Signals from load sensors underlie interjoint coordination during stepping movements of the stick insect leg

During stance and swing phase of a walking stick insect, the retractor coxae (RetCx) and protractor coxae (ProCx) motoneurons and muscles supplying the thorax-coxa (TC)-joint generate backward and forward movements of the leg. Their activity is tightly coupled to the movement of the more distal leg segments, i.e., femur, tibia, and tarsus. We used the single middle leg preparation to study how this coupling is generated. With only the distal leg segments of the middle leg being free to move, motoneuronal activity of the de-afferented and -efferented TC-joint is similarly coupled to leg stepping. RetCx motoneurons are active during stance and ProCx motoneurons during swing. We studied whether sensory signals are involved in this coordination of TC-joint motoneuronal activity. Ablation of the load measuring campaniform sensilla (CS) revealed that they substantially contribute to the coupling of TC-joint motoneuronal activity to leg stepping. Individually ablating trochanteral and femoral CS revealed the trochanteral CS to be necessary for establishing the coupling between leg stepping and coxal motoneuron activity. When the locomotor system was active and generated alternating bursts of activity in ProCx and RetCx motoneurons, stimulation of the CS by rearward bending of the femur in otherwise de-afferented mesothoracic ganglion terminated ongoing ProCx motoneuronal activity and initiated RetCx motoneuronal activity. We show that cuticular strain signals from the trochanteral CS play a major role in shaping TC-joint motoneuronal activity during walking and contribute to their coordination with the stepping pattern of the distal leg joints. We present a model for the sensory control of timing of motoneuronal activity in walking movements of the single middle leg.