Leg muscle activity during tandem stance and the control of body balance in the frontal plane

Abstract

Objectives

We investigated the pattern of activity of the tibialis anterior (TA), soleus (SOL) and peroneus longus (PER) muscles of both legs during tandem stance, in order to highlight their respective role in maintaining balance.

Methods

Twelve young healthy subjects were asked to stand with feet in line for successive 15 s-epochs, on a dynamometric platform with (EO) and without (EC) vision. EMG was recorded from the six muscles simultaneously. Collected signals were displacement of the centre of feet pressure (CoP) and EMG. Variables calculated for each recorded epoch were mean level, variability and distribution between legs of EMG, and cross-correlation between EMG and CoP traces and between EMG of homonymous muscles.

Results

CoP motion was larger along the medio–lateral (M–L) than antero–posterior (A–P) axis, and larger with EC than EO particularly in the M–L axis. Muscle activity was larger in the rear than in the front leg, as expected, except for PER. Activity increased with the increase in M–L CoP oscillations, except for SOL, which was tonically active, both legs, regardless of the amplitude of the oscillations. Manipulating vision had no effect on the variability of the EMG for equal mean levels of activity, for any muscle. Cross-correlation between EMG of rear leg muscles and M–L CoP sway gave higher coefficients for TA and PER than SOL, and appropriate time-delays between TA or PER and CoP motion, indicating a role of these muscles in the control of M–L sway. Except for the tonically active SOL, the homonymous muscles of the two legs were active out-of-phase, indicating a mutual push–pull action of the pairs. This was confirmed by the reciprocal activation of TA and PER of the same leg.

Conclusions

Overall, in spite of a large inter-trial and inter-subject variability, the neural command to the leg muscles during tandem stance implies a task-sharing rule, whereby SOL keeps the body upright while the reciprocal PER and TA activities produce the alternate impulses necessary for body stabilization in the frontal plane.

Significance

Knowledge of the normal mode of control of balance in frontal plane can foster new investigation in both posture and gait control, in addition to offering tools for understanding balance problems of elderly persons and patients at risk of fall.

Introduction

Standing with feet in line along the sagittal plane is a demanding posture, both because the medio–lateral limits of stability are narrow (Goodworth and Peterka, 2010) and because the effort for balance control elicits a meaningful metabolic energy demand (Houdijk et al., 2009). This posture is not natural, but it is often used during clinical balance evaluation in order to sharpen measures of balance in patients affected by various ailments, and predicts their capacity to withstand the risk of falling under critical conditions (Lord et al., 1999, Morris et al., 2000, Hile et al., 2012).

During an unstable balance condition like tandem stance, rapid integration of sensory input is crucial for motor control (Peterka, 2002, Sozzi et al., 2012), because the base of support diminishes considerably in medio–lateral direction, thereby increasing the likelihood for the centre of feet pressure (CoP) to reach a precarious position. Investigation of body motion during stance with narrow base width or during tandem stance, with or without vision, can highlight differences that cannot be seen when standing in normal stance (Sozzi et al., 2011), and is appropriate for getting insight into the neural mechanisms controlling medio–lateral stability (Day et al., 1993, Winter et al., 1996, Gatev et al., 1999, O’Connor and Kuo, 2009). Notwithstanding the widespread use of this procedure in both the laboratory and the clinic (see Hile et al., 2012), and in spite of early (Gantchev and Draganova, 1986, Schieppati et al., 1994) and recent research (Tanaka et al., 2007, Bingham et al., 2011) into the neuromuscular control of standing, little is known of the basic features of the spatio-temporal organization of the command for this tandem posture and, in general, of the balance control in the frontal plane. This is known to be degraded to some extent in elderly subjects, in which lateral instability and falls pose a serious challenge (Rogers and Mille, 2003, Nitz et al., 2003).

Contrary to detailed EMG, kinematic, reflex and modelling studies of the balancing strategy in the sagittal plane (see Saffer et al., 2008, Tokuno et al., 2009, Kiemel et al., 2011, Li et al., 2012), the interplay of the activity of the various leg muscles and its effects on the oscillation pattern of the standing body in the frontal plane have not been described during tandem stance, and little information exists on the distribution of the command to the muscles of each leg. While load-limb asymmetry may be present even under quiet stance (Anker et al., 2008), during tandem stance, the rear leg is surely more important than the front leg in supporting body weight (Kirby et al., 1987, Nichols et al., 1995, Jonsson et al., 2005, Wang and Newell, 2012). But it is not known whether it also contributes more to the control of the equilibrium or whether it leaves this role to the front leg. Moreover, it is not clear whether the brain commonly or separately exploits the homonymous muscles of the front and rear leg in order to maintain equilibrium, or else whether a mixed strategy exists. Further, there is the possibility that the muscle strategy differs when balance control relies on proprioception (without vision) with respect to proprioception and vision. In tandem stance, closing the eyes is more destabilising than during normal stance, feet parallel (Reynolds, 2010, Sozzi et al., 2011), necessarily enhancing the role of proprioception.

Therefore, we recorded the activity of three major postural leg muscles (tibialis anterior, TA; soleus, SOL; peroneus longus, PER) of both legs during tandem stance, and characterised the relationship between CoP and EMG. Our working hypothesis was that under tandem stance, where the support base is much wider along the sagittal than frontal plane, PER muscle plays the major role in the control of medio–lateral balance, owing to its functional invertor role. As a corollary, the PER muscles of the two legs should be active out of phase, since a simultaneous invertion of both feet in tandem stance would complicate stance, further reducing the width of the support base to a narrow strip along the frontal plane.