Postural activation of the human medial gastrocnemius muscle: are the muscle units spatially localised? - PubMed (original) (raw)
Postural activation of the human medial gastrocnemius muscle: are the muscle units spatially localised?
Taian M M Vieira et al. J Physiol. 2011.
Abstract
In cat medial gastrocnemius (MG), fibres supplied by individual motoneurones (muscle units) distribute extensively along the muscle longitudinal axis. In the human MG, the size of motor unit territory is unknown. It is uncertain if the absolute size of muscle unit territory or the size relative to the whole muscle is most comparable with the cat. By comparing intramuscular and surface electromyograms we tested whether muscle units extend narrowly or widely along the human MG muscle. Due to the pennation of the MG, if individual motoneurones supply fibres scattered along the muscle, then action potentials of single motor units are expected to appear sparsely on the surface of the skin. In nine healthy subjects, pairs of wire electrodes were inserted in three locations along the MG muscle (MG60%, MG75% and MG90%). A longitudinal array of 16 surface electrodes was positioned alongside the intramuscular electrodes. While subjects stood quietly, 55 motor units were identified, of which, significantly more units were detected in the most distal sites. The surface action potentials had maximum amplitude at 4.40 ±1.67 (mean±S.D.), 8.02±2.16 and 11.63±2.09 cm (P <0.001) from the most proximal surface electrode, for motor units in the MG60%, MG75% and MG90% locations, respectively. Single motor unit potentials were recorded by five consecutive surface electrodes, at most, indicating that muscle units extend shortly along the MG longitudinal axis. It is concluded that relative to the whole muscle, and compared with the cat, muscle units in human MG are localised. The localisation of muscle units might have implications for the regional control of muscle activity.
Figures
Figure 1. Distribution of muscle units within the medial gastrocnemius muscle
A, shows the localisation of muscle fibres innervated by a single motoneuron (muscle unit; fast fatiguing). The muscle unit was identified by direct counting of glycogen-depleted muscle fibres (grey bands in the longitudinal section) at several cross-sections taken along the longitudinal axis of the cat medial gastrocnemius (MG) muscle. Dark bands denote muscle fibres appearing in two cross sections, due to the pennation of gastrocnemius fibres. Cross-hatchings in the plane view indicate the territory of the muscle unit. The number of muscles fibre identified in five cross-sections of the MG muscle is shown in the right column. B, illustrates the hypothesis of muscle units extending widely along the human MG muscle. The body of one motoneuron is located at the ventral root in the spinal cord, while its axon runs through the tibial nerve and branches to supply muscle fibres scattered along the whole MG muscle. C, shows the hypothesis of spatially localised muscle units. Axonal branching occurs close to the muscle and supplies muscle fibres distributed locally. Due to the pennate arrangement of MG muscle fibres, and since action potentials propagate along muscle fibres and not along the muscle, intramuscular potentials might appear locally or widely on the surface of the skin, depending on how extensive are the MG muscle units (compare the schematic representation of action potentials on the surface for case B and case C).
Figure 2. Spatial distribution of intramuscular and surface EMG recordings during standing
A, the positioning of the surface array of 16 electrodes and the approximate locations (MG60%, MG75% and MG90%) for insertion of the wire electrodes along the MG muscle. Surface electrodes were spaced by 1 cm and intramuscular recording locations were spaced by 15% of the distance (d) between the popliteal crease and the superficial extremity of the most distal MG fascicle (dashed line). B, the position of body centre of pressure (thin black line) and centre of gravity (thick grey line) (top), the surface (middle) and the intramuscular electromyograms (bottom) recorded from MG muscle during 20 s out of 60 s of quiet standing (subject 3). Intramuscular signals detected by electrodes inserted in different MG locations (as shown in A) are depicted in shades of grey (MG60%: black; MG75%: dark grey; MG90%: light grey).
Figure 5. Local manifestation of surface motor unit action potentials
A, a typical example of surface (top) and intramuscular (bottom) electromyograms recorded from the MG muscle of subject 7. The grey level of intramuscular traces denotes from which location these signals were recorded (see Fig. 2). Note the clear correspondence of the intramuscular potentials in the MG75% and MG90% locations with the surface action potentials on the middle (channels 8 and 9) and on the distal (from channel 9 to 15) portions of the array of electrodes, respectively. B, the surface potentials (top, black lines) and their average (thick grey line), triggered with the discharge pattern of intramuscular potentials shown at the bottom. Consistent and local representation of intramuscular action potentials is evident on the surface.
