Research ReportAntagonist muscle co-activation during straight walking and its relation to kinematics: Insight from young, elderly and Parkinson's disease
Highlights
► Parkinson disease and aging lead to loss of balance. ► Antagonist muscle co-activation has been suggested to be an adaptative process aimed to allow stabilization around a join. ► The co-activation index (CAI) seems to increase when the gait is faster. ► We analyzed the CAI and gait kinematics of healthy subjects and parkinsonian patients. ► We used Multiple Linear Regression models to study the relation between CAI, velocity and cadence.
Introduction
Muscle co-activation has been studied for a better understanding of motor control of gait. From a theoretical point of view it seems that antagonist muscles in the lower limb should be activated sequentially, avoiding interference in their functions. However it is not clear whether this pattern represents the actual sequence of activation, even in healthy humans. In fact, an increase in antagonist co-activation in the shank and thigh muscles, as a function of the gait velocity, has been reported (Hortobágyi et al., 2009, Schmitz et al., 2009). This suggests an adaptive process aimed at allowing greater stabilization around the joint (Peterson and Martin, 2010, Schmitz et al., 2009). This seems to be supported by the fact that aging can lead to loss of balance (Woollacott, 1993) and stability in gait (Hausdorff, 2007, Hausdorff et al., 2001). Therefore, the larger amount of co-activation displayed by the elderly for a given velocity might contribute to further increase the stability. However, this explanation has been recently challenged since the relationship between aging and increased co-activation of antagonist calf muscles has not been confirmed (Peterson and Martin, 2010). Insight on the role of antagonist muscle co-activation in gait can be gained by evaluating other populations with postural instability, such as people suffering from Parkinson's disease, but very few studies have evaluated this feature in PD during gait (Dietz et al., 1995).
Experiments investigating EMG activity during gait in PD have provided intriguing results. In this case, co-activation in PD seems to follow a different pattern to the one mentioned before, and a reduction in the co-activation index while increasing velocity has been reported (it has also been obtained in healthy subjects when walking on a treadmill, Dietz et al., 1995). Interestingly, the study also indicated greater co-activation in the patient than in the healthy group for a given velocity, probably reflecting the above mentioned strategy to increase stability around the joint. It seems that a better understanding on the role of co-activation in gait in these two populations may be obtained by further analyzing different sub-types of subjects, for instance PD with freezing of gait (FOG). EMG analysis from patients suffering FOG revealed an alteration in the timing of discharge of antagonist muscles, tibialis anterior (TA) and gastrocnemius (GA), in the strides prior to the FOG episode (Nieuwboer et al., 2004).
On the other hand, we reasoned that the evaluation of antagonist co-activation can be better achieved employing several variables instead of using only gait velocity. Velocity is just a relation between step/stride cadence and step/stride length which means that a given velocity can be obtained with a whole range of cadence/step length patterns, and so questioning if the co-activation index can be a useful parameter to characterize a given physiological or pathological gait pattern, if only related to one gait variable.
This study is aimed to characterize the co-activation index in gait by examining its relationship to gait velocity and step cadence. We have evaluated different patterns of gait: physiological gait (young and elderly subjects), and pathological gait (advanced PD during ON-dose, and OFF-dose; with and without FOG). The group of patients, with marked postural instability during gait, was included because increasing CAI seems an adaptive process to gain joint stability while walking (Peterson and Martin, 2010, Schmitz et al., 2009). Subjects were asked to walk in synchrony to a metronome beat. This approach has been useful to modulate a whole range of velocities, step lengths, and step cadences in a previous study (Arias and Cudeiro, 2008).
Section snippets
Characterization
Trochanteral height was comparable across groups, F(2,44) = 0.376 p = 0.689; there was however a main effect of age when comparing the groups F(2,44) = 132.825 p < 0.001; as expected post-hoc analysis showed that age of Young Control was significantly lower than that of Elderly and PD (p < 0.001 in both cases); but Elderly Controls and PD were comparable in age (p = 0.449). During preferred walking, CAI for the Young Controls was 0.32 ± 0.04 (mean ± SD), for the Elderly Controls was 0.41 ± 0.06 and for the PD − FOG
Discussion
This works shows that antagonist muscle co-activation of TI and SO during straight gait patterns in different sets of subjects, displaying physiological (young and elderly) and pathological (parkinsonian) gait, presents high variability, not successfully explained by kinematics.
The analysis of antagonist CAI during gait has been chiefly focused on the study of physiological aging (Hortobágyi et al., 2009, Peterson and Martin, 2010, Schmitz et al., 2009) and on some pathologies like stroke (
Subjects
47 subjects were recruited for this study; 7 young; 20 elderly; 20 PD in stages III–IV of the Hoehn and Yahr scale (Hoehn and Yahr, 1967). Subjects presented lack of un-correctable auditory–visual impairment, lack of musculoskeletal injury, and scored > 24 points in Mini Mental Examination Score (Folstein et al., 1975) when checking cognitive impairment.
Acknowledgments
This work was supported by Xunta de Galicia (Conselleria de Educación-2007/000140-0 and Dirección Xeral de I+D+i; 2010–2012), Spain. We are thankful to the Asociación Parkinson Galicia. We are indebted to Dr Kenneth L. Grieve for his helpful advice and corrections in the manuscript.
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