Unilateral balance training enhances neuromuscular reactions to perturbations in the trained and contralateral limb

TL;DR: The results suggest that concomitant with improved balance recovery and neuromuscular reactions in TR, there is also a cross-education effect in UTR, which might be predominantly related to supraspinal adaptations shared between interconnected structures in the brain.

About: This article is published in Gait & Posture.The article was published on 2013-09-01 and is currently open access. It has received 37 citations till now. The article focuses on the topics: Cross education.

Summary

1. Introduction

• The ability of reacting to unexpected perturbations to balance relies on the interaction between reflexes (modulated by spinal and supraspinal pathways), automatic responses and voluntary responses [1,2].
• These mechanisms have essential implications for avoiding falls and assuring safe locomotion during daily life.
• This phenomenon has been extensively described in the literature concerning strength and resistance training [16,17], in which the untrained limb also shows positive gains in strength elicited by training stimuli.
• Understanding cross-education from balance training may have significant implications in neurophysiology and sports medicine.
• The main hypothesis was that balance training could enhance balance recovery from unexpected perturbations for the trained leg and also for the untrained leg.

2.1. Subjects

• Twenty-three healthy men volunteered for the experiment.
• All subjects were right-dominant as determined by a kicking test.
• Exclusion criteria included history of knee or ankle ligament injury, current lower-extremity injury, recent (within six months) low back injury, or vestibular dysfunction.
• All subjects provided written informed consent before participation and the procedures were approved by the ethical committee of Northern Jutland (N-20100042).

2.2. Experimental setup

• Pre-training and post-training measurements consisted of single-leg stance perturbations to balance.
• Both left and right limbs were tested in a random order in TG, in one single session while for CG only the right limb was tested (Fig. 1).
• The free leg had to be elevated at least 5 cm above the platform while the hands were kept akimbo.
• The target perturbation was the forward displacement, however, perturbations backward were included to assure unpredictability but were not analyzed.
• Subjects of the control group were asked to maintain normal daily life activities during the 6- week training program in between the two measurements.

2.3. Kinetics

• A three-dimensional force platform (AMTI, OR6-5, Watertown, MA) mounted to a hydraulic system [20] provided perturbation stimuli and simultaneous measures of vertical (Fz), anterior–posterior (Fy) and medial–lateral (Fx) ground reaction forces and moments (Mx, My and Mz).
• Custom-made software (MrKick II, Aalborg University, Aalborg, Denmark) was used for force recordings (1024 Hz).
• Signals were digitally low-pass filtered with a 4th order zero-lag Butterworth filter (8 Hz cut-off).
• A series of identical platform movements (the same delivered during the experiment) were recorded with no loads over it, in order to determine the forces and moments generated only by moving the device.
• Subsequently, these inertial forces and moments were subtracted from the real forces and moments used to determine the CoP.

2.4. Electromyography

• Surface EMG signals were recorded in bipolar configuration with pairs of Ag/AgCl electrodes (Ambu Neuroline 720 01-K/12; Ambu, Ballerup, Denmark) with 22 mm of center-to-center spacing.
• A reference electrode was placed at the right wrist.
• The EMG signals of the right limb were recorded from tibialis anterior (TA), rectus femoris (RF), vastus lateralis (VL) and biceps femoris (BF) according to Hermens et al. [21].
• EMG signals were synchronized to the ground reaction force by the trigger signal to the perturbation onset.

2.5. CoP analysis

• CoP data were analyzed for each trial from the perturbation onset to 1000 ms after it, a period in which it is possible to regain stability after a similar perturbation on both trained and untrained legs, whereas subjects from the control e that elicited backward displacement of the center of mass (10 cm translation).
• (B) set, as well as burst duration and other variables were calculated before (gray) and EO: eyes open; EC: eyes closed; reps: repetition; low difficulty: the ball was catch only in front of the subject; high difficulty: the ball was catch closely or far away from the trunk, on the sides, below the knee height or above the head height.
• The following variables were analyzed to evaluate postural balance: CoP maximal excursion length defined as the distance covered within 1000 ms.
• CoP speed defined as the average speed of the CP during the recovery period.
• CPLEN and CPSPD were calculated for both AP and ML directions.

