Hindlimb unweighting for 2 weeks alters physiological properties of rat hindlimb motoneurones

Abstract

We sought to determine whether decreased neuromuscular use in the form of hindlimb unweighting (HU) would affect the properties of innervating motoneurones. Hindlimb weight-bearing was removed in rats for a period of 2 weeks via hindlimb suspension by the tail. Following this the electrophysiological properties of tibial motoneurones were recorded under anaesthesia in situ. After HU, motoneurones had significantly (P < 0.05) elevated rheobase currents, lower antidromic spike amplitudes, lower afterhyperpolarization (AHP) amplitudes, faster membrane time constants, lower cell capacitances, and depolarized spike thresholds. Frequency-current (f -I) relationships were shifted significantly to the right (i.e. more current required to obtain a given firing frequency), although there was no change in f -I slopes. 'Slow' motoneurones (AHP half-decay times, > 20 ms) were unchanged in proportions in HU compared to weight-bearing rats. Slow motoneurones had significantly lower minimum firing frequencies and minimum currents necessary for rhythmic firing than 'fast' motoneurones in weight-bearing rats; these differences were lost in HU rats, where slow motoneurones resembled fast motoneurones in these properties. In a five-compartment motoneurone model with ion conductances incorporated to resemble firing behaviour in vivo, most of the changes in passive and rhythmic firing properties could be reproduced by reducing sodium conductance by 25% and 15% in the initial segment and soma, respectively, or by increasing potassium conductance by 55% and 42%, respectively. This supports previous conclusions that changes in chronic neuromuscular activity, either an increase or decrease, may result in physiological adaptations in motoneurones due to chronic changes in ion conductances. The rat model of hindlimb unloading (HU), also known as hindlimb suspension, has proven to be a valuable ground-based model of the weightlessness that occurs during space flight (Morey-Holton & Globus, 2002). Despite the wealth of information from studies using HU on changes that occur in muscle following the removal of weight-bearing, very little is known about changes in the electrophysiological properties of the innervating motoneurones. Reported changes in voluntary recruitment and locomotor patterns following space flight and HU are consistent with possible changes in the excitability of motoneurones (Layne et al. 1997;Canu & Falempin, 1997Anderson et al. 1999;Edgerton et al. 2000;Recktenwald et al. 2000;Hodgson et al. 2000;Canu et al. 2001). Changes have been reported in hindlimb Hoffman reflex gain following 3 weeks of HU; however, it is unknown to what extent motoneurone excitability versus synaptic efficacy were involved in this adaptation (Anderson et al. 1999). During various models of decreased neuromuscular activity, including joint immobilization, bed rest, 'dry' water immersion and space flight, the ability to maximally activate muscles voluntarily is compromised, and there is EMG evidence that motor control is significantly altered (Duch...

Characteristics and Organization of Discharge Properties in Rat Hindlimb Motoneurons

“…Much of this information has been obtained for turtle or cat motoneurons or rat sacrocaudal (tail) motoneurons. Several studies have been performed on the discharge properties of rat hindlimb motoneurons to assess normal function or changes following spinal injury, hindlimb disuse, or hindlimb exercise (Beaumont et al 2004(Beaumont et al , 2008Button et al 2006Button et al , 2008Cormery et al 2005), but direct measurements of PIC activation have not been made in rat hindlimb motoneurons.…”

The influence of a 5-wk whole body vibration on electrophysiological properties of rat hindlimb spinal motoneurons

“…Adaptations to an increased or a decreased functional motor demand can be observed as early as after 2-4 wk of an altered motor behavior (Cormery et al 2000(Cormery et al , 2005. Considerable changes in passive or active membrane properties, motoneuron excitability, or firing properties have been established in rat spinal motoneurons as effects of spontaneous running or a locomotor training Gardiner 2002, 2003), in muscle unweighting (Cormery et al 2005) or tetrodoxininduced paralysis (Cormery et al 2000).…”

Activation of respiratory muscles does not occur during cold-submergence in bullfrogs,Lithobates catesbeianus

“…To reconcile our findings that bullfrogs do not undergo respiratory motor decline following overwintering submergence (Santin and Hartzler, 2016a,b), we hypothesized that bullfrogs would utilize these mechanics during cold-submergence to circumvent the loss of function typically associated with extended disuse in less-active motor systems of non-hibernating mammals (Bonaldo and Sandri, 2013;Cormery et al, 2005;Seki et al, 2007) and certain muscles of heterothermic hibernators (Wickler et al, 1991). We found that underwater lung ventilation cycles, but not buccal oscillations, were present in diving bullfrogs at 20°C, but respiratory muscle activation did not occur during cold-submergence at any time point in this study.…”

“…Our findings demonstrate that cold-submergence associated with overwintering produces neuromotor inactivity; a phenomenon that does not usually occur naturally in highly active motor systems as it incurs detrimental consequences to motor function (Banzrai et al, 2016;Bonaldo and Sandri, 2013;Cormery et al, 2005). Muscle plasticity in natural models of inactivity has received considerable attention (Hudson and Franklin, 2002;James et al, 2013;Nowell et al, 2011;Reid et al, 1995;Wickler et al, 1991).…”

“…Overwintering submergence presents a springtime challenge because disuse of neuromotor processes typically leads to loss-offunction through muscle atrophy and neuroplastic motor defects, especially in humans and laboratory rodents (Bonaldo and Sandri, 2013;Clark et al, 2006;Cormery et al, 2005;Deschenes et al, 2002;Seki et al, 2007). Hibernating, overwintering and estivating vertebrates provide interesting exceptions to this rule as they use integrative mechanisms to curtail muscle atrophy and motor decline during extended inactivity (Hudson and Franklin, 2002).…”