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Color vision deficiencies in Gilles de la Tourette syndrome
Journal of the Neurological Sciences 186 Ž2001. 107–110 www.elsevier.comrlocaterjns
Color vision deficiencies in Gilles de la Tourette syndrome Jean-Pierre Melun a,) , Louise M. Morin a,1, J. Gerard Muise b, Marc DesRosiers b a b
Departement de Psychiatrie, Hopital Dr. Georges-L. Dumont, 330 AÕenue de l’UniÕersite, ´ ˆ ´ Moncton, NB, Canada E1C 2Z3 Laboratoire de Psychologie CognitiÕe, Departement de Psychologie, UniÕersite´ de Moncton, Moncton, NB, Canada E1A 3E9 ´ Received 8 June 2000; received in revised form 16 March 2001; accepted 19 March 2001
Abstract Color perception was tested using the Farnsworth–Munsell 100-Hue Test in a sample of persons with Gilles de la Tourette syndrome ŽGTS., and compared to norms from three age cohorts in the early second, fourth and sixth decades. Red-green color errors on the Farnsworth–Munsell did not appear to change appreciably as a function of age or GTS. Blue-yellow error scores did, however, increase with age and were exaggerated in the GTS group. It is concluded that sensory and perceptual disturbances are present in GTS as in other basal cell ganglia disorders. The results are discussed in terms of converging retinal dopaminergic mechanisms also associated with Parkinson’s and Huntington’s diseases and even with normal aging. Suggestions are offered that daily activities and behavior may be affected by spatial and chromatic deficiencies. q 2001 Elsevier Science B.V. All rights reserved. Keywords: Color vision; Tourette; Dopamine; Basal ganglia
1. Introduction It is difficult to overlook the flamboyant symptomatology of motor and vocal tics associated with Gilles de la Tourette syndrome ŽGTS.. However, the person with GTS oftentimes presents a clinical profile with much more subtle and subdued elements, which may reveal hidden processes and covert effects of the disease w1x. Some of us have noticed a preoccupation with inkblot shading on the Rorschach Test ŽJ.-P. Melun, L. Morin, presented at the Annual Symposium of the Tourette Syndrome Association of Canada, 1996., and a fondness for cloud gazing Žnephelococcygia.. Since GTS has possibly been associated with visual field deficits w2x, these factors may implicate anomalous visual information processing at the sensory and perceptual level. Because GTS affects dopamine neurotransmission w3x, it may share comparable visual consequences with similar basal cell ganglia disorders w4,5x. For example, color perception along the blue-yellow axis, as measured by the Farnsworth–Munsell 100-Hue
)
Corresponding author. Tel.: q1-506-862-4177; fax: q1-506-8624325. E-mail address: [email protected] ŽJ.-P. Melun.. 1 Tel.: q1-506-862-4177; fax: q1-506-862-4325.
Test is perturbed in Parkinson’s w6–10x and Huntington’s w11x diseases. Color perception depends on highly differentiated visual structures and neural mechanisms. Specific chromatic deficiencies often signal explicit deficits in neuronal integrity and functioning w12x. The visual subsystem associated with the peripheral encoding by the blue cone photoreceptors appears to be especially vulnerable to systemic and environmental factors, due to its sparsity of receptors and its anatomical distribution w13x. Retinal dopaminergic changes have been suggested to alter the properties of horizontal and amacrine cells, thus affecting visual receptive fields associated with the blue cone network. Research from a number of avenues appears to lend converging evidence for this retinal dopaminergic model. Protracted effects of the use and withdrawal of dopaminergic altering drugs, such as cocaine w14x, and even normal dopamine level changes associated with aging w5x may be related to the severity of blue-yellow, viz. Tritan–Tetartan deficiencies. More importantly, these deficiencies appear to be present in several of the members of the family of basal cell ganglia disorders w7–11x. Animal studies have also corroborated the presence and the extensive involvement of retinal dopaminergic mechanisms both in color w5x and spatial w4x vision. Given the empirical evidence on the role of dopamine and basal ganglia cell involvement in GTS,
0022-510Xr01r$ - see front matter q 2001 Elsevier Science B.V. All rights reserved. PII: S 0 0 2 2 - 5 1 0 X Ž 0 1 . 0 0 5 1 6 - 0
108
J.-P. Melun et al.r Journal of the Neurological Sciences 186 (2001) 107–110
All testing was performed in darkened ambient conditions using a tabletop illuminated stand. The illuminance of the white testing surface was maintained at 700 lx, measured by a Minolta CS-100 chroma meter, using Macbeth Fluorescent Lamps, which approximate natural lighting from an overcast northern sky in the Northern Hemisphere. The observers were allowed ample time to complete the ordering task without undue pressure.
