Intrinsic properties of spinal motoneurons degrade ankle torque control in humans

Abstract

Motoneurons are the final common pathway for all motor commands and possess intrinsic electrical properties that must be tuned to control muscle across the full range of motor behaviors. Neuromodulatory input from the brainstem is likely essential for adapting motoneuron properties to match this diversity of motor tasks. A primary mechanism of this adaptation, control of dendritic persistent inward currents (PICs) in motoneurons by brainstem monoaminergic systems, generates both amplification and prolongation of synaptic inputs. While essential, there is an inherent tension between this amplification and prolongation. Although amplification by PICs allows for quick recruitment and acceleration of motoneuron discharge during discrete motor tasks, PICs must be deactivated to de-recruit motoneurons upon movement cessation. In contrast, during stabilizing or postural tasks, PIC-induced prolongation of synaptic inputs is likely critical for sustained motoneuron discharge. Here, we designed two motor tasks that show PIC amplification and prolongation may conflict and generate errors that degrade the precision of motor output in humans. This included a paradigm comprised of a discrete motor task superimposed atop a stabilizing task and a paradigm with muscle length-induced changes to the balance of excitatory and inhibitory inputs available for controlling PICs. We show that prolongation from PICs introduces deficits in ankle torque control and that these deficits are further degraded at shorter muscle lengths when PIC prolongation is greatest. These results highlight the necessity for inhibitory control of PICs and showcase issues that are introduced when inhibitory control is perturbed or constrained. Our findings suggest that, like sensory systems, errors are inherent in motor systems. These errors are not due to problems in the perception of movement-related sensory input but are embedded in the final stage of motor output.

Antagonism of 5‐HT2 receptors attenuates self‐sustained firing of human motor units

“…We have previously detailed MU discharge and recruitment properties using trapezoidal-shaped contractions generated by ankle dorsiflexors (Goodlich et al, 2023a), where subtle signs of hysteretic behaviour are observable for contraction intensities up to 30% MVC. In the current study we reinforce that self-sustained firing in motoneurones is more readily observable during the performance of a 10% MVC trapezoidal-shaped contraction that includes a brief period where additional descending drive was delivered to the motoneurone pool (Beauchamp et al, 2023). Additional descending drive will necessarily recruit higher threshold MUs (Adrian & Bronk, 1929;Henneman, 1977) and the linear ramp will cause PIC activation for these MUs (Binder et al, 2020).…”

“…1A). Since a shortened agonist muscle can enhance self-sustained MU firing in humans (Beauchamp et al, 2023), the right foot was positioned at 10°of dorsiflexion A, the right foot of the participant was secured to a torque sensor and HDsEMG electrodes were fixed over the tibialis anterior muscle belly. B, trapezoid and sombrero-shaped isometric dorsiflexions were performed during testing.…”

“…Following this, participants then performed five repetitions of pre-drug sombrero contractions. The sombrero contraction has been previously used during ankle dorsiflexions (Beauchamp et al, 2023) and is comprised of two 10 s plateaus at 10% MVC, separated by a 20 s superimposed triangular contraction which peaked at 30% MVC (Fig. 1B).…”

Voluntary co-contraction of ankle muscles alters motor unit discharge characteristics and reduces estimates of persistent inward currents

“…Another limitation is that we only analyzed the isometric condition in a single ankle position (i.e., at 100º). Alterations in the ankle angle can modify passive and active joint moments (Jamwal et al, 2017), contractile properties of the muscles (i.e., tension-length relationship) (Rassier et al, 1999;Cadeo et al, 2023) and, in particular, motor unit discharge rate profiles and estimates of PICs (Beauchamp et al, 2023b). Thus, a different ankle position could influence the recruitment threshold and discharge rate of the motor units required to maintain zero torque at the ankle during voluntary co-contraction.…”