LASTING EFFECTS OF EARLY BLINDNESS A CASE STUDY
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1 Quarterly rournal of Experimental Psychology (1974) 26, I LASTING EFFECTS OF EARLY BLINDNESS A CASE STUDY CAROL ACKROYD, N. K. HUMPHREY AND ELIZABETH K. WARRINGTON National Hospital, Queen Square, London A young woman, blinded by the development of corneal opacity at the age of 3 years, was given a corneal graft at the age of 27. Though the image-forming powers of the eye were largely restored, the patient showed little recovery of functional vision. Six months after operation she could detect and locate conspicuous objects and had some degree of ambient spatial vision but she could not learn to recognize simple visual patterns. Eventually she reverted to the life of a blind person. Her failure to recover is discussed in terms of the known deleterious effects of restricted early visual experience on the development of the visual cortex in animals. Introduction In cases of severe cataract or opacity of the cornea no patterned light reaches the retina of the eye. By surgical removal of the lens or the graft of a new cornea the power to form a focussed image may be largely restored. But if the opacity has been present from early childhood the image is now offered to a brain which is wholly unpractised at analysing it; and practice at this stage may come too late. Von Senden (1960) reviewed 66 reports of cataract operation between the years 1920 and 1931 and showed convincingly that in the majority of cases of early blindness the mere restoration of eyesight is not sufficient to bring about much useful vision. There was much variability among his cases and in some at least a semblance of normal vision emerged after training but in many the ability to see remained rudimentary. In marked contrast to this general picture is the report by Gregory and Wallace (1963) of the case of a 52-year-old man, blind since 10 months of age, who on being given a corneal graft rapidly developed efficient pattern vision. The interpretation of these cases has been debated, yet the issue remains one of both theoretical and medical importance. Although one new case cannot resolve the clash of evidence, these cases are now so rare that each one merits detailed study. We report here the case of a young woman, blind since the age of 3 years, who was given a corneal graft at the age of 27. Despite her high hopes for the success of the operation and her exceptional intelligence she made little if any worthwhile progress in learning to see. Seven months after the operation she gave up the attempt and returned to the life of a blind person. We describe the few visual * University of Cambridge, Sub-Department of Animal Behaviour, Madingley Cambridge. 4
2 LASTING EFFECTS OF EARLY BLINDNESS 5 capacities which were restored to her and some of her continuing deficiencies. In conclusion, drawing on recent evidence about the brain mechanisms underlying vision in animals, we suggest a possible neurological basis for her disability. Personal and Clinical History 1I.D. was born and lived in the Middle East. As a baby, so far as we know, she had normal vision, until at the age of 3 years she contracted smallpox. The smallpox caused severe scarring of the corneas of both eyes and she became effectively blind. At the age of 18 an opaque shell was fitted to her right eye for cosmetic reasons. H.D. lived at home with her family until the age of 15, receiving no formal education. At I 5 she was sent to a school for the blind and learned braille for the first time. In spite of this late start, 6 years later at the age of 21 she passed the entrance examination for university in open competition with sighted students. Four years later she was awarded a B.A. degree. She was first taught English at school and displayed a remarkable talent for the language, so that by the time she left university her English was almost as good as her native tongue. She obtained a post, teaching English, after completing her studies. Her comprehension and expression of English were in our opinion almost faultless. Although her vision was so blurred that she had no pattern vision, H.D. remained sensitive to light. No detailed records are available of the extent, if any, to which she continued to use her eyes. But her recollection, when we saw her after operation, was that her limited light sense had not been without value to her. During the years of her blindness she had been able to perceive small changes in the ambient light which reached her eyes, and she claimed that, for instance, she could detect passing shadows or the movements of large objects and that she could tell whether a door in front of her was open or closed. Her light sense had, moreover always been a source of comfort to her and, for example, if she awoke in the night from a bad dream she would switch on the room light for reassurance. At the age of 27 she was examined in her home town by Mr Ainslie, who found dense corneal scarring and disorganization of the anterior chamber of the left eye. He advised that a corneal graft offered a possibility of improving her vision. With considerable determination she raised sufficient funds to cover the costs of travel and medical expenses and came to London for the operation. A left corneal graft was performed, which remained clear. The operation was technically satisfactory and the physical condition of the eye was judged by the surgeon to permit acuity as good as 6/18 or 6/12. Immediately after the operation her vision was little if at all improved. Crude random eye movements, typical of patients blind from early life, were present. No significant recovery of vision took place during the next few months and 22 weeks after operation she was referred to the Psychology Department of the National Hospital for assessment of her perceptual functions. At the time of referral to the National Hospital the following psychophysical tests were administered at Moorfields Hospital : (I) Electroretinogram: her ERG was of normal amplitude.
