Characterization of Muscle Spindle Afferents in the Adult Mouse Using an In Vitro Muscle-Nerve Preparation

• Type of Material: Article
• Authors: Katherine A. Wilkinson, Emory University; Heidi E. Kloefkorn, Georgia Institute of Technology; Shawn Hochman, Emory University
• Language: English
• Date: 2012-06-20
• Publisher: Public Library of Science
• Publication Version: Final Published Version
• Copyright Statement: © 2012 Wilkinson et al.
• License: Creative Commons Attribution 4.0 International
• Final Published Version (URL): http://dx.doi.org/10.1371/journal.pone.0039140
• Title of Journal or Parent Work: PLoS ONE
• ISSN: 1932-6203
• Volume: 7
• Issue: 6
• Start Page: e39140
• End Page: e39140
• Grant/Funding Information: This work was supported by a grant from Pfizer (WS753098; http://www.pfizer.com/home/) to S. Hochman and an individual fellowship from the United States National Institutes of Health (K12 GM000680; http://www.nigms.nih.gov/Training/CareerDev/TWDInstRes.htm) to K. Wilkinson.; The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
• Keywords: MULTIDISCIPLINARY SCIENCES; RAMP-AND-HOLD; ECCENTRIC CONTRACTION; PHYSIOLOGICAL-PROPERTIES; CONTRACTILE PROPERTIES; SECONDARY ENDINGS; GOLGI TENDON ORGANS; Science & Technology; RAT SOLEUS MUSCLE; DYNAMIC-RESPONSE; MAMMALIAN MUSCLE; SKELETAL-MUSCLE; Multidisciplinary Sciences; Science & Technology - Other Topics
• Research Categories: Health Sciences, General; Biology, Animal Physiology

Abstract

We utilized an in vitro adult mouse extensor digitorum longus (EDL) nerve-attached preparation to characterize the responses of muscle spindle afferents to ramp-and-hold stretch and sinusoidal vibratory stimuli. Responses were measured at both room (24°C) and muscle body temperature (34°C). Muscle spindle afferent static firing frequencies increased linearly in response to increasing stretch lengths to accurately encode the magnitude of muscle stretch (tested at 2.5%, 5% and 7.5% of resting length [Lo]). Peak firing frequency increased with ramp speeds (20% Lo/sec, 40% Lo/sec, and 60% Lo/sec). As a population, muscle spindle afferents could entrain 1:1 to sinusoidal vibrations throughout the frequency (10-100 Hz) and amplitude ranges tested (5-100 μm). Most units preferentially entrained to vibration frequencies close to their baseline steady-state firing frequencies. Cooling the muscle to 24°C decreased baseline firing frequency and units correspondingly entrained to slower frequency vibrations. The ramp component of stretch generated dynamic firing responses. These responses and related measures of dynamic sensitivity were not able to categorize units as primary (group Ia) or secondary (group II) even when tested with more extreme length changes (10% Lo). We conclude that the population of spindle afferents combines to encode stretch in a smoothly graded manner over the physiological range of lengths and speeds tested. Overall, spindle afferent response properties were comparable to those seen in other species, supporting subsequent use of the mouse genetic model system for studies on spindle function and dysfunction in an isolated muscle-nerve preparation.