3. Results The data were collapsed for men and women because analyses revealed no sex differences as a function of age. Analyses of variance based on the separate red-green and blue-yellow components of the test showed no overall significant differences among groups for the red-green Fig. 1. Red-green and blue-yellow error scores as a function of age contrasted with the GTS group. The panel shows the mean error scores and standard error of the means for each group on the red-green and the blue-yellow components of the Farnsworth–Munsell 100-Hue Test. The GTS group may be compared to the normative 40-year-old group since their mean age was 35.4 years.
we attempted to ascertain the presence and the extent of dyschromatopsia in GTS compared to normal aging.
2. Method For the present experiment, we obtained a GTS sample of eight men and three women who met all the intensive criteria of the DSM-IV w15x for GTS from the psychiatric outpatient pool of the Dr. Georges-L. Dumont Hospital in Moncton, NB, Canada. Two men were rejected after ophthalmic investigation because of deuteranomaly, leaving nine observers with a mean age of 35.4 years ŽSD s 13.94.. Two of the remaining GTS probands were medication-free, and seven GTS observers were on a stable medication regimen. Three received antidopaminergic drugs to control the more flagrant symptoms of GTS. The age control norms were obtained from 60 healthy observers divided into three age cohorts: early twenties Ž M s 21.9, SD s 2.76., early forties Ž M s 42.5, SD s 2.93. and early sixties Ž M s 63.4, SD s 2.89., with 10 men and 10 women at each level of age. None of the observers used in the experiment had Protan–Deutan deficiencies as indicated by the Ishihara Pseudoisochromatic plates, and all had at least 20r25 Snellen binocular acuity. Color vision was assessed binocularly using the Farnsworth–Munsell 100-Hue Test, which consists of 85 color-graded discs or caps, sampled from a hue circle, divided into four series with anchor comparison stimuli at each end. The measure of color discrimination error is derived from the sum of the weighted distance of displaced adjacent discs from a naturally ordered color gradient w16x.
Fig. 2. Polar chart of the errors on the Protan, Deutan, Tritan and Tetartan axes within the Munsell hue circle. The hue circle is a continuous approximation within reproduction constraints of the discrete hues presented in the Farnsworth–Munsell 100-Hue Test. The first colored disc of the ordered series of the Farnsworth–Munsell is at top of the hue circle, and the following graded hue discs Ž2–85. are spaced at approximately equal intervals around the circle in a counter-clockwise direction. The four elliptical data plots Ž-B-, - Ø -, -'-, -l-. represent the errors made by the different age groups Žthe 20-year-olds, the 40-year-olds, the 60-year-olds and the GTS group.. Errors are represented along any radial on a scale from 0 to 20. Line thickness increases as a function of age with the GTS group having the thickest line width around the perimeter. The poles depicted by the filled circles around the circumference define the centre caps of the joined extremities of four major axes: Protan, Deutan, Tritan and Tetartan. Protan and Deutan attributes contribute to the red-green components, while Tritan and Tetartan elements represent the blue-yellow components. If the reader would like to experience an approximation of a Tritan–Tetartan deficiency associated with many ophthalmic conditions, almost any pair of easily available yellow-tinged driving or sports lenses would make the discrimination of these hues more difficult.
J.-P. Melun et al.r Journal of the Neurological Sciences 186 (2001) 107–110
error scores, but revealed a highly significant difference among groups for the blue-yellow axis w F Ž3,65. s 4.49, P - 0.005x. Pairwise comparisons showed that these differences could be attributed to differences between the young and the senior group w t Ž38. s 2.44, P s 0.02x and the differences between the GTS group with the 20-year-old w t Ž27. s 4.05, P - 0.001x and with the 40-year-old groups w t Ž27. s 2.20, P s 0.037x. Fig. 1 presents the red-green and blue-yellow mean error scores as a function of age contrasted with the GTS group. Since the nature of the color confusions is of theoretical importance, we present in Fig. 2 a finer grained graphical representation of the results, which is interpretable within the circular and graded hue structure of the Farnsworth– Munsell 100-Hue Test. As suggested by Parker w17x, the error scores were partitioned according to four major chromatic axes with two poles: Protan, Deutan, Tritan and Tetartan. In a modified procedure, the unweighted sum of "5 adjacent cap errors from the center cap on a given pole was used as a composite error score. Fig. 2 shows a polar plot of the normal progression of mean errors as a function of age and GTS membership. The GTS group makes more errors along the Tritan–Tetartan axes at the nadir of the polar chart than the reference 40-year-old group, and even seems to be less adept with these hues than the 60-year-olds. Their color discrimination performance along the Protan and Deutan axes is within the normal aging range.
