European Pyha Archives of Eur Arch Psychiatr Neurol Sci (1988) 237:237-243 and Neurological Sciences © Springer-Verlag 1988 Pure Homonymous Hemiachromatopsia Findings with Neuro-ophthalmologic Examination and Imaging Procedures Hans W Kolmel Department of Neurology, Freie Universitat Berlin, Spandauer Damm 130, D-1000 Berlin 19, Germany Summary The study describes neuro-ophthalmologic findings in two patients with brain infarction who developed homonymous hemiachromatopsia with resolution to pure homonymous achromatopsia in an upper quadrant All other visual parameters were normal; only color perimetry was capable of demonstrating the visual disorder The results are presented with special emphasis on the macular region Computed tomography studies and magnetic resonance imaging revealed lesions in the caudal and medial occipitotemporal gyri as well as in adjacent cortical regions The lesions were secondary to disordered circulation in a proximal occipitotemporal branch of the posterior cerebral artery The anatomical findings and functional relations of color vision in man are discussed in the light of animal findings. Key words: Homonymous hemiacromatopsia Medial occipitotemporal gyrus Color perimetry - Introduction Pure homonymous hemiachromatopsia is rare among the visual disorders of central origin Most studies of homonymous hemiachromatopsia in the literature report a rather large homonymous scotoma for white light (Albert et al 1975 ; Green and Lessell 1977 ; Damasio et al 1980), color agnosia (Meadows 1974), or color anomia (Zihl and von Cramon 1980) The current study presents clinical findings including extensive testing of color vision and results of imaging techniques in two patients with brain infarction and homonymous quadrant achromatopsia without any other visual impairment The fundamental anatomical and functional relations of central color vision in man are discussed in the light of animal findings (Zeki 1969 ; van Essen and Zeki 1978 ; Michael 1978). Methods Both patients were physicians who gave informed consent to the numerous tests required and who were highly cooperative throughout the course of the study Their participation and ability to concentrate allowed time-consuming testing Followup examinations were performed several times during the first 3 weeks, at 6 and 12 weeks, at 6 months, and at 1 and 2 years. Visual acuity was tested with a Snellen chart Visual fields were documented with dynamic Goldmann perimetry using at least three isopters Small targets with low luminosity were preferred Visual fields were determined by computer-assisted static perimetry using the Octopus Approximately 400 measurements were made at 73 points within 30° of the fixation point, giving a resolution of 6° in this visual field Finally profile perimetry was made with a Humphrey field analyzer (distance between stimuli 1° on both eyes in the 450/225° and 135 °/ 315 ° meridians). The technique described by Zihl and von Cramon (1980) was employed to determine critical flicker fusion fields for 15 2 and 25 Hz (stimulus: 116 min arc diameter, 320 cd/m luminance) Object recognition (circles and squares) was tested in each hemifield as far as possible using the Tiibinger perimeter. Monocular dark adaptation was tested with the GoldmannWeekers adaptometer Stereoscopic vision was tested with the stereoeidometer designed by Monie (1948) and with Titmus tables Visual neglect was demonstrated with the tests designed by Luria (1960), Albert (1973), and by Heilman and Valenstein (1979) Patients were tested for pattern recognition with the Benton Facial Recognition Test (1968) Finger pursuit movement of the eyes and optokinetic nystagmus using a rotating drum with vertical stripes were tested. Examination of Color Vision The patients were asked to identify and sort wood blocks painted with the four primary colors (Hering 1920) and to identify and sort Holmgren's colored wool strands (containing 30 pairs of thick colored wool strands) Ishihara-Color-Plates and the Farnsworth-Munsell 100-hue test (Farnsworth 1943) were also employed. Standardized color perimetry was performed on each eye with the Tiibinger perimeter Blue (480 nm) 238 Fig 1 Patient 1: Magnetic resonance imaging in the T2 mode Increased signal intensity in the left occipitotemporal region corresponding to the medial occipitotemporal (MOT) gyrus and red (656 nm) targets ( 116 min arc diameter, 