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Comparative Study
, 564 (Pt 1), 295-311

Human Postural Sway Results From Frequent, Ballistic Bias Impulses by Soleus and Gastrocnemius

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Comparative Study

Human Postural Sway Results From Frequent, Ballistic Bias Impulses by Soleus and Gastrocnemius

Ian D Loram et al. J Physiol.

Abstract

It has been widely assumed for nearly a century, that postural muscles operate in a spring-like manner and that muscle length signals joint angle (the mechano-reflex mechanism). Here we employ automated analysis of ultrasound images to resolve calf muscle (soleus and gastrocnemius) length changes as small as 10 mum in standing subjects. Previously, we have used balancing of a real inverted pendulum to make predictions about human standing. Here we test and confirm these predictions on 10 subjects standing quietly. We show that on average the calf muscles are actively adjusted 2.6 times per second and 2.8 times per unidirectional sway of the body centre of mass (CoM). These alternating, small (30-300 microm) movements provide impulsive, ballistic regulation of CoM movement. The timing and pattern of these adjustments are consistent with multisensory integration of all information regarding motion of the CoM, pattern recognition, prediction and planning using internal models and are not consistent with control solely by local reflexes. Because the system is unstable, errors in stabilization provide a perturbation which grows into a sway which has to be reacted to and corrected. Sagittal sway results from this impulsive control of calf muscle activity rather than internal sources (e.g. the heart, breathing). This process is quite unlike the mechano-reflex paradigm. We suggest that standing is a skilled, trial and error activity that improves with experience and is automated (possibly by the cerebellum). These results complement and extend our recent demonstration that paradoxical muscle movements are the norm in human standing.