4. Discussion We have demonstrated for the first time that persons with GTS appear to have specific color perception anomalies along the Tritan–Tetartan axes. This finding is consistent with other studies implicating altered retinal dopaminergic mechanisms w6–11x in color vision. These fundamental mechanisms remain unclear, and may entail changes in dopamine production, transport, uptake or receptor sensitivity. The elongated elliptical pattern in the Farnsworth diagram found in the present study suggests that we are able to discount attentional, task-related variables and medication status as plausible explanations. If, for example, GTS or comorbidity factors provoked overall performance deficits related to frontal and limbic dopaminergic sites associated with executive functions w18x, then we would expect a more circular random pattern in the Farnsworth diagram. Schizophrenics, in our unreported pilot control experiments, show either this diffuse, random profile of color discrimination or appropriate age-related errors. Our GTS sample showed a greater than two-fold ratio of blue-yellow vs. red-green errors irrespective of their medication history and status. We conclude, as others have shown with ‘de novo’ parkinsonian patients w9x, that the color deficiencies reflect basic correlates of the GTS disease process. One apparent paradox is that a hypokinetic
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disease such as parkinsonism and a hyperkinetic disorder such as GTS both generate similar color deficiencies or dyschromatopsias. However, the behavioral effect of basal ganglia anomalies is not solely anatomically determined, but is developmentally sensitive. Dopamine alterations in mature animals lead to hypoactivity, while the same procedure in newborns results in hyperactivity w19x. It is possible that retinal dopaminergic mechanisms reflect a common expression of seemingly disparate and chaotic basal cell and dopamine anomalies. This hypothesis would even extend to color perception changes found with aging. Blue-yellow deficiencies have normally been attributed to the yellowing of the aging crystalline lens, which filters blue light. As pointed out by Weale w20x, performance as a function of age on the Farnsworth–Munsell 100-Hue Test cannot be totally explained by this mechanism. We suggest that the reduction in normal dopamine levels with age w21x may be partly responsible for the Tritan–Tetartan deficiency associated with aging. The results also support our clinical observations and intuitions that persons with GTS may have a distinctive perceptual world view, mediated by anomalous early visual information processing, which might generate seemingly anomalous behavior. For example, reports of sungazing in GTS w22x and other psychiatric diseases w23x without apparent retinal damage may represent a pursuit of dopamine flooding from a bright light source in a dopamine-starved retina. On the other hand, it may simply be due to enhanced selective spatial processing of medium spatial frequencies of cloud configurations, analogous to Rorschach shading responses. Since the yellow-minus-blue chromatic information appears to be deficient, the observer may have to depend more on the available information from the achromatic channel Žred-plus-green. and the redminus-green chromatic channel w24x. Although it is always tenuous to presume the perceptual qualia of others, it may be instructive for clinical intuitions to simulate distorted color appearance based on cone fundamentals w25x with digital image enhancement w26x, or, to a first approximation, by filtering a primary color. Young observers wearing commonly available night-driving yellow lenses w20x, which subjectively enhance the contrast of objects and filter blue light, show a very similar functional profile to the Tritan– Tetartan deficiencies reported here. This would certainly have considerable adverse consequences in situations where adequate color perception would be needed for critical color-coded tasks in daily and occupational activities. Under such conditions, the professional assessment of Tritan–Tetartan challenged persons by means of psychological tests with a sizable color component, such as the Rorschach or others, may be more parsimoniously approached in terms of visual sensory disturbances than by the tenets of ego or cognitive psychology. Changes in dopaminergic mechanisms associated with the amacrine and horizontal cells of the retina also affect the temporal and spatial characteristics of vision w27x, and
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J.-P. Melun et al.r Journal of the Neurological Sciences 186 (2001) 107–110
it is likely that there are substantial chromatic, temporal and spatial interactions. For example, spatial frequency distortions and relative enhancements, as found in Parkinson’s disease w4x, may be present in GTS and would yield a unique perceptual view which would be manifested in daily activities requiring visual rendering of the environment, whether it be reading a text or operating a vehicle. Color perception deficits associated with GTS, along with other vision and sensory disturbances, may open avenues for the ongoing search for behavioral markers for genetic linkage analyses w28,29x. Future research is needed to assess the implications of retinal dopaminergic models, for the understanding of the fundamental nature of GTS and the daily living consequences of sensory anomalies associated with the spectrum of basal cell ganglia disorders, at all stages of development and throughout the life span.
Acknowledgements We are grateful for the support from the Psychiatric Research Funds of the Georges-L. Dumont Hospital, and would like to thank posthumously Claude Savoie of the Campagne Impact of the Universite´ de Moncton. We also acknowledge Genevieve ` Doucet, Maria Babin and Christian Watier for their experimental work and Dr. Benoit Grenier for ophthalmic screening.
