Delayed depolarization and firing behavior of human motoneurons during voluntary muscle contractions

INTRODUCTION The firing behavior of motoneurons is governed by the interaction between the intrinsic properties of motoneurons and the synaptic inputs that they receive. In particular, long-lasting afterhyperpolarization (AHP) following each motoneuron spike and thus decreasing motoneuron excitability immediately after spike was found to be a key mechanism in controlling of interspike interval (ISI) duration (Eccles et al., 1958; Kernell, 1965). As a result, motoneurons commonly fire single discharges at rather low firing rates, especially during gentle voluntary muscle contractions and postural tasks. However, some motoneurons, under conditions of weak synaptic drive, can fire double discharges (doublets) with very short intradoublet ISIs (up to a few ms). Each doublet is commonly followed by a prolonged post-doublet (interdoublet) ISI resulting from the AHP summation (Calvin and Schwindt, 1972). Two types of doublets have been observed: single and repetitive ones. Single doublets have been reported many times in cat and human motoneurons (e.g., Eccles and Hoff, 1932; Hoff and Grant, 1944; Denslow, 1948; Calvin and Schwindt, 1972; Kudina, 1974; Kudina and Churikova, 1990; Kirkwood and Munson, 1996; Piotrkiewicz et al., 2008; Stephenson and Maluf, 2010). Repetitive doublets have also been demonstrated in some of the reports above, but as a rule by the way; and only a few studies have directly addressed this topic (Bawa and Calancie, 1983; Kudina and Alexeeva, 1992; Kudina and Andreeva, 2010). However, a number of questions are still unanswered, in particular the question of whether there are certain muscles and (or) certain motoneurons for which repetitive doublet firing is likely to appear. This question will be taken up below based on an analysis of doublet firing in different limb and trunk muscles in healthy humans. With regard to the origin of this surprising firing, currently, the short delayed depolarization (DD) appearing as a “hump” on the falling phase of an action potential, preceding the AHP (Granit et al., 1963; Kernell, 1964; Nelson and Burke, 1967; Kernell, 2006) and thus shortly increasing MN excitability is widely accepted as the mechanism responsible for single doublets in cat (Calvin and Schwindt, 1972; Kirkwood and Munson, 1996; see also Kernell, 2006), and human motoneurons (Kudina, 1974; Bawa and Calancie, 1983; Kudina and Alexeeva, 1992; Bawa and Lemon, 1993; Garland and Griffin, 1999; Piotrkiewicz et al., 2008; Stephenson and Maluf, 2010). As to the origin of repetitive doublets, the question still remains open. At first sight, one could assume that they have the same underlying mechanism like single doublets. However, as known from findings by Granit et al. (1963) and Calvin (1975), in cat motoneurons, the hump-DD changes systematically during rhythmic firing evoked by intracellular depolarization, becoming smaller with each successive spike. Therefore, as may be expected, in firing motoneurons the DD can reach the threshold only occasionally and generate single doublets only. Consequently, it might be suggested that the DD alone can hardly play a pivotal role in producing repetitive doublets. In our recent studies (Kudina and Andreeva, 2010, 2013), we hypothesized that the mechanism underlying repetitive doublet firing in human motoneurons during voluntary muscle contraction is complex, including the hump-DD as the primary determinant that possibly becomes persistent due to a plateau potential probably activated in parallel with a common synaptic input. The assumption about a plateau potential role in repetitive doublet mechanisms was inferred from the comparison between essential characteristics of human motor unit (MU) repetitive doublet firing and properties of cat motoneuron firing in the presence of a plateau potential (e.g., Conway et al., 1988). If this assumption is true, then the question arises what are the DD characteristics which become persistent during repetitive doublet firing. The question will be considered below.