Disturbances of motor unit rate modulation are prevalent in muscles of spastic-paretic stroke survivors

Abstract

Mottram CJ, Heckman CJ, Powers RK, Rymer WZ, Suresh NL. Disturbances of motor unit rate modulation are prevalent in muscles of spastic-paretic stroke survivors. J Neurophysiol 111: 2017-2028, 2014. First published February 26, 2014 doi:10.1152/jn.00389.2013.-Stroke survivors often exhibit abnormally low motor unit firing rates during voluntary muscle activation. Our purpose was to assess the prevalence of saturation in motor unit firing rates in the spastic-paretic biceps brachii muscle of stroke survivors. To achieve this objective, we recorded the incidence and duration of impaired lower-and higherthreshold motor unit firing rate modulation in spastic-paretic, contralateral, and healthy control muscle during increases in isometric force generated by the elbow flexor muscles. Impaired firing was considered to have occurred when firing rate became constant (i.e., saturated), despite increasing force. The duration of impaired firing rate modulation in the lower-threshold unit was longer for spasticparetic (3.9 Ϯ 2.2 s) than for contralateral (1.4 Ϯ 0.9 s; P Ͻ 0.001) and control (1.1 Ϯ 1.0 s; P ϭ 0.005) muscles. The duration of impaired firing rate modulation in the higher-threshold unit was also longer for the spastic-paretic (1.7 Ϯ 1.6 s) than contralateral (0.3 Ϯ 0.3 s; P ϭ 0.007) and control (0.1 Ϯ 0.2 s; P ϭ 0.009) muscles. This impaired firing rate of the lower-threshold unit arose, despite an increase in the overall descending command, as shown by the recruitment of the higher-threshold unit during the time that the lower-threshold unit was saturating, and by the continuous increase in averages of the rectified EMG of the biceps brachii muscle throughout the rising phase of the contraction. These results suggest that impairments in firing rate modulation are prevalent in motor units of spastic-paretic muscle, even when the overall descending command to the muscle is increasing.

Distinguishing intrinsic from extrinsic factors underlying firing rate saturation in human motor units

“…For most units recorded, firing rate initially increased steeply as a function of force and then leveled off (i.e., saturated) at relatively low rates, usually Ͻ20 imp/s. This result is qualitatively similar to that described previously by other investigators for biceps (Mottram et al 2009(Mottram et al , 2014 and in a variety of other human muscles (rectus abdominis, latissiumus dorsi, pectoralis major, triceps, and brachioradialis, Bracchi et al 1966;genioglossus, Bailey et al 2007;vastus lateralis, De Luca and Contessa 2012;deltoid, De Luca et al 1982; soleus and tibialis anterior, Kiehn and Eken 1997;medial gastrocnemius, McGill et al 2005; extensor digitorum, Monster and Chan 1977; first dorsal interosseus, Moritz et al 2005; rectus femoris, Person and Kudina 1972). We have also shown in this work that augmenting descending excitatory drive to biceps MNs with peripheral excitation mediated by tendon vibration had little effect on the discharge of MUs that were firing at saturation frequencies but robustly increased firing rates of the same units when active at lower frequencies.…”

“…This value is nearly identical to that (15.2 imp/s) reported for biceps MUs in healthy control subjects by Mottram et al (2014). There was no significant (P ϭ 0.53) relation Black traces indicate MUs (n ϭ 123) whose firing rate-force data were significantly better fit by a rising exponential function (Eq.…”

“…1A). Nevertheless, such intriguing asymmetry in firing rate modulation has been noted previously (e.g., Mottram et al 2014) and warrants dedicated further investigation. Figure 2 shows an example recording in which the activities of two units were clearly discernable during the ramp contraction.…”

“…Specifically, firing rate increases only modestly over a relatively narrow range of isometric force beyond which little further increase in firing rate is seen (Bailey et al 2007;Bracchi et al 1966;De Luca and Contessa 2012;De Luca et al 1982;Kiehn and Eken 1997;McGill et al 2005;Monster and Chan 1977;Moritz et al 2005;Mottram et al 2009Mottram et al , 2014Person and Kudina 1972). Such saturation of firing rate with maximum rates often Ͻ20 impulses/s (imp/s) in response to presumed increases in synaptic drive is in contrast to that observed with intracellular current injection during which, for example, cat hindlimb MNs increase firing rates linearly up to high levels (usually Ͼ50 imp/s, occasionally Ͼ100 imp/s) with increased current (Granit et al 1966;Kernell 1965;Schwindt and Calvin 1972;Schwindt and Crill 1982).…”

Submovements during reaching movements after stroke

“…A recent study has shown that, in addition to the enhanced reflex response at rest, the spastic-paretic muscle shows impaired rate modulation during voluntary movements that could result from higher levels of proportional inhibition or the disruption of signals coming from the corticospinal tracts. 15 Moreover, it has been shown that SS without sensory deficits might maintain intact their ability to plan the movement while the execution of the movement is strongly affected by altered stiffness and damping values. 16 Therefore, spasticity might also play a role in the emergence of type 2 submovements since SS that had increased incidence of type 2 submovements had also higher MAS scores.…”