Speed and Accuracy of Saccades, Vergence and Combined Eye Movements in Subjects with Strabismus Before and After Eye Surgery
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CORE Metadata, citation and similar papers at core.ac.uk Provided by Elsevier - Publisher Connector Vision Research 49 (2009) 460–469 Contents lists available at ScienceDirect Vision Research journal homepage: www.elsevier.com/locate/visres Speed and accuracy of saccades, vergence and combined eye movements in subjects with strabismus before and after eye surgery Maria Pia Bucci a,*, Dominique Brémond-Gignac a,b, Zoï Kapoula a a IRIS FRE 3154, CNRS, Pôle chirurgie ORL-OPH, Hôpital Robert Debré, Paris, France b Hôpital Robert Debré, Service d’Ophtalmologie, 48 Bld Sérurier, 75019 Paris, France article info abstract Article history: The purpose of the study was to examine spatio-temporal characteristics of horizontal eye move- Received 28 August 2008 ments in the natural space (saccade, vergence and combined movements) in young subjects with Received in revised form 4 December 2008 early onset convergent or divergent strabismus. Nine young subjects (8–20 years old) were tested: three with divergent strabismus, six with convergent strabismus. A standard paradigm was used to elicit pure horizontal saccades at far and at close viewing distance, pure vergence along the median Keywords: plane (convergence and divergence) and saccades combined with vergence movements. Horizontal Strabismus eye movements from both eyes were recorded by a photoelectric device. Eye movements were Saccades recorded before surgery, and, for the majority of the subjects, two times after surgery. Before surgery Vergence Combined movements the accuracy of convergence and divergence movements in their pure or combined form was poor Eye surgery with respect to normal values. The mean velocity of convergence was also abnormally slow. Strabis- mus surgery improved significantly the accuracy of these types of eye movements. The speed of pure convergence and of divergence combined movements increased significantly after surgery. We con- cluded that poor vergence eye movement’s performance, particularly those found for convergence in strabismic subjects could be due to impairment in the central structures related to sensory dispar- ity inputs. Adaptive mechanisms promoted by the realignment of the eyes could be at the origin of the improvement in the vergence performances observed in our subjects after strabismus eye surgery. Ó 2008 Elsevier Ltd. All rights reserved. 1. Introduction alone and combined with saccades in young subjects with conver- gent or divergent strabismus. To shift the gaze to the image of interest, humans use saccades To our knowledge studies examining the accuracy of saccades and vergence eye movements. Saccades are the most rapid move- and vergences eye movements in 3D space in young subjects with ments allowing changing rapidly the fixation to the target; ver- strabismus are scarce. Indeed, the few studies examining the accu- gences are slow movements allowing to adjust the angle of racy of saccades were limited at far viewing distance in strabismic visual axes according to the target’s distance. The most common subjects (Bucci, Kapoula, Yang, Roussat, & Brémond-Gignac, 2002; movements used for exploring the natural world are the combined Kapoula & Bucci, 2002); studies dealing with saccades at near dis- saccade–vergence movements. For a correct localization of the tar- tance do not exist. It should be recalled that reading occurs at near get in direction as well as in depth both sensory and motor fusion distance and to study oculomotor behavior at near is of particular mechanisms are necessary. In about 4% of young population sen- importance. (Kenyon, Ciuffreda, & Stark, 1990) ‘‘also reported that sory and/or motor pathways are not correctly developed leading the vergence movements were considerably reduced in strabismus to a misalignment of the visual axis and strabismus. Strabismus subjects and that, in order to foveate the target, strabismic subjects eye surgery is one of the methods used for treatment (von Noorden made asymmetric vergence movements. More recently, Tychsen & Campos, 2002). and Scott (2003) examined convergence eye movements in esotro- The first question addressed in this study concerns the accuracy pic monkeys and they reported that convergence movements were and the velocity of saccades at different viewing distances; the highly hypometric particularly for the monkey with large devia- accuracy and velocity of vergence (convergence or divergence), tion. The authors suggested that these abnormal convergence re- sponses were due to weak detection of binocular disparity, which is the capacity to perceive depth information from the two differ- * Corresponding author. Fax: +33 1 40 03 53 62. ent retinal images of an object