Intrinsic mechanisms contributing to the biophysical signature of mouse gamma motoneurons.

Abstract

Precise motor control relies on continuous sensory feedback from muscles, a process in which gamma motoneurons play a key role. These specialized spinal neurons innervate intrafusal muscle fibres, modulating their sensitivity to stretch and maintaining proprioceptive signalling during movement. Gamma motoneurons are characterized by a distinct biophysical profile, including low recruitment thresholds and high firing rates that enable rapid activation of intrafusal fibres at contraction onset. Despite their importance, the intrinsic mechanisms that underlie these properties remain poorly understood. In the present study, we analysed published and unpublished data to identify a population of low-threshold, high-gain motoneurons with features consistent with gamma motoneurons, emerging during the third postnatal week in mice. Their low recruitment threshold was linked to lower membrane capacitance, higher input resistance, a more hyperpolarized activation of persistent inward currents (PICs) and a narrower axon initial segment. By contrast, higher firing rates were associated not with PIC amplitude but with shorter action potential durations and smaller medium afterhyperpolarizations. Notably, 92% of putative gamma motoneurons exhibited a sodium pump-mediated ultra-slow afterhyperpolarization, which was absent in slow alpha motoneurons. This difference could not be attributed to h-current activity or expression of the alpha 3 subunit of the sodium-potassium ATPase. These findings reveal key intrinsic properties that support the unique excitability of gamma motoneurons, offering new insight into their contribution to motor control. This work provides a foundation for future studies into their development, regulation and involvement in neuromuscular disorders. KEY POINTS: A distinct cluster of motoneurons with low recruitment current and high firing gain, characteristic of gamma motoneurons, emerges in the third week of postnatal development. Gamma motoneurons have a low recruitment current as a result of lower capacitance, higher input resistance and a more hyperpolarized activation voltage for persistent inward currents. Their high firing rates are not driven by differences in persistent inward current amplitude but are instead attributed to shorter duration action potentials and smaller amplitude medium afterhyperpolarizations. A narrower axon initial segment in gamma motoneulrons may contribute to their increased excitability compared to alpha motoneurons. Gamma motoneurons present with a higher prevalence of ultra slow afterhyperpolarization than slow alpha motoneurons that cannot be accounted for by differences in h-current or expression of alpha 3 subunits of the sodium potassium ATPase pump.