A dynamic network involving M1-S1, SII-insular, medial insular, and cingulate cortices controls muscular activity during an isometric contraction reaction time task

Abstract

Magnetoencephalographic, electromyographic (EMG), work, and reaction time (RT) were recorded from nine subjects during visually triggered intermittent isometric contractions of the middle finger under two conditions: unloaded and loaded (30% of maximal voluntary contraction). The effect of muscle fatigue was studied over three consecutive periods under both conditions. In the loaded condition, the motor evoked field triggered by the EMG onset decreased with fatigue, whereas movement-evoked fields (MEFs) increased (P < 0.01). Fatigue was demonstrated in the loaded condition, since (i) RT increased due to an increase in the electromechanical delay (P < 0.002); (ii) work decreased from Periods 1 to 3 (P < 0.005), while (iii) the myoelectric RMS amplitude of both flexor digitorum superficialis and extensor muscles increased (P < 0.003) and (iv) during Period 3, the spectral deflection of the EMG median frequency of the FDS muscle decreased (P < 0.001). In the unloaded condition and at the beginning of the loaded condition, a parallel network including M1-S1, posterior SII-insular, and posterior cingulate cortices accounted for the MEF activities. However, under the effect of fatigue, medial insular and posterior cingulate cortices drove this network. Moreover, changes in the location of insular and M1-S1 activations were significantly correlated with muscle fatigue (increase of RMS-EMG; P < 0.03 and P < 0.01, respectively). These results demonstrate that a plastic network controls the strength of the motor command as fatigue occurs: sensory information, pain, and exhaustion act through activation of the medial insular and posterior cingulate cortices to decrease the motor command in order to preserve muscle efficiency and integrity.

Figure 1

From left to right: (a) nonmagnetic ergometer: P = load, d = displacement; (b) arrows: LED triggering, RT (reaction time) is the sum of the premotor time (PMT) and electromechanical delay (EMD); (c) schematic positions of the EMG electrodes.

Figure 2

(a) Pattern of static work (W (J)); (b) reaction time (RT (ms)); (c) RMS (%) of the flexor digitorum superficialis (FDS) EMG expressed as a percentage of the RMS‐EMG of the maximal voluntary force of the FDS; (d) spectral deflection of median FDS‐EMG frequency (mf (Hz)); (e) heart rate (HR (bpm). Black bars: loaded; white bars: unloaded (*P < 005, **P < 001).

Figure 3

Upper row: Isocontour maps of the MF at the EMG onset (grand averaged data). Lower row: Isocontour maps of MEF at the mean peak latency (grand averaged data). Arrows represent an estimation of the main “equivalent dipole.”

Figure 4

On the left: grand average across subjects of the motor field (MF) and movement‐evoked field (MEFs) during the unloaded (up) and loaded conditions (down) for the three periods. Respectively for MF and MEF: Period 1, light green and blue lines; Period 2, gray and purple lines; Period 3, black and dark blue lines. On the right: mean amplitude of the peak across subjects. Gray bars: MF, Black bars: MEFs (*P < 005, **P < 001).

Figure 5

Dipole localization for the MF during the loaded condition for Subject 4. Upper MRI: The motor field during the Period 1 is labeled MF1; lower MRI: The motor field of the Period 3 is labeled MF3. The location of the MF dipole was found in the central sulcus whatever the load.

Figure 6

Examples of dipole shifts for the Subject 6 during the MEF. The two upper rows show the shift of the dipole location from the precentral to the postcentral gyrus. The two lower rows show the dipole shift from the posterior SII‐insula (in Period 1, labeled here MEF1) to the medial insula (in Period 3: MEF3). Note that for this subject SII‐insula and medial insula activations precede M1 and S1 activations by about 100 ms.