Degradation of mouse locomotor pattern in the absence of proprioceptive sensory feedback

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 111; no. 47; pp. 16877 - 16882
• Main Authors: Akay, Turgay, Tourtellotte, Warren G., Arber, Silvia, Jessell, Thomas M.
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 25.11.2014; National Acad Sciences
• Series: From the Cover
• Subjects: Animals; Ankle; Biological Sciences; Biomechanical Phenomena; Biomechanics; Electromyography; Feedback; Flexors; Locomotion; Mammals; Mice; Motor ability; Muscle spindles; Proprioception; Rodents; Sensory feedback; Sensory perception; Swimming; Walking; pattern generation; proprioception; sensory feedback; locomotion
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.1419045111

Significance Terrestrial locomotion is thought to be generated by the actions of a circuit of interconnected interneurons (central pattern generator) in the spinal cord that drive the patterned activity of pools of motor neurons, causing sequential contraction of dozens of leg muscles. Sensory feedback exerts a strong modulatory influence on this pattern; nevertheless, it remains unclear whether sensory feedback also plays a role in the generation of the normal locomotor pattern. Through the use of a combination of electrophysiology, behavior, and mouse genetics, we provide evidence that the absence of proprioceptive sensory feedback degrades locomotor pattern, indicating that proprioceptive feedback is required for the construction of locomotor pattern. Mammalian locomotor programs are thought to be directed by the actions of spinal interneuron circuits collectively referred to as “central pattern generators.” The contribution of proprioceptive sensory feedback to the coordination of locomotor activity remains less clear. We have analyzed changes in mouse locomotor pattern under conditions in which proprioceptive feedback is attenuated genetically and biomechanically. We find that locomotor pattern degrades upon elimination of proprioceptive feedback from muscle spindles and Golgi tendon organs. The degradation of locomotor pattern is manifest as the loss of interjoint coordination and alternation of flexor and extensor muscles. Group Ia/II sensory feedback from muscle spindles has a predominant influence in patterning the activity of flexor muscles, whereas the redundant activities of group Ia/II and group Ib afferents appear to determine the pattern of extensor muscle firing. These findings establish a role for proprioceptive feedback in the control of fundamental aspects of mammalian locomotor behavior.