Responses of medial rectus motoneurons in monkeys with strabismus

Abstract

Purpose: Monkeys reared under conditions of alternating monocular occlusion during their first few months of life show large horizontal strabismus, "A" patterns, and dissociated vertical deviation. "A" patterns manifest as an inappropriate horizontal component in the deviated eye during vertical eye movements (cross-axis movement). The objective of this study was to investigate response properties of medial rectus motoneurons (MRMNs) in relation to strabismus properties.

Methods: Burst-tonic activity of 21 MRMNs in the oculomotor nucleus were recorded from two monkeys with exotropia as they performed horizontal and vertical smooth pursuit (0.2 Hz, ±10°) under monocular viewing conditions. Neuronal responses and horizontal component of eye movements were used to identify regression coefficients in a first-order model for each tracking condition.

Results: Comparison of position, velocity, and constant parameter coefficients, estimated from horizontal tracking data with either eye viewing, showed no significant differences (P > 0.07), indicating that neuronal activity could account for the horizontal misalignment. Comparison of the position, velocity, and constant parameter coefficients estimated from horizontal tracking and the cross-axis condition showed no significant differences (P > 0.07), suggesting that motoneuron activity could account for most of the inappropriate horizontal cross-axis movement observed in the covered eye during vertical smooth pursuit.

Conclusions: These data suggest that, in animals with sensory-induced strabismus, central innervation to extraocular muscles is responsible for setting the state of strabismus. Mechanical factors such as muscle length adaptation (for horizontal misalignment) and pulley heterotopy or static torsion (for "A" patterns) likely do not play a major role in determining properties in a sensory-induced strabismus.

Figure 1.

Eye misalignment patterns observed during horizontal and vertical smooth pursuit under monocular viewing conditions (Left: right eye viewing; Right: left eye viewing). In this and other plots upward and rightward eye positions are positive. Left eye data are shown in blue, whereas right eye data are red. Both animals showed significant horizontal misalignment (exotropia) that varied with vertical gaze.

Figure 2.

Plot showing raw eye movement data in animal S2 during horizontal and vertical smooth pursuit (0.2 Hz, ±10°), left eye viewing. The viewing eye (left eye, blue trace) makes a pure horizontal or vertical tracking eye movement. The nonviewing eye (right eye, red trace) shows an inappropriate cross-axis component, that is, inappropriate horizontal eye movement during vertical smooth pursuit (A) and inappropriate vertical eye movement during horizontal smooth pursuit (D). The animal exhibits a small latent nystagmus as seen most clearly on the horizontal left eye trace in (A).

Figure 3.

Single-unit activity in an example right burst-tonic cell (RTBT) motoneuron recorded from the left OMN and projecting to the left eye in S2. Top and middle rows show the averaged horizontal and vertical eye movements from both eyes (right eye, red trace; left eye, blue trace). The bottom row shows the associated neuronal activity. The neuronal activity is correlated with horizontal movements of the left eye for horizontal smooth pursuit with either eye viewing. There is a decrease in baseline activity of the cell during right eye viewing because the left eye is deviated to the left. Fit equations in the two tracking conditions are (A): FR(t) = 5.35E(t) + 1.41E′(t) + 150. (B) FR(t) = 4.06E(t) + 1.25E′(t) + 109.

Figure 4.

Comparison of position sensitivity (K), velocity sensitivity (R), and constant term (C, signifying neuronal response when fixating a straight-ahead stationary target at 0°) during horizontal tracking under left and right eye viewing conditions. On the x-axis is the estimated value during horizontal smooth pursuit when the eye to which the neuron projects is viewing the target; on the y-axis is the estimated value during horizontal smooth pursuit when the eye to which the neuron projects is the nonfixating eye. Note that for sake of simplicity of illustration, the parameter estimates are plotted without signs; otherwise, left-BT motoneurons would have negative parameter estimates. In this figure and in Figure 6, the circles denote left burst-tonic cells (LTBTs), whereas the triangles denote RTBTs. Cells recorded from monkey S1 are shown in red and cells recorded from monkey S2 are shown in green.

Figure 5.

Single-unit activity in a sample binocular motoneuron that was sensitive to rightward eye movements (RTBT motoneuron recorded from left OMN). We observed significant modulation of activity during all four tracking conditions, including during vertical tracking with the left eye viewing (C), when only the right eye shows a horizontal cross-axis component. Binocular fit equations obtained for the horizontal and vertical tracking conditions with combined left eye and right eye viewing data are as follows. (A) and (B): FR(t) = 4.60E_i(t) + 0.39E_i(t) + 1.78E_c(t) + 1.98E_c(t) + 100; CD = 0.98. (C) and (D): FR(t) = 2.85E_i(t) + 0.67E_i(t) + 2.31E_c(t) + 1.23E_c(t) + 77; CD = 0.99.

Figure 6.

Comparison of position (K_i), velocity (R_i), and constant (C) coefficients during horizontal tracking versus cross-axis horizontal component during vertical tracking. On the x-axis are estimated parameter values obtained from the model fits for horizontal smooth tracking with left and right eye viewing data combined. On the y-axis are estimated parameter values obtained from the model fit for the horizontal component during vertical tracking with left and right eye viewing data combined. Color legends as in Figure 4.