Both the control subjects showed normal retinal correspondence. The exotropic state of the eye was manifested in Subject 2 under dissociated conditions (monocular viewing) across the whole field. Note that this results in a field expansion but with erroneously perceived visual directions. This subject reported the fixation cross to appear double intermittently in the binocular viewing conditions. Retinal correspondence was mapped only when the fixation cross appeared single in the binocular viewing condition. The subject found it tiring to do the binocular viewing condition, as it forced fusion to be maintained. The subject was unable to perform the task for certain targets in the pericentral region under the binocular fixation condition. When maintaining fusion, the targets were more closely aligned. Subject 3 had the targets all closely aligned in all the three conditions.
Torsional HARC is interpreted clinically from mere absence of torsional diplopia in the presence of monocularly measured torsion.28 Lack of complaints of torsional diplopia could be because of torsional motor fusion or from the masking by large horizontal or vertical deviations that might interfere with the patient's ability to perceive torsional diplopia.27 However, it is also possible that HARC could develop with torsional strabismus because distances between corresponding directions on both retinas increases gradually with retinal eccentricity in conjunction with the increase in Panum's fusional areas.48 This suggests that if torsional strabismus can be induced in adult onset hemianopes either surgically or optically, it could provide much better field expansion, particularly the lower field needed for safe mobility as well as the overhead field protecting from obstacles such as tree branches. With better directional adaptation possibly with HARC-like adaptation, such a field expansion would be beneficial. Optical rotation is currently possible with either Dove prisms, which in addition to rotation also invert the image and are too large and heavy to be used in spectacle lenses, or with twisted fiber optic bundle used in night vision devices, which is also not suitable for this application. It may be possible to create an image-rotating lens using some novel optical techniques (and a lens of that sort may provide an improved approach to optical correction for hemianopia). Such lens may be restricted to the periphery, as in the Peli peripheral prisms,19 maintaining central single binocular vision but increasing field expansion with eccentricity. The image rotation may be introduced gradually, thus facilitating more tolerable cyclofusion in the larger peripheral Panum's area, as the development of ARC in adults are not documented. Testing of this concept may be initiated using a binocular head-mounted display in which the image in one eye is rotated computationally. Such a device would make it possible to determine the viability of the concept, and if successful, motivate efforts to develop the required optical elements.
ARC is more easily observed in testing conditions that closely resemble real-world targets or natural viewing tests such as Bagolini striated glasses, when compared with other dissociating tests such as the Worth four-dot test.44,49 The DVF system used in this study can provide a natural viewing state as well as dissociated conditions in the same instrument and with the same targets. In the present study, we did not use real-world images with the DVF resulting in a dissociated (or weakly associated) conditions. The presence of ARC under this condition is a stronger indication of HARC as seen in subject 1.
Retinal correspondence has been reported to vary between the central and peripheral visual fields on some strabismic patients50 without any visual field defects. One study noted the correspondence to be normal centrally and more anomalous in the peripheral visual field,51 whereas another study reported the opposite findings.52 With the DVF system we found that subject 1 maintained HARC both centrally and pericentrally (within the tested 50° visual field diameter) and under both primary and secondary deviations. Invariant level of HARC would be more useful as an adaptation for hemianopia. We believe that our method of direct measure of visual directions at different eccentricities provides a better estimate for retinal correspondence.
Lateral and vertical strabismus is manifested only in binocular viewing. Under monocular viewing, each eye takes up foveal fixation even with ARC (except in some paretic strabismus and eccentric fixation conditions). The difference in the strabismic eye position between monocular and binocular viewing (i.e., cover-uncover test) establishes the diagnosis (i.e., phoria/tropia). In purely torsional deviation (phoria/tropia), the eye's torsional movement is much harder to detect with direct observation under cover-uncover test. Most objective tests such as fundus photography indirect ophthalmoscopy and blind spot perimetry for measuring torsion are essentially monocular. The double Maddox rod subjective test though viewed with both eyes dissociates binocular vision (in particular torsional fusion) and does not differentiate between a phoria and a tropia, similar to regular Maddox rod test for lateral and vertical deviation. Torsional rotation only under dissociated condition is indicative of cyclophoria and lack of diplopia under associated condition could result from torsional fusion (cyclofusion). The presence of homonymous hemianopia as in our subject 1 enables documentation with the DVF of the rotation of the vertical meridian (as well as the physiological scotoma's rotation) under associated binocular fixation, thus establishing the torsion to be tropic. Such observation is not possible in standard perimetry without hemianopia. Further, the standard perimetry is only weakly binocularly associated in regard to torsion as the central fixation target while providing a sound fusional stimulus for lateral/vertical phoria provides minimal stimulus for torsional phoria. Additional peripheral targets are necessary to facilitate torsional fusion. With dichoptic perimetry system, rotation of the physiological blind spot can be measured (without hemianopia) and compared under both monocular (not shown) and binocular fixation conditions (Fig. 6). The DVF can also present visually rich background for the perimetry that can serve as stimulus for torsional fusion. This enables differentiation of the torsional posture under associated and dissociated binocular conditions (with a tropic eye remaining in the torsional position under both conditions). Thus, a dichoptic perimeter with the capabilities of the DVF provides a unique testing environment for a more complete evaluation of torsion and of torsional HARC. In our patient, despite the less optimal blank background, HARC was demonstrated indicating a stronger adaptation.
