SEARCH

SEARCH BY CITATION

Keywords:

  • strabismus;
  • strabismic amblyopia;
  • fixation;
  • scanning laser ophthalmoscope (SLO)

Abstract.

  1. Top of page
  2. Abstract.
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. References

Purpose: We performed a qualitative assessment of fixation behaviour in relation to the fovea in patients with strabismic amblyopia.

Methods: The fixation of 25 patients with strabismic amblyopia was examined using a scanning laser ophthalmoscope (SLO). A digital frame grabber board was programmed to scan onto the patient's retina single solid black discs of 5, 10 and 15 degrees in diameter and Landolt Cs in different orientations and corresponding to a visual acuity (VA) of 0.01−0.2 in European decimals. The relative position of the fovea was video-recorded. Fifty video fields per second were plotted as x/y (fixational positions in relation to the fovea) and x/t (motion over time) graphs.

Results: Three main groups of patients were seen. Group 1 (n = 6), with a VA of < 0.1, showed a grossly eccentric and unstable locus of fixation independent of size/type of test stimulus used. Group 2 (n = 15), with VA of 0.1−0.8, initially used an eccentric retinal area for fixation that, however, shifted to the fovea with decreasing size and increasing detail of the target for fixation. Group 3 (n = 4), with VA of 0.3−0.8, had stable central fixation throughout.

Conclusions: We speculate that the reduced VA associated with strabismic amblyopia is due to a defective motor control of fixation that can be modulated by recognitional effort.


Introduction

  1. Top of page
  2. Abstract.
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. References

Strabismic amblyopia is always unilateral and is caused by active inhibition within the cortical pathways of visual input originating from the deviating eye. It is thought to be due to an abnormal binocular experience during early childhood and has long been deemed a deficit in visual resolving capacity alone. Psychophysical investigations have contributed greatly to a better understanding of the amblyopic process as an abnormal binocular experience early in life. The light sense of amblyopic eyes is normal (Schor 1983). However, the reduction in visual acuity (VA) with decreasing luminance is less than that of normal individuals and much less than that of individuals with reduced VA due to morphological changes (Herzau et al. 1989, 1993). Strabismic amblyopes exhibit a distortion of space perception in the deviated eye (Oppel 1962; Hess et al. 1978), as well as impaired localization of objects in space (Bedell & Flom 1981; Bedell et al. 1985). Marked spatial uncertainty and distortion occur in the deviated eye of squinters with both normal and reduced VA (Levi & Klein 1983) but cannot be found in normal eyes in which VA has been artificially reduced (Stigmar 1971; Williams et al. 1984), suggesting that uncertainty in strabismic amblyopic eyes does not result from reduced acuity. It has also long been known that the locus of fixation (normally the foveola) in around 50% of all amblyopic patients is shifted to an eccentric retinal area, without the sensation of eccentric viewing (Mimura et al. 1984). Von Noorden (1966) therefore suggested that eccentric fixation may be caused by an abnormal fixation reflex due to a shift of retinal co-ordinates. We studied the fixation behaviour in strabismic amblyopes using a scanning laser ophthalmoscope (SLO) with the aim of analysing whether fixational control was in any way modulated by recognitional effort.

Materials and Methods

  1. Top of page
  2. Abstract.
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. References

Patients

Twenty-five patients (12 females, 13 males) with strabismic amblyopia (Table 1) were examined according to the tenets of the Declaration of Helsinki. Their ages ranged from 7 to 64 years (mean 28.44 years). Seventeen patients suffered from congenital esotropia, six from exotropia and two from consecutive exotropia. Of the latter two patients, one had suffered from congenital esotropia in childhood and had turned spontaneously exotropic in her early teens, while the other had undergone strabismus surgery abroad as a child. The details of the operation, however, could not be retrieved. Each patient underwent a full orthoptic and ophthalmic examination including assessment of best corrected VA prior to the SLO investigation. Nine patients had a VA ≤ 0.1, whereas 16 had VA of 0.2−0.8 in their amblyopic eye (Table 1). All patients presented to our department with the intention of undergoing squint surgery. Patients exhibiting a strong latent nystagmus were excluded.

Table 1.  Summary of main patient data.
SexForm ofAmblyopicVisual acuityFixationFixationFoveal fixation
 strabismuseye(OD/OS)(Visuscope)SLOpossible?
  1. N/A = not applicable; ND = not done.