3 I 16 C. ACKROYD, N. K. HUMPHREY AND E. K. WARRINGTON (2) Visual evoked responses: cortical VERs were recorded using a single midline occipital lead. Cortical VERs were present to a flash stimulus and though of relatively low amplitude were within normal limits. (3) Brightness thresholds and dark-adaptation : Absolute thresholds were measured using a Goldmann-Weekers dark adaptometer. The stimulus was a small light source subtending a 5 arc. Her brightness threshold and the shape of her dark adaptation curve were entirely normal (see Figure I). 10! FIGURE I. Dark adaptation curve. Qualitative Observations Over the course of the 2 months which H.D. spent at the National Hospital we were able to examine certain aspects of her vision in laboratory tests and also to observe how she got on in more informal settings. Before we describe our findings, something must be said about her general state of mind over this period. By the time she came to the National Hospital, H.D. had already begun to feel intense disappointment at the limited extent of her recovery of sight. As time passed and it became clear to her that the operation had, in her own words, been a failure and that she could not see as other people do, she suffered a form of reactive depression very similar in kind to that of several of Von Senden s cases (Von Senden 1960, pp ). At this time her attitude to the visual tasks and to ourselves became increasingly ambivalent. On some days she would be friendly and co-operative, but on others depressed and therefore unwilling to attempt the test problems. Seeing, far from being a rewarding activity, had become a tiresome duty for her, and left to herself she soon lost interest in it. The laboratory tests were, of necessity, carried out at times when she was prepared to co-operate, and we can be reasonably sure that her performance at those times represented the best that she could do; how much her vision might have improved if she had been less despondent between times, we cannot say. H.D. was an active person, who despite her blindness was experienced at travelling and getting about large cities. While resident at the National Hospital she went out on occasion in the streets and parks of London, and on some of these trips we accompanied her. Before giving the results of the formal tests of her vision, we record here some qualitative impressions from these outings.
4 LASTING EFFECTS OF EARLY BLINDNESS 1 7 Detection of the presence and location of an object H.D. could detect and point with reasonable accuracy to any well-defined visual object, such as a door handle, provided there was sufficient contrast with the background. If the contrast was low she had difficulty. While, for instance, she could easily pick out a pigeon on a dark patch of earth she could not see one on a grey pavement. If the object moved the task was made much easier. She could see the pigeons as they alighted in Trafalgar Square but she said that they appeared to vanish as they came to rest. Spatial vision In addition to being able to point to objects H.D. had some degree of more general spatial vision. When walking around she would avoid large obstacles such as trees and walls, claiming that she did indeed see them. She was able to detect the yellow lines at the kerb of the street, and would step up or down when she came to them; on one occasion we saw her stop and take a step up into the air on coming to a white line at the centre of the road. On another occasion she stopped in front of a manhole cover in the pavement and carefully skirted round it. Movement Moving objects were more easily seen than any others, and H.D. claimed that her most vivid visual impressions were to be had from the window of a moving car. She was excited by the sight of moving fishes in the brightly-lit tanks of the aquarium at the London Zoo, and she was able to follow their movements with her finger. She could not, however, make out the small darting birds in the hummingbird house. Brightness H.D. clearly had a good sense of overall brightness (present also before her operation) and she would for instance comment on the change in the light when a cloud passed across the sun. She could correctly pick out the flowers in a bed which were brighter, or, as she often put it, more glittery than others. Colour Although H.D. claimed to have a sense of colour and would sometimes use colour words to describe things, our own impression was that she was colour-blind. She mistook the colours of traffic lights, of cars, and of people s clothes and she could, for instance, neither give the names nor remember the names we gave her for the colours of clumps of crocuses growing in the grass. The colour word she used most frequently was red, but she did not limit it to red-coloured objects and our impression was that she meant, rather, bright or vivid. Form and size H.D. never showed any convincing evidence of recognizing things by shape. She was, however, able in some situations to judge relative size and she could