To our knowledge, this is the first reported torsional HARC in a patient with homonymous hemianopia.
Supported in part by NIH grants EY07957 and EY12890 and P30EY003790. Henry Apfelbaum helped prepare the illustrations.
The appendix is available online at http://links.lww.com/OPX/A99.
1. Huber A. Homonymous hemianopia. Neuroophthalmology 1992;12:351–66.
2. Zhang X, Kedar S, Lynn MJ, Newman NJ, Biousse V. Homonymous hemianopias: clinical-anatomic correlations in 904 cases. Neurology 2006;66:906–10.
3. Bosley TM, Kiyosawa M, Moster M, Harbour R, Zimmerman R, Savino PJ, Sergott RC, Alavi A, Reivich M. Neuro-imaging and positron emission tomography of congenital homonymous hemianopias. Am J Ophthalmol 1991;111:413–8.
4. Shinder R, Wolansky L, Turbin RE. Congenital homonymous hemianopia and cortical migration abnormalities in a young adult. J Pediatr Ophthalmol Strabismus 2009;46:38–41.
5. Kedar S, Zhang X, Lynn MJ, Newman NJ, Biousse V. Pediatric homonymous hemianopia. J AAPOS 2006;10:249–52.
6. Herzau V, Bleher I, Joos-Kratsch E. Infantile exotropia with homonymous hemianopia: a rare contraindication for strabismus surgery. Graefes Arch Clin Exp Ophthalmol 1988;226:148–9.
7. Göte H, Gregersen E, Rindziunski E. Exotropia and panoramic vision compensating for an occult congenital homonymous hemianopia: a case report. Binocul Vis Eye Muscle Surg Q 1993;8:129–32.
8. Iwashige H, Hirose O, Usui C, Shoda S, Miyasaka H, Maruo T. Surgical and botulinum toxin treatment in two cases of abnormal retinal correspondence-exotropia with congenital homonymous hemianopsia [in Japanese]. Nihon Ganka Gakkai Zasshi 1995;99:1036–44.
9. Levy Y, Turetz J, Krakowski D, Hartmann B, Nemet P. Development of compensating exotropia with anomalous retinal correspondence after early infancy in congenital homonymous hemianopia. J Pediatr Ophthalmol Strabismus 1995;32:236–8.
10. Donahue SP, Haun AK. Exotropia and face turn in children with homonymous hemianopia. J Neuroophthalmol 2007;27:304–7.
11. Gamio S, Melek N. When the patient says no. Management of exotropia with hemianopic visual field defects. Binocul Vis Strabismus Q 2003;18:167–70.
12. Duke-Elder S, Wybar K. System of Ophthalmology. London, UK: H. Kimpton; 1973.
13. Phillips PH. Treatment of diplopia. Semin Neurol 2007;27:288–98.
14. Rucker JC, Tomsak RL. Binocular diplopia. A practical approach. Neurologist 2005;11:98–110.
15. Hoyt CS, Good WV. Ocular motor adaptations to congenital hemianopia. Binocul Vis Eye Muscle Surgery Q 1993;8:125–6.
16. Smith JL, Weiner IG, Lucero AJ. Hemianopic Fresnel prisms. J Clin Neuroophthalmol 1982;2:19–22.
17. Cohen JM, Waiss B. Visual field remediation. In: Cole RG, Rosenthal BP, eds. Remediation and Management of Low Vision. St. Louis, MO: Mosby; 1996:1–25.
18. Gottlieb DD. Living with Vision Loss. Atlanta, GA: St. Barthelemy Press, Ltd.; 1996.
19. Peli E. Field expansion for homonymous hemianopia by optically induced peripheral exotropia. Optom Vis Sci 2000;77:453–64.
20. Giorgi RG, Woods RL, Peli E. Clinical and laboratory evaluation of peripheral prism glasses for hemianopia. Optom Vis Sci 2009;86:492–502.
21. Pickwell D. Binocular Vision Anomalies: Investigation and Treatment, 2nd ed. London, UK: Butterworths; 1989.
22. Daw NW. Visual Development. New York, NY: Plenum Press; 1995.
23. Verma A. Anomalous adaptive conditions associated with strabismus. Ann Ophthalmol (Skokie) 2007;39:95–106.
24. Rutstein RP, Daum KM. Anomalies of Binocular Vision: Diagnosis and Management. St. Louis, MO: Mosby; 1998.
25. Kirschen DG. Understanding sensory evaluation. In: Rosenbaum AL, Santiago AP, eds. Clinical Strabismus Management: Principles and Surgical Techniques. Philadelphia, PA: Saunders; 1999:22–36.