References w1x Cohen AJ, Leckman JF. Sensory phenomena associated with Gilles de la Tourette’s syndrome. J Clin Psychiatry 1992;53:319–23. w2x Enoch JM, Lakshminarayanan V, Itzhaki A, Khamar BM, Landau K, Lowe T, et al. Anomalous kinetic visual fields found in family members of patients with a confirmed diagnosis of Gilles de la Tourette syndrome. Optom Vision Sci 1991;68:807–12. w3x Singer HS, Hahn IH, Moran TH. Abnormal dopamine uptake sites in postmortem striatum from patients with Tourette’s syndrome. Ann Neurol 1991;30:558–62. w4x Bodis-Wollner I., Regan D., Spatiotemporal contrast vision in Parkinson’s Disease and MPTP-treated monkeys: the role of dopamine. In: Cronly-Dillon J.R., series editor, Regan D., volume editor. Vision and visual dysfunction: vol. 10, Spatial vision. Boca Raton, FL: CRC Press; 1991, p. 250–60. w5x Djamgoz MBA, Hankins MW, Hirano J, Archer SN. Neurobiology of retinal dopamine in relation to degenerative states of the tissue. Vision Res 1997;37:3509–29. w6x Price MJ, Feldman RG, Adelberg D, Kayne H. Abnormalities in color vision and contrast sensitivity in Parkinson’s disease. Neurology 1992;42:887–90. w7x Haug BA, Kolle RU, Trenkwalder C, Oertel WH, Paulus W. Predominant affection of the blue cone pathway in Parkinson’s disease. Brain 1995;118:771–8.
w8x Muller T, Buttner T, Przuntek H. Distorted colour discrimination in ¨ ¨ Parkinson’s disease is related to severity of the disease. Acta Neurol Scand 1997;96:293–6. w9x Buttner T, Kuhn W, Muller T, Patzold T, Heidbrink K, Przuntek H. ¨ ¨ Distorted color discrimination in Ade novoB parkinsonian patients. Neurology 1995;45:386–7. w10x Pieri V, Diederich NJ, Raman R, Goetz CG. Decreased color discrimination and contrast sensitivity in Parkinson’s disease. J Neurol Sci 2000;172:7–11. w11x Buttner T, Schulz S, Kuhn W, Blumenschein A. Impaired colour ¨ discrimination in Huntington’s disease. Eur J Neurol 1994;1:153–7. w12x Krastel H., Moreland J.D., Color vision deficiencies in ophthalmic diseases. In: Cronly-Dillon J.R., series editor, Foster D.H., volume editor. Vision and visual dysfunction: vol. 7, Inherited and acquired color deficiencies. Boca Raton, FL: CRC Press; 1991, p. 115–72. w13x Sperling H.G., Vulnerability of the blue-sensitive mechanism. In: Cronly-Dillon J.R., series editor, Foster D.H., volume editor. Vision and visual dysfunction: vol. 7, Inherited and acquired color deficiencies. Boca Raton, FL: CRC Press; 1991, p. 72–87. w14x Desai P, Roy M, Roy A, Brown S. Impaired color vision in cocaine-withdrawn patients. Arch Gen Psychiatry 1997;54:696–9. w15x Diagnostic and Statistical Manual of Mental Disorders. 4th edn. Washington, DC: American Psychiatric Association, 1994. w16x Farnsworth D. The Farnsworth–Munsell 100-Hue dichotomous tests for color vision. J Opt Soc Am 1943;33:568–76. w17x Parker JA. Farnsworth 100-Hue scoring for acquired color vision deficiencies by weighted functions. Computers in ophthalmology, IEEE, 1979;97–9, April. w18x Flowers KA, Robertson C. Perceptual abnormalities in Parkinson’s disease: top-down or bottom-up processes. Perception 1995;24: 1201–21. w19x Visser JE, Bar ¨ PR, Jinnah HA. Lesch–Nyhan disease and the basal ganglia. Brain Res Rev 2000;32:449–75. w20x Weale R.A., Effects of senescence. In: Cronly-Dillon J.R., series editor, Foster D.H., volume editor. Vision and visual dysfunction: vol. 5, Limits of vision. Boca Raton, FL: CRC Press; 1991, p. 277–85. w21x Meng SZ, Osawa Y, Itoh M, Takashima S. Developmental and age-related changes of dopamine transporter, and dopamine D1 and D2 receptors in human basal ganglia. Brain Res 1999;843:136–44. w22x Kobylski TP, Licamele WL. Sun gazing by patients with Tourette’s disorder. Am J Psychiatry 1991;148:394. w23x Kamp PS, Dietrich AM, Rosse RB. Sun gazing by psychiatric patients. Am J Psychiatry 1990;147:810–1. w24x King-Smith P.E., Chromatic and achromatic visual systems. In: Cronly-Dillon J.R., series editor, Gouras P., volume editor. Vision and visual dysfunction: vol. 6, The perception of colour. Boca Raton, FL: CRC Press; 1991, p. 22–42. w25x Vos JJ, Estevez ´ O, Walraven PL. Improved color fundamentals offer a new view on photometric additivity. Vision Res 1990;30:937–43. w26x Brettel H, Vienot ´ F, Mollon JD. Computerized simulation of color appearance for dichromats. J Opt Soc Am A 1997;14:2647–55. w27x Trick GL, Kaskie B, Steinman SB. Visual impairment in Parkinson’s disease: deficits in orientation and motion discrimination. Optom Vision Sci 1994;71:242–5. w28x Enoch JM, Schreier HA, Barroso L. Visual field defects in psychiatric disorders: possible genetic implications. Biol Psychiatry 1995; 37:275–7. w29x Whitefield L, Middleton EM, Brazier DJ, Robertson MM. Visual fields in Gilles de la Tourette syndrome. Br J Psychiatry 1995; 167:825–6.
