: Converging evidence from humans, computational modeling, monkeys, and mice

“…We studied source-localized human MEG data from the hand area of SI and from IFC. These signals were investigated in prior studies (1,15), where we applied inverse modeling techniques to estimate the location, magnitude, and temporal evolution of spontaneous activity. Here, we investigated the signatures of spontaneous beta activity in the prestimulus period in each of these signals (Experimental Procedures, MEG Data).…”

“…A key unifying theme for sensorimotor beta expression is its negative correlation with active processing (7,11,18). Sensorimotor beta shows an inverse relationship with attention (2,14,15,29), sensory detection probability (2), accurate decision-making (62), and movement planning and initiation (6). Together, these results suggest that beta rhythms inhibit processing and decrease focally to allow optimal information relay.…”

“…Building on our prior work (1, 2, 15, 33), we studied MEG-measured spontaneous beta activity in two brain areas: (i) primary somatosensory neocortex (SI), where beta emerges as part of the so-called "mu rhythm" and typically contains a complex of alpha and beta events, and (ii) frontal cortex, specifically the right inferior frontal cortex (IFC), where beta can be expressed without a strong alpha signal. We previously have shown that beta activity in each of these areas is coordinated, with synchrony in the beta band increasing during inattention (15) and increased beta power in SI predicting failed detection (2).…”

“…They are found with magnetoencephalography (MEG) (1-4), EEG (5, 6), and local field potential (LFP) recordings from neocortex (7-9) and are preserved across species (10). Local beta oscillations and their coordination between regions are implicated in numerous functions, including sensory perception, selective attention, and motor planning and initiation (2,3,6,7,9,(11)(12)(13)(14)(15). Neocortical beta oscillations are disrupted in various neuropathologies, most notably Parkinson's disease (PD), in which treatments that alleviate motor symptoms also reverse the neocortical beta disruption (16,17).…”

“…These findings make several predictions about optimal states for perceptual and motor performance and guide causal interventions to modulate beta for optimal function. beta rhythm | magnetoencephalography | computational modeling | sensorimotor processing | Parkinson's disease B eta band rhythms (15)(16)(17)(18)(19)(20)(21)(22)(23)(24)(25)(26)(27)(28)(29) are a commonly observed activity pattern in the brain. They are found with magnetoencephalography (MEG) (1)(2)(3)(4), EEG (5,6), and local field potential (LFP) recordings from neocortex (7)(8)(9) and are preserved across species (10).…”