The Journal of Experimental Biology © 2015. Published by The Company of Biologists Ltd | The Journal of Experimental Biology (2015) 218, 451-457 doi:10.1242/jeb.113688 451 ABSTRACT While running on uneven ground, humans are able to negotiate visible but also camouflaged changes in ground level. Previous studies have shown that the leg kinematics before touch down change with ground level. The present study experimentally investigated the contributions of visual perception (visual feedback), proprioceptive feedback and feed-forward patterns to the muscle activity responsible for these adaptations. The activity of three bilateral lower limb muscles (m. gastrocnemius medialis, m. tibialis anterior and m. vastus medialis) of nine healthy subjects was recorded during running across visible (drop of 0, −5 and −10 cm) and camouflaged changes in ground level (drop of 0 and −10 cm). The results reveal that at touchdown with longer flight time, m. tibialis anterior activation decreases and m. vastus medialis activation increases purely by feed-forward driven (flight time-dependent) muscle activation patterns, while m. gastrocnemius medialis activation increase is additionally influenced by visual feedback. Thus, feed-forward driven muscle activation patterns are sufficient to explain the experimentally observed adjustments of the leg at touchdown. KEY WORDS: EMG, Pre-activation, Gastrocnemius, Force feedback, Uneven ground INTRODUCTION While running, humans must routinely negotiate varied and sometimes unpredictable changes in ground level, e.g. running across an uneven forest track covered with stones and roots (visible perturbation) or stepping into a puddle of unknown depth (camouflaged perturbation). In preparation for such perturbations, humans flex their ankle joint angle (dorsiflexion) at touchdown for visible elevations in ground level (Grimmer et al., 2008; Müller and Blickhan, 2010) and extend their ankle joint angle (plantar flexion) for visible drops in ground level (Müller et al., 2012a). Interestingly, they also extend their ankle joint if the drop is invisible because of camouflage (Müller et al., 2012a). In this study, we investigated the muscle activity and neuronal control strategy responsible for these findings with perturbation experiments. The muscles responsible for plantar flexion and dorsiflexion are, amongst others, m. gastrocnemius medialis (gastrocnemius) and m. tibialis anterior (tibialis), respectively. As these muscles are located close to the skin, their activity can be observed with muscle surface electromyography (EMG). The activity of leg muscles continuously changes throughout the running cycle. During unperturbed level RESEARCH ARTICLE 1 Motionscience, Institute of Sport Sciences, Friedrich Schiller University Jena, Seidelstraße 20, 07749 Jena, Germany. 2 Department of Sport and Exercise Science, University of Stuttgart, Allmandring 28, 70569 Stuttgart, Germany. *Author for correspondence (roy.mueller@uni-jena.de) Received 8 September 2014; Accepted 25 November 2014 running, gastrocnemius activity starts before touchdown and ends before take-off, with peak activation after touchdown. The shape of this peak is similar to the quadriceps peak but delayed. Tibialis activity starts at take-off and ends at touchdown, with peak activation before touchdown (Gazendam and Hof, 2007; Müller et al., 2010). On level ground, the movement is periodic and the activity patterns are fairly repetitive (Gazendam and Hof, 2007; Guidetti et al., 1996; Ishikawa et al., 2007; Müller et al., 2010). In case of a variation of the movement, e.g. due to a variation in ground level, however, the muscle activity differs from the periodic case to adapt to the perturbation. Gastrocnemius activity prior to the touchdown (pre-activation) decreases with a visible elevated contact (Müller et al., 2010). This seems to be sufficient to adjust the preparing ankle angle (Müller et al., 2012b) and, consequently, its antagonist, the tibialis does not alter activity dependent on step elevation (Müller et al., 2010). In the present study, we investigated running across visible and camouflaged drops in ground level. We report on the altered muscle activity resulting in increased plantar flexion before touchdown for these perturbations. Furthermore, we address here the neuro-mechanical strategy behind these adjustments. Such an adaptation could be a result of visual perception of the perturbation, principally allowing an adaptation of the pre-activation prior to the perturbed touchdown. Based on experience, a few visual cues might suffice to recall appropriate stored information. The error signal (unevenness of the ground) generated by the perception of the hurdle (visual feedback) allows action to be taken in advance of the perturbed ground contact. This way, the plantar flexion angle at touchdown could be increased. A different strategy is required if such a visually guided adaptation is not possible, e.g. when the changes in ground level are invisible as a result of camouflage (e.g. stepping into a puddle of unknown depth). In this case, a trained muscle activity pattern can generate an increasing plantar flexion angle in time, e.g. by constantly increasing gastrocnemius activity with time, as already observed in the EMG recordings of level running. As the flight time during running on uneven ground depends on ground level height (the higher the next ground contact, the shorter the flight time, and the lower the next ground contact, the longer the flight time), such a trained muscle activity pattern allows an adapted muscle activation and plantar flexion angle at touchdown without the need for any neural feedback. This strategy can thus be seen as a feed-forward muscle activity pattern created, for example, by central pattern generators (Dickinson et al., 2000; Ijspeert, 2008; Prochazka and Yakovenko, 2007). In such rhythmical feed-forward activation, the timing of the pattern has to be adapted to the walking cycle (Prochazka and Yakovenko, 2007; Rybak et al., 2002), e.g. the onset of muscle pre-activation depends on the preceding take-off time. Thus, the preceding take-off is the trigger event for the pattern. There is experimental evidence for the contribution of both feed- forward and feedback control to running (Dickinson et al., 2000; MacKay-Lyons, 2002; Nielsen, 2003; Prochazka and Yakovenko, Preparing the leg for ground contact in running: the contribution of feed-forward and visual feedback Roy Müller 1, *, Daniel Florian Benedict Häufle 2 and Reinhard Blickhan 1