fMRI analysis for motor paradigms using EMG-based designs: a validation study

Abstract

The goal of the present validation study is to show that continuous surface EMG recorded simultaneously with 3T fMRI can be used to identify local brain activity related to (1) motor tasks, and to (2) muscle activity independently of a specific motor task, i.e. spontaneous (abnormal) movements. Five healthy participants performed a motor task, consisting of posture (low EMG power), and slow (medium EMG power) and fast (high EMG power) wrist flexion-extension movements. Brain activation maps derived from a conventional block design analysis (block-only design) were compared with brain activation maps derived using EMG-based regressors: (1) using the continuous EMG power as a single regressor of interest (EMG-only design) to relate motor performance and brain activity, and (2) using EMG power variability as an additional regressor in the fMRI block design analysis to relate movement variability and brain activity (mathematically) independent of the motor task. The agreement between the identified brain areas for the block-only design and the EMG-only design was excellent for all participants. Additionally, we showed that EMG power variability correlated well with activity in brain areas known to be involved in movement modulation. These innovative EMG-fMRI analysis techniques will allow the application of novel motor paradigms. This is an important step forward in the study of both the normally functioning motor system and the pathophysiological mechanisms in movement disorders.

Figure 1

(A) An example of bipolar extensor EMG before (top) and after (bottom) fMRI artifact correction, for 6 s during two subsequent tasks (rest and fast movement) in participant 1. Note that the signal is not corrected for movement artifacts. Scan starts are indicated. Note that positive is down according to neurophysiological standards. (B) An example of bipolar extensor EMG before (top) and after (bottom) fMRI artifact correction, for 100 ms during the initial stage of scan acquisition. The artifacts due to preparation and repeated slice acquisition have been indicated.

Figure 2

An example of mean EMG power for the posture (EMG _posture: see text) and movement (EMG _movement: see text) tasks in participant 1. Top: session 1. Middle: session 2. A blow‐up (right upper and middle panel) is provided for each session to show more details of EMG during posture. Bottom: mean EMG power after convolution and scaling with its SD. Bottom left: session 1, bottom right: session 2. (Mean EMG power: bipolar EMG after artifact correction, frequency extraction and averaging per scan; drawn line: movement, dotted line: posture, a.u.: arbitrary units. F/S: fast/slow movement.)

Figure 3

Details of the design matrices for participant 1, session 1 (302 scans). Movement parameters, illustrated here only for design A1, were the same for all designs per participant. (A1) Block‐only design, two tasks: block posture and movement regressors and six movement parameters. (A2) EMG‐only design: “EMG‐only” regressor. Note that the gray values correspond with EMG power, as in Figure 2, bottom left. (B1) Block plus residual EMG design: block posture and movement and residual EMG posture and movement regressors. (B2) Block‐only design, three tasks: block posture, fast, and slow movement regressors.

Figure 4

The resulting activation maps for the different regressors per design are shown for participant 1. From top to bottom: design A1 (left: block movement, right: block posture), design A2 (EMG only), design B1 (left: block movement, right: block posture), design B1 (left: residual EMG movement, right: residual EMG posture) and design B2 (fast–slow movement). Activation maps are projected on a normalized single‐participant T1 image (Montreal Neurological Institute, MNI). Transversal section at MNI (−32, −30, 62): contralateral SMC (central sulcus) and coronal section at MNI (9, −56, −18): ipsilateral cerebellum IV–V. Only significant activations (T ≫ 4.83) have been plotted. Note the different color scales for the movement and posture contrasts.

Figure 5

Activation maps for participants 1–5 (left to right) projected on the same T1‐image as in Figure 4. Top: design A1, block movement; bottom: design A2, EMG‐only. Transversal section at MNI (−32, −30, 62): contralateral SMC (central sulcus). Only significant activations (T ≫ 4.83) have been plotted.

Figure 6

Activation maps for participants 1–5 (top to bottom) projected on the same T1‐image as in Figure 4. Left column: design B1, residual EMG movement; right column: design B2, fast–slow movement. Transversal section at MNI (−32, −30, 62): contralateral SMC (central sulcus) and coronal section at MNI (9, −56, −18): ipsilateral cerebellum IV‐V. Only significant activations (T ≫ 4.83) have been plotted. Note that images for participant 5 are uncorrected (P < 0.001), but at the same cluster size (8). For participant 5, activations where T ≫ 3.1 are plotted.

Figure 7

(A) Illustration of Gram‐Schmidt orthogonalization for the movement task in participant 1 for the first 200 scans of session 1. Horizontal axis: scans; vertical axis: regressor, a.u.:arbitrary units. Gray: movement task intervals. Top: block _movement: block design (boxcar type) regressor for movement; the task is performed in an on/off fashion. Middle: EMG _movement: EMG regressor for movement. The EMG power was averaged per scan (3 s) and equals zero, except during task execution. Note that the movement task was evenly divided in fast (higher EMG power) and slow movement (lower EMG power). Cf. Figure 2, top left. Bottom: Gram‐Schmidt orthogonalization of EMG _movement with respect to block _movement results in the residual EMG vector EMG _movement,res. This is the additional EMG (positive or negative) relative to the mean EMG power (shown here before convolution with the canonical haemodynamical response function and scaling with the standard deviation). (B) Example of mean signal intensity in ROIs for the contralateral sensorimotor cortex (top) and the ipsilateral cerebellum (bottom). Here, ROIs were derived from the active clusters in the block movement contrast in design A1 at T ≥ 14, for participant 1.