Acute superior oblique palsy in the monkey: effects of viewing conditions on ocular alignment and modelling of the ocular motor plant

Abstract:

We investigated the immediate and long-term changes in static eye alignment with acute superior oblique palsy (SOP) in the monkey. When the paretic eye was patched immediately after the lesion for 6–9 days, vertical alignment slowly improved. When the patch was removed and binocular viewing was allowed, alignment slowly worsened. In contrast when a monkey was not patched immediately after the lesion vertical alignment did not improve. We also show that a model of the eye plant can reproduce the observed acute deficit induced by SOP, but only by abandoning Robinson's symmetric simplification of the reciprocal innervation relationship within pairs of agonist–antagonist muscles. The model also demonstrated that physiologic variability in orbital geometry can have a large impact on SOP deficits.

Introduction

In human patients with strabismus, vertical misalignment of the eyes that is more pronounced when the higher eye is in adduction is usually attributed to a palsy of the superior oblique muscle (SOP). In many patients, however, it is difficult to reliably differentiate a ‘congenital’ from an acquired SOP. Furthermore, orbital imaging suggests that many patients with a presumed congenital SOP do not have a trochlear (IV) nerve palsy but rather an anatomical abnormality in the orbit that mimics SOP (Chan and Demer, 1999). And even when the evidence points to a complete trochlear nerve palsy, the degree and pattern of the static deviations are variable (Graf et al., 2005; Khawam et al., 1967). Inherent variation in the anatomical configuration of the SO muscle and tendon (Fink, 1962; Helveston et al., 1992), secondary changes in the mechanical properties of the palsied muscle and its antagonists (Robinson, 1985; Jampolsky, 1994; Scott, 1994), and central adaptive processes (Maxwell and Schor, 2006) all conspire against a correct diagnosis.

To provide a frame of reference for analysing the clinical presentation of both acute and chronic SOP in humans, and to gather experimental data for developing better models of the eye plant, we developed an experimental monkey model of acute SOP using intracranial trochlear nerve section (Shan et al., 2007). We sought to isolate the deficit caused by muscle palsy, and to determine what changes in the alignment of the eyes might occur afterwards. Two surprising findings emerged from this study (Fig. 1). First, when the animals (M1 and M2) wore a patch in front of the palsied eye during the days immediately after the IV nerve section, the vertical misalignment gradually decreased over days (left arrow). Second, once the eye patch was removed and binocular vision was allowed, the vertical misalignment worsened again, and even exceeded the initial deficit (right arrow).

These findings point to a critical influence of the pattern of habitual viewing (out of one eye or both) on ocular alignment just after the onset of an acute paralytic strabismus. We speculated that the early improvement in alignment during habitual monocular viewing was mediated by signals from the proprioceptors in the paretic eye, and that the subsequent deterioration was driven, at least in part, by overriding central mechanisms. Here we present some new findings that confirm the importance of the habitual state of viewing (monocular versus binocular) in the early changes in alignment after acute trochlear nerve palsy. We also present preliminary modelling results that help explain the patterns of misalignment observed with SOP.