Extraocular muscle motor units characterized by spike-triggered averaging in alert monkey

Single-unit recording in macaque monkeys has been widely used to study extraocular motoneuron behavior during eye movements. However, primate extraocular motor units have only been studied using electrical stimulation in anesthetized animals. To study motor units in alert, behaving macaques, we combined chronic muscle force transducer (MFT) and single-unit extracellular motoneuron recordings. During steady fixation with low motoneuron firing rates, we used motoneuron spike-triggered averaging of MFT signals (STA-MFT) to extract individual motor unit twitches, thereby characterizing each motor unit in terms of twitch force and dynamics. It is then possible, as in conventional studies, to determine motoneuron activity during eye movements, but now with knowledge of underlying motor unit characteristics.We demonstrate the STA-MFT technique for medial rectus motor units. Recordings from 33 medial rectus motoneurons in three animals identified 20 motor units, which had peak twitch tensions of 0.5–5.25 mg, initial twitch delays averaging 2.4 ms, and time to peak contraction averaging 9.3 ms. These twitch tensions are consistent with those reported in unanesthetized rabbits, and with estimates of the total number of medial rectus motoneurons and twitch tension generated by whole-nerve stimulation in monkey, but are substantially lower than those reported for lateral rectus motor units in anesthetized squirrel monkey. Motor units were recruited in order of twitch tension magnitude with stronger motor units reaching threshold further in the muscle's ON-direction, showing that, as in other skeletal muscles, medial rectus motor units are recruited according to the “size principle”.

Graphical abstractFigure optionsDownload full-size imageDownload as PowerPoint slideHighlights► We record physiological medial rectus (MR) force using a custom transducer (MFT). ► We simultaneously measure MR motoneuron activity in alert, behaving primates. ► Spike-triggered averaging of MFT signals (STA-MFT) extracts motor unit twitches. ► MR motor units are recruited in order of twitch tension magnitude (size principle). ► Individual extraocular motor units can now be characterized in alert animals.