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, 587 (Pt 10), 2399-416

The Proprioceptive and Agonist Roles of Gastrocnemius, Soleus and Tibialis Anterior Muscles in Maintaining Human Upright Posture

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The Proprioceptive and Agonist Roles of Gastrocnemius, Soleus and Tibialis Anterior Muscles in Maintaining Human Upright Posture

Irene Di Giulio et al. J Physiol.

Abstract

Humans can stand using sensory information solely from the ankle muscles. Muscle length and tension in the calf muscles (gastrocnemius and soleus) are unlikely to signal postural sways on account of balance-related modulation in agonist activity. These facts pose two questions: (1) Which ankle muscles provide the proprioceptive information? (2) Which peripheral mechanism could modulate agonist activity? To address these issues, subjects were asked to stand normally on two force plates. Ultrasound and surface EMG were recorded from the calf and tibialis anterior (TA) muscles. For all nine subjects, changes in muscle length of TA were mainly (84 +/- 9% whole trial duration) orthodoxly correlated with bodily sway (centre of gravity, CoG), i.e. in accordance with passive ankle rotation. When orthodox, TA had the highest correlation with CoG (-0.66 +/- 0.07, deep compartment, P < 0.001). For five subjects, the superficial TA compartment showed counter-intuitive changes in muscle length with CoG, probably due to the flattening of the foot and proximal attachment geometry. Gastrocnemius and soleus were usually (duration 71 +/- 23 and 81 +/- 16%, respectively) active agonists (paradoxically correlated with CoG) but, for short periods of time, they could be orthodox and then presented a moderate correlation (0.38 +/- 0.16 and 0.28 +/- 0.09, respectively) with CoG. Considering the duration and extent to which muscle length is orthodox and correlated with CoG, TA may be a better source of proprioceptive information than the active agonists (soleus and gastrocnemius). Therefore, if a peripheral feedback mechanism modulates agonist activity then reciprocal inhibition acted by TA on the calf muscles is more likely to be effective than the autogenic pathway.

