Research Article: Analysis of Proprioceptive Sensory Innervation of the Mouse Soleus: A Whole-Mount Muscle Approach

Date Published: January 25, 2017

Publisher: Public Library of Science

Author(s): Martha J. Sonner, Marie C. Walters, David R. Ladle, William D Phillips.


Muscle proprioceptive afferents provide feedback critical for successful execution of motor tasks via specialized mechanoreceptors housed within skeletal muscles: muscle spindles, supplied by group Ia and group II afferents, and Golgi tendon organs, supplied by group Ib afferents. The morphology of these proprioceptors and their associated afferents has been studied extensively in the cat soleus, and to a lesser degree, in the rat; however, quantitative analyses of proprioceptive innervation in the mouse soleus are comparatively limited. The present study employed genetically-encoded fluorescent reporting systems to label and analyze muscle spindles, Golgi tendon organs, and the proprioceptive sensory neuron subpopulations supplying them within the intact mouse soleus muscle using high magnification confocal microscopy. Total proprioceptive receptors numbered 11.3 ± 0.4 and 5.2 ± 0.2 for muscle spindles and Golgi tendon organs, respectively, and these receptor counts varied independently (n = 27 muscles). Analogous to findings in the rat, muscle spindles analyzed were most frequently supplied by two proprioceptive afferents, and in the majority of instances, both were classified as primary endings using established morphological criteria. Secondary endings were most frequently observed when spindle associated afferents totaled three or more. The mean diameter of primary and secondary afferent axons differed significantly, but the distributions overlap more than previously observed in cat and rat studies.

Partial Text

Continual monitoring of alterations in muscle length, corresponding joint angle changes, and forces produced during muscle contraction are critical for execution of motor tasks. Proprioceptive sensory neurons (PSNs) encode and relay this information to the central nervous system for interpretation and response via spinal circuits and ascending pathways into the brain [1,2]. Axons extending into the periphery from PSN cell bodies localized in the dorsal root ganglia (DRG), supply specialized sensory receptors located in skeletal muscle, known as muscle spindles (MS) and Golgi tendon organs (GTOs).

In this study we used a transgenic reporter system to analyze the sensory innervation of MS and GTOs using an intact mouse soleus muscle preparation. Robust fluorescence in PSN axons permitted visualization of afferent pathways and terminations within a muscle with a minimum of specimen preparation and no tissue sectioning, representing a substantial gain in efficiency compared with serial section or teased preparation techniques. This whole-mount muscle approach enabled quantification of proprioceptive receptors and their respective afferents as well as comparison of spindle sensory ending classifications obtained via morphological identification and intramuscular axonal diameter measurement.




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