Color vision deficiencies in Gilles de la Tourette syndrome Jean-Pierre Melun a,) , Louise M. Morin a,1, J. Gerard Muise b, Marc DesRosiers b a b
Departement de Psychiatrie, Hopital Dr. Georges-L. Dumont, 330 AÕenue de l’UniÕersite, ´ ˆ ´ Moncton, NB, Canada E1C 2Z3 Laboratoire de Psychologie CognitiÕe, Departement de Psychologie, UniÕersite´ de Moncton, Moncton, NB, Canada E1A 3E9 ´ Received 8 June 2000; received in revised form 16 March 2001; accepted 19 March 2001
Abstract Color perception was tested using the Farnsworth–Munsell 100-Hue Test in a sample of persons with Gilles de la Tourette syndrome ŽGTS., and compared to norms from three age cohorts in the early second, fourth and sixth decades. Red-green color errors on the Farnsworth–Munsell did not appear to change appreciably as a function of age or GTS. Blue-yellow error scores did, however, increase with age and were exaggerated in the GTS group. It is concluded that sensory and perceptual disturbances are present in GTS as in other basal cell ganglia disorders. The results are discussed in terms of converging retinal dopaminergic mechanisms also associated with Parkinson’s and Huntington’s diseases and even with normal aging. Suggestions are offered that daily activities and behavior may be affected by spatial and chromatic deficiencies. q 2001 Elsevier Science B.V. All rights reserved. Keywords: Color vision; Tourette; Dopamine; Basal ganglia
1. Introduction It is difficult to overlook the flamboyant symptomatology of motor and vocal tics associated with Gilles de la Tourette syndrome ŽGTS.. However, the person with GTS oftentimes presents a clinical profile with much more subtle and subdued elements, which may reveal hidden processes and covert effects of the disease w1x. Some of us have noticed a preoccupation with inkblot shading on the Rorschach Test ŽJ.-P. Melun, L. Morin, presented at the Annual Symposium of the Tourette Syndrome Association of Canada, 1996., and a fondness for cloud gazing Žnephelococcygia.. Since GTS has possibly been associated with visual field deficits w2x, these factors may implicate anomalous visual information processing at the sensory and perceptual level. Because GTS affects dopamine neurotransmission w3x, it may share comparable visual consequences with similar basal cell ganglia disorders w4,5x. For example, color perception along the blue-yellow axis, as measured by the Farnsworth–Munsell 100-Hue
)
Corresponding author. Tel.: q1-506-862-4177; fax: q1-506-8624325. E-mail address: [email protected] ŽJ.-P. Melun.. 1 Tel.: q1-506-862-4177; fax: q1-506-862-4325.
Test is perturbed in Parkinson’s w6–10x and Huntington’s w11x diseases. Color perception depends on highly differentiated visual structures and neural mechanisms. Specific chromatic deficiencies often signal explicit deficits in neuronal integrity and functioning w12x. The visual subsystem associated with the peripheral encoding by the blue cone photoreceptors appears to be especially vulnerable to systemic and environmental factors, due to its sparsity of receptors and its anatomical distribution w13x. Retinal dopaminergic changes have been suggested to alter the properties of horizontal and amacrine cells, thus affecting visual receptive fields associated with the blue cone network. Research from a number of avenues appears to lend converging evidence for this retinal dopaminergic model. Protracted effects of the use and withdrawal of dopaminergic altering drugs, such as cocaine w14x, and even normal dopamine level changes associated with aging w5x may be related to the severity of blue-yellow, viz. Tritan–Tetartan deficiencies. More importantly, these deficiencies appear to be present in several of the members of the family of basal cell ganglia disorders w7–11x. Animal studies have also corroborated the presence and the extensive involvement of retinal dopaminergic mechanisms both in color w5x and spatial w4x vision. Given the empirical evidence on the role of dopamine and basal ganglia cell involvement in GTS,
0022-510Xr01r$ - see front matter q 2001 Elsevier Science B.V. All rights reserved. PII: S 0 0 2 2 - 5 1 0 X Ž 0 1 . 0 0 5 1 6 - 0
108
J.-P. Melun et al.r Journal of the Neurological Sciences 186 (2001) 107–110
All testing was performed in darkened ambient conditions using a tabletop illuminated stand. The illuminance of the white testing surface was maintained at 700 lx, measured by a Minolta CS-100 chroma meter, using Macbeth Fluorescent Lamps, which approximate natural lighting from an overcast northern sky in the Northern Hemisphere. The observers were allowed ample time to complete the ordering task without undue pressure.