Figures

Figure 2
Figure 2. Normal standing
Normal standing typical sways of representative subject showing A, sagittal centre of gravity relative to the ankle joint centre (CoG) (continuous line, left scale) and ankle flexion angle (dashed line, right scale), B, left ankle plantarflexion torque (T). C, low-pass filtered EMG of gastrocnemius medialis (G). D, change in muscle length of gastrocnemius medialis (δG) (continuous line, left scale) and soleus (δS) (dashed line, right scale). E, tibialis anterior EMG (TA). F, change in muscle length of superficial (δTAs) (continuous line) and deep (δTAd) (dashed line) compartment of tibialis anterior, G, displacement of the aponeuroses of tibialis anterior (TA Aps), distal aponeuroses of the two compartments (continuous line), proximal aponeurosis of the superficial one (dashed) and proximal aponeurosis of the deep compartment (dotted line). The forward sway corresponds to an increase in ankle angle and torque. Positive muscular change in muscle length means lengthening and positive aponeuroses displacement means distal movement. Surprisingly, it is clear that the two compartments of tibialis anterior show opposite behaviours (F) and this is explained by the different behaviour of the aponeuroses of this muscle (G) which are all moving distally but to a different extent during forward sway (e.g. at 4–5 s).
Figure 1
Figure 1. Anatomy and model of human standing
A, the calf muscles (soleus and gastrocnemius) connect the Achilles tendon to the back of the lower leg bones and the back of the knee respectively. Tibialis anterior is situated anterior to the tibia and attached to the upper part of this bone. Its tendon traverses the front of the tibia and ankle joint and passes along the medial side of the foot to the base of the first metatarsal bone. B, sonograph of the superficial and deep compartment of tibialis anterior. a, proximal aponeurosis of the deep compartment; b, distal aponeurosis of the deep compartment; c, distal aponeurosis of the superficial compartment; d, proximal aponeurosis of the superficial compartment. b and c are morphologically distinct but moved as a unit and were tracked using a triple set of markers. A 1 cm white scale is shown horizontally (perpendicular to the aponeuroses) and a 2 cm white scale is shown vertically (parallel to the aponeuroses). C, model of the muscle tendon unit. The muscle is modelled as a contractile element in series with the tendon spring. The changes in muscle length based on the sonograph and calculated through our method, are representative of shortening and lengthening of the whole muscle as a series component in this muscle–tendon unit.
Figure 3
Figure 3. Muscular behaviour during normal standing
Muscular change in muscle length and EMG during normal standing sways of representative subject (same trial as Fig. 2). The horizontal axis is the centre of gravity relative to the ankle joint centre position (CoG), 0 mm is the ankle joint centre position. The following panels show the muscular change in muscle length of A, soleus; B, gastrocnemius; D, superficial compartment of tibialis anterior; E, deep compartment of tibialis anterior. The following panels show the low-pass filtered superficial EMG of C, gastrocnemius and F, tibialis anterior. Negative displacement means shortening relative to the initial length. The two compartments of tibialis anterior show an opposite correlation (D vs. E) and the EMG does not appear to be modulated (F), but also soleus and gastrocnemius show different behaviour, in particular when the CoG is further backwards (A vs. B).
Figure 6
Figure 6. All muscle behaviour during normal standing
For each 3 s interval of a whole trial the correlation between each muscle and the CoG was calculated (G, gastrocnemius: S, soleus, TAd, deep compartment of tibialis anterior and TAs, superficial compartment of tibialis anterior). The intervals were classified into negatively (white bars) and positively correlated intervals (black bars) and whole trial (grey bars). For these groups the following quantities are shown: A, correlation between the change in muscle length and the CoG, B, percentage duration in each condition. The values shown are the mean and s.e.m. for each subject. On average, gastrocnemius is negatively correlated with CoG (G, white bars), though this is not very consistent among the subjects. Soleus behaviour is similar but more consistent among the subjects. The deep compartment of tibialis anterior is overall negatively correlated.
Figure 4
Figure 4. Calf muscles change in muscle length
Gastrocnemius (left column) and soleus (right column) change in muscle length relative to CoG, during normal standing for all the other subjects (representative subject of Fig. 3 not shown). The green portions were manually identified from the surface EMG of gastrocnemius recognizing periods in which the activity was un-modulated. It is very clear that for several subjects the two calf muscles present a different behaviour: while soleus shows almost always a negative correlation with CoG, gastrocnemius, when CoG is nearer the ankle joint, shows also periods where the correlation with CoG is positive in some participants (S1, S4, S6, S8). Both muscles presented parallel lines when the muscles were un-modulated in their activity; their similar slope is an indication that even if the overall correlation is quite low, for short periods of time it might be high and for those durations the changes in muscle length appeared to be a good source of proprioceptive information. That is also the reason why we performed a trial partition analysis using intervals of 3 s.
Figure 5
Figure 5. Two compartments of tibialis anterior change in muscle length
Deep compartment (TAd; left column) and superficial compartment (TAs; right column) of tibialis anterior change in muscle length relative to CoG, during normal standing for all the other subjects (representative subject of Fig. 3 not shown). The green portions were manually identified from the surface EMG of tibialis anterior recognizing periods in which the activity was un-modulated. The two compartments of tibialis anterior show different behaviour: the change in muscle length of the deep compartment is for all the participants negatively correlated with body position (CoG) while, for the superficial compartment, when the participants are standing with the CoG backwards, still in absence of modulation of EMG activity (green portions), some of them show also intervals positively correlated with CoG. Both compartments, when the person was standing away from the ankle, showed parallel lines when the muscles were un-modulated in their activity. Again their slope is locally very similar which indicates high local correlation.
Figure 7
Figure 7. Gastrocnemius muscular behaviour during normal standing
For each 3 s interval of a whole trial the correlation between gastrocnemius and the CoG was calculated. The intervals were classified into negatively (white bars) and positively correlated intervals (black bars) and whole trial (grey bars). For these groups the following quantities are shown: A, correlation between the gastrocnemius change in muscle length and the CoG; B, gastrocnemius standard deviation of EMG levels (modulation of activity); C, mean gastrocnemius EMG levels (tonic activity); D, percentage duration in each condition. The horizontal axis represents each subject tested (1–9); values are the mean for each subject and error bars show the standard error of the mean. The ‘Mean’ column is the average for all the individuals. On average gastrocnemius is negatively correlated with CoG (A) and the negatively correlated portion are associated with a higher level of modulation of EMG (B) and tonic activity (C). The negative correlated portions have the longest duration (D). The muscle lengths of S1 and S9 are overall positively correlated with CoG (A) and for longer duration (D) when the muscle activity is not modulated (B).
Figure 8
Figure 8. Behaviour of the deep compartment of tibialis anterior during normal standing
For each 3 s interval of a whole trial the correlation between the deep compartment of tibialis anterior and CoG was calculated. The intervals were classified into negatively (white bars) and positively correlated intervals (black bars) and whole trial (grey bars). For these groups the following quantities are shown: A, correlation between the deep compartment of tibialis anterior change in muscle length and CoG; B, tibialis anterior standard deviation of EMG levels (modulation of activity); C, mean tibialis anterior EMG levels (tonic activity); D, percentage duration in each condition. The horizontal axis represents each subject tested (1–9); values are the mean for each subject and error bars show the standard error of the mean. The ‘Mean’ column is the average and s.e.m. for all the individuals. For all the subjects, the deep compartment of tibialis anterior is mainly negatively correlated with CoG (A and D) and its negative correlation portions are associated with a low modulation in the EMG activity (B) and in tonic activity (C).
Figure 9
Figure 9. Soleus interlinked behaviour during normal standing
For each 3 s interval of a whole trial the correlation between soleus and body position was calculated. The intervals were classified into negatively (white bars) and positively correlated intervals (black bars) and whole trial (grey bars). For these groups the following quantities are shown: A, correlation between the soleus change in muscle length and CoG; B, correlation between the gastrocnemius change in muscle length and CoG, based on the trial partition obtained from soleus correlation; C, correlation between the deep compartment of tibialis anterior change in muscle length and CoG, based on the trial partition obtained from soleus correlation; D, correlation between the superficial compartment of tibialis anterior change in muscle length and CoG, based on the trial partition obtained from soleus correlation. The average values from the nine subjects are presented and error bars show the standard error of the mean. On average soleus is negatively correlated with body position (A) and when soleus changes from a negative to positive correlation (A), gastrocnemius’ correlation with CoG becomes less negative (or more positive) (B), and the superficial compartment of tibialis anterior shows a more negative correlation (D). The deep compartment of the same muscle does not show any difference in behaviour related to soleus (C). The association between soleus and the superficial compartment of tibialis anterior is evidence that the counter-intuitive behaviour in the superficial compartment of tibialis anterior has an anatomical or physiological explanation.

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