Absence of lateral gastrocnemius activity and differential motor unit behavior in soleus and medial gastrocnemius during standing balance

Abstract

In a standing position, the vertical projection of the center of mass passes in front of the ankle, which requires active plantar-flexor torque from the triceps surae to maintain balance. We recorded motor unit (MU) activity in the medial (MG) and lateral (LG) gastrocnemius muscle and the soleus (SOL) in standing balance and voluntary isometric contractions to understand the effect of functional requirements and descending drive from different neural sources on motoneuron behavior. Single MU activity was recorded in seven subjects with wire electrodes in the triceps surae. Two 3-min standing balance trials and several ramp-and-hold contractions were performed. Lateral gastrocnemius MU activity was rarely observed in standing. The lowest thresholds for LG MUs in ramp contractions were 20-35 times higher than SOL and MG MUs (P < 0.001). Compared with MUs from the SOL, MG MUs were intermittently active (P < 0.001), had higher recruitment thresholds (P = 0.022), and greater firing rate variability (P < 0.001); this difference in firing rate variability was present in standing balance and isometric contractions. In SOL and MG MUs, both recruitment of new MUs (R(2) = 0.59-0.79, P < 0.01) and MU firing rates (R(2) = 0.05-0.40, P < 0.05) were associated with anterior-posterior and medio-lateral torque in standing. Our results suggest that the two heads of the gastrocnemius may operate in different ankle ranges with the larger MG being of primary importance when standing, likely due to its fascicle orientation. These differences in MU discharge behavior were independent of the type of descending neural drive, which points to a muscle-specific optimization of triceps surae motoneurons.

Keywords: human; motor units; standing balance; triceps surae.

Fig. 1.

Experimental setup and procedures. A: a total of 14 fine wire electrodes were inserted with ultrasound guidance in the triceps surae. Black dots indicate approximate site for each insertion. B: triceps surae motor unit (MU) activity was recorded during two 3-min standing balance trials. Subjects stood with their right foot on a forceplate from which vertical force, anterior-posterior (A-P) torque, and medio-lateral (M-L) torque were recorded. C: subjects were braced to a rigid board at the level of the chest and pelvis. MU activity was recorded during a series of ramp-and-hold isometric plantar flexion contractions at three different contraction intensities.

Fig. 2.

Example of motor unit activity from all three muscles during standing balance and ramp-and-hold trials. A: 60 s of standing balance data from five recordings from medial gastrocnemius (MG) and four from lateral gastrocnemius (LG), and three recordings from soleus (SOL) of one subject (top); A-P torque, M-L torque, and vertical force (bottom). Although there is clear MU on all MG and SOL recordings, there was absolutely no LG activity. B: data from the same subjects for a ramp-and-hold 90% maximum A-P torque trial. Although numerous MUs are recruited in MG and SOL in the early part of the ramped plantar-flexion contraction, LG MUs are recruited considerably later.

Fig. 3.

Recruitment thresholds of earliest recruited MUs in the triceps surae. The recruitment threshold of the first three MUs recorded on each recording with good quality signals were identified for MG, LG, and SOL. Recruitment thresholds for MG MUs were significantly higher than for SOL MUs. More dramatically, LG MUs had much higher recruitment thresholds than both MG and SOL MUs.

Fig. 4.

Example of MU activity during standing balance. Top: data from two recordings from MG and two recordings from SOL from one subject. Above each recording in the instantaneous discharge frequency of one decomposed MU for each recording. The superimposed templates of for each MU are plotted to the right of each recording. The horizontal line in each instantaneous discharge plot indicates 4 Hz. Bottom: A-P torque, M-L torque, and vertical force recorded during this 30 s period.

Fig. 5.

MG and SOL MU behavior during standing balance and ramp-and-hold trials. A: activation ratio results indicate that MUs from SOL were active much more consistently than those from MG during standing balance trials (sway). B: these results are in line with the higher recruited thresholds found for MG MUs during ramp-and-hold trials (braced). C: mean interspike intervals (ISI) were comparable between MG and SOL during standing balance trials. This was also the case for the ramp-and-hold trials. Overall, mean ISI was slightly higher during standing balance trials compared with the ramp-and-hold trials. D: the ISI coefficient of variation was slightly but significantly higher during standing balance trials compared with ramp-and-hold trials. The difference in ISI variability between MG and SOL MUs was marked and this for both standing balance and ramp-and-hold trials. *P < 0.05; **P < 0.001.

Fig. 6.

Relationship between MU discharge rates and kinetic variables during standing balance trials. A: forceplate data from both standing balance trials with A-P torque along the y-axis and vertical force along the x-axis (left); 2-dimensional heat maps for two MG and one SOL MU (three right panels). Motor unit discharge rates were separated into bins and averaged to create these plots. Discharge rates were much lower for the SOL MU, and all three MUs increased their discharge rate with increasing plantar flexor torque. The two MG MUs also increased their discharge rate with increasing vertical force. B: data from the same three MUs are replotted with M-L torque along the x-axis. C: results from the stepwise linear regression between MU discharge rate and A-P torque, M-L torque, and vertical force. Overall, A-P torque was retained in 70% of the regression models compared with 41% for M-L torque and 46% for vertical force, and R² values were significantly greater for SOL MU compared with MG MU. *P < 0.05.

Fig. 7.

Relationship between MU recruitment and kinetic variables during standing balance trials. Results of the linear regression between the overall number of active MG and SOL MUs across subjects and normalized to vertical force (A), A-P torque (B), and M-L torque (C). Kinetic variables were normalized to the minimum and maximum values produced during the standing balance trials and the count of active MU was determined in 10% bins. There was a moderate to strong linear relationship between the number of active MUs and A-P and M-L torque for both MG and SOL, whereas no relationship was present for vertical force.