3. Results The data were collapsed for men and women because analyses revealed no sex differences as a function of age. Analyses of variance based on the separate red-green and blue-yellow components of the test showed no overall significant differences among groups for the red-green Fig. 1. Red-green and blue-yellow error scores as a function of age contrasted with the GTS group. The panel shows the mean error scores and standard error of the means for each group on the red-green and the blue-yellow components of the Farnsworth–Munsell 100-Hue Test. The GTS group may be compared to the normative 40-year-old group since their mean age was 35.4 years.
we attempted to ascertain the presence and the extent of dyschromatopsia in GTS compared to normal aging.
2. Method For the present experiment, we obtained a GTS sample of eight men and three women who met all the intensive criteria of the DSM-IV w15x for GTS from the psychiatric outpatient pool of the Dr. Georges-L. Dumont Hospital in Moncton, NB, Canada. Two men were rejected after ophthalmic investigation because of deuteranomaly, leaving nine observers with a mean age of 35.4 years ŽSD s 13.94.. Two of the remaining GTS probands were medication-free, and seven GTS observers were on a stable medication regimen. Three received antidopaminergic drugs to control the more flagrant symptoms of GTS. The age control norms were obtained from 60 healthy observers divided into three age cohorts: early twenties Ž M s 21.9, SD s 2.76., early forties Ž M s 42.5, SD s 2.93. and early sixties Ž M s 63.4, SD s 2.89., with 10 men and 10 women at each level of age. None of the observers used in the experiment had Protan–Deutan deficiencies as indicated by the Ishihara Pseudoisochromatic plates, and all had at least 20r25 Snellen binocular acuity. Color vision was assessed binocularly using the Farnsworth–Munsell 100-Hue Test, which consists of 85 color-graded discs or caps, sampled from a hue circle, divided into four series with anchor comparison stimuli at each end. The measure of color discrimination error is derived from the sum of the weighted distance of displaced adjacent discs from a naturally ordered color gradient w16x.
Fig. 2. Polar chart of the errors on the Protan, Deutan, Tritan and Tetartan axes within the Munsell hue circle. The hue circle is a continuous approximation within reproduction constraints of the discrete hues presented in the Farnsworth–Munsell 100-Hue Test. The first colored disc of the ordered series of the Farnsworth–Munsell is at top of the hue circle, and the following graded hue discs Ž2–85. are spaced at approximately equal intervals around the circle in a counter-clockwise direction. The four elliptical data plots Ž-B-, - Ø -, -'-, -l-. represent the errors made by the different age groups Žthe 20-year-olds, the 40-year-olds, the 60-year-olds and the GTS group.. Errors are represented along any radial on a scale from 0 to 20. Line thickness increases as a function of age with the GTS group having the thickest line width around the perimeter. The poles depicted by the filled circles around the circumference define the centre caps of the joined extremities of four major axes: Protan, Deutan, Tritan and Tetartan. Protan and Deutan attributes contribute to the red-green components, while Tritan and Tetartan elements represent the blue-yellow components. If the reader would like to experience an approximation of a Tritan–Tetartan deficiency associated with many ophthalmic conditions, almost any pair of easily available yellow-tinged driving or sports lenses would make the discrimination of these hues more difficult.
J.-P. Melun et al.r Journal of the Neurological Sciences 186 (2001) 107–110
error scores, but revealed a highly significant difference among groups for the blue-yellow axis w F Ž3,65. s 4.49, P - 0.005x. Pairwise comparisons showed that these differences could be attributed to differences between the young and the senior group w t Ž38. s 2.44, P s 0.02x and the differences between the GTS group with the 20-year-old w t Ž27. s 4.05, P - 0.001x and with the 40-year-old groups w t Ž27. s 2.20, P s 0.037x. Fig. 1 presents the red-green and blue-yellow mean error scores as a function of age contrasted with the GTS group. Since the nature of the color confusions is of theoretical importance, we present in Fig. 2 a finer grained graphical representation of the results, which is interpretable within the circular and graded hue structure of the Farnsworth– Munsell 100-Hue Test. As suggested by Parker w17x, the error scores were partitioned according to four major chromatic axes with two poles: Protan, Deutan, Tritan and Tetartan. In a modified procedure, the unweighted sum of "5 adjacent cap errors from the center cap on a given pole was used as a composite error score. Fig. 2 shows a polar plot of the normal progression of mean errors as a function of age and GTS membership. The GTS group makes more errors along the Tritan–Tetartan axes at the nadir of the polar chart than the reference 40-year-old group, and even seems to be less adept with these hues than the 60-year-olds. Their color discrimination performance along the Protan and Deutan axes is within the normal aging range.
