Plasticity of rat motoneuron rhythmic firing properties with varying levels of afferent and descending inputs

Abstract

MacDonell CW, Button DC, Beaumont E, Cormery B, Gardiner PF. Plasticity of rat motoneuron rhythmic firing properties with varying levels of afferent and descending inputs. J Neurophysiol 107: 265-272, 2012. First published September 28, 2011 doi:10.1152/jn.00122.2011.-Hindlimb motoneuron excitability was compared among exercise-trained (E), sedentary (S), and spinal cord transected (T) Sprague-Dawley rats by examining the slope of the frequency-current (F/I) relationship with standard intracellular recording techniques in rats anesthetized with ketamine-xylazine. The T group included spinal transected and spinal isolated rats; the E animals were either spontaneously active (exercise wheel) or treadmill trained; and rats in the S group were housed in pairs. An analysis of motoneuron initial [1st interspike interval (ISI)], early (mean of 1st three ISIs), and steady-state (mean of last 3 ISIs) discharge rate slopes resulting from increasing and decreasing 500-ms injected squarewave depolarizing current pulses was used to describe rhythmic motoneuron properties. The steepest slope occurred in the S group (55.3 Ϯ 22.2 Hz/nA), followed by the T group (35.5 Ϯ 15.3 Hz/nA), while the flattest slope was found in the E group (25.4 Ϯ 10.9 Hz/nA). The steepest steady-state slope occurred in the S group but was found to be similar between the T and E groups. Furthermore, a spikefrequency adaptation (SFA) index revealed a slower adaptation in motoneurons of the E animals only (ϳ40% lower). Finally, evidence for a secondary range of firing existed more frequently in the T group (41%) compared with the S (12%) and E (31%) groups. The lower F/I slope and lower SFA index of motoneurons for E rats may be a result of an increase in Na ϩ conductance at the initial segment. The results show that motoneuronal rhythmic firing behavior is plastic, depending on the volume of daily activation and on intact descending pathways.exercise; frequency-current relation; electrophysiology SEVERAL INVESTIGATIONS have illustrated plasticity of motoneurons by decreasing neuromuscular activity, eliminating supraspinal (spinal transected) and afferent (spinal isolation) activity, or increasing activity through exercise. Decreased neuromuscular activity tends to decrease excitability (Cormery et al. 2000(Cormery et al. , 2005 and shift the frequency-current (F/I) relation to the right (Cormery et al. 2005), while spinal transection and isolation result in motoneurons that show changes that lead to both increases and decreases in excitability. While the response of motoneurons to reduced activity is complex and may be mediated partly by descending drive and reduced neuromuscular activation, an increased activity paradigm (by way of exercise) results in adaptations that tend to increase the excitability of the motoneuron Gardiner 2002, 2003). The mechanisms for changes to motoneuron properties may be due to changes in ionic conductance, as suggested when the Dai et al. (2002) motoneuron model was applied to findings in the Cormery et al. (2005) study....

Differences in Supraspinal and Spinal Excitability during Various Force Outputs of the Biceps Brachii in Chronic- and Non-Resistance Trained Individuals

“…In animals, endurance training decreased the current required to discharge a motoneurone to fire but not the amount of current required to elicit an action potential 50% of the time (i.e. rheobase current) [47]. In humans, Van Cutsem et al [36] showed a shift in tibialis anterior motor unit recruitment thresholds (i.e.…”

Extensor motoneurone properties are altered immediately before and during fictive locomotion in the adult decerebrate rat

“…Differences in motoneurone properties between the non‐locomotor and locomotor states might be different in adult rats with different daily activity patterns (Barnett, ) compared to cats, given the increased excitability (Beaumont & Gardiner, , ) and decreased rate of adaptation (MacDonell et al . ) noted in ‘anaesthetized’ motoneurones in rats after endurance training.…”

“…) and have been shown to respond to training (Beaumont & Gardiner, , ; MacDonell et al . ) and disuse (Cormery et al . , ; Button et al .…”

Understanding exercise-dependent plasticity of motoneurons using intracellular and intramuscular approaches

“…More comprehensive reviews Gardiner 2006) of the changes observed in fast and slow MNs with different training loads suggests that these adaptations do not represent a simple shift in MN type but instead reflect more targeted changes in ionic conductances in different cell types that may function to enhance fatigue resistance during rhythmic firing. In keeping with this idea, exercise-trained animals (treadmill and voluntary wheel) exhibit a 40% lower rate of spike frequency adaptation and a lower frequency-current slope compared with controls (MacDonell et al 2012). These adaptations in rhythmic firing behaviour may optimize force production and allow MNs to maintain muscle output more efficiently during prolonged activity.…”

“…However, intracellular recordings from cat and rat MNs reveal a paradoxical effect of spinal cord transection on MN excitability. Changes in both passive and active electrophysiological MN properties indicate a reduction in MN excitability in cats (Cope et al 1986;Czéh et al 1978;Hochman and McCrea 1994) and rats (Beaumont et al 2004(Beaumont et al , 2008Button et al 2008;MacDonell et al 2012). On the other hand, there is an increase in spastic contractions that may reflect the activation of PIC (Bennett et al 2001a(Bennett et al , 2001bCôté et al 2017), which would enhance MN excitability or polysynaptic reflexes.…”