Figures

Figure 1
Figure 1. The dynamic bias model
The body is represented by an inverted pendulum with its centre of mass (CoM) indicated. The gastrocnemius and soleus muscles together are represented by the contractile element (CE). These muscles act through a spring-like element which connects them to the ground through the foot. The total stiffness of this elastic link is represented by K. The system operates by dynamically altering the length of the CE thus altering the position of one end of K. We refer to the length of the CE as the bias of the spring. In angular terms, the length of the spring is given by the angle of the CoM relative to the vertical (θ) minus the length of the bias (θ0). Ankle torque is then given by T = K(θ−θ0). All quantities are expressed in angular terms.
Figure 2
Figure 2. The bandwidth of postural control
A, shows the coherence between the CoM angle and muscle length (continuous line) and between CoM angle and EMG activity (•–•). Both soleus and gastrocnemius muscles have been averaged together for muscle length and EMG activity. B, shows the coherence between soleus EMG and gastrocnemius EMG activity (continuous line) and between soleus muscle length and gastrocnemius muscle length (•–•). In both A and B the lines represent the combined average of 10 subjects. The dashed lines represent 95% confidence intervals in the mean values. Muscle length was sampled at 25 Hz and thus the frequency range shown is 0–12.5 Hz. A coherence of one means that the two signals are perfectly phase locked at that frequency. A coherence of zero means that at that frequency, sinusoids in one signal are initiated and terminated entirely randomly with respect to the other signal.
Figure 3
Figure 3. CoM sway and bias movements
A, shows the velocity power spectrum of CoM angle (continuous line) and muscle length (•–•). The power spectra are calculated relative to their maximal values. Muscle length is the average of soleus and gastrocnemius which were very similar across the range shown. The lines represent the combined average of 10 subjects. The dashed lines represent 95% confidence intervals in the mean values. For all 10 subjects, mean values plotted against SEC stiffness are shown for sway size (B), bias movement size (C), sway duration (D) and bias movement duration (E). The filled circles are a mean of the three eyes open trials and the crosses are a mean of three eyes closed trials. A sway is defined as a unidirectional movement of the CoM. A bias movement is defined as a unidirectional change in muscle length. Relative stiffness is defined as the stiffness of the SEC divided by the load stiffness of the human inverted pendulum and has been calculated by the cross correlation between CoM angle and muscle length, averaged for soleus and gastrocnemius muscles (Loram et al. 2005). The mean range and standard deviation of the relative stiffness for an individual subject are 0.35 and 0.14, respectively.
Figure 4
Figure 4. Locating micro falls and bias reversals
Time records are shown for a representative subject of CoM angle (A), CoM velocity (B), acceleration (C) and soleus (dashed line) and gastrocnemius (continuous line) muscle length (D). The asterisks identify micro falls when the CoM speed rises to a maximum value while the subject is swaying forwards. All values are shown relative to a mean of zero. Positive angle, velocity and acceleration are forwards, away from the vertical. Positive changes in muscle length indicate lengthening. All quantities are expressed relative to their mean value.
Figure 5
Figure 5. Averaged bias reversals – variation with subject
For each subject, all cases of bias reversals from six trials have been averaged. An average n= 297 events per subject for six trials. Time zero represents the averaging point which is the local minimum in muscle length. A, shows CoM velocity. B and C, show gastrocnemius and soleus muscle length, respectively. Velocity, angle and muscle length all increase positively. The marker lines, a and b, indicate the beginning and end of the impulse. The continuous lines indicate subjects with a SEC stiffness greater than 100%. All quantities are expressed relative to their mean value.
Figure 6
Figure 6. Averaged bias reversals
For each subject, all cases of bias reversals from six trials have been averaged. The time-locked patterns from all 10 subjects have been averaged to produce this Figure which incorporates 2870 and 2867 events for the minima and maxima, respectively. AD, show muscle length minima. EH, show muscle maxima. Time zero represents the averaging point. Velocity and muscle length increase positively and are expressed relative to their mean value. A, CoM velocity; B, gastrocnemius (continuous line) and soleus (dashed line) muscle length; C, soleus, rectified EMG signal; D, gastrocnemius, rectified EMG signal. EH, as in A to D. The marker lines a and b indicate the beginning and end of the impulse.
Figure 7
Figure 7. Averaged micro falls
For each subject, all cases of micro falls from six trials have been averaged. The time-locked pattern from all 10 subjects have been averaged to produce this Figure which incorporates 1541 events into the average. A micro fall is a rise in speed of the CoM to a maximum while the subject is swaying forwards. Time zero represents the averaging point which is a velocity maximum while falling forwards. Positive changes in torque represent increases. Positive angle and velocity are forwards from the vertical. Positive changes in muscle length indicate lengthening. All quantities except EMG activity are expressed relative to their mean value. A, ankle torque from both legs (continuous line) and ankle torque required to balance the CoM (dashed line); B, CoM acceleration; C, CoM velocity (dashed line) and ankle joint velocity (continuous line); D, CoM angle (dashed line) and ankle angle (continuous line); E, gastrocnemius (continuous line) and soleus (dashed line) muscle length; F, muscle length predicted by the dynamic bias model, gastrocnemius (continuous line), soleus (dashed line); G, soleus, rectified EMG signal; H, gastrocnemius, rectified EMG signal. The marker lines indicate the preceding loss of balance (a), the initial increase in EMG activity (b), the consequent decrease in muscle length (c), the subsequent increase in muscle length (d), the cancellation of CoM velocity (e) and the attainment of zero acceleration (f).
Figure 8
Figure 8. Averaged micro falls show paradoxical length changes
This Figure shows the same averaged micro falls data as Fig. 7. Averaged ankle torque has been plotted against averaged muscle length. The asterisk shows the averaging point. Torque and muscle length both increase positively.
Figure 9
Figure 9. Averaged micro falls - variation with subject
For each subject, all cases of micro falls from six trials have been averaged. An average n= 159 events per subject for six trials. A micro fall is a rise in speed of the CoM to a maximum while the subject is swaying forwards. Time zero represents the averaging point which is a velocity maximum while falling forwards. A, shows CoM velocity. B and C, show gastrocnemius and soleus muscle length, respectively. Velocity and muscle length increase positively and are expressed relative to their mean value. The continuous lines indicate subjects with a SEC stiffness greater than 100%.

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