  2. Visual acuity provided in European decimals.

FEsotropiaOD0.1/1.0NDNasal/superiorYes
MExotropiaODCF/0.8NDNasal/superiorNo
FExotropia (consecutive)OS1.3/0.05NDTemporalNo
MEsotropiaOS1.3/0.05NasalNasalNo
MEsotropiaOS1.0/0.2NDTemporalYes
MEsotropiaOD0.3/1.3NDNasalYes
MEsotropiaOD0.7/1.3CentralCentralN/A
FEsotropiaOD0.05/1.0NDNasal/inferiorNo
FEsotropiaOD0.5/0.3NDNasalYes
FEsotropiaOS0.6/1.3CentralCentralN/A
MEsotropiaOD0.6/1.0NDNasalYes
MEsotropiaOS1.0/CFNDNasal/inferiorNo
MEsotropiaOS1.3/0.3NDNasalYes
MExotropia (consecutive)OD0.3/1.0CentralCentralN/A
FEsotropiaOS1.3/0.1Foveal (wandering)NasalYes
FExotropiaOD0.5/1.0CentralCentralN/A
FExotropiaOD0.8/1.0CentralTemporal/superiorYes
MExotropiaOD0.6/1.3NDTemporalYes
FEsotropiaOS1.0/0.2NDNasalYes
MEsotropiaOD0.2/1.0CentralNasalYes
MEsotropiaOS0.1/1.0NDNasal/superiorNo
FEsotropiaOD0.2/1.0NDNasalYes
MExotropiaOD0.4/1.3Foveal (wandering)TemporalYes
FEsotropiaOD0.1/1.0NDNasalYes
FExotropiaOS0.8/0.2NDTemporalYes

Scanning laser ophthalmoscopy

An SLO (Model 101; Rodenstock, Munich, Germany) was used to image the fundus (He-Ne laser) and to present stimuli simultaneously using an acousto-optic modulator. A frame grabber board was programmed to present black stimuli that were generated on a bright red background of 3.6 * 104 trolands (contrast 0.986). For fixation targets three solid discs of 15, 10 and 5 degrees and Landolt Cs in decreasing order of size ranging from a linear VA of 0.01–0.2 in European decimals were used (Fig. 1.). This not only allows for exact determination of the position of the fovea in relation to the fixation target and stimulus over time, but also for the measurement of eye movements without calibration. Although the SLO per se allows presentation of smaller stimuli, for the purpose of analysis, the gap of the smallest Landolt C could not be smaller than two video lines corresponding to approximately 5 minutes of arc, equalling a VA of 0.2. The temporal resolution is 50 video fields per second, and the spatial resolution at least 12 minutes of arc.

image

Figure 1. Snapshot of an SLO video sequence. The patient sees a black disc in the middle of a bright red field in the SLO (see inset). The retina and the stimuli are simultaneously observed by the investigator. For offline analysis, the video sequences were digitized and the position of the vessel branching was marked in every video field (50 fields per second). For technical reasons the origin of the co-ordinate system is set at the top left hand corner of the video image. The program calculated the position of the fovea and its change over time.

Download figure to PowerPoint

Procedure

Each patient was asked to fixate on the centre of each of the black discs as if trying to aim at the centre of a target. Then Landolt Cs in decreasing size were presented (Fig. 2.) and the patient was asked to identify the clock orientation of the gap and then to fixate exactly on the gap itself. When the subjective limit of detection (i.e. the gap of the Landolt C could no longer be located correctly) was reached, the examination was terminated. All examinations were performed in both the amblyopic and the sound eye.

Data analysis

A video-recording of each examination was made on S-VHS tape. The fixation was tracked using a semiautomatic program using fundus images that were digitized and transferred to a PC. Fixational eye movements were measured by marking a high contrast landmark (e.g. vessel branching) in every video field of a continuous sequence of at least 4 seconds (200 fields) for each stimulus. The program calculated the landmark's change of position (i.e. its vertical and horizontal co-ordinates) field by field. By referring all values to the anatomical fovea by simple vector calculation (Fig. 1), a continuous trace of fixation plotted as x/y (fixational positions in relation to the fovea) and x/t (motion over time) could be drawn.

