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Clinical Trial
. 2001 Jun 1;21(11):4059-65.
doi: 10.1523/JNEUROSCI.21-11-04059.2001.

Large involuntary forces consistent with plateau-like behavior of human motoneurons

D F Collins  1 , D Burke, S C Gandevia
Affiliations
Clinical Trial

Large involuntary forces consistent with plateau-like behavior of human motoneurons

D F Collins et al. J Neurosci. .

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 +/- 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.

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Figures

Fig. 1.
Fig. 1.
Forces during 100 Hz stimuli over the calf muscles in relaxed subjects. A, Force during a stimulation for 55 sec delivered at the threshold for motor axon stimulation for one subject. B, Force during a train lasting 60 sec delivered above motor threshold for one subject. Note the gradual increase in force to ∼30% MVC and the reduction in response to the test train after the prolonged stimulation. C, Mean responses (± SEM) to five stimulus trains of 7 sec duration in one subject before and during a complete anesthetic block of the tibial nerve. Error bars (shown at 0.5 sec intervals throughout the stimulation) are very small on the “nerve block” trace.
Fig. 2.
Fig. 2.
Responses to “triangular-shaped” changes in stimulus frequency for one subject before and during complete tibial nerve block. A, Responses to trains of increasing then decreasing frequency (between 10 and 100 Hz) over ∼20 sec. Thearrow marks the onset of the “extra” force.B, Corresponding force–frequency relationship.
Fig. 3.
Fig. 3.
Forces during control trains (25 Hz) and during trains with additional 100 Hz stimulation. A, Force responses from one subject to three successive stimulus trains.B, Superimposed responses (n = 10) to control (thin lines) and test trains (thick lines) for one subject. C, Average responses for seven subjects (mean ± SEM). Data expressed relative to the force 0.5 sec after stimulus onset in control trains.
Fig. 4.
Fig. 4.
Force and EMG activity during two successive stimulus trains of 25 Hz stimulus with a 100 Hz burst. Ashows the force and EMG activity (recorded with a monopolar recording electrode) before, during, and after the stimuli. Bshows the unitary activity at the four points (1–4) during the stimulation shown by the arrows in A. Note the change in gain. The data from point 4 encompass the last five stimulus pulses and the period immediately after that. Theinset at the bottom of Bshows the morphology of the spike highlighted by thearrows in traces 3 and 4(6 superimposed spikes, 3 during the stimulation and 3 after).
Fig. 5.
Fig. 5.
Recording from a subject during and after a train of increasing then decreasing frequency (between ∼4 and 100 Hz in 6 sec). Force continued to increase as the stimulus frequency declined, and sustained plantarflexion force and Sol EMG remained after stimulation. This persisted despite two brief efforts to dorsiflex the ankle but disappeared when the subject was asked to relax completely. EMG occurred in TA during the voluntary dorsiflexions but not when asked to relax completely. Stimulus artifacts have been truncated.
Fig. 6.
Fig. 6.
Recordings from a sleeping subject to a complex stimulus train that included repeated bursts of 100 Hz stimulation followed by a decline in frequency. Force did not decline smoothly during the slow reduction in frequency and residual force developed after the train (accompanied by EMG in Sol and MG and LG, but not TA). Stimulus artifacts have been truncated. Instantaneous discharge rate of a single motor unit in soleus is shown.
Fig. 7.
Fig. 7.
Recordings from two patients with spinal cord injury (mean ± SEM, n = 5). A,Data from one subject with a complete spinal cord lesion at T12. Forces during trains of stimuli with 2 sec at 25 Hz, 2 sec at 100 Hz, and then 3 sec at 25 Hz. For the control sequence stimulus rate was constant at 25 Hz. B, Data from a subject with an incomplete lesion at T8. Force response to the triangular pattern of stimulation. Maximal voluntary plantarflexion force was <10% predicted for healthy subjects.
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