320 cd/m2 luminance) were used. In a further test the patients sat at 2 m from a tangent screen, fixed the center of the screen, and attempted to identify the colors of wool strands presented in the periphery of the visual quadrants at 20° . With the help of a second examiner color anomia was detected by simultaneous presentation of colored targets at the center and in the periphery of the visual field In addition, the patients were asked to respond to the examiner's suggestions for sorting the colored strands All tests were conducted under identical ambient light conditions Constant fixation of the center of the screen was verified. In a subsequent examination isopters for white and colored targets were tested in the macular region. Case Reports and Results Case 1 The patient, a 34-year-old right-handed radiologist had observed occasional flickering scotomas in the right lower quadrant associated with fatigue for the past 7 years There 239 Fig 2 Patient 2: Magnetic resonance imaging in the T2 mode Same findings as in patient 1 Involvement of the rostral portion of the right lingual gyrus and the MOT gyrus was no history of headache One morning he suddenly felt pressure behind the left eye, followed by paraesthesia in the right arm and an unsteady gait He examined himself in a mirror, noted that vision was limited to the left hemifield and made the diagnosis of right homonymous hemianopia. Examination by a neurologist 1 day later documented normal findings with the exception of right homonymous hemianopia The patient recognized his visual disorder and was fully oriented to time, place, and situation Reading, writing and calculation were undisturbed. The visual field defect quickly resolved to right upper quadrantanopia with entirely normal findings 6 days after the acute event At 6 weeks Goldmann perimetry and computerassisted perimetry with the Octopus showed normal findings. The patient complained of photophobia and easy fatigability during reading Color perimetry revealed homonymous hemiachromatopsia in the right upper quadrant The test results are given in Table 1 and Figs 3-6 Initial EE Gs documented slowing in the left temporal region Computed tomography (CT) studies revealed that the lesion was located primarily in the 240 Table 1 Test results of the two patients with homonymous achromatopsia in an upper quadrant Visual acuity Goldmann perimetry Octopus perimetry Profile perimetry Color perimetry Naming/separating mixed colors Ishihara plates Farnsworth-Munsell test Stereoscopy Dark adaptation Flicker fusion frequency Visual neglect/prosopagnosia Patient 1 (6 weeks after onset of visual disorder) Patient 2 (20 days after onset of visual disorder) 1.2/1 2 Normal (Fig 5a) Normal Normal* Homonymous achromatopsia in the right upper quadrant (Fig 5b), no change 2 years later No mistakes No mistakes Slight to moderate disturbance (Fig 3a), 2 years later: normal (Fig 4a) 1.0/1 0 Normal (Fig 6a) Normal Normal* Homonymous achromatopsia in the left upper quadrant (Fig 6 b)**, no change 2 years later No mistakes No mistakes Slight to moderate disturbance (Fig 3 b), 1.5 years later: slight uncertainty in blue range (Fig 4 b) Normal Normal Equal on both sides No pathological findings Normal Normal Equal on both sides No pathological findings * 2 years after onset of visual disorder ** 3 months after onset of visual disorder a U Fig 3 a Results of the Farnsworth-Munsell test in patient 1 6 weeks after onset of the visual disorder b Tests results in patient 2 20 days after onset of the visual disorder occipital white matter There was no evident involvement of area 17 The T 2 weighted images in magnetic resonance imaging demonstrated increased signal intensity in the left occipitotemporal region corresponding to the location of the medial occipitotemporal (MOT) gyrus (Fig 1) Increased signal intensity extended to the parahippocampal gyrus Xenon clearance studies with single photon emission tomography showed reduced perfusion in the left occipitotemporal region. Case 2 The patient, a 66-year-old right-handed surgeon with a 10-year history of diabetes mellitus controlled by diet, reported occasional palpitations After a party he noted unsteady gait and a reduction in visual acuity On admission to hospital the patient was fully conscious and aware of his surroundings. Neurologic examination demonstrated left hemianopia and in- creased deep tendon