Prefrontal theta modulates sensorimotor gamma networks during the reorienting of attention

Abstract

The ability to execute a motor plan involves spatiotemporally precise oscillatory activity in primary motor (M1) regions, in concert with recruitment of "higher order" attentional mechanisms for orienting toward current task goals. While current evidence implicates gamma oscillatory activity in M1 as central to the execution of a movement, far less is known about top-down attentional modulation of this response. Herein, we utilized magnetoencephalography (MEG) during a Posner attention-reorienting task to investigate top-down modulation of M1 gamma responses by frontal attention networks in 63 healthy adult participants. MEG data were evaluated in the time-frequency domain and significant oscillatory responses were imaged using a beamformer. Robust increases in theta activity were found in bilateral inferior frontal gyri (IFG), with significantly stronger responses evident in trials that required attentional reorienting relative to those that did not. Additionally, strong gamma oscillations (60-80 Hz) were detected in M1 during movement execution, with similar responses elicited irrespective of attentional reorienting. Whole-brain voxel-wise correlations between validity difference scores (i.e., attention reorienting trials-nonreorienting trials) in frontal theta activity and movement-locked gamma oscillations revealed a robust relationship in the contralateral sensorimotor cortex, supplementary motor area, and right cerebellum, suggesting modulation of these sensorimotor network gamma responses by attentional reorienting. Importantly, the validity difference effect in this distributed motor network was predictive of overall motor function measured outside the scanner and further, based on a mediation analysis this relationship was fully mediated by the reallocation response in the right IFG. These data are the first to characterize the top-down modulation of movement-related gamma responses during attentional reorienting and movement execution.

Keywords: Posner cueing task; magnetoencephalography; oscillations; top-down.

Figure 1

Posner cueing task and epoch definition. A fixation cross was presented for 1,500 (±50) ms, followed by a cue (green bar) presented in the left or right visual hemifield for 100 ms. After 200 ms, the target stimulus (box with opening) appeared in either the left or right visual hemifield for 2,500 ms. Participants responded as to whether the opening was on the bottom or top of the target with their index and middle fingers, respectively. The cue was valid (presented on the same side as the subsequent target) 50% of the time. To evaluate the responses involved in attentional reorientation (cue‐locked), the neuromagnetic data were defined with the onset of the cue as 0 ms (denoted in red) and the baseline was defined as the 600 ms preceding cue onset. To evaluate motor responses (movement‐locked), the data were defined with movement onset as 0 ms (denoted in blue) and the baseline was defined as a 600 ms period prior to movement (and prior to the cue onset) that was individually adjusted based on reaction time [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 2

Magnetoencephalography (MEG) sensor‐level spectrograms. (a) Cue‐locked time–frequency spectrograms for two sensors near the parietal cortices. The x axis denotes time (ms) with the onset of the cue occurring at 0 ms (red dotted line) and target onset occurring at 300 ms. The y axis represents frequency (Hz). Power is shown in percentage units relative to the baseline period (−600 to 0 ms), with color scale bars beneath the spectrograms. Data have been averaged across all trials and participants. Strong decreases in alpha (8–14 Hz) and beta (14–22 Hz) oscillations were observed at the onset of the target stimulus. Additionally, large increases in theta (4–8 Hz) activity were seen following the cue and during target processing. (b) Movement‐locked time–frequency spectrograms for two sensors near the sensorimotor cortices. The x axis denotes time (ms) with the onset of movement occurring at 0 ms (blue dotted line) and the y axis represents frequency (Hz). Percent power changes relative to the baseline period (600 ms period preceding cue onset) are shown as color scales beneath each spectrogram. Strong decreases in beta (16–26 Hz) activity were observed prior to and after movement onset. Additionally, transient increases in gamma (66–76 Hz) activity were seen during movement onset. Finally, strong increases in beta (16–26 Hz) activity (i.e., the PMBR) were observed following movement termination [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 3

Cue‐ and movement‐locked oscillatory activity during target processing. (Top) Grand‐averaged beamformer images (pseudo‐t) for cue‐locked theta, alpha, and beta activity across both conditions and all participants revealed increases in theta activity in bilateral IFG and visual cortices. In contrast, decreases in alpha activity were observed in bilateral superior parietal lobules stretching anteriorly, and lateral occipital cortices. Decreases in beta activity were also observed in lateral occipital cortices and intraparietal sulci bilaterally. (Bottom) Grand‐averaged beamformer images (pseudo‐t) for the movement‐locked beta and gamma activity across both conditions and all participants revealed the well‐known perimovement beta ERD in bilateral precentral gyri (stronger contralateral to movement). Further, increases in gamma movement‐related synchrony (i.e., MRGS) were observed in the precentral gyrus contralateral to movement [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 4

Conditional effects during target processing in the prefrontal cortex. The results from the whole‐brain analyses of condition‐related effects (paired t tests) on theta (left) and alpha (right) activity are shown. Significant conditional differences (i.e., validity effects) in bilateral inferior frontal gyri (IFG) theta activity were observed, with participants exhibiting stronger theta increases during invalid relative to valid trials (p < .001, corrected). Similarly, participants had significantly stronger alpha increases during invalidly relative to validly cued targets in the right IFG (p < .001, corrected) [Color figure can be viewed at http://wileyonlinelibrary.com]

Figure 5

Relationship between prefrontal theta and movement‐related gamma. (Top) Whole‐brain correlation between the validity difference effect theta cluster in the right inferior frontal gyri (IFG; extracted peak is denoted by yellow star in the top image within the dashed box—from Figure 4) and whole‐brain gamma validity difference maps (image below the right IFG map in dashed box) revealed significant clusters in the sensorimotor cortex contralateral to movement, right supplementary motor area (SMA), and right cerebellum. This indicates that a greater theta validity difference effect in the right IFG is associated with an increased gamma validity difference effect in a distributed sensorimotor network. (Bottom) Group‐wise gamma validity in the contralateral sensorimotor cortex and right cerebellum, extracted from the peak voxel of the voxel‐wise correlation maps described above, was significantly associated with overall motor function measured independently using a neuropsychological testing battery. Mediation analyses using regression revealed that the theta validity difference effect in the right IFG fully mediated the sensorimotor gamma validity/motor function and cerebellar gamma validity/motor function relationships across participants. These analyses survived bootstrapping of 5,000 samples with confidence intervals of 95% [Color figure can be viewed at http://wileyonlinelibrary.com]