Repetitive doublet firing in human motoneurons: evidence for interaction between common synaptic drive and plateau potential in natural motor control

Abstract

The firing behavior of spinal motoneurons (MNs) is a result of processing synaptic inputs by MN membrane properties, including plateau potentials, fundamentally explored in animals. However, there is much less data about a plateau potential role in human motor control. We explored human MN repetitive doublet firing during gentle isometric voluntary muscle contractions with the aim of revealing possible evidence for interaction between plateau potentials and common synaptic drive known as an important determinant of MN pool firing behavior. Single-motor unit (MU) repetitive firing of trapezius and triceps brachii was analyzed. Subjects were asked to recruit MUs capable of firing repetitive doublets. The analysis of interspike intervals (ISIs) of background firing of simultaneously recorded MUs showed that beyond doublet series ISIs varied, often in unison with significant correlation coefficients, demonstrating common synaptic drive. During doublet series, MUs showed persistent doublet ISIs (typically 4–7 ms) and a tendency to increase the number of doublets in series throughout the experiment. This was consistent with involvement of MN plateau potentials resulting in persistent delayed depolarization (underlying each doublet) and warm-up effect. Common synaptic drive “started” doublet series; probably both mechanisms controlled postdoublet ISIs. However, convincing effects of plateau potentials on MU firing behavior during single firing were not found. Thus our results suggest a plateau potential role in specifying the essential firing pattern, doubling, of some MUs rather than its effect on firing behavior of the MN pool, on the whole, during voluntary muscle contractions in humans. NEW & NOTEWORTHY Properties of human motoneuron repetitive doublet firing were explored during voluntary muscle contractions. It was shown for the first time that these properties seem to be consistent with properties of both plateau potentials, resulting in persistent delayed depolarization (underlying each doublet) and common synaptic drive, starting this unusual firing; both mechanisms could probably control postdoublet intervals. A convincing effect of plateau potentials on motoneuron single-spike firing, despite doublet firing, was not found.