A Gradient in Synaptic Strength and Plasticity among Motoneurons Provides a Peripheral Mechanism for Locomotor Control

The recruitment of motoneurons during force generation follows a general pattern that has been confirmed across diverse species [1–3]. Motoneurons are recruited systematically according to synaptic inputs and intrinsic cellular properties and corresponding to movements of different intensities. However, much less is known about the output properties of individual motoneurons and how they affect the translation of motoneuron recruitment to the strength of muscle contractions. In larval zebrafish, spinal motoneurons are recruited in a topographic gradient according to their input resistance (Rin) at different swimming strengths and speeds. Whereas dorsal, lower-Rin primary motoneurons (PMns) are only activated during behaviors that involve strong and fast body bends, more ventral, higher-Rin secondary motoneurons (SMns) are recruited during weaker and slower movements [4–6]. Here we perform in vivo paired recordings between identified spinal motoneurons and skeletal muscle cells in larval zebrafish. We characterize individual motoneuron outputs to single muscle cells and show that the strength and reliability of motoneuron outputs are inversely correlated with motoneuron Rin. During repetitive high-frequency motoneuron drive, PMn synapses undergo depression, whereas SMn synapses potentiate. We monitor muscle cell contractions elicited by single motoneurons and show that the pattern of motoneuron output strength and plasticity observed in electrophysiological recordings is reflected in muscle shortening. Our findings indicate a link between the recruitment pattern and output properties of spinal motoneurons that can together generate appropriate intensities for muscle contractions. We demonstrate that motoneuron output properties provide an additional peripheral mechanism for graded locomotor control at the neuromuscular junction.