Feedforward neural control of toe walking in humans

Abstract

Key points: Activation of ankle muscles at ground contact during toe walking is unaltered when sensory feedback is blocked or the ground is suddenly dropped. Responses in the soleus muscle to transcranial magnetic stimulation, but not peripheral nerve stimulation, are facilitated at ground contact during toe walking. We argue that toe walking is supported by feedforward control at ground contact.

Abstract: Toe walking requires careful control of the ankle muscles in order to absorb the impact of ground contact and maintain a stable position of the joint. The present study aimed to clarify the peripheral and central neural mechanisms involved. Fifteen healthy adults walked on a treadmill (3.0 km h^-1 ). Tibialis anterior (TA) and soleus (Sol) EMG, knee and ankle joint angles, and gastrocnemius-soleus muscle fascicle lengths were recorded. Peripheral and central contributions to the EMG activity were assessed by afferent blockade, H-reflex testing, transcranial magnetic brain stimulation (TMS) and sudden unloading of the planter flexor muscle-tendon complex. Sol EMG activity started prior to ground contact and remained high throughout stance. TA EMG activity, which is normally seen around ground contact during heel strike walking, was absent. Although stretch of the Achilles tendon-muscle complex was observed after ground contact, this was not associated with lengthening of the ankle plantar flexor muscle fascicles. Sol EMG around ground contact was not affected by ischaemic blockade of large-diameter sensory afferents, or the sudden removal of ground support shortly after toe contact. Soleus motor-evoked potentials elicited by TMS were facilitated immediately after ground contact, whereas Sol H-reflexes were not. These findings indicate that at the crucial time of ankle stabilization following ground contact, toe walking is governed by centrally mediated motor drive rather than sensory driven reflex mechanisms. These findings have implications for our understanding of the control of human gait during voluntary toe walking.

Keywords: TMS; ischemia; toe walking; ultrasound.

Figure 1. Comparison of kinematics and EMG activity during normal heel walking (black) and toe walking (red) in a single subject

A, stick diagrams of the left and right limb positions in a full gait cycle obtained by 3‐D motion analysis. B–F, averaged traces of knee (B) and ankle (C) joint position, Sol EMG activity (D), TA EMG activity (E) and tension measured from the Achilles tendon (F). All traces were obtained by averaging the respective measurements triggered on ground contact (marked by green dotted vertical line). The averaging was performed for a 1 s period (time scale indicted by horizontal bar bottom right) covering one gait cycle. Scaling of measurements is indicated to the right as vertical bars in each graph.

Figure 2. Changes in muscle–tendon length during toe walking

A, ultrasound (US) probes were placed over the belly of the MG muscle and the junction between the MG muscle and the Achilles tendon. Sol EMG activity and joint kinematics were measured simultaneously. Examples of US images from the two probes are shown for early and late stance. The upper row of images is from the probe placed over the MG muscle belly. The superficial (SA) and deep aponeuroses (DA) are clearly visible. A single MG muscle fascicle spanning from SA to DA has been marked by a yellow dashed line in the two images. Note, that the images only represent the upper 50% of the original US image, so that the Sol muscle is only partly visible below the MG muscle. For measurement of Sol muscle fascicles, the entire depth (70 mm) of the image was used. The lower row of images is from the probe placed over the junction between the MG muscle and the Achilles tendon. The junction has been marked in the images by a yellow cross. B–E, averaged traces (n = 60) of Sol EMG activity in μV (B), ankle joint position in degrees (C), MG muscle fascicle length in mm (D) and the Sol muscle fascicle length in mm (E) triggered on ground contact (vertical dotted green line). The Achilles tendon length was calculated from the movement of the junction between the MG muscle and the Achilles tendon relative to the movement of the muscle–tendon complex as measured from markers placed on the heel, the US probe and the knee. The time axis is given by the horizontal line in the bottom right.

Figure 3. Toe walking with (red) and without (black) block of transmission in large‐diameter sensory fibres induced by ischaemia

A, ischaemia was induced by inflating a blood pressure cuff placed around the thigh to 240 mmHg. Transmission in large‐diameter afferents was checked by stimulating the tibial nerve and recording Sol H‐reflexes before ischaemia. Twenty‐two minutes after induction of ischaemia, H‐reflexes had disappeared, while an M‐response could still be elicited after ischaemia. B–D, averaged traces (n = 45) of the ankle joint position (B), Sol EMG activity (C) and TA EMG activity (D) during toe walking before (black lines) and after ischaemia (red lines). The averaging was triggered on ground contact (indicated by vertical dotted green line). The grey shaded box indicates the period of Sol EMG activity, which was quantified and compared with and without ischaemia. The time axis is given by the horizontal line in the bottom right.

Figure 4. Sudden drop in ground support

Participants were asked to walk barefoot on their toes over a force platform placed in the floor. A, averaged traces (n = 40) of the vertical force from the platform (upper traces), the sol EMG activity (middle traces) and the TA EMG activity (lower traces) during control steps without perturbations. x‐ and y‐scale bars are given to the right and below the traces. B and C, averaged traces (n = 10) of vertical force and Sol EMG activity in control steps (black lines) and steps in which the platform was suddenly dropped 8 cm at 0.8 g (red lines). The traces were triggered on ground contact (vertical, dotted green line). In B, the platform was dropped immediately when the subject made ground contact, whereas the drop was delayed by 400 ms so that it occurred in late stance in C. The time of the drop is indicated by the black, dotted vertical lines in B and C. The grey shaded box in B indicates the period of Sol EMG activity, which was quantified and compared with and without drop of the platform. x‐ and y‐scale bars are indicated below and to the right of the individual traces.

Figure 5. Modulation of Sol MEP and H‐reflex during toe and heel walking

A and B, modulation of Sol H‐reflexes (A) and Sol MEPs (B) elicited by TMS during heel (filled circles) and toe walking (open circles). C, background Sol EMG activity. D, the size of Sol M‐responses. The size of the H‐reflexes, MEPs and M‐responses is expressed as a percentage of M_max measured at the same time point. E, the size of H‐reflexes (filled circles) and MEPs (open circles) recorded during toe walking (open circles in A and B) divided by the size of the reflexes and MEPs recorded during heel walking (filled circles in A and B). Data are population averages from all 8 investigated participants. Vertical bars in B–D are SEM. In E shaded red and grey areas indicate 95% confidence intervals.