Results

  1. Top of page
  2. Abstract.
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. References

When analysing fixation strategy two very distinct patterns were evident: One group of patients (patients 2, 3, 4, 8, 12, 21) fixated eccentrally far away from the fovea. Although all patients in this group correctly identified the gap orientation of the Landolt C (the smal- lest Landolt C recognized defined the highest individual recognitional effort), the locus of fixation did not change to any large extent and remained eccentric throughout the examination (see Figs 3B and 4C, D for examples of fixation strategy and pattern). Four patients in this group had VAs of either 0.05 (patients 3, 4, 8) or 0.1 (patient 21). Two patients in this group at routine VA testing were able to count fingers (CF) only. However when examined with the SLO there was a slight discrepancy (possibly due to the high contrast of the SLO stimuli on the bright red background). Both were able to see the 0.02 or 0.03 Landolt ring, respectively, and thus qualified for analysis. None of the patients when questioned had the impression of ‘indirect viewing’ and all confirmed that the stimulus was ‘straight ahead’.

image

Figure 3. (A) Fixation strategy of patient 20 (exemplary of group 2). The black line shows the sound eye, the grey line the amblyopic eye, respectively, when fixating the target stimulus. ‘0 eccentricity’ describes the fovea. (B) Fixation strategy of patient 4 (exemplary of group 1).

Download figure to PowerPoint

image

Figure 4. Fundus images of patient 20 while fixating (A) the centre of the 15-degree disc (nasally eccentric) and (B) the gap in the Landolt C. Fundus images of patient 21 while fixating (C) the centre of the 15-degree disc (nasosuperiorly eccentric) and (D) the gap in the Landolt C.

Download figure to PowerPoint

The larger group of patients (n = 15), which was also the cohort with better VA (0.2–0.8), showed very clear and consistent fixational strategies (Figs 3A and 4A, B). Initially, fixation remained eccentric when looking at the black discs and the larger Landolt rings. However, it was able to switch to the fovea as soon as recognitional effort was required. Although all the patients were able to keep their fixation foveal as long as they were looking at the required stimulus, some very small nystagmic jerks through the fovea (Fig. 3A) could be detected in almost all cases.

The third group of patients (n = 4) fixated centrally throughout the examination.

