In humans, during standing the calf muscles soleus and gastrocnemius actively prevent forward toppling about the ankles. It has been generally assumed that these postural muscles behave like springs with dynamic stiffness reflecting their mechanical properties, reflex gain including higher derivatives, and central control. Here, for the first time, we have used an ultrasound scanner and automated image analysis to record the tiny muscular movements occurring in normal standing. This new, non-invasive technique resolves changes in muscle length as small as 10 μm without disturbing the standing process. This technical achievement has allowed us to test the long-established mechano-reflex, muscle spring hypothesis that muscle length changes in a spring-like way during sway of the body. Our results contradict that hypothesis. Muscle length changes in a non-spring-like manner: on average, shortening during forward sway and lengthening during backwards sway (paradoxical movements). This counter-intuitive result is a consequence of the fact that calf muscles generate tension through a series elastic component (SEC, Achilles tendon and foot) which limits maximal ankle stiffness to 92 ± 20% of that required to balance the body. Paradoxical movements cannot be generated by stretch reflexes with constant intrafusal drive but might be produced by reflex coupling of extrafusal (α) and intrafusal (β, γ) drive or by positive force feedback. Standing requires the predictive ability to produce the observed muscle movements preceded (110 ± 50 ms) by corresponding changes in integrated EMG signal. We suggest higher level anticipatory control is more plausible.