4. Discussion We have demonstrated for the first time that persons with GTS appear to have specific color perception anomalies along the Tritan–Tetartan axes. This finding is consistent with other studies implicating altered retinal dopaminergic mechanisms w6–11x in color vision. These fundamental mechanisms remain unclear, and may entail changes in dopamine production, transport, uptake or receptor sensitivity. The elongated elliptical pattern in the Farnsworth diagram found in the present study suggests that we are able to discount attentional, task-related variables and medication status as plausible explanations. If, for example, GTS or comorbidity factors provoked overall performance deficits related to frontal and limbic dopaminergic sites associated with executive functions w18x, then we would expect a more circular random pattern in the Farnsworth diagram. Schizophrenics, in our unreported pilot control experiments, show either this diffuse, random profile of color discrimination or appropriate age-related errors. Our GTS sample showed a greater than two-fold ratio of blue-yellow vs. red-green errors irrespective of their medication history and status. We conclude, as others have shown with ‘de novo’ parkinsonian patients w9x, that the color deficiencies reflect basic correlates of the GTS disease process. One apparent paradox is that a hypokinetic
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disease such as parkinsonism and a hyperkinetic disorder such as GTS both generate similar color deficiencies or dyschromatopsias. However, the behavioral effect of basal ganglia anomalies is not solely anatomically determined, but is developmentally sensitive. Dopamine alterations in mature animals lead to hypoactivity, while the same procedure in newborns results in hyperactivity w19x. It is possible that retinal dopaminergic mechanisms reflect a common expression of seemingly disparate and chaotic basal cell and dopamine anomalies. This hypothesis would even extend to color perception changes found with aging. Blue-yellow deficiencies have normally been attributed to the yellowing of the aging crystalline lens, which filters blue light. As pointed out by Weale w20x, performance as a function of age on the Farnsworth–Munsell 100-Hue Test cannot be totally explained by this mechanism. We suggest that the reduction in normal dopamine levels with age w21x may be partly responsible for the Tritan–Tetartan deficiency associated with aging. The results also support our clinical observations and intuitions that persons with GTS may have a distinctive perceptual world view, mediated by anomalous early visual information processing, which might generate seemingly anomalous behavior. For example, reports of sungazing in GTS w22x and other psychiatric diseases w23x without apparent retinal damage may represent a pursuit of dopamine flooding from a bright light source in a dopamine-starved retina. On the other hand, it may simply be due to enhanced selective spatial processing of medium spatial frequencies of cloud configurations, analogous to Rorschach shading responses. Since the yellow-minus-blue chromatic information appears to be deficient, the observer may have to depend more on the available information from the achromatic channel Žred-plus-green. and the redminus-green chromatic channel w24x. Although it is always tenuous to presume the perceptual qualia of others, it may be instructive for clinical intuitions to simulate distorted color appearance based on cone fundamentals w25x with digital image enhancement w26x, or, to a first approximation, by filtering a primary color. Young observers wearing commonly available night-driving yellow lenses w20x, which subjectively enhance the contrast of objects and filter blue light, show a very similar functional profile to the Tritan– Tetartan deficiencies reported here. This would certainly have considerable adverse consequences in situations where adequate color perception would be needed for critical color-coded tasks in daily and occupational activities. Under such conditions, the professional assessment of Tritan–Tetartan challenged persons by means of psychological tests with a sizable color component, such as the Rorschach or others, may be more parsimoniously approached in terms of visual sensory disturbances than by the tenets of ego or cognitive psychology. Changes in dopaminergic mechanisms associated with the amacrine and horizontal cells of the retina also affect the temporal and spatial characteristics of vision w27x, and
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it is likely that there are substantial chromatic, temporal and spatial interactions. For example, spatial frequency distortions and relative enhancements, as found in Parkinson’s disease w4x, may be present in GTS and would yield a unique perceptual view which would be manifested in daily activities requiring visual rendering of the environment, whether it be reading a text or operating a vehicle. Color perception deficits associated with GTS, along with other vision and sensory disturbances, may open avenues for the ongoing search for behavioral markers for genetic linkage analyses w28,29x. Future research is needed to assess the implications of retinal dopaminergic models, for the understanding of the fundamental nature of GTS and the daily living consequences of sensory anomalies associated with the spectrum of basal cell ganglia disorders, at all stages of development and throughout the life span.
Acknowledgements We are grateful for the support from the Psychiatric Research Funds of the Georges-L. Dumont Hospital, and would like to thank posthumously Claude Savoie of the Campagne Impact of the Universite´ de Moncton. We also acknowledge Genevieve ` Doucet, Maria Babin and Christian Watier for their experimental work and Dr. Benoit Grenier for ophthalmic screening.
References w1x Cohen AJ, Leckman JF. Sensory phenomena associated with Gilles de la Tourette’s syndrome. J Clin Psychiatry 1992;53:319–23. w2x Enoch JM, Lakshminarayanan V, Itzhaki A, Khamar BM, Landau K, Lowe T, et al. Anomalous kinetic visual fields found in family members of patients with a confirmed diagnosis of Gilles de la Tourette syndrome. Optom Vision Sci 1991;68:807–12. w3x Singer HS, Hahn IH, Moran TH. Abnormal dopamine uptake sites in postmortem striatum from patients with Tourette’s syndrome. Ann Neurol 1991;30:558–62. w4x Bodis-Wollner I., Regan D., Spatiotemporal contrast vision in Parkinson’s Disease and MPTP-treated monkeys: the role of dopamine. In: Cronly-Dillon J.R., series editor, Regan D., volume editor. Vision and visual dysfunction: vol. 10, Spatial vision. Boca Raton, FL: CRC Press; 1991, p. 250–60. w5x Djamgoz MBA, Hankins MW, Hirano J, Archer SN. Neurobiology of retinal dopamine in relation to degenerative states of the tissue. Vision Res 1997;37:3509–29. w6x Price MJ, Feldman RG, Adelberg D, Kayne H. Abnormalities in color vision and contrast sensitivity in Parkinson’s disease. Neurology 1992;42:887–90. w7x Haug BA, Kolle RU, Trenkwalder C, Oertel WH, Paulus W. Predominant affection of the blue cone pathway in Parkinson’s disease. Brain 1995;118:771–8.