2.6. EMG analysis

• EMG signals were band-pass filtered (2nd order, zero-phase-lag Butterworth, 20–500 Hz), full-wave rectified, and smoothed (15 Hz low-pass, 4th order, zerophase-lag Butterworth).
• Temporal aspects of EMG responses to the postural perturbation were assessed by the EMG onset , burst duration , burst magnitude and time to peak EMG .
• The EMGON for each muscle was determined as the instant in time where the amplitude surpassed two standard deviations from baseline [23].
• EMGDUR was defined as the time where EMG activity remained above the onset level within the first second after perturbations.
• In addition, EMG approximate entropy was calculated.

2.7. Statistical analysis

• A 2-way repeated measures analysis of variance (RM-ANOVA) was used to analyze all CoP and EMG parameters.
• The first factor was the tested leg with three levels (TG right leg [trained leg, TR], TG left leg [untrained leg, UTR] and CG right leg [control leg, CTR]).
• The second factor was time with two levels (pre-training and post-training).
• The Tukey LSD test was used for post hoc analysis when necessary.
• The data are presented as mean and standard deviation (SD).

3.1. Center of pressure

• No legs time interaction was observed for any CoP measurements (p > 0.05).
• In addition, no training effects for CPLEN on both anterior–posterior and medial–lateral components were found as rior–posterior (AP) and medial–lateral (ML) directions.
• CoP measurements were l group was tested only the right leg before training (gray bars) and after < 0.05).
• Y denotes significant difference in relation to untrained and control legs well as the medial–lateral CPSPD for TR, UTR and CTR legs (Fig. 2).
• On the other hand, anterior–posterior CPSPD was reduced after training for TR ( 35%, training effect p < 0.01), whereas for UTR and CTR the percental changes were 6% and 8%, respectively.

3.2. Electromyography

• Burst magnitude was increased for TA and reduced for BF after training only for TR (p < 0.05, Table 2), with no changes for UTR and CTR legs.
• In addition, TA, RF and BF muscles had a reduced EMGTP before training for the UTR (p < 0.05).
• After training, EMGTP was similar among limbs (Table 2) and EMGENT showed no training effects for TR, UTR and CTR.
• Opposedly, UTR showed higher EMGENT in comparison to TR and CTR before and after training (p < 0.05, Table 2).

4. Discussion

• This study aimed at verifying whether unilateral balance training would improve balance recovery after forward perturbations in the rectus femoris (RF), vastus lateralis (VL) and biceps femoris (BF) muscles.
• Y denotes significant difference in relation to untrained and EMG measurements were conducted for the trained leg (TR) and untrained leg (UTR) for the trained subjects, whereas the control group was tested only the right leg (CTR) before training (pre) and after training (post).
• Therefore, further investigations are needed in order to explain neurophysiologic mechanisms of adaptation following balance training.
• Improved initial ankle position and higher preactivation may both enhance TA responses to perturbation [33].
• In practical terms, the results of the present investigation suggest that neuromuscular properties of postural responses can be enhanced by a cross-education mechanism.

Figures

Table 1 Balance training protocol and progression.

Fig. 2. Mean (SD) center of pressure (CoP) total length and average speed in the ante conducted for the trained and untrained leg for the trained subjects, whereas the contro training (black bars). * denotes a significant difference in relation to post-training (p (p < 0.05).

Table 2 Mean (SD) burst magnitude, EMG time to peak and approximate entropy extracted from tibialis anterior (TA), rectus femoris (RF), vastus lateralis (VL) and biceps femoris (BF) muscles.

Fig. 1. Illustrative experimental design. (A) Subjects from the training group were tested group were tested only in the dominant leg. The test consisted in perturbations to balanc Surface electromyography was recorded from the perturbations and the perturbation on after balance training (black).

Fig. 3. Mean (SD) EMG onsets and EMG burst magnitude for tibialis anterior (TA), measurements were conducted for the trained leg (TR) and untrained leg (UTR) for the tr training (pre) and after training (post). * denotes a significant difference in relation to p control legs (p < 0.05).

Frequently asked questions

Q1. What are the contributions mentioned in the paper "Unilateral balance training enhances neuromuscular reactions to perturbations in the trained and contralateral limb" ?

The aim of this study was to investigate the effect of unilateral balance training on the reactive recovery of balance for both trained and untrained limbs. Furthermore, the EMGTP of UTR was predominantly greater before training ( 17 ms, p < 0. 05 ). These results suggest that concomitant with improved balance recovery and neuromuscular reactions in TR, there is also a cross-education effect in UTR, which might be predominantly related to supraspinal adaptations shared between interconnected structures in the brain. 

Q2. What are the future works mentioned in the paper "Unilateral balance training enhances neuromuscular reactions to perturbations in the trained and contralateral limb" ?

