Psychology

Electrophysiological Confirmation of Orientation-specific Contrast Losses in Multiple Sclerosis

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Electrophysiological Confirmation of Orientation-specific Contrast Losses in Multiple Sclerosis
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  Electrophysiological Confirmation of Orientation-specific Contrast Losses in Multiple Sclerosis“ MARK J. KUPERSMITH? JEREMIAH I. NELSON, WILLIAM H. SEIPLE, AND RONALD E. CARR Department of Ophthalmology bDepartment of Neurology New York University Medical Center New York New York 10016 INTRODUCHON Visual evoked potentials are often abnormal in patients with multiple sclerosis. Prolongation of the latency of the first major positive wave of the transient visual evoked potential (VEP) reflects the typical conduction defects in the retinocortical pathway in patients without obvious clinical complaints. However, the transient VEP may be delayed less frequently in those patients without retrobulbar neuritis or normal visual system, found with careful neuro-ophthalmic exam. In addition, there is only fair correlation of VEP defects with the typical visual complaints in patients with 20 20 Snellen acuity even when performed with a low-contrast visual pattern.’ In contrast to VEP testing, subjective tests of color or contrast are often abnormal in MS patients. These defects in visual performance usually reflect the subjective complaints, so frequently described by patients, of color desaturation or feeling as if the world always appears cloudy.* In a clinical setting psychophysical testing of contrast thresholds can be variable and is dependent on the subject’s comprehension and cooperation in giving reliable responses. The clinician needs an objective measure of visual performance. The VEP is capable of objectively evaluating the visual system but the typical computer-averaged VEP studies are too slow, they fatigue patients, and are too marred by adaptation3 to obtain accurate contrast thresholds in a clinical setting. Additionally, the test stimuli (such as checkerboard) used to elicit the pattern VEP are too complex4 to reflect the functioning of select groups of cortical neurons that may respond to pattern stimuli of a specific spatial frequency or orientation. Bodis-Wollners has advocated the use of reversing sinusoidal bar gratings as a simple stimulus for VEP studies similar to those used to determine contrast sensitivity psychophysically. Camisa6 has further applied these gratings to demonstrate prolongation in latency which is selective for specific orientations of the bar stimulus. However, a delay in latency of the VEP cannot be related to a visual performance deficit. Real time retrieval of visual responses to continuously changing, or “swept” stimuli e.g.. contrast levels increasing with time) can give visual performance data. Such methods have been pioneered in the study of evoked potential responses to spatial frequency’.’ and color’ and extended by us to swept contrast.” We have recently ‘This work was supported by NEI grant no. I P50 EY 02179, a contract from the Naval Air Systems Command, and an unrestricted departmental award from Research to Prevent Blind- ness, Inc. 487  aa ANNALS NEW YORK ACADEMY OF SCIENCES 8’ 6- 4. 2. 8’ reported finding an oblique effect in contrast and acuity threshold using these methods.” In this study, we have applied the technique to the study of contrast sensitivity to study objectively whether orientation-selective losses previously reported only with psychophysical methods’* ndeed occur in patients with MS. RESULTS Twenty-six patients with probable or definite MS (according to McAlpine’s criteria) had evoked potential contrast sensitivity determinations for three spatial frequencies 1,4, 8 cycles/deg) and four orientations (0, 5, 90, and 135 deg) of sine wave gratings. Contrast threshold deficits (above the 99 confidence interval calcu- lated for controls) were observed for at least one combination of spatial frequency and orientation in all cases. Both eyes were affected in 5 cases. The