5 I 18 C. ACKROYD, N. K. HUMPHREY AND E. K. WARRINGTON correctly distinguish large from small fish in the aquarium. She said that she could see how tall people were-and certainly she did sometimes judge their relative height correctly, but always when cues other than visual ones were potentially available to her (e.g. the height from which their voices came). Formal Tests The tests consisted of simple visual discrimination problems in which H.D. was asked to distinguish two alternative visual stimuli presented successively in random order. She made her response either verbally or with some appropriate movement of her hand. Trials were given in blocks of 30 per problem, and four problems were usually given at each session though this depended on how she was feeling; on successive sessions she either attempted the same problems or started a new one. We set a criterion level of 27 correct responses out of 30 (90 /0), as a measure of %uccessful ) discrimination ; H.D. was well aware that our supposedly random schedule had certain in-built regularities to it (e.g. equal numbers of positive and negative trials) and consequently her chance level of performance was above 50%. On several problems there was clear evidence of improvement with practice, and for these we present the results in the form of Yearning curves. Throughout the sessions we gave H.D. whatever advice and encouragement we could. Presence or absence of an object H.D. was seated at a table and simply required to state whether the stimulus, a white square (on the wooden surface of the table) was present or not. The square was absent on half of the trials and on the other trials it was placed directly in front of her. Four sizes of square were used; 4, 2, I and 0.5 cm, and they were presented in blocks of 10 trials with each size, starting with the largest. No fixed distance was imposed and for the most part she relied on close-up scanning, with her head not more than a few inches from the stimulus. Her performance was good from the start with the two larger squares, but 90 trials were required for her to reach the criterion of success with the I-cm square, and 150 trials with the o.5-cm square (see Figure 2). In addition to these quantitative changes, qualitative changes were observed in her strategy of visual search. As her performance improved on this task she appeared to rely more on scanning eye movements than on gross movements of the head. Location H.D. was seated in front of a table on which was a sheet of black paper marked with six positions along a line from left to right, approximately 15 cm apart. A white 2.5 cm cube was placed in one of these positions at random, and she was required to locate the cube visually, and having done so to reach out and touch it with her index finger. We found it impossible to obtain a reliable quantitative measure of performance on this task ; however, with successive trials she became able to locate the block far more quickly and to point with greater assurance and accuracy. She also learned to do the task while sitting back in her chair and by
6 LASTING EFFECTS OF EARLY BLINDNESS + 0 E lo Session FICUREZ. Detection of presence or absence of four squares of different sizes. M-., 4-cm square; , z-cm square; A --- A, I-cm square; A- A, 4-cm square. scanning with her eyes rather than moving her head, although she frequently reverted to her earlier strategy of close scrutiny of the board on those trials on which she had difficulty in locating the block. Movement To provide a moving stimulus we used an oscilloscope screen on which was displayed a horizontal line of bright spots, about 0-5 cm across, which could be made to move uniformly to right or left at a speed of about 10 cm/s. H.D. sat facing the screen and was asked to say whether the spots were stationary or moving, and in the latter case to indicate with her hand the direction of movement. We found that she never failed to distinguish correctly between stationary and moving stimuli, and with moving stimuli she indicated the direction correctly 27 times in the first 30 trials. Brightness and colour We knew from informal observations that H.D. could discriminate between objects of different degrees of brightness contrast. But having heard her on one occasion describe a dark object on a light background as appearing "bright" to her, we thought that she might be responding merely to the size of the brightness step at the contour of the object and not to its sign, i.e. to the absolute contrast independent of whether the object was darker or fighter than the background. So we tested
7 I20 C. ACKROYD, N. K. HUMPHREY AND E. K. WARRINGTON her on a task where she was asked to distinguish a I-cm white square on a grey background (5.5 cm square) from a I-cm black square on the same background, the absolute contrast of the two squares being the same. On this task she had no success at all and failed to reach the criterion in 450 trials (see Figure 3). The results for colour discrimination were puzzling and rather inconclusive. The first task she attempted was the discrimination of a red plastic disc from a green one of the same diameter (3.8 cm), the subjective brightness of the two stimuli 30 t + 0 E 0 0 z FIGURE 3. Discrimination of a black I-cm square on a mid-grey background 5.5-cm square from a white I-cm square on a similar background; and discrimination of a red plastic disc (diameter 3.8 cm) from a green one of approximately the same brightness and of the same size. a- 0, Red-green discrimination; , black-white discrimination. having been roughly matched. On this she failed to reach criterion in 570 trials (Figure 3). In the hope of making the task easier, we tried using much larger and more intense stimuli projected on to a wall in a darkened room. On a straight discrimination of red and green stimuli, presented singly and at a constant intensity, she reached the criterion level of 27/30 after a total of 60 trials on this task. When we now introduced a third colour, blue, between trials with red and green, her performance deteriorated and she claimed that she had difficulty remembering which name was associated with which colour. To try to obviate this difficulty, we gave what we supposed to be a much simpler task where she was presented simultaneously with two patches of colour side by side and was asked to say only whether they were the same or different in colour. However, she continued to perform badly, and even with only the red and green stimuli at constant intensity she failed to reach the criterion after 50 trials. We then reverted to a task which had been tried briefly on a previous occasion, discrimination of a single stimulus, either red or green, but with both colours being independently varied in intensity. She now reached the criterion level of performance, 27/30 correct, after a total of 70 trials on