Other adaptations such as improved attention and confidence due to training might also elicit adaptations to UTR, therefore further studies must be conducted in order to clarify the underlying mechanisms related to cross-education on balance training. It is not possible yet to determine whether injured patients can benefit from this cross-education effect, which could be confirmed by further studies involving injured patients. In practical terms, the results of the present investigation suggest that neuromuscular properties of postural responses can be enhanced by a cross-education mechanism. This suggests that balance training facilitates postural reactions when perturbations occur. 

Q3. What is the main mechanism to elicit cross-education after balance training?

Since interhemispheric connections might induce contralateral adaptations [15], the authors may suggest that supraspinal adaptation could be the primary mechanism to elicitcross-education following balance training. 

Q4. What is the effect of balance training on the body?

Balance training has been effective in altering muscular reaction time (or muscle/electromyographic (EMG) onsets) to perturbations [8,10–13], improved joint positioning sense, hamstring/quadriceps ratio and joint stiffness [10,11], as well as postural sway while standing on a force platform [8,14]. 

Q5. What is the role of reflexes in balance training?

The ability of reacting to unexpected perturbations to balance relies on the interaction between reflexes (modulated by spinal and supraspinal pathways), automatic responses and voluntary responses [1,2]. 

Q6. How long did the free leg rest after the perturbations?

After habituation, 12 perturbations forward and 12 perturbations backwards were delivered in random order, with a rest interval of 10–15 s between them. 

Q7. What is the role of BF in the stance recovery?

BF may act knee flexor and hip extensor, this muscle is essential for hip stability, therefore a reduced BF EMG might indicate adaptations in the agonist/antagonist relationship, since there was also reduced RF EMG (not significant). 

Q8. What is the effect of balance training on the BF muscle?

Reduced EMG magnitude is generally found after balance training [4,6], which might be related to the simplification of the motor task by learning it [6]. 

Q9. What is the effect of a simple device on the lower limb?

The use of simple devices such as wobble boards (also called ankle discs) for training purposes may reduce the injury incidence in athletes by* 

Q10. What is the main effect of the training on the neuromuscular properties of the injured leg?

In summary, unilateral balance training over six weeks was effective in improving neuromuscular reactions to perturbations during single-leg stance for the trained leg and to a lesser extent for the untrained leg. 

Q11. What is the meaning of the term "Complexity extracted from emg signals"?

The complexity extracted fromEMG signals is used in order to better understand neural strategies to recover balance, since highly complex EMG may suggest healthier system and/or more adaptable to environmental changes [25,26], favoring performance. 

Q12. What is the effect of balance training on the sway patterns?

the proposed balance training protocol induced reduction in the CoPSPD in the anterior–posterior direction, which indicates an enhanced ability to recover balance. 

Q13. What is the effect of training on balance?

these balance skills might be stimulated by a cross-education effect, leading to reduced balance loss in cases of unilateral lower limb injury. 

Q14. What is the main effect of the study on the neuromuscular properties of the untrained?

In practical terms, the results of the present investigation suggest that neuromuscular properties of postural responses can be enhanced by a cross-education mechanism. 

Q15. What was the gain of the EMG signals?

The EMG signals were amplified with a gain of 2000 (EMG-USB, LISiN; OT Bioelettronica, Turin, Italy), A/D converted (12 bit), sampled at 2048 Hz and band-pass filtered (second-order Butterworth, 10–500 Hz). 

Q16. What is the effect of balance training on the lower extremities?

Despite the fact that balance can be trained for both lower extremities, it remains to be shown whether adaptations to unilateral balance training can be transferred to the untrained limb by a cross-education effect [15]. 

Q17. What is the effect of balance training on the lower limb?

This phenomenon has been extensively described in the literature concerning strength and resistance training [16,17], in which the untrained limb also shows positive gains in strength elicited by training stimuli. 

Q18. How did the authors determine the positive adaptations from training?

The authors have hypothesized that the positive adaptations from training could be also identified by an increased complexity in the EMG signals, measured by EMGENT. 

Q19. What was the effect of training on the anterior and posterior CPSPD?

On the other hand, anterior–posterior CPSPD was reduced after training for TR ( 35%, training effect p < 0.01), whereas for UTR and CTR the percental changes were 6% and 8%, respectively. 

Q20. What were the effects of cross-education on the limb?

In the present investigation, cross-education effects were predominantly limited to neuromuscular properties (muscular onsets, magnitudes).