losses were spotty with respect to stimulus orientation, spatial frequency and viewing eye FIG. . The deficits were the same among 10 patients with or 16 without retrobulbar neuritis except in 4 cases with acuity worse than 20/70 wherecontrast thresholds were elevated beyond the . C 0 0 P A n W I c n U I z a 4 CPD V RO ti LO GRATING ORIENTATION FIGURE 1. Actual contrast thresholds for orientations V vertical, R right oblique, H horizontal, LO left oblique) and three spatial frequencies I, 4 and 8 cycles/deg) for right eye (circles) and left eye squores). Cross-hatched region extends from the mean contrast to the 99 confidence limit for controls. Losses are variable with regard to both eye and orientation or spatial frequency changes.  KUPERSMITH et al.: ORIENTATION-SPECIFIC CONTRAST LOSSES 489 V RO H LO GRATING ORIENTATION FIGURE 2. Contrast thresholds for a second case, key same as in FIGURE 1 Losses are similar in the two eyes and are selective for orientation but not spatial frequency. 20% contrast tested. Multiple orientations were affected in 24 cases. Orientation- specific losses which were the same in both eyes were found in 18 cases FIG. ). Discrete spatial frequency losses were present in only 5 cases and were not selective for orientation in only one case. Contrast abnormalities at 1 cycle/deg occurred twice as frequently as those at 4 or 8 cycles/deg. In comparison the averaged pattern-evoked potentials (using a reversing checker- board stimulus') were abnormally prolonged in 14/26 cases. Only 6/ 16 patients without retrobulbar neuritis had delayed VEP. n clinical exam 16 had 20/20 acuity, 9 dyschromatopsia, 14 abnormal funduscopy of the optic disc or nerve fiber layer, 10 different pupillary defects, and 16 abnormal psychophysical Arden contrast thres- holds. DISCUSSION Contrast threshold elevations selective for a combination of orientation and spatial frequency were demonstrated by VEP n all patients with multiple sclerosis. These  490 ANNALS NEW YORK ACADEMY OF SCIENCES occurred even in those subjects without a history of retrobulbar neuritis or clinical evidence of optic nerve dysfunction. The averaged VEP was less sensitive in identifying visual pathway defects, particularly in those cases without clinical optic neuropathy. The importance of measuring contrast sensitivity by psychophysical methods in this group of MS patients has been previously reported,' but now this can be objectively performed. Orientation-specific losses of contrast sensitivity were as often uniocular as binocular. Discrete spatial frequency losses were rare. These results are similar to and extend those which we described in a previous preliminary report. These findings provide an objective electrophysiological confirmation of psychophysically determined orientation-specific contrast threshold elevations reported by Regan.12 In comparison, patients with macula retina lesions or optic neuropathy not secondary to demyelinating disease have contrast threshold elevations which are not orientation-specific. Additionally, three other patients, referred with a wrong diagnosis of MS, had no contrast sensitivity abnormalities. Further evaluation uncovered a glioma of the spinal cord found at surgery, an intrinsic brainstem tumor diagnosed by computed tomography using intrathecal metrizamide and nuclear magnetic resonance scanning, and a hereditary familial spastic spinal paraparesis in each of the three, respectively. VER contrast losses which are not orientation-specific can help distin- guish patients with other neurological diseases wrongly suspected of MS. Orientation-selective contrast deficits in MS strongly suggest cortical involvement in these patients. True orientation tuning in the retino-cortical pathway is first found at the level of the visual cortex, beyond the neurons in layer IV.14 Columnar organization of orientation-selective neurons in the cortex has been neurophysiologically and anat~mically'~~'' emonstrated by Hubel and Wiesel. Additionally, intralaminar cortical fibers, which are myelinated, have recently been revealed to extend up to 