Large Involuntary Forces Consistent with Plateau-Like Behavior of Human Motoneurons

Abstract

When electrical stimulation is applied over human muscle, the evoked force is generally considered to be of peripheral origin. However, in relaxed humans, stimulation (1 msec pulses, 100 Hz) over the muscles that plantarflex the ankle produced more than five times more force than could be accounted for by peripheral properties. This additional force was superimposed on the direct response to motor axon stimulation, produced up to 40% of the force generated during a maximal voluntary contraction, and was abolished during anesthesia of the tibial nerve proximal to the stimulation site. It therefore must have resulted from the activation of motoneurons within the spinal cord. The additional force could be initiated by stimulation of low-threshold afferents, distorted the classical relationship between force and stimulus frequency, and often outlasted the stimulation. The mean firing rate of 27 soleus motor units recorded during the sustained involuntary activity after the stimulation was 5.8 Ϯ 0.2 Hz. The additional force increments were not attributable to voluntary intervention because they were present in three sleeping subjects and in two subjects with lesions of the thoracic spinal cord. The phenomenon is consistent with activation of plateau potentials within motoneurons and, if so, the present findings imply that plateau potentials can make a large contribution to forces produced by the human nervous system.

High-frequency submaximal stimulation over muscle evokes centrally generated forces in human upper limb skeletal muscles

“…The patterns of stimulation were similar to those used in previous studies (1,8,9,41). In the first pattern, there was a 3-s "100-Hz burst" in a 7-s stimulation train.…”

“…In fact, the development of extra torques was similar for the biceps and FPL despite their different Ia monosynaptic connectivity. Furthermore, the enhanced torques had similar profiles to those in lower limb muscles (8,9,33) and wrist flexors (1). The extra torque development in FPL shows that strong Ia monosynaptic projections are not required for the development of enhanced force of central origin (see Ref.…”

“…High-frequency trains have been hypothesized to trigger enhanced force of central origin through the activation of motoneuron plateau potentials by positive feedback of Ia afferents on the motoneurons. This mechanism has been postulated because the phenomenon can be abolished in the lower limb by proximal nerve block (8,9). However, the most compelling evidence of the likely involvement of motoneuron plateau potentials during high-frequency trains comes from the presence of extra torque observed in the lower limb muscles of some patients with clinically complete spinal cord injury at the thoracic level (41).…”

“…One technique frequently used to elicit sustained muscle contractions in humans is through high-frequency trains of electrical stimuli (1,8,9,33,41). High-frequency (100-Hz) burst of electrical stimulation can reliably induce enhanced contractions in lower limb muscles of able-bodied and some spinal cord-injured subjects (9,41).…”

Beginning at the end: Repetitive firing properties in the final common pathway

“…Studies have also been undertaken on humans, with an emphasis on recording the discharge of single motor units (e.g., Kiehn and Eken, 1997). In selected instances, the data have suggested that plateau potentials are involved in the observed firing patterns (Eken and Kiehn, 1989;Kiehn and Eken, 1997;Gorassini et al, 1999Gorassini et al, , 2000Collins et al, 2001Collins et al, , 2002aWalton et al, 2002). To study the mechanisms (i.e., PICs and their modulation) underlying repetitive firing during behavior, however, it is necessary to use intracellular recording techniques.…”