While motor neuron activity has been studied for many decades, the relative contribution of synaptic and non-synaptic mechanisms underlying this activity during natural behaviors is not well understood. Thus, the goal of this dissertation was to further understand the role of non-synaptic properties of motor neurons during voluntary activity. In particular, I considered three non-synaptic properties: persistent inward currents (PICs) that boost synaptic inputs, spike-threshold accommodation that affects recruitment threshold as excitation rates of rise slow, and spike-frequency adaptation that leads to a decrease in firing rate despite constant excitation levels. Computer simulations were employed to understand the potential effect that these properties could have on firing rate behavior. In particular, the focus was on paired motor unit recordings where a lower threshold motor unit’s firing rate served as a proxy for synaptic drive, and differences in firing rate (ΔF) were compared at a higher threshold unit’s recruitment and derecruitment. While ΔF has been used by others to estimate PIC activation, the simulation results indicated that each of these non-synaptic mechanisms could lead to positive ΔF. Furthermore, by varying contraction speed and duration it seemed possible to determine which property contributes to ΔF in vivo. The results from human experiments indicated that adaptation is most likely the predominant contributor to ΔF during natural behaviors. Additionally, positive ΔF was even observed in the genioglossus muscle of the tongue, where the role of PICs has been debated. These results suggested that ΔF may not the best method to detect PICs during natural behaviors. As such, I also considered whether there might be another metric to infer PIC activation during natural behaviors. Motor unit firing rates tend to plateau, or saturate, despite continued force increase, and one hypothesis is that PICs contribute to this behavior. Indeed, motor unit firing rate saturation was diminished by the addition of inhibition, which should have limited PIC activation. Therefore, this final study provided possible evidence for PIC activation during natural behaviors. Overall, this dissertation highlights that non-synaptic properties of motor neurons are activated during natural behaviors and that they contribute significantly to firing rate output.