Discussion

  1. Top of page
  2. Abstract.
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. References

Strabismic amblyopes show distorted space perception in their deviated eye (Pugh 1958; Hess et al. 1978), as well as an impaired localization of objects in space (Bedell 1981; Bedell et al. 1985). It has been shown that amblyopes make large errors in partitioning horizontal lines (Bedell 1981) as well as in vertical alignment when compared to strabismics without amblyopia (Bedell 1981; Bedell et al. 1985; Fronius & Sireteanu 1989). Bedell et al. (1985) speculated that reduced VA and abnormal eye movements are not the causes but, rather, the consequences of distortions and uncertainty originating at a central level, possibly ‘at the visual cortex’. Strabismics with normal or nearly normal acuity frequently exhibit oculomotor abnormalities such as unsteady and eccentric fixation (Flom & Weymouth 1961; Ciuffreda et al. 1979) and inaccurate pursuit tracking (van Hof-van Duin & Mohn 1982). These strabismics are often uncertain in making visual discriminations and in performing visually guided tasks with the deviated eye (Pugh 1958; May et al. 1983). Quantitatively more severe oculomotor and sensory abnormalities occur in strabismic amblyopic eyes (Flom & Weymouth 1961; Ciuffreda et al. 1979; Schor 1983), suggesting that these abnormalities exist as a manifestation of the same phenomenon and may be related roughly to the acuity level. It is indeed important to consider the relation between the fixation pattern and VA. The normal decrease in VA is a function of the distance of the object image from the fovea. However, this does not hold true for the amblyopic eye, where factors other than eccentricity of fixation alone determine the degree of visual acuity (von Noorden & Helveston 1970), although eyes with low VA tend to have greater eccentricity of their fixation pattern (von Noorden & Mackensen 1962; Mackensen et al. 1967; von Noorden 1969; von Noorden & Helveston 1970). Some amblyopic eyes can be induced to assume spontaneous central fixation relatively easily. Such eyes do not, however, necessarily attain normal vision, although it is also true that unless foveolar fixation is achieved, the physiological basis for a normal VA is absent. There are basically two opposing theories with regard to the pathogenesis of non-foveolar fixation. The Cüppers Theory, often referred to as the ‘Correspondence Theory’, states that the ‘straight-ahead’ sensation is no longer transmitted by the fovea but rather by some eccentric retinal area and due to this shift the patient no longer fixates with the fovea (Cüppers 1956). Cüppers equated loss of the straight-ahead sensation by the fovea with loss of the principal visual direction in anomalous correspondence (Cüppers 1956, 1961, 1966), as he never found normal correspondence in patients with eccentric fixation. As a consequence of this theory the degree of eccentricity of fixation should be identical to the angle of anomaly, which according to Cüppers is true for 50% of cases. A great deal of work has gone into verifying Cüppers' claim and the results obtained were equivocal (von Noorden & Mackensen 1962; von Noorden 1969). The other, even older, theory is the ‘Scotoma Theory’, according to which the amblyopic eye fixates with that retinal area adjacent to the scotoma that has the highest resolving power (Böhme 1955; Oppel 1962; Aggarwal & Verma 1980). This theory has also failed to achieve unanimous support (Mackensen 1957; Aulhorn 1967; Aulhorn & Lichtenberg 1972; Hess 1977; Avetisov 1979; Mimura et al. 1984). An alternative explanation for the eccentric fixation in strabismic amblyopes was given by von Noorden (1969), who suggested that eccentric fixation may be caused by an abnormal fixation reflex. A visual object falling on the peripheral retina of a normal eye elicits a fixation reflex that will cause the eye to move so that the image is shifted from the periphery to the fovea. In contrast to acquired maculopathy, where patients fixate eccentrically but still have the sensation of ‘indirect viewing’, in strabismic amblyopes the situation is quite different. Due to suppression early in life when abnormal conditions produce abnormal visual behaviour, the decreased foveal VA leads the fixation reflex to become associated with the eccentric fixation area. This motor adaptation will position the image of an object of interest directly onto the eccentric fixation area without placing it first on the fovea. In that sense the fovea has lost its ‘zero retinomotor value’, which may now be found at the eccentric fixation area. So far it is unclear, however, whether this adaptation is absolute and complete in all cases or whether the abnormal fixation reflex can be overcome by increased recognitional effort. The scanning laser ophthalmoscope provides a unique way of carrying out real-time examination of strabismic amblyopes. It offers the advantage to the observer of being able to visualize and simultaneously place an image onto the patient's retina. In our studies we found that patients with a VA of < 0.1 showed a stable area of fixation in a location outside the fovea. In amblyopes with better VA, fixation became more and more ‘foveolized’ as the recognitional effort increased.

Our observations provide further evidence that eccentric fixation in strabismic amblyopes is indeed part of a spectrum of sensory and motor adaptations of visual functions in patients with strabismus. Some amblyopes (with better acuity) may fixate randomly at the margin of a central suppression scotoma to obtain better vision when the non-amblyopic eye is covered. In others (with severely reduced VA) the adaptation is more complete and the motor component of the fixation reflex becomes more stably associated with the new (eccentric) centre of retinomotor orientation for fixational eye movements. Further experiments under different viewing conditions are needed to characterize the nature of this retinomotor adaptation.

