Hand sensory-motor cortical network assessed by functional source separation

Abstract

The functional source separation procedure (FSS) was applied to identify the activities of the primary sensorimotor areas (SM1) devoted to hand control. FSS adds a functional constraint to the cost function of the basic independent component analysis, and obtains source activity all along different processing states. Magnetoencephalographic signals from the left SM1 were recorded in 14 healthy subjects during a simple sensorimotor paradigm--galvanic right median nerve stimuli intermingled with submaximal isometric thumb opposition. Two functional sources related to the sensory flow in the primary cortex were extracted requiring maximal responsiveness to the nerve stimulation at around 20 and 30 ms (S1a, S1b). Maximal cortico-muscular coherence was required for the extraction of the motor source (M1). Sources were multiplied by the Euclidean norm of their corresponding weight vectors, allowing amplitude comparisons among sources in a fixed position. In all subjects, S1a, S1b, M1 were successfully obtained, positioned consistently with the SM1 organization, and behaved as physiologically expected during the movement and processing of the sensory stimuli. The M1 source reacted to the nerve stimulation with higher intensity at latencies around 30 ms than around 20 ms. The FSS method was demonstrated to be able to obtain the dynamics of different primary cortical network activities, two devoted mainly to sensory inflow, and the other to the motor control of the contralateral hand. It was possible to observe each source both during pure sensory processing and during motor tasks. In all conditions, a direct comparison of source intensities can be achieved.

Figure 1

(Top) From left: Subject position during recordings from Rolandic area contralateral to the moved/stimulated hand. Nonmagnetic device, i.e., a water sphygmomanometer, to control the level of contraction. Particular of the thumb position during OP contraction, with electrodes recording the EMG signal as well as the median nerve stimulation at wrist. (Bottom) From the top: Trigger indicating a tone beep for starting/stopping the isometric contraction. Trigger indicating sensory stimuli to the median nerve at wrist. EMG signal, where relax and contraction periods are clearly noticeable, as well as the sensory stimulus artifact. Off line‐generated signal code differentiating the three experimental conditions as follows: Relax (R), Sensory (S), Motor (M). [Color figure can be viewed in the online issue, which is available at www.interscience.wiley.com.]

Figure 2

In each subject, comparison between maximal channel cortico‐muscular coherence (original data, dotted line, columns 1 and 3) and the coherence which has been calculated between rectified EMG and signal obtained by retro‐projecting only the M1 source (MEG_rec_M1, solid line, columns 2 and 4). Horizontal line indicates the confidence limit (see Materials and Methods section, 0.015). In all cases, it is evident that cortico‐muscular coherence is higher for the M1 retro‐projected signal than for the original channels.

Figure 3

Single subject: For each subject, superimposition of S1a (solid line), S1b (dotted line), and M1 (dashed line) sources averaged by centring on the median nerve stimulation (t = 0, vertical solid line) in the time window [−30, 100] ms. For reference, 20 and 30 ms are indicated (vertical dotted lines). Mean across subjects: The three source signals averaged on nerve stimuli are reported separately, as well as the superimposed ones (bottom). It clearly results that the S1a source reacts maximally at around 20 ms, S1b at around 30 ms, and M1 less than S1a and S1b, but with higher reaction at 30 ms than at 20 ms. [Color figure can be viewed in the online issue, which is available at www.interscience.wiley.com.]

Figure 4

Single subject: Superimposition of the coherences of the S1a (solid line), S1b (dotted line), and M1 (dashed line) sources with the rectified EMG in the frequency interval [0, 45] Hz, for each subject. The horizontal line indicates the confidence limit. Mean across subjects: For S1a, S1b, and M1, source‐muscular coherence averaged across subjects. M1 displays an evidently greater coherence than S1a and S1b. [Color figure can be viewed in the online issue, which is available at www.interscience.wiley.com.]

Figure 5

Mean positions across subjects of the three M1, S1b, and S1a FSs, after normalization of individual data in the MNI space (for the procedure, see the legend of Table I). The magnification of the source position in the axial view is shown in the corresponding inset, where the topographical relationship with ω‐shaped Rolandic sulcus tract is clearly identifiable. [Color figure can be viewed in the online issue, which is available at www.interscience.wiley.com.]

Figure 6

Evoked activity during median nerve stimulation in one representative subject. All parietal channels' superimposition averaged on median nerve stimuli, in the time window [−10, 80] ms, t = 0 the stimulus arrival being at wrist (vertical solid line). The time points corresponding to M20 and M30 components are indicated (vertical dashed lines). Left: Original data. Centre: Retro‐projected data with only the S1a source (top, MEG_rec_S1a) and with only the S1b source (bottom, MEG_rec_S1b). Right: Original data minus MEG_rec_S1a (top) and original data minus MEG_rec_S1b (bottom). The grey area indicates the time interval (Δ₂ t ₂₀ + Δ₁ t ₂₀ + 1 up, Δ₂ t ₃₀ + Δ₁ t ₃₀ + 1, bottom) where the discrepancy indices (discr_S1a up, discr_S1b, bottom) are calculated. Note that both S1a and S1b well explain the generated field at their respective latencies. Cortico‐muscular coherence during voluntary contraction. Superimposition of all channels' coherences with the rectified EMG in the frequency window [0, 45] Hz. The confidence limit is indicated (0.015, horizontal dashed line). Left: Original MEG channels. Centre: Retro‐projected channels with only M1 (MEG_rec_M1). All channels display the same coherence with the EMG signal; this is because all the channels obtained by retro‐projecting only one FS display the same time evolution, unless a multiplicative factor and the coherence are independent from the signals amplitude. Right: Original MEG data minus MEG_rec_M1 channels. The grey area indicates the frequency interval (Δ₂ω_max + Δ₁ω_max + 1) where the discrepancy index (discr_M1) is calculated. [Color figure can be viewed in the online issue, which is available at www.interscience.wiley.com.]

Figure A1

Mean and standard errors across subjects for the tested λ‐values of the R_S1a (solid line), R_S1b (dotted line), and R_M1 (dashed line) indices (top), and of the computational times for the three source extractions (bottom)r. [Color figure can be viewed in the online issue, which is available at www.interscience.wiley.com.]