Regular article
Compared effects of hindlimb unloading versus terrestrial deafferentation on muscular properties of the rat soleus

https://doi.org/10.1016/S0014-4886(03)00111-0Get rights and content

Abstract

Hindlimb unloading is known to induce some neuromuscular changes especially in postural muscles such as the soleus. Our goal was to determine the role of proprioceptive inputs on these modifications by comparing soleus muscle properties of rats being either hindlimb unloaded or terrestrial deafferented. Under deep anesthesia, a first group of rats were submitted to a bilateral deafferentation (DEAF group, n = 6) performed by section of the dorsal roots L3 to L5 after laminectomy. A second group of rats was submitted to a hindlimb-unloading period (HU group, n = 6). After 14 days, the morphological and contractile properties as well as the content in myosin heavy-chain (MHC) isoforms were studied in the right soleus muscle in HU and DEAF groups. The results were compared to those obtained in control animals (CON group). After HU versus CON group, the soleus muscle was atrophied and presented a decrease in muscle forces in relation with a slow-to-fast transition characterized by a decrease in kinetic contractile parameters and by an overexpression in the fast MHC isoforms. The DEAF soleus muscle showed both a significant muscle atrophy and a loss of forces when compared with CON rats. The comparison between DEAF and HU rats indicated that some modifications occurring after HU are purely of motor origin (i.e., slow to fast transition), whereas muscle atrophy and decrease in muscle force are partly the result of an afferent silent. Our study underlined the importance of afferent input integrity in the maintenance of muscle characteristics.

Introduction

Hindlimb unloading (HU) is a well-known model to mimic the effects of real weightlessness (Morey et al., 1979). In hindlimb muscles, an exposure to HU induces marked changes in extensor muscles such as soleus or vastus intermedius, whereas the HU impact is less important in fast muscles such as the tibialis anterior and the extensor digitorum longus (for review see Thomason and Booth 1990, Edgerton and Roy 1996, Fitts et al 2000, Ohira 2000. In the rat soleus, after HU, decreases in muscle mass and cross-sectional area of muscle fiber have been currently described. A shift of the muscle type from a slow to a fast one is reported; the contractile properties and the contractile protein isoforms evolve toward those characterizing a fast muscle Stevens et al 1999, Fitts et al 2000, Ohira 2000, Bastide et al 2002, Stevens et al 2002. Some muscular changes observed after HU could be attributed to modifications in EMG activity. Indeed, it has been demonstrated by Alford et al. (1987) that this experimental condition induced, in the soleus muscle, a total EMG disappearance in the 3 s following HU. However, these authors described a progressive return of EMG activity closer to normal values after only 7 days of HU (81% of control EMG activity). This result is in partial disagreement with those of Blewett and Elder (1993), who have demonstrated more recently that the EMG soleus activity remained quantitatively and qualitatively decreased even after 28 days of HU. Moreover, the EMG pattern was shifted from a tonic to a phasic-type characteristic of a fast muscle type (Riley et al., 1990). Consequently, taking into account these latter results, it was tempting to speculate that some muscle changes observed after HU are directly related to both the nature and the level of EMG activity, as suggested by Leterme and Falempin (1994). The muscle position during HU could also be a trigger to changes observed in simulated microgravity. In this situation the soleus muscle is often in a shortened position (Riley et al., 1990), and it can be supposed that muscle spindles which are stretch sensors, are probably not activated. During real or simulated microgravity this deficiency in the muscular afferent message may be considered as a functional deafferentation as previously suggested by several authors Money and Cheung 1991, De-Doncker et al 2000. As the contractile properties of the soleus muscle and its composition in myosin isoforms have never been studied after deafferentation, the aims of this study were thus (1) to determine whether a chronical deafferentation induces significant modifications in the morphological and contractile properties of the soleus muscle and in its myosin heavy-chain (MHC) content and (2) to compare the effects of a terrestrial deafferentation with changes induced by a HU period in the soleus muscle. We were then able to predict whether afferent activity had a real impact on muscular modifications observed in HU.

Section snippets

Animal groups

Male Wistar rats (Iffa Credo, l’Arbresle, France) weighing 280–300 g were divided randomly into three groups: control (CON, n = 6), hindlimb unloading (HU, n = 6), and terrestrial deafferentation (DEAF, n = 6). The rats were housed individually in conventional plastic cages and had free access to food and water. The rats were kept at a 25°C room temperature and under a 12:12 h light:dark cycle. All procedures described below were approved by both the Agricultural and Forest Ministry and

Muscle weight and cross-sectional area of muscle fibers

The data of each experimental group are reported in Table 1. For all three groups, the animals’ body weight (BW) remained similar after 14 days of experimentation with values between 284 and 300 g. However, compared with the CON group, the DEAF and HU groups showed a significant decrease in both MWW and MWW to BW ratio. These two parameters remained significantly different when DEAF was compared to HU group. MWW and MMW/BW in the DEAF group presented intermediate values between those of CON and

Discussion

The aim of this study was to determine whether the abolition of the afferent message induced muscular changes similar to those observed after a HU period.

Our results showed, after HU, a muscle atrophy assessed by a decrease in the CSA of all fiber types. This atrophy, correlated with a decrease in normalized muscle force, has usually been attributed to a decrease in muscle protein synthesis and to an increase in protein degradation Thomason et al 1987, Bock 1998. Moreover, the muscle type

Acknowledgements

This study was supported by grants from the “Centre National d’Etudes Spatiales” (3194) and the “Conseil Régional du Nord-Pas-de-Calais.” The authors thank Dr. G.S. Butler-Browne for the growing of hybridomas producing SC-71 and BF-F3 antibodies initially developed by Dr. Schiaffino et al. (1989). The hybridomas are commercialized by DSMZ (Deutsche Sammlung von Mikroorganismen und Zellkulturen Gmbh, Germany).

References (40)

  • L. De-Doncker et al.

    Effects of cutaneous receptor stimulation on muscular atrophy developed in hindlimb unloading condition

    J. Appl. Physiol.

    (2000)
  • V.R. Edgerton et al.

    Neuromuscular adaptations to actual and simulated spaceflight

  • M. Falempin et al.

    Time-course of soleus muscle-change in and-recovery from disuse atrophy

    Physiologist

    (1990)
  • M. Falempin et al.

    Influence of brief daily tendon vibration on rat soleus muscle in non-weight-bearing situation

    J. Appl. Physiol.

    (1999)
  • S.P. Fauteck et al.

    Sensitive detection of myosin heavy chain composition in skeletal muscle under different loading conditions

    Am. J. Physiol. Cell Physiol.

    (1995)
  • R.H. Fitts et al.

    Physiology of a microgravity environment invited reviewmicrogravity and skeletal muscle

    J. Appl. Physiol.

    (2000)
  • P. Hnik et al.

    EMG changes in rat hind limb muscles following bilateral deafferentation

    Pflugers Arch.

    (1982)
  • J. Kucera

    Myofibrillar ATPase activity of intrafusal fibers in chronically deafferented rat muscle spindles

    Histochemistry

    (1980)
  • D. Leterme et al.

    Compensatory effects of chronic electrostimulation on unweighted rat soleus muscle

    Pflugers Arch.

    (1994)
  • E. Loukianov et al.

    Enhanced myocardial contractility and increased Ca2+ transport function in transgenic hearts expressing the fast-twitch skeletal muscle sarcoplasmic reticulum Ca2+-ATPase

    Circ. Res.

    (1998)
  • Cited by (0)

    View full text