Adult mouse motor units develop almost all of their force in the subprimary range: a new all-or-none strategy for force recruitment?

Abstract

Classical studies of the mammalian neuromuscular system have shown an impressive adaptation match between the intrinsic properties of motoneurons and the contractile properties of their motor units. In these studies, the rate at which motoneurons start to fire repetitively corresponds to the rate at which individual twitches start to sum, and the firing rate increases linearly with the amount of excitation ("primary range") up to the point where the motor unit develops its maximal force. This allows for the gradation of the force produced by a motor unit by rate modulation. In adult mouse motoneurons, however, we recently described a regime of firing ("subprimary range") that appears at lower excitation than what is required for the primary range, a finding that might challenge the classical conception. To investigate the force production of mouse motor units, we simultaneously recorded, for the first time, the motoneuron discharge elicited by intracellular ramps of current and the force developed by its motor unit. We showed that the motor unit developed nearly its maximal force during the subprimary range. This was found to be the case regardless of the input resistance of the motoneuron, the contraction speed, or the tetanic force of the motor unit. Our work suggests that force modulation in small mammals mainly relies on the number of motor units that are recruited rather than on rate modulation of individual motor units.

Figure 1.

Force profile of a fast motor unit. A, From top to bottom: force, surface EMG, frequencygram, membrane potential, injected current. B₁, B₂, Magnifications of the regions indicated in A. Arrowheads indicate the fast subthreshold oscillations characteristic of the SPR. C, Instantaneous firing frequency versus the intensity of the injected current. Vertical dashed line indicates the limit between SPR and PR. D, Peak force versus the intensity of current. The maximal force developed by the motor unit (“max”) and 90% of the force range are indicated. The vertical dashed line represents I_90%.

Figure 2.

Force profile of a slow motor unit. A, Same organization as in Figure 1A. B, Same as in Figure 1C. C, Same as in Figure 1D.

Figure 3.

Most of the force is developed in the SPR. Current necessary to recruit 90% of the force range (I_90%) versus current at the SPR/PR transition (I_trans) is plotted. There was a highly significant correlation between the two parameters (r = 0.99, p < 0.0001). The dashed line represents the identity line.

Figure 4.

Motoneurons are faster than their muscle fibers. A, Single motor unit twitch (average of 10 sweeps) from the same motor unit as in Figure 1. B, Single twitch (average of 10 sweeps) from the same motor unit as in Figure 2. C, Twitch duration versus AHP duration. The solid line represents the best linear fit (r = 0.89, p < 0.0001), and the dashed line represents the identity line. D, Histogram of the ratio twitch duration over AHP duration. Range 0.9–2.2, mean ± SD 1.3 ± 0.3; N = 33.

Figure 5.

The SPR/PR transition is matched to the contractile and electrophysiological properties of the motor unit. A, Schema illustrating how the current–frequency relationship would be modified if mouse motoneurons did not have subthreshold oscillations and an SPR of firing. B, Frequency at the SPR/PR transition (F_trans) versus TFF. Dashed line is the best linear fit (r = 0.90, p = 0.0005). C, F_trans was strongly correlated to the inverse of the AHP duration (r = 0.95, p < 0.0001), but was always greater (dashed line represents the identity line).

Figure 6.

Size principle in mouse motoneurons. A, Semilogarithmic plot of the twitch peak amplitude versus the input resistance in our sample of 33 motor units. There was a strong correlation between these two properties (r = −0.67, p < 0.0001). The solid line represents the best linear fit. B, The peak twitch force (empty squares) is strongly correlated to the recruitment current of the motor unit (r = 0.79, p < 0.0001). The tetanic force (filled squares) also strongly depended on the recruitment current (r = 0.90, p = 0.0009).