seen by each eye; poor disparity E-mail address: [email protected] (M.P. Bucci). detection could also be at the origin of the asymmetric vergence 0042-6989/$ - see front matter Ó 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.visres.2008.12.006 M.P. Bucci et al. / Vision Research 49 (2009) 460–469 461 made by the animals for fixating targets in depth. Thus, poor accu- common characteristic of all subjects examined was lack of normal racy of convergence in strabismics would be a consequence of the binocular vision and reduced capacity to process binocular visual cortical deficiency in processing disparate stimuli rather disparities. than ocular motor limitation. All subjects underwent to strabismus surgery: recession or Bucci et al. (2002) showed in young subjects with strabismus an tightening of the medial rectus or of the lateral rectus. For subjects improvement of the binocular coordination of their saccades after S4 and S7 the Cuppers technique (Faden procedure, see Roggenk- strabismus surgery. They attributed this to central adaptive mech- amper, 1989) was applied. anisms reducing the initial large saccade disconjugacy; such After eye surgery, at the time indicated in Table 1 (2 weeks to 2 improvement occurred regardless of the type of strabismus, and months) another ophthalmologic and orthoptic examination was of the presence of binocular fusion. The novelty of the present done for all subjects. At this time, the squint angle was reduced study is to examine speed-accuracy characteristics not only of sac- for all subjects. The AC/A ratio, measured for the three subjects cades but also for vergence and combined saccade–vergence with strabismus with an accommodative component (S4, S5 and movements in subjects with strabismus. Moreover, we examined S7) decreased after surgery (S4: from 12.6 to 8.6; S5: from 9 to speed-accuracy for all movements before and after surgery. 7.3 and S7: from 15.6 to 6.6). Our hypothesis is that in the absence of normal binocular dis- After surgery one subject (S7) only developed gross stereopsis parity and sensory capabilities for fusion, vergence eye movements (400” of arc); the two subjects, S1 and S2, who showed stereopsis could be inaccurate or slow, and the interaction of the vergence before surgery maintained the same level afterward. with the saccades could be also abnormal; strabismus surgery All but one subject (S8) were examined a second time, from 3 to could improve, via adaptive mechanisms eye movement perfor- 10 months after the eye surgery, and the deviation was found to be mances. The results confirm these predictions for all individual stable or small improved with respect the previous examination subjects presenting different types of strabismus (convergent, (see Table 1, post-2). Importantly, one subject (S7) with late-onset divergent, distance dependent, partially accommodative). strabismus gained stereopsis of 400”. Given the late-onset of stra- bismus, this subject had some potential for bi-ocular vision. Most 2. Methods likely the realignment of the eyes by the surgery combined with spectacle correction allowed him to recover a certain degree of 2.1. Subjects bi-ocular vision. The investigation adhered to the principles of the Declaration of Nine subjects (8–20 years old) with strabismus participated to Helsinki and was approved by our institutional human experimen- the study. The day before surgery all subjects underwent a com- tation committee. Informed parental consent was obtained for plete ophthalmologic and orthoptic examination. Clinical charac- each subject after explanation of the procedure of the experiment. teristics of each subject are shown in Table 1. Strabismus was Note that six of these subjects participated already to our previ- measured by the cover-uncover test and the bar of prisms. Two ous study (Bucci, Kapoula, Yang, & Brémond-Gignac, 2006)in subjects (S1 and S2) had divergent intermittent strabismus; for which only eye movement’s latencies have been analyzed. the subject S2 and S3 divergent strabismus depended on viewing distance. The other six subjects (S4, S5, S6, S7, S8 and S9) had con- 2.2. Visual display vergent strabismus depending on viewing distance. Strabismus had appeared early (before the age of 2) for all but one subject A horizontal surface placed at eye level of the subject was used (S7). The strabismus was at least partially accommodative for three to provide target-LEDs in the space (see Fig. 1). It consisted of two subjects (S4, S5 and S7). Only subject S5 was amblyopic; only two isovergence circles placed at different distance: one at 20 cm and subjects with divergent strabismus (S1 and S2) had stereopsis the other at 150 cm from the subject. On the circle close to the sub- (examined with the TNO test of stereoacuity). In conclusion, the ject three LEDs were placed; one at the center and the other at