Motoneuronal pre-compensation for the low-pass filter characteristics of muscle. A quantitative appraisal in cat muscle units

1. The relevance of motoneurone dynamic sensitivity in compensating for the low-pass filter properties of muscle was assessed by Stimulating cat muscle units (MUs) with impulse discharges generated by two current to-rate converters: (i) a spinal motoneurone, sensitive to both the input intensity and its first derivative, and (ii) a linear current-to-rate converter, i.e. a neurone model with the same static sensitivity as the motoneurone but lacking dynamic sensitivity. 2. Discharges generated by injection of sine-wave currents in three motoneurones of the 'fast' type and in the three related model versions were applied to the axon of forty-six MUs. The MU isometric tension was modulated at the frequency of the current sine wave (0.5-20 Hz). Phase and gain of the current-to-force transduction were measured. 3. When MUs were driven by the model, the force lagged the current by 90 deg at 1 Hz in slow MUs and at around 5 Hz in fast MUs. Under motoneurone drive, the 90 deg phase lag was attained at frequencies about twice as high. 4. The gain of the transduction (peak-to-peak force modulation/peak-to-peak current modulation) decayed when the modulation frequency was increased. In all but five units, the cut-off frequency, F(co) (gain attenuated by -3 dB), was higher when the unit was motoneurone driven (F(co)Cell) then when it was model driven (F(co)Mod). In both conditions, F(co) was inversely correlated with the MU's time-to-peak. The advantage conferred by the motoneurone dynamic sensitivity was expressed by the F(co) ratio (F(co) cell/F(co)Mod). Across the MU population this ratio ranged from 0.6-2.8, was inversely correlated with the time-to peak, and was directly correlated with the half-tension rate, i.e. the impulse rate at which MUs develop 50% of their maximal tetanic force. The largest improvement (F(co), ratio > 2.0) was found in units with mechanical features similar to those presumably coupled 'in vivo' to the motoneurones utilized for stimulation. 5. This estimate was confirmed in experiments in which trains of pulses, generated by injection of ramp currents in another motoneurone and the related model, were used to activate eight MUs, selected for being similar to that connected 'in vivo' to the motoneurone. As expected, for any given current slope the rising phase of isometric tension TT as steeper when units were motoneurone driven than when they were model driven. The gain (force slope/current slope) was plotted against the ramp slope to identity the cut-off slope, S(co), at which the gain was attenuated by -3 dB. In this homogeneous MU sample, the ratio expressing the advantage of the motoneurone drive (S(co)Cell/S(co)Mod, equivalent to the F(co) ratio), ranged from 2.62-2.97, values comparable with those observed in sine-wave experiments when the motoneurone and muscle units were properly matched.