Regular cannabis use alters the neural dynamics serving complex motor control

Abstract

Cannabis is the most widely used recreational drug in the United States and regular use has been linked to deficits in attention and memory. However, the effects of regular use on motor control are less understood, with some studies showing deficits and others indicating normal performance. Eighteen users and 23 nonusers performed a motor sequencing task during high-density magnetoencephalography (MEG). The MEG data was transformed into the time-frequency domain and beta responses (16-24 Hz) during motor planning and execution phases were imaged separately using a beamformer approach. Whole-brain maps were examined for group (cannabis user/nonuser) and time window (planning/execution) effects. As expected, there were no group differences in task performance (e.g., reaction time, accuracy, etc.). Regular cannabis users exhibited stronger beta oscillations in the contralateral primary motor cortex compared to nonusers during the execution phase of the motor sequences, but not during the motor planning phase. Similar group-by-time window interactions were observed in the left superior parietal, right inferior frontal cortices, right posterior insular cortex, and the bilateral motor cortex. We observed differences in the neural dynamics serving motor control in regular cannabis users compared to nonusers, suggesting regular users may employ compensatory processing in both primary motor and higher-order motor cortices to maintain adequate task performance. Future studies will need to examine more complex motor control tasks to ascertain whether this putative compensatory activity eventually becomes exhausted and behavioral differences emerge.

Keywords: beta; gamma; marijuana; motor sequencing; movement; oscillations.

FIGURE 1

Task paradigm and behavioral performance. (a) Participants fixated on a crosshair for 3750 ms. After this period, a sequence of three numbers, each corresponding to a digit on the right hand, was displayed on the screen for 500 ms. Numbers then changed color, indicating the cue to move, with the sequence disappearing after 2250 ms (i.e., the participant had 2250 ms to complete the sequence). (b) Behavioral results for both groups. Percentage correct (accuracy) is shown on the left, reaction time (time between cue to move and movement onset) in the middle, and movement duration (time to complete the sequence) on the right. There were no main effects of group for accuracy (p = .487), reaction time (p = .631), or movement duration (p = .707).

FIGURE 2

Time‐frequency spectrogram and source reconstruction. (a) Grand‐averaged time‐frequency spectrogram across all participants from a sensor near the left sensorimotor cortex (i.e., MEG0432). Time (ms) is displayed on the x‐axis with frequency (Hz) on the y‐axis. Signal power is expressed as a percent change from baseline. Before and during movement, there was a strong beta event‐related desynchronization (ERD; 16–24 Hz), followed by a post‐movement beta rebound (PMBR). The white box displays the two time‐frequency bins selected for beamforming analyses (planning: −500 to 0 ms; execution: 0–500 ms; both at 16–24 Hz) to isolate the motor planning and execution phases. Note that we did not image the PMBR because it is tightly linked to motor termination, and our study was focused on motor planning and execution processes. (b) Grand‐averaged beamformer image across both time windows and groups showed that the beta ERD was strongest in the contralateral primary motor cortices. The peak voxel was located at the same coordinates in the grand‐averaged image computed using the planning and execution images separately, as well as combined. Voxel time series data were extracted using the peak voxel in this grand‐averaged map.

FIGURE 3

Time series of the β‐ERD response in the primary motor cortex. Time series of the peak β‐ERD voxel, separated by group. The shaded area indicates the two β‐ERD time windows, with the motor planning window (−500 to 0 ms) in light gray and the motor execution window (0–500 ms) shown in darker gray. The asterisk (*) denotes the significant main effect of window (p = .002) and group‐by‐window interaction (p = .014). The inset in the bottom left shows the grand‐averaged β‐ERD beamformer image; the time series was extracted from the peak voxel, which was within the primary motor cortex contralateral to movement.

FIGURE 4

Group‐by‐window interaction effect. Cannabis users exhibited stronger β‐ERD responses during the execution phase compared to nonusers in the (a) left superior parietal cortices, (b) right inferior frontal cortices, (c) right posterior insula, and the left primary motor cortices (p < .001, corrected). The groups did not differ during the motor planning phase. (Top) Rain cloud plots showing peak voxel pseudo‐t values per participant from the region with the green circle in the images below each plot. Users are shown in green and nonusers in blue. The x‐axis is separated into the planning and execution windows (i.e., −500 to 0 and 0 to 500, respectively), and the y‐axis displays pseudo‐t values. (Bottom) Statistical maps showing the group‐by‐window interaction effect. In addition to the three regions noted above, significant clusters were found in the right (ipsilateral) precentral gyrus and the left (contralateral) precentral gyrus.