Known and unexpected constraints evoke different kinematic, muscle, and motor cortical neuron responses during locomotion

During navigation through complex natural environments, people and animals must adapt their movements when the environment changes. The neural mechanisms of such adaptations are poorly understood, especially with respect to constraints that are unexpected and must be adapted to quickly. In this study, we recorded forelimb-related kinematics, muscle activity, and the activity of motor cortical neurons in cats walking along a raised horizontal ladder, a complex locomotion task requiring accurate limb placement. One of the crosspieces was motorized, and displaced before the cat stepped on the ladder or at different points along the cat's progression over the ladder, either towards or away from the cat. We found that, when the crosspiece was displaced before the cat stepped onto the ladder, the kinematic modifications were complex and involved all forelimb joints. When the crosspiece displaced unexpectedly while the cat was on the ladder, the kinematic modifications were minimalistic and primarily involved distal joints. The activity of M. triceps and M. extensor digitorum communis differed based on the direction of displacement. Out of 151 neurons tested, 69% responded to at least one condition; however, neurons were significantly more likely to respond when crosspiece displacement was unexpected. Most often they responded during the swing phase. These results suggest that different neural mechanisms and motor control strategies are used to overcome constraints for locomotor movements depending on whether they are known or emerge unexpectedly.