Elsevier

Neuroscience

Volume 17, Issue 4, April 1986, Pages 929-933, 935-952
Neuroscience

Behavior of neurons in the abducens nucleus of the alert cat—I. Motoneurons

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Abstract

The activity of 53 antidromically identified abducens motoneurons was analyzed in alert cats during spontaneous and vestibular induced eye movements. Conduction velocities ranged from 13 to 70 m/s and all motoneurons increased their discharge rates with successive eye positions in the abducting direction. Motoneurons were recruited from −19° to +7°. Within the oculomotor range frequency saturation was never observed for any cell. The slope of rate-position (k) relationships ranged from 2 to 17.7 spikes/s/deg (n = 40, mean 8.7 ± 2.5). Regression analysis showed that the rate-position plots could be fit by straight lines but in most cases exponential curves produced slightly better statistical fits. Steeper slopes suggest that successively larger increases in k are required for the lateral rectus muscle to maintain more eccentric fixations in the on direction.

Interspike intervals for a constant eye position exhibited low variability (< < 3.5%) for fixations shorter than I s. Over longer periods, variability increased in proportion to the duration of the fixation in exponential-like fashion up to 14%. Abducens motoneurons showed considerable variability in frequency during repeated fixations of the same eye position. Discharge rates were found to depend upon both the direction of the previous eye movement and, more importantly, the animal's level of alertness. The rate-position regression lines for fixation periods after saccades in the on direction significantly differed in slopes (100%) and thresholds (20%) from those in the off direction. The observed static hysteresis in abducens motoneuron behavior was in opposite direction to that previously described for the mechanical properties of the lateral rectus. This suggests both neural and mechanical factors are significantly involved in determining final eye position. The animal's level of alertness was evaluated in this study by counting the number of saccadic movements/s occurring in “alert” (1 ± 0.2 saccades/s), and “drowsy” (0.5 ± 0.2 saccades/s) circumstances. Comparison of the rate-position regression lines between the two conditions showed a significant decrease in slopes (100%) and elevation of thresholds (70%).

Discharge rate of abducens motoneurons increased abruptly 8.9 ± 2.8 ms prior to saccades in the horizontal on direction, and decreased 14.8 ± 4.05 m before saccades in the off direction. During purely vertical saccades the firing frequency of abducens motoneurons did not change. Burst frequency did not saturate during saccades, but increased with saccadic velocity in a linear fashion. Slopes (rs) of rate-velocity regression lines ranged from 0.64 to 2.2 spikes/s/deg/s (n = 14, mean 1.13 ± 0.45). During saccades in the off direction, discharge frequency always decreased, but it was not necessarily extinguished. Rate-velocity regression lines measured after spontaneous saccades (rs) and during the fast phase of vestibular nystagmus (rsv = 1.11 ± 0.40spikes/s/deg/s) showed no significant differences. However, rs and rsv values were significantly different from slow phase velocity during vestibular stimulation (rv = 1.31 ± 0.34spikes/s/deg/s) in 4/14 motoneurons. These data suggest that in a minority of motoneurons a different source and/or pattern of synaptic innervation produces the two types of eye movements.

Firing rate showed a continuously changing profile during saccades. Maximum intra-burst frequency was reached before peak velocity and decayed in exponential-like fashion with time constants ranging from 10 to 150 ms. For saccades in the off direction the opposite relationship held. During lowered states of alertness the sharp increase in frequency during saccades was less noticeable and in many cases occurred after onset of eye movement. Wide variations in burst onset and intra-burst frequency including the absence of saturation largely explains the observation that saccades in the cat are generally 60% slower than in monkey.

Sinusoidal head rotation in the dark produced a phase lead of abducens motoneurons with respect to eye position. Time constants (T0) calculated from phase leads between firing rate profiles and eye position during the sinusoidal rotation ranged from 90.0 to 197 ms with a mean of 143.1 ± 35.1. The ranges and means were not significantly different from time constants calculated from individual Ts = r/sk (126.6 ± 58.0), Tsv = rsv/k (123.0 ± 51.7) and Tv = rv/k (143.4 ± 32.2) quotients.

Qualitatively and quantitatively, every motoneuron participated in all types of horizontal conjugate eye movements. A significant correlation was found between the eye position threshold at which a motoneuron began to fire and the slope of its rate-position regression line (k). The slope for the linear regression was 0.3. In addition, there was a correlation between the proportionality constant (k) and conduction velocity. The above relationships suggest a basis for relating the functional characteristics of abducens motoneurons to their electrophysiological properties. As such these data underline the advantages of evaluating the individual role of motoneurons in eye movement from the perspective of a continuous structure-function entity centered around, but not dependent on, features attributed to the size principle.33.34

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