reflexes on the left The patient reported a slight disorder of spatial orientation and difficulty in recognizing faces during the first few days 16 days later Goldmann perimetry and computer-assisted static perimetry demonstrated normal findings but color perimetry showed complete left homonymous hemiachromatopsia The patient complained of easy fatigability during reading and found that the letters appeared to move before his eyes after a short period He also felt binded by bright light At this point the initial problems with spatial orientation and facial recognition had resolved completely Neurologic findings at 6 months and 2 years after the acute event were normal, as were the visual fields Left homonymous hemiachromatopsia had improved to upper left quadrant achromatopsia The test results are given in Table 1 and in Fig 3-6 The patient was not able to assess the extent of 241 D Fig 4 a Farnsworth-Munsell test in patient 1 24 months after onset of the visual disorder: normal findings b Farnsworth-Munsell test in patient 2 18 months after onset of the visual disorder: very slight uncertainty in the blue range a a a left red right b Fig 5 (Patient 1) a Goldmann perimetry 6 weeks after onset of the illness: normal visual fields b Color perimetry Blue (480 nm), red ( 656nm) Size of targets 116min arc diameter. Luminance 320 cd/m 2 Achromatopsia of the right upper quadrant Fig 6 (Patient 2) a Goldmann perimetry 20 days after onset of the visual disorder: normal visual fields b Color perimetry. Achromatopsia of the left upper quadrant with splitting of the macula No change 30 months later his visual disorder He noticed a deficiency in the left visual field but was not aware of the disturbance of color vision He reported that reading for long periods of time tended to tire him, but he returned to his professional activity as a surgeon 6 months after brain infarction. The EEG documented temporary slowing in the right temporoparietal region The CT studies revealed an oblong hypodense zone that appeared to be limited to the white matter in the right occipitotemporal region Magnetic resonance imaging 6 months after the acute event demonstrated increased signal intensity in the right occipital lobe white and grey matter without apparent involvement of area 17 (Fig 2) The lesion extended to the temporal region and corresponded roughly to the MOT gyrus Xenon clearance studies showed reduced perfusion in this area. Discussion Reports from a number of experienced neuro-ophthalmologists may have contributed to the limited recognition of color perimetry Wilbrand and Saenger ( 1917) reported a slight but constant reduction in light perception in hemiachromatopsias and suggested that conventional perimetry with white light would be sufficient in such cases Brouwer ( 1936) and Critchley ( 1967) were in general agreement with this evaluation Teuber et al ( 1960) reported additional visual disorders in all patients with hemiachromatop- 242 sia These included a reduction in flicker fusion frequency and disorders of dark adaptation Harrington ( 1981) claimed that disorders affecting central color vision could be demonstrated with white light if the targets used were small enough. However, many reports have shown that color perimetry is the best technique for demonstrating the presence and extent of unilateral disorders of visual perception In some cases tests with white light and small targets showed normal visual fields, while color perimetry documented homonymous hemiachromatopsia or quadrantanopia Bjerrum ( 1881) described a patient with a brain abscess in the temporobasal region who had normal visual fields and acuity but homonymous hemiachromatopsia In the same year Samelsohn ( 1881) reported on a patient with homonymous left hemiachromatopsia due to a stroke with normal visual fields determined by white light and small targets Bender and Kanzer (1939) described incomplete hemiachromatopsia as the only sequela of subarachnoid hemorrhage in a 23-year-old woman. Color perimetry demonstrated total loss of color vision in an upper quadrant in both our patients All other examinations produced normal findings, which underscores the particular value of color perimetry. The patients made no errors in sorting and naming colors when the undisturbed visual fields were tested. Color anomia such as that described by Geschwind and Fusillo (1965) was not present, nor