Elastic tissue forces mask muscle fiber forces underlying muscle spindle la afferent firing rates in stretch of relaxed rat muscle

• Type of Material: Article
• Authors: Kyle P. Blum, Georgia Institute of Technology; Paul Nardelli, Georgia Institute of Technology; Timothy Cope, Emory University; Lena Ting, Emory University
• Language: English
• Date: 2019-08-01
• Publisher: Company Biologists LTD.
• Publication Version: Final Published Version
• Copyright Statement: © 2019. Published by The Company of Biologists Ltd.
• Final Published Version (URL): http://dx.doi.org/10.1242/jeb.196287
• Title of Journal or Parent Work: journal of Experimental Biology
• Volume: 222
• Issue: 15
• Grant/Funding Information: This work was supported by the Eunice Kennedy Shriver National Institute of Child Health and Human Development [R01 HD90642 to L.H.T. and T.C.C.],; National Institute of Neurological Disorders and Stroke [F31 NS093855 to K.P.B.]. Deposited in PMC for release after 12 months.; National Institute of Neurological Disorders and Stroke [P01 NS057228 to T.C.C.]
• Keywords: Life Sciences & Biomedicine - Other Topics; Muscle thixotropy; Endings; Proprioception; Life Sciences & Biomedicine; Science & Technology; Sensorimotor control; Somatosensation; Biology
• Research Categories: Biology, General; Biology, Physiology; Engineering, Biomedical

Abstract

Stretches of relaxed cat and rat muscle elicit similar history-dependent muscle spindle Ia firing rates that resemble history-dependent forces seen in single activated muscle fibers (Nichols and Cope, 2004). Owing to thixotropy, whole musculotendon forces and muscle spindle firing rates are history dependent during stretch of relaxed cat muscle, where both muscle force and muscle spindle firing rates are elevated in the first stretch in a series of stretch–shorten cycles (Blum et al., 2017). By contrast, rat musculotendon exhibits only mild thixotropy, such that the measured forces when stretched cannot explain history-dependent muscle spindle firing rates in the same way (Haftel et al., 2004). We hypothesized that history-dependent muscle spindle firing rates elicited in stretch of relaxed rat muscle mirror history-dependent muscle fiber forces, which are masked at the level of whole musculotendon force by extracellular tissue force. We removed estimated extracellular tissue force contributions from recorded musculotendon force using an exponentially elastic tissue model. We then showed that the remaining estimated muscle fiber force resembles history-dependent muscle spindle firing rates recorded simultaneously. These forces also resemble history-dependent forces recorded in stretch of single activated fibers that are attributed to muscle cross-bridge mechanisms (Campbell and Moss, 2000). Our results suggest that history-dependent muscle spindle firing in both rats and cats arise from history-dependent forces owing to thixotropy in muscle fibers.