How motoneurones control velocity of tension development

Recently, Del Vecchio et al. (2019) presented an original method for extracting the activity of single motor units (MUs) from the mass EMG even during explosive contractions, thus offering a new instrument for studying the firing activity of motoneurones during human movement. With this technique, the authors analysed the factors that control the velocity of development of muscle tension, namely the recruitment of MUs and the firing frequency of motoneurones (MNs). Having analysed for many years (Baldissera & Parmiggiani, 1975; Baldissera & Campadelli, 1977) how single motoneurones control the velocity of tension development we could not help but observe that, when interpreting their results, those authors ignored all our published pertinent results and interpretations. Briefly, our experimental work demonstrated that the MN discharge transduces the two physical dimensions of the MN current input, the intensity and the velocity of rising, into a neural code in which none of the two parameters is directly detectable. However, a measure of both is simultaneously present, translated in the temporal dimension, as the instantaneous firing frequency f (1/interspike interval, ISI). In turn, muscle is able to decode the MN instantaneous frequency and generate a force time course that approximates, within a definite range, the time profile of the input commands to MNs. Concerning the double sensitivity of the MN encoder, analysis of the MN response to injection of ramp currents of different slope (Baldissera et al. 1979, 1982) reveals that MN initial firing pattern undergoes significant modifications linked to both the current intensity and the ramp slope. After a current step (maximal slope) the highest instantaneous frequency is reached by the first ISI; then follows a rapid frequency reduction, called ‘early adaptation’. During a ramp stimulus, instead, f progressively increases over the entire ramp. A straightforward calculation shows that each framp value is the sum of two components, f(i), proportional to the current intensity at that point of the ramp, and f(δi/δt), linearly linked to the ramp slope: framp = f(i) + f(δi/δt). Stimulation with sinusoidal currents (Baldissera et al. 1984) confirmed the simultaneous linear sensitivity of MNs to both the current intensity and its first time-derivative and showed that the in/out relation accurately fits the response of an ideal linear transducer sensitive to both the input intensity and velocity of change through two different proportionality constants: out(t) = K1in(t) + K2δin(t)/δt), thus allowing the encoder transfer function to be described. Well established results strongly suggest that this elaborated transduction, including ‘early adaptation’, is operated by the dynamics of the K+ conductance that produce the single MN after-hyperpolarization (AHP) and its summation during repetitive firing. In their discussion, Del Vecchio et al. state that ‘the present results show for the first time the strategies used by the central nervous system to achieve the maximal rate of force development’, in this way overlooking our (and others’) studies and interpretations on this topic. Also, when interpreting their results they quoted, implicitly accepting it, the hypothesis of Miles et al. (2005) that firing early adaptation is essentially due to inactivation of the fast inactivating Na+ conductance of the spike. In this regard, we want to reconfirm here that the ‘summation’ of the large and prolonged AHP refractoriness that produces adaptation in MN (Baldissera et al 1976, 1978) is indeed the unique mechanism that can generate the ‘right’ frequency code for transmitting to muscles the neural input of MNs, since it satisfies a basic principle of communication: the code generated by the transmitter (MNs) is only significant if it can be decoded by the receiver (muscle fibres). Why muscle is the natural decoder of MN firing is explained by the ingenious observations of Bakels & Kernell (1993) that, in each motor unit, the MN AHP and the single muscle twitch have about the same duration and time course. Thus, within each MU, the ‘clock’ (the AHP time course) that encodes the MN input current into f, is a replica of the ‘clock’ (the time course of the single muscle twitch) that decodes f into proportionate force levels. Also, the dynamics of the AHP summation and of the temporal accumulation of the twitch force are calibrated so that the high pass filter properties of MN transduction pre-compensate for the low-pass filter properties of the muscles ‘tetanic’ contraction, thus approximating the force temporal profile to the time course of the motor commands reaching the motoneurones (Baldissera et al. 1987, 1998). Let us return to the above-mentioned Miles’ hypothesis, which was formulated after evaluating the firing response of MNs obtained after blocking with apamin the gK channels that generate the AHP. Miles found that, in a MN deprived of the AHP by apamin, the range of the steady-state firing rate evoked by current steps extended from 1 to 80 Hz, being 3–4 times larger than the range ( 2 to 24 Hz), displayed by the same cell before applying the drug. Thus, apamin-treated MNs would generate, over a large part of their firing range, more than 90% of the maximal tetanic force. Since the physiological synaptic currents should have the same order of magnitude as the currents injected for defining the firing response in normal MNs, it follows that the increased excitability produced by AHP suppression makes the natural synaptic currents largely overcalibrated. A second negative effect of the AHP removal is the strong increase in the variability of the steady-state rhythmic discharge, which in turn will induce in muscle an irregular series of force oscillations – quite a bad approximation to a constant input. No information is given about the initial firing pattern nor on the transduction during transients. A simple control experiment, i.e. stimulation of single mouse MUs in vivo, by the discharges recorded in vitro (see Baldissera et al. 1998), would quickly disclose which of the two adaptation processes is essential for granting meaningful input–output relations in MUs. All this considered, knowledge of the notions supported by our results might provide a more comprehensive reference frame and open new perspectives to the future studies on MN activity in man.