Incomitance in monkeys with strabismus

Abstract

Purpose: Rhesus monkeys reared with restricted visual environment during their first few months of life develop large ocular misalignment (strabismus). The purpose of this study was to describe 'A and V' patterns and DVD in these animals during fixation and eye movements and suggest that this form of rearing produces animals that are suitable model to study the mechanisms that might cause 'A/V' pattern incomitant strabismus and dissociated vertical deviation (DVD) in humans.

Methods: Eye movements were recorded during fixation, smooth-pursuit and saccades using binocular search coils in one monkey with esotropia, three monkeys with exotropia and one normal monkey.

Results: 1) Monkeys reared with Alternating Monocular Occlusion or Binocular deprivation (tarsal plates intact) showed both horizontal and vertical misalignment during monocular and binocular viewing. 2) Large 'A' patterns were evident in 2 out of 3 exotropes while a 'V' pattern was observed in the esotrope. 3) Similar 'A/V' patterns were observed with either eye viewing and during fixation or eye movements. 4) The vertical misalignment, which consisted of the non-viewing eye being higher than the fixating eye, appeared to constitute a DVD.

Conclusion: Visual sensory deprivation methods that induce large strabismus also induce 'A/V' patterns and DVD similar to certain types of human strabismus. The source of pattern strabismus could be central, i.e., altered innervation to extraocular muscles from motor nuclei, or peripheral, i.e., altered location of extraocular muscle pulleys.

FIGURE 1

Hess screen chart showing alignment patterns during monocular viewing in strabismic monkeys S1–S4 and in the normal monkey N1. The left column shows alignment data collected during right eye viewing and the right column shows alignment data collected during left eye viewing. Abduction is positive and Adduction is negative. Upward eye positions are positive and downward eye positions are negative. All the strabismic animals suffered from significant horizontal and vertical misalignment during either eye viewing. The horizontal misalignment was either an exotropia (S1, S2, S4) or an esotropia (S3). The following eye was always higher than the fixing eye suggesting the presence of DVD. In each case, there is a change in horizontal misalignment with vertical gaze position resulting in an ‘A’ or ‘V’ pattern. In addition, all the strabismic animals also showed a change of vertical misalignment with horizontal gaze position. The normal animal showed no misalignment and no evidence for ‘A/V’ patterns. The dark line shown in each plot is a linear regression of the vertical gaze positions of the non-viewing eye. The angle ‘θ’ as shown in the top panel of the figure was used to quantify the severity of the incomitance.

FIGURE 2

Correlation of degree of A/V pattern incomitance with initial horizontal misalignment. The horizontal ocular mis-alignment during primary gaze is plotted vs. the degree of A/V pattern strabismus (measured as the angle at the apex of the ‘A’ or ‘V,’ = ‘θ’). On the X-axis, exotropia is plotted as positive and esotropia as negative. On the Y-axis, the ’A’-pattern results in positive angles, while a ‘V’ pattern results in negative angles. A significant correlation was discovered between the degree of horizontal misalignment (ranging from esotropia to exotropia) and the angular subtense (‘θ’) of the A/V pattern.

FIGURE 3

A time series of data collected in exotropic animal S2 during horizontal and vertical saccades and smooth-pursuit (SP) while viewing with the right eye. The top panel shows horizontal position of the viewing (right) and non-viewing (left) eyes. The bottom panel shows vertical position of the viewing (right) and non-viewing (left) eyes. In each case, the viewing eye makes purely horizontal or vertical saccades or smooth-pursuit while the non-viewing left eye shows an inappropriate cross-axis component. Also, the magnitude of horizontal and vertical misalignment for specific gaze positions is similar to that obtained during static fixation as shown in Figure 1. The saccadic data shows that the cross-axis component includes both pulse and step components that occur simultaneously with the purposeful eye movement. Positive values indicate rightward or upward eye positions.

FIGURE 4

(A + B). Panels A and B compare the horizontal and vertical misalignment observed during monocular and binocular viewing in animal S3. Horizontal and vertical misalignment in the OU condition is similar to the OS condition in monkey S3. (C + D). Panels C and D show horizontal and vertical eye position data during a saccade tracking sequence in monkey S2 as he viewed the target binocularly. This animal also chose to fixate and track the target with his left eye. The right eye shows horizontal and vertical misalignment and also cross-axis movements.