Beta-band activity during motor planning reflects response uncertainty

Abstract

It has been known for many years that the power of beta-band oscillatory activity in motor-related brain regions decreases during the preparation and execution of voluntary movements. However, it is not clear yet whether the amplitude of this desynchronization is modulated by any parameter of the motor task. Here, we examined whether the degree of uncertainty about the upcoming movement direction modulated beta-band desynchronization during motor preparation. To this end, we recorded whole-head neuromagnetic signals while human subjects performed an instructed-delay reaching task with one, two, or three possible target directions. We found that the reduction of power of beta-band activity (16-28 Hz) during motor preparation was scaled relative to directional uncertainty. Furthermore, we show that the change of beta-band power correlates with the change of latency of response associated with response uncertainty. Finally, we show that the main source of beta-band desynchronization was located in the peri-Rolandic region. The results establish directional uncertainty as an important determinant of beta-band power during motor preparation and indicate that neural activity in the sensorimotor cortex during motor preparation covaries with directional uncertainty.

Figure 1.

Schematic sequence of events in a trial of the instructed-delay task. The subjects held the joystick-controlled cursor in the center of the display for 3 s. Then, N = 1, 2, or 3 cues (circles) were presented on the screen for 1–1.5 s. The cues indicated the locations at which the upcoming target could appear. The figure shows a case with two cues located at 45° and at 165°. Each cue had the same chance to become the target. In the example, the cue at 45° became the target (disc) onto which the subjects had to move the cursor quickly and accurately. The subjects were instructed to fixate the center of the screen during the trial. The RT was defined as the duration between the onset of the target and the onset of the response, which was determined by the exit of the cursor from the center window. The MT was the duration between the onset of the response and the time when the cursor entered the target. An ITI of 3 s followed each trial.

Figure 2.

Examples of time–frequency (T–F) power plots for target-aligned data of subject 3. The range of cue onset and response onset is displayed below the time axis. The data originated from two channels identified on the two-dimensional map of the MEG 248-detector array. The anteroposterior (A–P) and left–right (L–R) axes are indicated as reference. The T–F plots show typical patterns of increase and decrease of power relative to the baseline in different frequency bands and with different time courses. We can notice the decrease of power in the beta-band (16–28 Hz) after cue onset for the channel from the left sensorimotor region.

Figure 3.

Average RT and MT for each number of cue condition. The error bars represent the SEM (N = 5 subjects).

Figure 4.

A, Channels with similar time-varying large decrease of beta-band power during the perimovement period. The channels, selected using a hierarchical cluster analysis, are shown in red on the map of the MEG 248-detector array for each subject (S1–S5). B, Cumulated clusters of channels across subjects. For each channel, the color code indicates the number of subjects that had that channel selected. All subjects had channels selected over the left sensorimotor region.

Figure 5.

Time course of relative beta-band power for each number of cue condition. The power was centered relative to the baseline and normalized relative to the average power during all motor responses. The plots show the average time-series across subjects, and its SE, aligned to the onset of the cue period (left) and to the onset of the motor response (right). The gray rectangle indicates the range of target onset times.

Figure 6.

Relation between RT and beta-band power. The scattergram shows the deviation of RT from the mean against the difference between beta-band power during the response and beta-band power preceding target onset for each number of cue condition and subject. The data from a same subject are connected by a gray line. The black line across the data points represents the least-squares fit considering subject as a random factor.

Figure 7.

Source of reduction of beta-band power estimated by the beamformer analysis. A, For each subject (S1–S5), the blue shading on the transverse slices of the subject's brain MRI indicates the region associated with 50–100% reduction of beta-band activity between baseline level and minimum level. The anteroposterior (A–P) and left–right (L–R) axes are indicated as reference. The left–right orientation of the MRI follows the radiological convention. B, Brain MRI and source of reduction of beta-band activity averaged across subjects after Talairach transformation. The yellow lines on the transverse slice identify the central sulcus. These analyses showed that the reduction of beta-band activity was originating mainly from the peri-Rolandic region contralateral to the hand used in the task.