The interesting and intriguing paper by Khan et al. (2016) investigated the changes of excitability in spinal motoneurones following both sustained voluntary contractions (with different intensities) and repetitive peripheral nerve electrical stimulations (with different frequency). The Authors made use of the F wave, that is the electromyographic counterpart of the recurrent discharge (Eccles, 1955), to assess these excitability changes.
They did not take into account, however, some limitations of the F‐wave test in monitoring the spinal motoneurones’ excitability, which have been reported, even recently, in the literature (Gogan et al. 1984; Hultborn & Nielsen, 1995; Espiritu et al. 2003; Burke, 2014; Balbi et al. 2014).
Prompted by the unexpected results Khan and colleagues found, and in the light of such F‐wave limitations, I will try to provide some further and alternative interpretations of their interesting and original data.
Firstly, when an antidromic wave is set in all the motor fibres of a peripheral nerve by means of a distal supramaximal stimulus, it is conducted without interruption to the initial segment of each motor axon. Depending on what happens at the junction between axonal initial segments and motoneurone somata, three distinct sets of neurones can be theoretically distinguished, in which (1) the antidromic action potential (AP) fails to invade the soma, (2) the antidromic AP invades the soma after a junctional delay able to start a recurrent discharge, and (3) the antidromic AP invades the soma but no recurrent discharge develops (too short a junctional delay). Among these three distinct sets, the second one is responsible for the F wave and accounts for about 2–5% of the entire motoneurone pool (Kimura, 2001). The relative proportions of these three sets of neurones, which are undetectable, depend on the biophysical features of single neurones and on the net sum of the excitatory and inhibitory inputs. In these conditions it is not always true that a reduced excitability throughout the motoneurone pool results in a smaller size of the second set (i.e. reduced amplitude or area, or persistence of the F wave), as initially expected by Khan and colleagues.
A reduced generalized (i.e. assumed equally distributed through the motoneurone pool) excitability, indeed, will shift some neurones from set 2 to set 1: in some neurones which formerly exhibited the recurrent discharge, the backfiring is now absent because the antidromic invasion of the soma does not any more occur. The same reduced excitability will shift some other neurones from set 3 to set 2: a prolongation of the junctional delay in neurones of set 3 happens, to the point that in some of them a recurrent discharge can develop. Paradoxically, if the second transition (from set 3 to set 2) is wider than (or equal to) the first one, an increase (or no modifications) of the F‐wave parameters will be detected in the presence of a reduced generalized excitability.
That is just what happens, in my opinion, with experiment 2 in the paper by Khan and colleagues, when a diffuse hyperpolarization is induced by the repetitive peripheral stimulation of the ulnar nerve, but no F‐wave depression develops. In fact, this finding can represent a direct experimental proof of the limited role of the F wave in unidirectionally detecting excitability changes of the motoneurone pool.
Secondly, the fraction of the motoneurone pool which is responsible of the F wave (representing only a minor portion of the entire motoneurone pool) and the one activated by the voluntary contraction are presumably two different and only partially overlapping sets of neurones. Therefore, it appears unlikely that the behaviour of a small (and in the interpretation above described, variable) set of spinal motoneurones can provide faithful information on the direction and amount of the excitability changes of the entire motoneurone pool.
The limitations of the F‐wave test here described show how a reliable method to directly detect the motoneurones’ excitability is still lacking, even though the present and past brilliant work by Khan and colleagues undoubtedly sheds light on the complex central mechanisms of voluntary motor control and on the correct interpretation of classical neurophysiological tests.
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Linked article This Letter to the Editor has a reply by Gandevia et al. To read this reply, visit http://dx.doi.org/10.1113/JP272663.
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