Extraocular motor unit and whole-muscle responses in the lateral rectus muscle of the squirrel monkey

Abstract

Because primate studies provide data for the current experimental models of the human oculomotor system, we investigated the relationship of lateral rectus muscle motoneuron firing to muscle unit contractile characteristics in the squirrel monkey. Also examined was the correlation of whole-muscle contractile force with the degree of evoked eye displacement. A force transducer was used to record lateral rectus whole-muscle or muscle unit contraction in response to abducens whole-nerve stimulation or stimulation of single abducens motoneurons or axons. Horizontal eye displacement was recorded using a magnetic search coil. (1) Motor units could be categorized based on contraction speed (fusion frequency) and fatigue. (2) The kt value (change in motoneuronal firing necessary to increase motor unit force by 1.0 mg) of the units correlated with maximum tetanic tension. (3) There was some tendency for maximum tetanic tension of this unit population to separate into three groups. (4) At a constant frequency of 100 Hz, 95% of the motor units demonstrated significantly different force levels dependent on immediately previous stimulation history (hysteresis). (5) A mean force change of 0.32 gm/ degrees and a mean frequency change of 4.7 Hz/ degrees of eye displacement were observed in response to whole-nerve stimulation. These quantitative data provide the first contractile measures of primate extraocular motor units. Models of eye movement dynamics may need to consider the nonlinear transformations observed between stimulation rate and muscle tension as well as the probability that as few as two to three motor units can deviate the eye 1 degrees.

Fig. 1.

Motoneuron and muscle unit twitch response of one unit (A, B) plus EMG and muscle unit twitch response (C, D) of another unit.A, Antidromic response of a lateral rectus motoneuron to abducens nerve stimulation, extracellularly recorded. B, Single-muscle unit twitch in response to activation of motoneuron inA through recording electrode (arrowindicates the time of the action potential of the cell; note different time scale). C, EMG response to stimulation of single abducens nerve axon with brush electrode. D, Simultaneously recorded single-muscle unit twitch response to axonal stimulation of same unit as in C. Calibration:B–D, 5.0 msec (horizontal bar);B, D, 21.0 mg; C, 1.0 mV (vertical bar).

Fig. 2.

A, Twitch tension among 58 units ( $\overline{x}$ = 10.7 ± 5.02 SD). B, Maximum tetanic tension among 53 units ( $\overline{x}$ = 186.2 ± 207.7 SD).C, Twitch contraction time among 58 units ( $\overline{x}$ = 5.2 ± 1.05 SD). D, Fusion frequency among 53 units ( $\overline{x}$ = 190 ± 24 SD).

Fig. 3.

Graphs of fusion frequency versus fatigue index (A) and maximum tetanic tension (B). FF, Fast fatigable;FR, fast fatigue-resistant; FU, fast unclassified as to fatigue; SF, slow fatigable;S, slow; SR, slow fatigue-resistant; SU, slow unclassified as to fatigue. Legend also applies to Figures 4 and 5.

Fig. 4.

Log–log plot of muscle unit kt value (slope of the constant frequency stimulation rate from 50 Hz until fusion frequency vs the resultant forces) versus maximum tetanic tension (r = 0.99). Average kt value of all units = 1.93 Hz/mg.

Fig. 5.

Muscle unit tetanic responses in a weak (A) and a powerful (B) unit. A, 100 Hz constant frequency compared with 100 Hz step after 500/250 Hz pulse starting at similar baselines.B, One hundred Hertz constant frequency compared with 100 Hz step after 500/250 Hz pulse starting at similar baselines.Arrows in A and B indicate the points at which tensions were compared. C, Maximum tetanic tension plotted against the ratio of step tension to constant frequency tension. Note that the weaker units tend to have higher ratios (greater hysteresis).

Fig. 6.

Whole lateral rectus muscle tetanic responses in grams. Degree of eye displacement is included for identical stimulation parameters in the same muscle. Constant frequency stimulation at 100, 150, 180, and 210 Hz from bottom to top. Calibration: 50 msec (horizontal bar), 1.84 gm (vertical bar).

Fig. 7.

A, Whole lateral rectus muscle tetanic tension versus degree of eye movement in four animals. Note slope of tension change (grams) per degree for each animal with an average of 0.32 gm/°. B, Constant frequency stimulation delivered to the whole sixth nerve versus degree of eye movement in four animals. Note slope of frequency change per degree for each animal with an average of 4.7 Hz/°.