Modular organization of murine locomotor pattern in the presence and absence of sensory feedback from muscle spindles

Abstract

Key points: Locomotion on land and in water requires the coordination of a great number of muscle activations and joint movements. Constant feedback about the position of own body parts in relation to the surrounding environment and the body itself (proprioception) is required to maintain stability and avoid failure. The central nervous system may follow a modular type of organization by controlling muscles in orchestrated groups (muscle synergies) rather than individually. We used this concept on genetically modified mice lacking muscle spindles, one of the two main classes of proprioceptors. We provide evidence that proprioceptive feedback is required by the central nervous system to accurately tune the modular organization of locomotion.

Abstract: For exploiting terrestrial and aquatic locomotion, vertebrates must build their locomotor patterns based on an enormous amount of variables. The great number of muscles and joints, together with the constant need for sensory feedback information (e.g. proprioception), make the task of controlling movement a problem with overabundant degrees of freedom. It is widely accepted that the central nervous system may simplify the creation and control of movement by generating activation patterns common to muscle groups, rather than specific to individual muscles. These activation patterns, called muscle synergies, describe the modular organization of movement. We extracted synergies through electromyography from the hind limb muscle activities of wild-type and genetically modified mice lacking sensory feedback from muscle spindles. Muscle spindle-deficient mice underwent a modification of the temporal structure (motor primitives) of muscle synergies that resulted in diminished functionality during walking. In addition, both the temporal and spatial (motor modules) components of synergies were severely affected when external perturbations were introduced or when animals were immersed in water. These findings show that sensory feedback from group Ia/II muscle spindles regulates motor function in normal and perturbed walking. Moreover, when group Ib Golgi tendon organ feedback is lacking due to enhanced buoyancy, the modular organization of swimming is almost completely compromised.

Keywords: Egr3; Lyapunov; locomotion; muscle synergies; proprioception; sensory feedback.