8 LASTING EFFECTS OF EARLY BLINDNESS I21 this particular task. At this point H.D. was unwilling to attempt any further tests with colours, and so it became impossible to verify this last finding, the only real evidence we have concerning her capacity for colour vision. Form We tested H.D. on various problems involving differences in form, viz. the discrimination of horizontal from vertical stripes, stripes from grey, a circle from a square, a triangle from a cross, and a plastic spoon from a pair of scissors. For each pair of stimuli one or other was laid down on the table in front of her in random order and she was asked to give its name or, in the case of the horizontal and vertical stripes, to indicate the direction of the stripes with her finger. We soon found that her only way of solving any of these problems was to scan the stimulus with her eye very close to it; though this makes it doubtful whether she was really discriminating form as such, we allowed her to adopt this method if she pleased. (a) Stripes vs. grey: horizontal vs. vertical stripes. The striped stimuli consisted of 5-5 cm-square cards bearing black and white stripes 0.5 cm wide ; the grey stimulus was a similar card of a uniform grey, equal in overall luminous flux. H.D.'s performance on these two problems, which were interspersed with each other, is shown in Figure 4. On both problems she reached Session FIGURE 4. Discrimination of S's-cm square card bearing black and white stripes 0.5 cm wide from a uniform grey card the same size and equal in overall luminous flux and discrimination of horizontal or vertical direction of stripes on a s*s-cm square card with stripes of width o'g-cm 0-0, Direction of stripes; , striped-plain discrimination. the criterion level in under 500 trials. She readily admitted, however, that by adopting her method of close-up scanning she turned these problems effectively into a kind of temporal brightness discrimination. (b) Circle vs. square; triangle vs. cross. The stimuli were cut out of white paper. The circle had a diameter of 9 cm, the square a side of 8 cm, the triangle a side of I 5 cm and height of 7.5 cm, and the cross arms of 14 by z cm. The circle/square problem, interspersed with other tasks, was
9 I22 C. ACKROYD, N. K. HUMPHREY AND E. K. WARRINGTON attempted repeatedly during the whole period we worked with H.D. : the triangle/ cross problem was given towards the end. Her performance is shown in Figure 5. She made no improvement on the circle/square problem over 1380 trials. She did, however, master the triangle/cross problem quite quickly, reaching the criterion within 90 trials, but again she relied on close-up scanning. I 1 FIGURE 5. Discrimination of a cardboard circle of diameter 9 cm from a square of side 8 cm over 1320 trials; discrimination of a triangle of base 15 cm and height 7.5 cm from a cross of arms 14 x 2 cm and discrimination of a white plastic spoon from a pair of scissors. A- A, Circle/square discrimination; triangle/cross discrimination; , spoon-scissors discrimination. (c) Spoon vs. scissors The spoon was made of white plastic and the scissors of shiny metal. H.D. s performance on this problem is also shown in Figure 5. She reached the criterion within 90 trials, and it is notable that on this problem alone did she show evidence of being able to make the discrimination without scanning. In this case there were, however, brightness cues in addition to form cues available to her, and we judged that it was these that helped her. Discussion The tests and informal observations together demonstrate the peculiarities and remarkably limited scope of H.D. s vision. After the operation she was able to detect, locate and follow the movement of conspicuous objects, to avoid large obstacles in moving around and to make certain discriminations on the basis of brightness and possibly gross colour differences; but she remained unable to do the one thing for which vision is chiefly valued, namely to recognize objects by their visual form. She has now-18 months after the operation-resumed her former effective way of life as a blind person. Compared to other cases of recovery from early blindness, H.D. must rank among the least successful. The contrast between her case and the case of S.B. reported by Gregory and Wallace is particularly striking. S.B. began to lose his sight at the age of 10 months, appreciably earlier than H.D., but after operation at the age of 52 he became able almost at once to name colours, to recognize complex shapes and