w8x Muller T, Buttner T, Przuntek H. Distorted colour discrimination in ¨ ¨ Parkinson’s disease is related to severity of the disease. Acta Neurol Scand 1997;96:293–6. w9x Buttner T, Kuhn W, Muller T, Patzold T, Heidbrink K, Przuntek H. ¨ ¨ Distorted color discrimination in Ade novoB parkinsonian patients. Neurology 1995;45:386–7. w10x Pieri V, Diederich NJ, Raman R, Goetz CG. Decreased color discrimination and contrast sensitivity in Parkinson’s disease. J Neurol Sci 2000;172:7–11. w11x Buttner T, Schulz S, Kuhn W, Blumenschein A. Impaired colour ¨ discrimination in Huntington’s disease. Eur J Neurol 1994;1:153–7. w12x Krastel H., Moreland J.D., Color vision deficiencies in ophthalmic diseases. In: Cronly-Dillon J.R., series editor, Foster D.H., volume editor. Vision and visual dysfunction: vol. 7, Inherited and acquired color deficiencies. Boca Raton, FL: CRC Press; 1991, p. 115–72. w13x Sperling H.G., Vulnerability of the blue-sensitive mechanism. In: Cronly-Dillon J.R., series editor, Foster D.H., volume editor. Vision and visual dysfunction: vol. 7, Inherited and acquired color deficiencies. Boca Raton, FL: CRC Press; 1991, p. 72–87. w14x Desai P, Roy M, Roy A, Brown S. Impaired color vision in cocaine-withdrawn patients. Arch Gen Psychiatry 1997;54:696–9. w15x Diagnostic and Statistical Manual of Mental Disorders. 4th edn. Washington, DC: American Psychiatric Association, 1994. w16x Farnsworth D. The Farnsworth–Munsell 100-Hue dichotomous tests for color vision. J Opt Soc Am 1943;33:568–76. w17x Parker JA. Farnsworth 100-Hue scoring for acquired color vision deficiencies by weighted functions. Computers in ophthalmology, IEEE, 1979;97–9, April. w18x Flowers KA, Robertson C. Perceptual abnormalities in Parkinson’s disease: top-down or bottom-up processes. Perception 1995;24: 1201–21. w19x Visser JE, Bar ¨ PR, Jinnah HA. Lesch–Nyhan disease and the basal ganglia. Brain Res Rev 2000;32:449–75. w20x Weale R.A., Effects of senescence. In: Cronly-Dillon J.R., series editor, Foster D.H., volume editor. Vision and visual dysfunction: vol. 5, Limits of vision. Boca Raton, FL: CRC Press; 1991, p. 277–85. w21x Meng SZ, Osawa Y, Itoh M, Takashima S. Developmental and age-related changes of dopamine transporter, and dopamine D1 and D2 receptors in human basal ganglia. Brain Res 1999;843:136–44. w22x Kobylski TP, Licamele WL. Sun gazing by patients with Tourette’s disorder. Am J Psychiatry 1991;148:394. w23x Kamp PS, Dietrich AM, Rosse RB. Sun gazing by psychiatric patients. Am J Psychiatry 1990;147:810–1. w24x King-Smith P.E., Chromatic and achromatic visual systems. In: Cronly-Dillon J.R., series editor, Gouras P., volume editor. Vision and visual dysfunction: vol. 6, The perception of colour. Boca Raton, FL: CRC Press; 1991, p. 22–42. w25x Vos JJ, Estevez ´ O, Walraven PL. Improved color fundamentals offer a new view on photometric additivity. Vision Res 1990;30:937–43. w26x Brettel H, Vienot ´ F, Mollon JD. Computerized simulation of color appearance for dichromats. J Opt Soc Am A 1997;14:2647–55. w27x Trick GL, Kaskie B, Steinman SB. Visual impairment in Parkinson’s disease: deficits in orientation and motion discrimination. Optom Vision Sci 1994;71:242–5. w28x Enoch JM, Schreier HA, Barroso L. Visual field defects in psychiatric disorders: possible genetic implications. Biol Psychiatry 1995; 37:275–7. w29x Whitefield L, Middleton EM, Brazier DJ, Robertson MM. Visual fields in Gilles de la Tourette syndrome. Br J Psychiatry 1995; 167:825–6.