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

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 creating and controlling movement a problem with overabundant degrees of freedom. It is widely accepted that the central nervous system might simplify the creation and control of movement. This could happen through the generation of activation patterns, which are common to many different muscles, rather than specific to individual muscles. These activation patterns, called muscle synergies, can be extracted from electromyographic data and describe the modular organization of movement. We extracted muscle synergies from the hindlimb muscle activities of wild type and genetically modified mice, in which sensory feedback from muscle spindles is eliminated. 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 components (motor modules) of muscle synergies were severely affected when external perturbations were introduced of when animals were immersed in water. These findings show that group Ia/II sensory feedback from muscle spindles regulates motor function in normal and perturbed walking. Moreover, when group Ib Golgi tendon organ feedback is lacking due to the reduction of gravitational load in conditions of enhanced buoyancy, the modular organization of swimming is almost completely compromised.\n\nSignificance statementLocomotion on land and in water requires the coordination of a great number of muscle activations and joint movements. Moreover, 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 theory of muscle synergies states that the central nervous system might control muscles in orchestrated groups (synergies) rather than individually. We used this concept on genetically modified mice, lacking one of the two classes of proprioceptors. Our results provide evidence that proprioceptive feedback is required by the central nervous system to accurately tune the modular organization of locomotion.