Mechanosensory encoding of forces in walking uphill and downhill: force feedback can stabilize leg movements in stick insects.

Force feedback could be valuable in adapting walking to diverse terrains but the effects of changes in substrate inclination on discharges of sensory receptors that encode forces have rarely been examined. In insects, force feedback is provided by campaniform sensilla, mechanoreceptors that monitor forces as cuticular strains. We neurographically recorded responses of stick insect tibial campaniform sensilla to 'naturalistic' forces (joint torques) that occur at the hind leg femur-tibia (FT) joint in uphill, downhill and level walking. The FT joint torques, obtained in a previous study that used inverse dynamics to analyze data from freely moving stick insects, are quite variable during level walking (including changes in sign) but are larger in magnitude and more consistent when traversing sloped surfaces. Similar to vertebrates, insects used predominantly extension torque in propulsion on uphill slopes and flexion torques to brake forward motion when going downhill. Sensory discharges to joint torques reflected the torque direction but, unexpectedly, often occurred as multiple bursts that encoded the rate of change of positive forces (dF/dt) even when force levels were high. All sensory discharges also showed hysteresis and substantial decrease or complete cessation during transient force decrements. These findings have been tested in simulation in a mathematical model of the sensilla (Szczecinski et al. 2021) which accurately reproduced the biological data. Our results suggest the hypothesis that sensory feedback from the femoro-tibial joint indicating force dynamics (dF/dt) can be used to counter the instability in traversing sloped surfaces in animals and, potentially, in walking machines.