26. Harley RD, Nelson LB, Olitsky SE. Harley's Pediatric Ophthalmology, 5th ed. Philadelphia, PA: Lippincott Williams & Wilkins; 2005.
27. Woo SJ, Seo JM, Hwang JM. Clinical characteristics of cyclodeviation. Eye (Lond) 2005;19:873–8.
28. Philips PH, Hunter DG. Evaluation of ocular torsion and principles of management. In: Rosenbaum AL, Santiago AP, eds. Clinical Strabismus Management: Principles and Surgical Techniques. Philadelphia, PA: Saunders; 1999:52–72.
29. Guyton DL. Strabismus complications from local anesthetics. Semin Ophthalmol 2008;23:298–301.
30. Holgado S, Enyedi LB, Toth CA, Freedman SF. Extraocular muscle surgery for extorsion after macular translocation surgery new surgical technique and clinical management. Ophthalmology 2006;113:63–9.
31. Dieterich M, Brandt T. Ocular torsion and perceived vertical in oculomotor, trochlear, and abducens nerve palsies. Brain 1993;116(Pt. 5):1095–104.
32. Guyton DL. Clinical assessment of ocular torsion. Am Orthoptic J 1983;33:7–15.
33. Morton GV, Lucchese N, Kushner BJ. The role of funduscopy and fundus photography in strabismus diagnosis. Ophthalmology 1983;90:1186–91.
34. Woods RL, Apfelbaum HL, Peli E. DLP-based dichoptic vision test system. J Biomed Opt 2010;15:016011.
35. Doherty AL, Bowers AR, Luo G, Peli E. Object detection in the ring scotoma of a monocular bioptic telescope. Arch Ophthalmol 2011;129:611–7.
36. Bowers AR, Keeney K, Peli E. Community-based trial of a peripheral prism visual field expansion device for hemianopia. Arch Ophthalmol 2008;126:657–64.
37. Kushner BJ, Hariharan L. Observations about objective and subjective ocular torsion. Ophthalmology 2009;116:2001–10.
38. Nugent AK, Keswani RN, Woods RL, Peli E. Contour integration in peripheral vision reduces gradually with eccentricity. Vision Res 2003;43:2427–37.
39. Hu SY, Schuchard RA, Fletcher DC, Sabates FN. Physiological blind spot characteristics and position relative to retinal locus for fixation by SLO testing. Invest Ophthalmol Vis Sci 1994;35:S1527.
40. Jamara RJ, Van De Velde F, Peli E. Scanning eye movements in homonymous hemianopia documented by scanning laser ophthalmoscope retinal perimetry. Optom Vis Sci 2003;80:495–504.
41. Colenbrander A. Visual standards, aspects and ranges of vision loss with emphasis on population surveys. Report prepared for the International Council of Ophthalmology at the 29th International Congress of Ophthalmology. Sydney, Australia: International Council of Ophthalmology; 2002:1–33.
42. Lovie-Kitchin J, Mainstone J, Robinson J, Brown B. What areas of the visual field are important for mobility in low vision patients? Clin Vis Sci 1990;5:249–63.
43. Katsumi O, Tanaka Y, Uemura Y. Anomalous retinal correspondence in esotropia. Jpn J Ophthalmol 1982;26:166–74.
44. Rutstein RP, Daum KM, Eskridge JB. Clinical characteristics of anomalous correspondence. Optom Vis Sci 1989;66:420–5.
45. Zangemeister WH, Meienberg O, Stark L, Hoyt WF. Eye-head coordination in homonymous hemianopia. J Neurol 1982;226:243–54.
46. Bowers AR, Keeney K, Apfelbaum DH, Peli E. Randomized controlled trial of oblique and horizontal peripheral prism glasses for hemianopia. Optom Vis Sci 2010;87:E-abstract 100960.
47. O'Neill EC, Connell PP, O'Connor JC, Brady J, Reid I, Logan P. Prism therapy and visual rehabilitation in homonymous visual field loss. Optom Vis Sci 2011;88:263–8.
48. Guyton DL. Ocular torsion: sensorimotor principles. Graefes Arch Clin Exp Ophthalmol 1988;226:241–5.
49. Nelson JI. A neurophysiological model for anomalous correspondence based on mechanisms of sensory fusion. Doc Ophthalmol 1981;51:3–100.
50. Sireteanu R, Fronius M. Different patterns of retinal correspondence in the central and peripheral visual field of strabismics. Invest Ophthalmol Vis Sci 1989;30:2023–33.
51. Haase W, Lung KH. Correspondence of foveal and peripheral areas in subjects with intact binocular vision and patients with strabismus [in German]. Klin Monbl Augenheilkd 1984;184:32–6.
52. Hallden U. The longitudinal horopter in a case of concomitant strabismus with anomalous correspondence. Acta Ophthalmol (Copenh) 1973;51:1–11.