was there color anomia in a half field such as that found by Zihl and von Cramon ( 1980) in their patient. Only the Farnsworth-Munsell test showed relatively inconsistent pathological findings Color perimetry in patient 2 demonstrated that the disorder for blue extended very close to the fovea We had suspected that more pronounced disorders in the bluegreen range demonstrated in the Farnsworth-Munsell test might be related to the visual field defect These results are similar to those reported by Zihl and Meyer (1981) The patients described by Meadows (1974) and by Zihl and von Cramon (1980) also had pathological results in the Farnsworth-Munsell test, but these patients also suffered from color agnosia or anomia Follow-up studies of color vision with the Farnsworth-Munsell test at 2 years after brain infarction showed normal findings in both patients despite persistence of disturbed color vision in an upper quadrant This would tend to limit the value of the Farnsworth-Munsell test and to underline the importance of color perimetry. Our results and those reported by other researchers (Zihl and Meyer 1981) suggest that the upper quadrants are particularly susceptible to disorders of color vision Homonymous hemiachromatopsia often resolves to upper quadrant achromatopsia Isolated homonymous achromatopsia in a lower quadrant has never been reported as far as we know These findings show that the lower quadrants are especially resistant to impairment of color vision Location and extent of the brain lesions detected in our patients were practically identical The findings in patient 2 extended farther into the occipital region than did the lesion in patient 1 The topographic findings underline the fact that the hemispheres are equally important for color vision in the contralateral hemifield. Areas 18 and 19 and marginal portions of areas 37 and 20 of the Brodmann classification were affected in these patients These involved the rostral portion of the lingual gyrus, the entire caudal and median portions of the MOT gyrus, and perhaps adjacent areas of the parahippocampal gyrus The CT studies demonstrated that the white matter was primarily affected, but magnetic resonance imaging showed approximately equal involvement of the cortex and white matter. There are a number of possible variations in blood flow to the occipital lobe through the posterior and medial cerebral arteries The MOT gyrus is also served by several branches of the posterior cerebral artery It may be assumed that a proximal branch of the posterior cerebral artery the temporooccipital artery without effective collaterals was involved in both of our cases. The location of the lesions causing hemiachromatopsia was a matter of controversy for many years (Wilbrand and Saenger 1917 ; Critchley 1967 ; Holmes 1918 ; Lenz 1921 a, b), although the significance of the MOT gyrus for color vision has been known for a long time Verrey (1888) was the first to suggest this relationship in his clinical and pathological study. Mackay and Dunlop (1899) and Lenz (1921 a, b) described identical topographic relations, and CT studies have demonstrated lesions in the same region in patients with hemiachromatopsia Disorders in this gyrus are found in almost all cases with disturbances of color vision, including hemiachromatopsia, color agnosia and anomia When the latter two disorders are found, additional lesions in connective visual pathways such as the splenium of the corpus callosum or in the contralateral MOT gyrus must be assumed (Green and Lessell 1977 ; Damasio et al 1980 ; Meadows 1974 ; Zihl and von Cramon 1980 ; Pearlman et al 1979) The importance of the MOT gyrus a part of area 19 for color vision in the contralateral hemifield suggests that specific visual functions are concentrated in a region relatively far from the striate area This corresponds to findings in rhesus monkeys reported by Zeki (1969), who demonstrated a high concentration of color-coded 243 neurons in area V4, which is located far from the primary visual fields Other investigators were unable to find a high concentration in area V4 (Schein et al. 1982), and definition of the topographic limits of this extrastriate area has encountered a number of problems (Ungerleider and Mishkin 1979) The region described by Zeki is located near the lunate sulcus, and it is not easy to find a relationship between this region in monkeys and the