The peak frequency of motor-related gamma oscillations is modulated by response competition

Abstract

Movement execution generally occurs in an environment with numerous distractors, and requires the selection of a motor plan from multiple possible alternatives. However, the impact of such distractors on cortical motor function during movement remains largely unknown. Previous studies have identified two movement-related oscillatory responses that are critical to motor planning and execution, and these responses include the peri-movement beta event-related desynchronization (ERD) and the movement-related gamma synchronization (MRGS). In the current study, we investigate how visual distractors cuing alternative movements modulate the beta ERD and MRGS responses. To this end, we recorded magnetoencephalography (MEG) during an arrow-based version of the Eriksen flanker task in 42 healthy adults. All MEG data were transformed in to the time-frequency domain and the beta ERD and MRGS responses were imaged using a beamformer. Virtual sensors (voxel time series) were then extracted from the peak voxels of each response for the congruent and incongruent flanker conditions separately, and these data were examined for conditional differences during the movement. Our results indicated that participants exhibited the classic "flanker effect," as they responded significantly slower during incongruent relative to congruent trials. Our most important MEG finding was a significant increase in the peak frequency of the MRGS in the incongruent compared to the congruent condition, with no conditional effect on response amplitude. In addition, we found significantly stronger peri-movement beta ERD responses in the ipsilateral motor cortex during incongruent compared to congruent trials, but no conditional effect on frequency. These data are the first to show that the peak frequency of the MRGS response is linked to the task parameters, and varies from trial to trial in individual participants. More globally, these data suggest that beta and gamma oscillations are modulated by visual distractors causing response competition.

Keywords: Beta ERD; Flanker; MEG; Magnetoencephalography; Movement; Oscillations.

Figure 1. Flanker task paradigm

In each trial, participants fixated on a crosshair for 1500 ± 50 ms, then a display with a series of five arrows appeared for 2500 ms, during which participants responded with their right hand as to whether the center arrow was pointing to the left (index finger) or right (middle finger). During “congruent” trials, the flanking arrows matched the target, whereas in “incongruent” trials the flanking arrows pointed in the direction opposite of the center arrow.

Figure 2. Behavioral results

In each bar graph, the congruent condition is shown in black, while the incongruent condition is shown in gray. Error bars denote the standard error of the mean (SEM). Accuracy (percentage correct) is shown on the left, and reaction time (in ms) is shown on the right. While there was no difference in accuracy between conditions, there was a significant difference in reaction time (p < .001), with participants responding more slowly in the incongruent compared to the congruent condition. * = p < .001.

Figure 3. Peri-movement beta ERD and MRGS responses

Group-averaged beamformer images (pseudo-t) for the peri-movement beta ERD (left panel) and MRGS (right panel) are shown for the congruent and incongruent conditions individually. Images are shown in radiologic convention (R = L). In both conditions, the task induced a strong peri-movement beta ERD in the bilateral primary motor cortices (stronger in the contralateral), and a MRGS response that was restricted to the contralateral primary motor cortex. Virtual sensors were extracted from the peak voxel(s) in the grand average image (congruent and incongruent) of each response, and these time series were used to assess the effects of condition on amplitude and peak frequency.

Figure 4. Virtual sensor time-frequency spectra for the peri-movement beta ERD and MRGS response

Voxel time series were extracted from each participant’s data using the peak voxels corresponding to the peri-movement beta ERD and MRGS in the grand average images. For the beta ERD, virtual sensors were extracted for the left (top row) and right primary motor cortices (not shown), while for the MRGS virtual sensors were extracted solely from the left primary cortex (bottom row). For each voxel time series, frequency (in Hz) is shown on the y-axis, with time (in seconds) on the x-axis. In each spectrogram, color depicts percentage increase (warmer colors) or decrease (cooler colors) from the baseline, with the scale bar shown to the far right of each row. Time-frequency spectrograms combined across both conditions are shown in the left column, while the congruent condition is shown in the middle column and the incongruent condition is shown in the right column. White boxes denote the time-frequency bins that were imaged prior to virtual sensor extraction.

Figure 5. MRGS peak frequency by condition

Box plots showing the peak frequency for the congruent (left) and incongruent (right) conditions. Frequency (in Hz) is denoted on the y-axis. The center line within each box denotes the median frequency, and the bottom and top of each box designate the first and third quartile, respectively. Each lower and upper stem reflects the minimum and maximum values. The peak frequency of the MRGS response was higher in the incongruent relative to the congruent condition, t(41) = 2.159, p = .037.