4 mm, giving rise to periodic clustered axonal arborizations thought to be related to the columnar architecture. The neurons from which these axons arise also have orientation specificity. Previous electron microscopic study has demonstrated myelination of many axons throughout the neuropil in the cortex. Though cortical abnormalities are commonly thought to result from plaques at the border between white and gray matter, true lesions of the myelinated fibers in the gray matter alone have been described.20 Demyelinating plaques which disrupt the myeli- nated intralaminar cortical axons could disrupt the functional architecture of the visual cortex. Thus, orientation-selective dysfunction could be found in otherwise random, nonselective patchy lesions in the visual cortex. REFERENCES 1 KUPERSMITH, . J. J. I. NELSON, W. H. SEIPLE . E. CARR P. WEISS. 983. The 20/20 2. REGAN, D., R. SILVER T. MURRAY. 977. Visual acuity and contrast sensitivity in 3. CAMPBELL, . W. J. J. KULIKOWSKI. 1971. An electrophysiological measure of the 4. DEVALOIS. . K., R. L. DEVALOIS E. W. FUND. 979. Responses of striate cortex cells to 5. BODIS-WOLLNER, I., C. HENDLEY, . H. MYLIN J. THORNTON. 978. Visual evoked 6. CAMISA, . L. H. MYLIN 1. BODIS-WOLLNER. 981. The effect of stimulus orientation on eye in multiple sclerosis. Neurology 33 1015-1020. multiple sclerosis: HiddCn visual loss Brain 100. 563-579. psychophysical contrast threshold. J. Physiol. 217: 54P. gratings and checkerboard patterns. J. Physiol. 291: 483-505. potentials and the visuogram in multiple sclerosis. Ann. Neurol. 5 4M7. the visual evoked potential in multiple sclerosis. Ann. Neurol. 10 532-539.  KUPERSMITH er ul : ORIENTATION-SPECIFIC CONTRAST LOSSES 491 7. 8. 9. 10 11 12. 13. 14. 15. 16. 17. 18. 19. 20. REGAN, . 1973. Rapid objective refraction using evoked brain potentials. Invest. Ophthal. Vis. Sci. 12 669479. function: An electronic sweep technique for the pattern visual evoked potential. Invest. Ophthal. Vis. Sci. 18: 703-71 3. REGAN, . 1975. Colour coding of pattern responses in man investigated by potential feedback and direct plot technique. Vis. Res. 15 175-183. NELSON, . I. W. H. SEIPLE, M. J. KUPERSMITH R. E. CARR. 984. Lock-in signal retrieval techniques for swept-parameter visual stimulation. J. Clin. Neurophys. In press. temporal conditions which elicit or abolish the oblique effect in man: Direct measurement with swept evoked potential. Vision Res. 24 579-586. REGAN, .. J. A. WHITLOCK. . J. MURRAY K. 1 BEVERLEY. 98O.Orientation-specific losses of contrast sensitivity in multiple sclerosis. Invest. Ophthal. Vis. Sci. 19 324-328. in multiple sclerosis: Selectivity by eye, orientation and spatial frequency measured with the evoked potential. Invest. Ophthal. Vis. Sci. 25 632-639. HUBEL, D. H. T. N. WIESEL. 1968. Receptive fields and functional architecture of monkey striate cortex. J. Physiol. 195 21 5-243. HUBEL, D. H. T. N. WIESEL. 974. Sequence regularity and geometry of orientation columns in the monkey striate cortex. J. Comp. Neurol. 158: 267-293. HUBEL. . H. . N. WlESEL M. P. STRYKER. 977. Orientation columns in macaque monkey visual cortex demonstrated by the 2-deoxyglucose autoradiographic technique. Nature 269 328-330. HUBEL, D. H.. T. N. WlESEL M. P. STRYKER. 978. Anatomical demonstration of orientation columns in macaque monkey. J. Comp. Neurol. 172 361-380. GILBERT, c. T. N. WIESEL. 1983. Clustered intrinsic connections in cat visual cortex. J. Neuroscience 3: 11 16-1 133. PETERS, A., S. . PALAY H. DE F. WEBSTER. 976. The Fine Structure of the Nervous System. The Neurons and Supporting Cells. Saunders. Philadelphia. pp. 308-3 15. PETERS, G. 1958. Multiple sklerose. In Handbuch der Pathologische Anatomie und Histologie. Zweiter Teil. W. Schotz, Ed.: 525402. Springer-Verlag. Berlin. TYLER, ., P. APKARIAN, D. LEV1 K. NAKAYAMA. 979. Rapid assessment of visual NELSON, J. I., M . KUPERSMITH, w. H. SEIPLE, P. A. WElSS R. E. CARR. 984. spatio KUPERSMITH, M . w. H. SEIPLE, J. I. NELSON R. E. CARR. 984. Contrast spatial loss
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