MOT gyrus in man. Meadows ( 1974) has already discussed this discrepancy In order to resolve the problem, Damasio et al ( 1980) postulated that color-selective neurons are located in a wide belt outside the striate area However, this does not alter the fact that a circumscribed lesion in the MOT gyrus is capable of causing complete hemiachromatopsia Therefore, we assume that this region corresponds to the area V4 described by Zeki ( 1969). References Albert ML, Reches A, Silverberg R (1975) Hemianopic color blindness J Neurol Neurosurg Psychiatry 38:546-549 Albert ML (1973) A simple test of visual neglect Neurology (Minneap) 23: 658-664 Bender MB, Kanzer MG (1939) Dynamics of homonymous hemianopsias and preservation of central vision Brain 62: 404-421 Benton AL, van Allen MW (1968) Impairment in facial recognition in patients with cerebral disease Cortex 4:344-358 Bjerrum J (1981) Hemianopsi for Farverne Dan Hosp Tid 8: 41-49 Brouwer B (1936) Chiasma, Tractus opticus, Sehstrahlung und Sehrinde In: Bumke O, Foerster O (eds) Handbuch der Neurologie, vol VI Springer, Berlin Heidelberg New York Critchley M (1967) Acquired anomalies of color perception of central origin Brain 88:711-724 Damasio A, Yamada T, Damasio H, Corbett J, Mckee J (1980) Central achromatopsia: Behavioral, anatomic and physiologic aspects Neurology (Minneap ) 30:1064-1071 Farnsworth D (1943) The Farnsworth-Munsell 100-hue and dichotomous tests for color vision J Opt Soc Am 33:568678 Geschwind N, Fusillo M (1965) Color naming in association with alexia Arch Neurol 15:137-146 Green JG, Lessell S (1977) Acquired cerebral dyschromatopsia Arch Ophthalmol 95:121-128 A textbook and Harrington DO (1981) The visual fields atlas of clinical perimetry Mosby, St Louis Heilman KM, Valenstein E (1979) Mechanism underlying hemispatial neglect Ann Neurol 5:160-170 Hering E (1920) Grundzige der Lehre vom Lichtsinn. Springer, Berlin Heidelberg New York Holmes G (1918) Disturbances of vision by cerebral lesions Br J Ophthalmol 2:353-384 Lenz G (1921 a) Zur Pathologie der cerebralen Sehbahn unter besonderer Beriicksichtigung ihrer Ergebnisse fur die Anatomie und Physiologie Graefes Arch Clin Exp Ophthalmol 72:1-85, 197-273 Lenz G (1921 b) Zwei Sectionsfille doppelseitiger zentraler Farbenhemianopsie Z Ges Neurol Psychiatrie 71:135-186 Luria AR (1960) Die hheren cortikalen Funktionen des Menschen und ihre Storungen durch ortliche Hirnschadigungen VEB Verlag d Wissenschaften, Berlin Mackay G, Dunlop JC (1899) The cerebral lesions in a case of complete acquired color blindness Scott Med Surg J 5: 503-512 Meadows JC (1974) Disturbed perception of color associated with localized cerebral lesions Brain 97:615-632 Michael CR (1978) Color sensitive complex cells in monkey striate cortex J Neurophysiol 41:1250-1266 Monie M (1948) Uber Untersuchungen der Tiefensehscharfe mit dem Stereoeidometer Graefes Arch Clin Exp Ophthalmol 148:343-357 Pearlman AL, Birch J, Meadows JC (1979) Cerebral Color Blindness: An acquired Defect in Hue Discrimination. Ann Neurol 5:253-261 Samelsohn J (1881) Zur Frage des Farbensinncentrums Zentralbl Med Wissensch 29:850-853, 900 Schein SJ, Marocco RT, De Monasterio FM (1982) Is there a high concentration of color-selective cells in area V4 of monkey visual cortex? J Neurophysiol 47:193-213 Teuber HL, Battersby SW, Bender MB (1960) Visual field defects after penetrating missile wounds of the brain Harvard Univ Press, Cambridge Ungerleider LG, Mishkin M (1979) The striate projection zone in the superior temporal sulcus of Macaca mulatta: location and topographic organization J Comp Neurol 188: 347-366 van Essen DC, Zeki SM (1978) The topographic organization of rhesus monkey prestriate cortex J Physiol 41: 193-226 Verrey D (1888) Hemiachromatopsia droite absolue Conversation partielle de la perception lumineuse et des Ancien kyste hemorrhagique de la partie informes ferieure du lobe occipital gauche Arch Ophthalmol 8: 289-300 Wilbrand H, Saenger A (1917) Die homonyme Hemianopsie. Bergmann JF, Wiesbaden Zeki SM (1969) Representation of central visual fields in prestriate cortex of monkey Brain Res 14:271-291 Zihl J, von Cramon D (1980) Color anomia restricted to the left visual hemifield after splenial disconnection J Neurol Neurosurg Psychiatry 43: 719-724 Zihl J, Mayer JC (1981) Farbperimetrie: Methode und diagnostische Bedeutung Nervenarzt 52:574-580 Received January 27, 1988