Adaptations of motoneuron properties to chronic compensatory muscle overload

Abstract

Krutki P, Hałuszka A, Mrówczyński W, Gardiner PF, Celichowski J. Adaptations of motoneuron properties to chronic compensatory muscle overload. J Neurophysiol 113: 2769 -2777, 2015. First published February 18, 2015 doi:10.1152/jn.00968.2014.-The aim of the study was to determine whether chronic muscle overload has measurable effect on electrophysiological properties of motoneurons (MNs), and whether duration of this overload influences intensity of adaptations. The compensatory overload was induced in the rat medial gastrocnemius (MG) by bilateral tenotomy of its synergists (lateral gastrocnemius, soleus, and plantaris); as a result, only the MG was able to evoke the foot plantar flexion. To assure regular activation of the MG muscle, rats were placed in wheel-equipped cages and subjected to a low-level treadmill exercise. The intracellular recordings from MG motoneurons were made after 5 or 12 wk of the overload, and in a control group of intact rats. Some of the passive and threshold membrane properties as well as rhythmic firing properties were considerably modified in fast-type MNs, while remaining unaltered in slow-type MNs. The significant changes included a shortening of the spike duration and the spike rise time, an increase of the afterhyperpolarization amplitude, an increase of the input resistance, a decrease of the rheobase, and a decrease of the minimum current necessary to evoke steady-state firing. The data suggest higher excitability of fast-type MNs innervating the overloaded muscle, and a shift towards electrophysiological properties of slow-type MNs. All of the adaptations could be observed after 5 wk of the compensatory overload with no further changes occurring after 12 wk. This indicates that the response to an increased level of chronic activation of MNs is relatively quick and stable. membrane properties; rat MUSCLE OVERLOAD CAN BE ACHIEVED by workload training (Fry 2004;McDonagh and Davies 1984), ablation or tenotomy of synergists (Gardiner et al. 1991;Noble and Pettigrew 1989;Olha et al. 1988), peripheral nerve damage, or denervation of synergistic muscles (Degens et al. 1995). Overload induces measurable adaptive effects in the whole muscle, its motor units (MUs), and individual muscle fibers. The most prominent response is muscle hypertrophy, reflected in the increase of muscle mass, cross-section area, and the increased strength (Allbrook 1981;Seynnes et al. 2006). Some biochemical adaptations related to this hypertrophy have been reported in muscle fibers (Baldwin et al. 1982;Dearth et al. 2013;Ianuzzo and Chen 1979). Several studies have reported changes in contractile properties of MUs in response to chronic muscle overload. They point on increased tetanic forces of all MU types, longer contraction times of fast resistant and slow MUs, decreased fatigue resistance of fast fatigable units, and altered proportions of MUs within an overloaded muscle (Noble and Pettigrew 1989;Olha et al. 1988).It is well documented that motoneurons are highly susceptible to altered levels of physical...

Adaptations of motoneuron properties after weight-lifting training in rats

“…The adaptations concern primarily fast motoneurons and occur before overt muscle hypertrophy. This study once again confirms several previous observations that motoneurons relatively quickly adapt to physical activity (14a), due to, e.g., running exercises, muscle overload, or limb immobilization (5,8,26). Moreover, the presented results at least partially explain recent findings that contractile properties of motor units have been considerably altered after 5 wk of the same strength-training regime despite the absence of changes in the myosin content in muscle fibers (30).…”

“…The final acute electrophysiological experiments were performed on rats from both groups within 48 h after completion of the training program. Surgical procedures proceeded as described in our previous papers (3,26). Rats were deeply anaesthetized by the intraperitoneal injection of sodium pentobarbital (the initial dose of 60 mg/kg supplemented by additional doses of 10 mg•kg Ϫ1 •h Ϫ1 ).…”

“…The antidromic character of a spike was confirmed by its constant and short latency and all-or-nothing appearance. Only stable recordings with the resting membrane potentials of at least Ϫ50 mV and the amplitudes of APs Ͼ50 mV with a positive overshoot were taken into consideration (3,16,26). For each motoneuron, the basic membrane properties were calculated from an average of 10 antidromic spikes: the resting membrane potential (RMP), the AP amplitude, the AP duration (measured at the level of half-amplitude to avoid the inflection of the interspike and the SD components of the spike), the afterhyperpolarization (AHP) amplitude, the AHP time to peak, and the AHP half-decay time (AHP-HDT).…”

Compensatory effects following unilateral diaphragm paralysis

“…With time, excitability of the phrenic motoneuron pool may be restored allowing near maximal recruitment during airway occlusion. Indeed, in limb muscles subjected to chronic compensatory loading induced by synergist ablation, motoneuron excitability (as measured by the threshold properties of motoneurons) reportedly increased over time (Krutki et al, 2015). In the case of the diaphragm muscle, both hemidiaphragms are activated synchronously and are synergistic during ventilatory behaviors (De Troyer et al, 2003).…”

Spinal circuits for motor learning

“…In attempting to answer these questions, we ask whether the development of ion channels in a-MNs depends on activity that will be regulated by the balance of (in this simplified example) feedback (Ia) and feed forward (Renshaw cell) input (see, for example [53]). As comparators, MNs would measure discrepancies between motor commands and motor output, and these discrepancies would provide the stimulus to shape motoneuronal biophysical properties such as channel densities and distributions.…”