References

  1. Top of page
  2. Abstract.
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. References
  • Aggarwal DP & Verma G (1980): Static perimetry in the study of amblyopia scotomata. Br J Ophthalmol 64: 713716.
  • Aulhorn E (1967): Die gegenseitige Beeinflussung abbildungsgleicher Netzhautstellen bei normalem und gestörten Binokularsehen. Doc Ophthalmol 23: 2661.
  • Aulhorn E & Lichtenberg C (1972): Central and peripheral visual acuity of eyes suffering from strabismus amblyopia. Orthoptics. Proceedings of the 2nd International Congress, Amsterdam. Excerpta Medica 153.
  • Avetisov ES (1979): Visual acuity and contrast sensitivity of the amblyopic eye as a function of the stimulated region of the retina. Am J Optom Physiol Optics 56: 465469.
  • Bedell HE & Flom MC (1981): Monocular spatial distortion in strabismic amblyopia. Invest Ophthalmol Vis Sci 20: 263268.
  • Bedell HE, Flom MC & Barbeito R (1985): Spatial aberrations and acuity in strabismus and amblyopia. Invest Ophthalmol Vis Sci 26: 909916.
  • Böhme G (1955): Zur Kenntnis der exzentrischen Fixation im Hinblick auf die Behandlung der Amblyopie. Klin Monatsbl Augenheilkd 126: 694719.
  • Ciuffreda KJ, Kenyon RV & Stark L (1979): Fixational eye movements in amblyopia and strabismus. J Am Optom Assoc 50: 12511258.
  • Cüppers C (1956): Moderne Schielbehandlung. Klin Monatsbl Augenheilkd 129: 579604.
  • Cüppers C (1961): Grenzen und Möglichkeiten der pleoptischen Therapie. In: Bücherei Des Augenarztes. Schielen-Pleoptik-Orthoptik-Operation 38. Stuttgart: Ferdinand Enke Verlag 168.
  • Cüppers C (1966): Some reflections on the possibility of influencing the pathological fixation act. Ann R Coll Surg Engl 38: 308325.
  • Flom MC & Weymouth FW (1961): Centricity of Maxwell's spot in strabismus and amblyopia. Arch Ophthalmol 66: 260268.
  • Fronius M & Sireteanu R (1989): Monocular geometry is selectively distorted in the central visual field of strabismic amblyopes. Invest Ophthalmol Vis Sci 30: 20342044.
  • Herzau V, Dessel A & Girrbach C (1989): Differential light sensitivity in strabismic amblyopia perimetric findings with the Tübingen automatic perimeter in 50 consecutive cases. In: KaufmannH (ed). Transactions of the 18th ESA-Meeting, Krakow. 109.
  • Herzau V, Girrbach C & Roth A (1993): Evaluation of the Ammann test in the clinical routine. In: KaufmannH (ed). Transactions of the 21st ESA-Meeting, Salzburg. 15.
  • Hess RF (1977): On the relationship between strabismic amblyopia and eccentric fixation. Br J Ophthalmol 61: 767773.
  • Hess RF, Campbell FW & Greenhalgh T (1978): On the nature of the neural abnormality in human amblyopia; Neural aberrations and neural sensitivity loss. Pflügers Arch 377: 201207.
  • Van Hof-van Duin J & Mohn G (1982): Stereopsis and optokinetic nystagmus. In: LennerstrandG, ZeeDS & KellerEL (eds). Functional Basis of Ocular Motility Disorders. New York: Pergamon Press 113115.
  • Levi DM & Klein SA (1983): Spatial localization in normal and amblyopic vision. Vision Res 23: 10051017.
  • Mackensen G (1957): Das Fixationsverhalten amblyopischer Augen. Graefes Arch Clin Exp Ophthalmol 159: 200211.
  • Mackensen G, Kröner B, Postic G & Kelck W (1967): Untersuchungen zum Problem der exzentrischen Fixation. Doc Ophthalmol 23: 228262.
  • May JG, Marx MS, Morgan KS, Reed JL & Loupe DN (1983): Perceptual distortion in non-amblyopic strabismic subjects. [ARVO Abstracts.] Invest Ophthalmol Vis Sci 24: 133.
  • Mimura O, Inui T, Kani K & Ohmi E (1984): Retinal sensitivity and spatial summation in amblyopia. Jpn J Ophthalmol 28: 389400.
  • Von Noorden GK (1966): Pathogenesis of eccentric fixation. Am J Ophthalmol 61: 399422.
  • Von Noorden GK (1969): The aetiology and pathogenesis of fixation anomalies in strabismus. Trans Am Ophthalmol Soc 67: 698751.
  • Von Noorden GK & Helveston EM (1970): Influence of eye position on fixation behaviour and visual acuity. Am J Ophthalmol 70: 199204.
  • Von Noorden GK & Mackensen G (1962): Phenomenology of eccentric fixation. Am J Ophthalmol 53: 642661.
  • Oppel O (1962): Zur Phänomenologie der exzentrischen Fixation. Klin Monatsbl Augenheilkd 141: 161199.
  • Pugh M (1958): Visual distortion in amblyopia. Br J Ophthalmol 42: 449460.
  • Schor CM (1983): Subcortical binocular suppression affects the development of latent and optokinetic nystagmus. Am J Optom Physiol Opt 60: 481502.
  • Stigmar G (1971): Blurred visual stimuli. II. The effect of blurred visual stimuli on Vernier and stereo acuity. Acta Ophthalmol 49: 364379.
  • Williams RA, Enoch JM & Essock EA (1984): The resistance of selected hyperacuity configurations to retinal image degradation. Invest Ophthalmol Vis Sci 25: 389399.