During quiet standing the human ‘inverted pendulum’ sways irregularly. In previous work where subjects balanced a real inverted pendulum, we investigated what contribution the intrinsic mechanical ankle stiffness makes to achieve stability. Using the results of a plausible model, we suggested that intrinsic ankle stiffness is inadequate for providing stability. Here, using a piezo‐electric translator we applied small, unobtrusive mechanical perturbations to the foot while the subject was standing freely. These short duration perturbations had a similar size and velocity to movements which occur naturally during quiet standing, and they produced no evidence of any stretch reflex response in soleus, or gastrocnemius. Direct measurement confirms our earlier conclusion; intrinsic ankle stiffness is not quite sufficient to stabilise the body or pendulum. On average the directly determined intrinsic stiffness is 91 ± 23 % (mean ±s.d.) of that necessary to provide minimal stabilisation. The stiffness was substantially constant, increasing only slightly with ankle torque. This stiffness cannot be neurally regulated in quiet standing. Thus we attribute this stiffness to the foot, Achilles’ tendon and aponeurosis rather than the activated calf muscle fibres. Our measurements suggest that the triceps surae muscles maintain balance via a spring‐like element which is itself too compliant to guarantee stability. The implication is that the brain cannot set ankle stiffness and then ignore the control task because additional modulation of torque is required to maintain balance. We suggest that the triceps surae muscles maintain balance by predictively controlling the proximal offset of the spring‐like element in a ballistic‐like manner.

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 μm 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 µm) 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.

In human standing, gravity causes forward toppling about the ankle joint which is prevented by activity in the soleus and gastrocnemius muscles. It has long been assumed that when people sway forwards the calf muscles are stretched and conversely that they shorten with backward sway. Consequently, for many years, two explanations for standing stabilization have flourished. First, tonic muscle activity itself may generate adequate intrinsic ankle stiffness. Second, if intrinsic ankle stiffness is inadequate, the resistance to stretch of the calf muscles may be augmented by stretch reflexes or by central control. These explanations require that the passive tissue (Achilles' tendon, foot) transmitting the calf muscle tension is stiff. However, our recent measurements have indicated that this passive tissue is not stiff during standing. Accordingly, we predicted a counterintuitive mode of control where the muscles and body must, on average, move in opposite directions (paradoxical movements). Here we use dynamic ultrasound imaging in vivo with novel automated tracking of muscle length to test our hypothesis. We show that soleus and gastrocnemius do indeed move paradoxically, shortening when the body sways forward and lengthening when the body returns. This confirms that intrinsic ankle stiffness is too low to stabilize human standing. Moreover, it shows that the increase in active tension is associated with muscle shortening. This pattern cannot be produced by muscle stretch reflexes and can only arise from the anticipatory neural control of muscle length that is necessary for balance.