Effects of persistent inward currents, accommodation, and adaptation on motor unit behavior: a simulation study

Abstract

Revill AL, Fuglevand AJ. Effects of persistent inward currents, accommodation, and adaptation on motor unit behavior: a simulation study. J Neurophysiol 106: 1467-1479. First published June 22, 2011 doi:10.1152/jn.00419.2011.-Motor neurons are often assumed to generate spikes in proportion to the excitatory synaptic input received. There are, however, many intrinsic properties of motor neurons that might affect this relationship, such as persistent inward currents (PICs), spike-threshold accommodation, or spike-frequency adaptation. These nonlinear properties have been investigated in reduced animal preparation but have not been well studied during natural motor behaviors because of the difficulty in characterizing synaptic input in intact animals. Therefore, we studied the influence of each of these intrinsic properties on spiking responses and muscle force using a population model of motor units that simulates voluntary contractions in human subjects. In particular, we focused on the difference in firing rate of low-threshold motor units when higher threshold motor units were recruited and subsequently derecruited, referred to as ⌬F. Others have used ⌬F to evaluate the extent of PIC activation during voluntary behavior. Our results showed that positive ⌬F values could arise when any one of these nonlinear properties was included in the simulations. Therefore, a positive ⌬F should not be considered as exclusive evidence for PIC activation. Furthermore, by systematically varying contraction duration and speed in our simulations, we identified a means that might be used experimentally to distinguish among PICs, accommodation, and adaptation as contributors to ⌬F. motor neuron; computer model; recruitment; muscle MAMMALIAN MOTOR NEURONS have long been considered as prototypical neurons (e.g., Eccles 1950) that integrate synaptic inputs from many sources and are thought to generate action potentials at rates proportional to the overall excitatory input (Granit et al. 1963). There are, however, a number of properties of motor neurons that may disrupt a simple relationship between synaptic input and firing rate output. In this report, we consider three such properties and their effects on motor neuron output, namely, persistent inward currents (PICs), spike-threshold accommodation, and spike-frequency adaptation.First described in the 1970s (Schwindt and Crill 1977), PICs have now been established as a robust intrinsic property of motor neurons

Contribution of intrinsic motoneuron properties to discharge hysteresis and its estimation based on paired motor unit recordings: a simulation study

“…Figure 4 compares ⌬F values for triangular contractions with three different rise times (short: 2.5 s, standard: 5 s, long: 10 s) as well as ramp and hold contractions with ramp rise times of 5 s, but different duration hold phases (5 and 10 s). In agreement with Revill and Fuglevand (2011), contraction duration had no significant effect on ⌬F values in the absence of any spike frequency adaptation (Fig. 4A, one-way ANOVA, F ϭ 1.068, nonsignificant).…”

“…The simulation results of Revill and Fuglevand (2011) suggested that the drop in firing rate produced by adaptation mechanisms should increase with contraction duration, and that the resulting increase in firing rate modulation in the lower threshold reporter unit between recruitment and de-recruitment of the higher threshold test unit would lead to higher ⌬F values. Figure 4 compares ⌬F values for triangular contractions with three different rise times (short: 2.5 s, standard: 5 s, long: 10 s) as well as ramp and hold contractions with ramp rise times of 5 s, but different duration hold phases (5 and 10 s).…”

“…The voltage-dependence of activation was taken from a recent model of the M-current in hippocampal cells (Hu et al 2009), but the kinetics of activation were made two orders of magnitude slower to mimic the outward current used by Revill and Fuglevand (2011) to produce spike frequency adaptation, which had a time constant of 22 s. Although an M-current has been reported in turtle motoneurons (Alaburda et al 2002) and KCNQ channels are present on the initial segments of mouse motoneurons (Duflocq et al 2011), there has been no report of an M-current with a time constant on the order of seconds: we have simply chosen this as a mechanism to produce a slow, outward current.…”

“…The models were driven with noisy, excitatory conductance commands that increased and decreased linearly at different rates, reaching the same peak conductance in 10, 5, or 2.5 s, as in the simulations of Revill and Fuglevand (2011). The excitatory conductance is generated as described in Destexhe et al (2001) and is meant to mimic the random arrival of multiple unitary synaptic events; for an increasing conductance command, the mean and variance increase in parallel (see Fig.…”

“…Subsequent studies have provided evidence that factors other than PIC can contribute to variation in ⌬F values, such as the amount of rate modulation in the reporter unit, and the difference in recruitment times between the reporter and test unit (Powers et al 2008;Stephenson and Maluf 2011). More recently, Revill and Fuglevand (2011) have suggested that other intrinsic properties of motoneurons, such as those underlying spike threshold accommodation and spike frequency adaptation, can lead to positive ⌬F values, even in the absence of a PIC contribution. They also proposed that, by varying contraction duration and speed, it might be possible to distinguish the contribution of PICs, accommodation and adaptation to ⌬F.…”