Figure 3. Method of localising intramuscular potentials in the surface EMG
A, the triggered (black lines) and the averaged surface potentials (grey lines) of one motor unit identified from the intramuscular EMG in the MG60% location. The discharge pattern of this motor unit was used to trigger and then average the intramuscular EMGs recorded from each MG location (traces below the array). B, the distribution of the averaged rectified value (ARV) amplitude (•) across channels (grey lines). The experimental distribution of ARV values was fitted with a Gaussian function (black line) by minimising the mean squared error function (shown in C). The theoretical mean (μ) was allowed to vary from –2 to +2 cm (see double arrows) with respect to the position of maximal ARV value, while the standard deviation (σ) value changed from 0.1 to 8 cm (see dotted Gaussian). C, the bi-dimensional distribution of the mean squared error. The optimal Gaussian had mean and standard deviation equal to 4.28 and 1.25 (cm), respectively. Note that a single minimum is clearly defined in the error function.
Figure 4. Surface representation of action potentials in pennate motor units
A, the distribution of the ARV amplitude (grey line), its optimal Gaussian curve (dashed line), the histogram created with the position of the superficial aponeuroses of all muscle fibres of a single, simulated motor unit and its surface potentials. Note how closely the amplitude and the location of surface potentials relate to the distribution of muscle fibres. B, the location of end-plates and muscle fibres simulated for this motor unit. The location of the superficial aponeuroses was distributed normally along the simulated territory (5.08 cm). C and D, same as in A and B, for a simulated unit whose muscle fibres were distributed uniformly along its territory (2.82 cm long). E, plots of the standard deviations of Gaussians against the actual, longitudinal size of the territories of simulated motor units, for different territory densities (▴: 200 fibres; □: 300 fibres; ×: 400 fibres; n = 300 motor units). The upper and lower graphs show that the distribution of muscle fibres along the territory of each unit was Gaussian and uniform, respectively. Both distributions of fibres resulted in Gaussian curves significantly correlated with the size of the motor unit territories (Pearson R > 0.9, P < 0.0001). F, shows the mean error values (whiskers: standard deviation; n = 300 units) obtained by fitting the Gaussian curves to the ARV distributions, for motor units with 200, 300 and 400 fibres. When the fibres were distributed normally (black bars) within the unit territory the mean error was significantly smaller than that obtained for fibres distributed uniformly (grey bars) along the territory (ANOVA, P < 0.0001, n = 1800 units).
Figure 6. Localisation and spread of surface action potentials in the MG muscle
A, the scatter plot of mean versus standard deviation values for the Gaussians optimally fitted to the distribution of surface ARV amplitude (n = 7 subjects), computed for intramuscular potentials in the three recording locations (•: MG60%; ○: MG75%; ×: MG90%). B, averaged values (whiskers indicate standard deviation) of the mean (left panel) and standard deviation (right panel) of the fitted ARV distributions. C, a short epoch (from 45 to 48 s) of raw intramuscular EMGs recorded from subject 3. The largest potentials in the MG75% location appear after the largest potentials in the most distal location, with a small and consistent delay, shown in D. This indicates that wire electrodes in both locations recorded from the same motor unit, resulting in Gaussians with the same mean and standard deviation (see arrows in A). The median delay of 3.08 ms is presumably due to small differences in the location of end-plates between different fibres of the same motor unit. Statistical significance for the multiple comparisons is reported as: *P < 0.05; **P < 0.001. n = 55 motor units.
Figure 7. Delay values estimated between consecutive surface potentials
A, plot of the delay between surface potentials recorded from adjacent channels versus the mean value of ARV distribution. Note that the delay estimated for surface potentials with highly dispersed ARV distribution (thicker crosses; σ > 1.5), is close to the delay expected for propagating potentials (2.5 ms is expected for electrodes spaced by 10 mm; propagation velocity of action potentials along muscle fibres range from 3 to 6 m s−1, Andreassen & Arendt-Nielsen, 1987). Therefore, on the most distal MG location, the amplitude of surface potentials reflects the length of muscle fibres rather than the territory of motor units (see Fig. 8 and Discussion). B, the mean values (whiskers correspond to the standard deviation) of the delay data shown in A. The delay values estimated for the MG90% location are higher (P = 0.0002) than those estimated for the other locations.
Figure 8. Propagation of action potentials along distal fibres influences the distribution of surface potentials
A illustrates how the fascicles of MG muscle were distributed below the array of surface electrodes. Electrodes in the distal portion of the array cover the same MG fibres, allowing the same intramuscular potential to be detected from different locations on the surface of the skin because of the propagation of action potentials. Proximal electrodes are located on the superficial extremity (aponeurosis) of different MG fascicles and are unlikely to have recorded from the same muscle fibres. B, raw surface action potentials (and their average; thick grey lines) triggered with the firing pattern of one motor unit identified in the MG90% location. Note the delay between potentials and the phase inversion for the potentials with similar amplitude in channels 14 and 15. C shows the sparse distribution of ARV amplitude for the averaged potentials shown in B.
References
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