10 LASTING EFFECTS OF EARLY BLINDNESS 23 even to read letters of the alphabet. Gregory and Wallace attribute part at least of this remarkable-and exceptional-recovery to S.B. s intelligence, enthusiasm and long-standing interest in the world of sight. But H.D. was not lacking in these qualities. Indeed it might well have been thought that H.D. had much in her favour: her comparative youth and the later onset of her blindness should both, if anything, have given her an advantage over S.B. We do not know how to account for the great difference in the two cases except to suggest as one possibility that S.B. s corneal opacity may have been slow to develop, so that he may have been partially sighted for much longer than Gregory and Wallace suppose: there are ample examples of recovery in cases of blindness which came on in late childhood. The evidence we collected leaves much still uncertain. Nonetheless, these in outline would appear to be the facts about H.D. As a child up to the age of 3 she had good sight and her brain presumably began its development normally; at 3 her eyes failed her and for the next 24 years no pattern information was present in the visual input to her brain. At 27, after operation, her brain was unable to take advantage of the additional information now present in the retinal image. What happened to her visual system in the interval from 3 to 27 years? Two recent discoveries about the visual systems of animals suggest an answer. First, there is the evidence of the effects of visual deprivation on the development of the visual cortex in kittens. Studies by Hubel and Wiesel, Blakemore, Spinelli and their colleagues have demonstrated the profound importance of early visual stimulation for the development and maintenance of specific feature analysers in the visual cortex (for reviews see Spinelli, Hirsch, Phelps and Metzler, 1972, Blakemore, 1973). There experiments suggest that there is a critical period in the development of a kitten s brain, extending roughly from 3 weeks to 4 months of age, during which single units in the visual cortex tune in, as it were, to the features of the visual environment: if during this period visual stimulation is absent or restricted, the range and specificity of cortical analysers is correspondingly permanently impoverished. Comparable electrophysiological evidence is not yet available for primates, but studies of the effects of visual deprivation on discrimination (von Noorden, Dowling and Ferguson, 1970) suggest that a similar story holds true for monkeys. It is risky, of course, to extrapolate to man, and we may only guess at what might be the length of the critical period. But simple matching for developmental age suggests that this period may extend at least to z and possibly beyond 3 years. On this basis, we propose that one consequence of H.D. s early blindness at a stage when her brain needed continual visual experience, was that by the age of 27 her cortical feature analysers were, if not absent altogether, grossly abnormal. The other line of evidence from animals supports this possibility. One of us (N.K.H.) has made a detailed study of the behaviour of a monkey whose primary visual cortex had been removed (Humphrey 1970, 1972). We notice certain striking similarities between the residual vision of this monkey and that of H.D. In contrast to the classical picture of cortical blindness, Humphrey found that the destriate monkey could be trained to show a surprisingly wide range of visuallyguided behaviour: it could locate small objects in space, avoid obstacles, and make fine discriminations between objects which differed in their relative salience or
11 24 C. ACKROYD, N. K. HUMPHREY AND E. K. WARRINGTON conspicuousness (movement, size and brightness contrast being the major determinants); it could not, however, ever identify objects on the basis of their colour or visual form. The monkey s acuity and spatial resolution was in fact superior to that of H.D., but the qualitative picture is very much the same. In H.D. we were dealing with a complex person with a complex history and any explanation of her failure to recover her sight has to be hedged with caution. Yet our evidence strongly supports the notion that the visual cortex of H.D. s brain, having been deprived of adequate stimulation at a critical period in early childhood, had become by the time of operation virtually useless to her. We wish to thank Mr D. Ainslie for his permission to investigate H.D. and report our findings. We are grateful to Mr A. Bird for undertaking the physiological tests quoted in this paper. H.D. was under Dr R. T. C. Pratt s care during the course of this investigation and we wish to thank him for his support and for the facilities he provided throughout the whole period of this investigation. References BLAKEMORE, C. (1973). Environmental constraints on development in the visual system. In Constraints on Learning: Limitations and Predispositions. Academic Press. Pp London: GREGORY, R. L. and WALLACE, J. G. (1963). Recovery from early blindness: a case study. Experimental Psychology Society Monographs, 2. HUMPHREY, N. K. (1970). What the frog s eye tells the monkey s brain. Brain, Behaviour, Evolution, 3, HUMPHREY, N. K. (1972). Seeing and nothingness. New Scientist, 53, VON NOORDEN, G. K., DOWLING, J. E. and FERCUSON, D. C. (1970). Experimental amblyopia in monkeys. Archive OphthalmoZogy, 84, VON SENDEN, M. (1960). Space and Sight. London: Methuen. SPINELLI, D. M., HIRSCH, H. V. B., PHELPS, R. W. and METZLER, J. (1972). Visual experience as a determinant of the response characteristics of cortical receptive fields in cats. Experimental Brain Research, 15, Received 12 March 1973
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