15 (1985) 227-240 elsevier 227 bbr00441 - university of liverpool

Behavioural Brain Research, 15 (1985) 227-240 Elsevier 227

BBR00441

APPERCEPTIVE AGNOSIA DUE TO CARBON MONOXIDE POISONING. AN INTERPRETATION BASED ON CRITICAL BAND MASKING FROM DISSEMINATED

LESIONS*

JOHN CAMPION and RICHARD LATTO

Department of Psychology, University of Liverpool, Liverpool (U.K.)

(Received April 12th, 1984) (Revised version received February 16th, 1985)

(Accepted February 20th, 1985)

Key words: visual agnosia - apperception - visual cortex lesion - disseminated lesion - spatial frequency channel - orientation channel - critical band masking - scotoma - carbon monoxide poisoning

Apperceptive visual agnosia is normally held to be a specific deficit in 'apperception' - a hypothetical postsensory stage in visual processing. This paper describes the investigation of a patient diagnosed as suffering from a classical apperceptive agnosia resulting from carbon monoxide poisoning. Controlled behavioural testing confirmed the apparent agnosia but revealed that he could be trained to make a number of visual discriminations which had not been apparent from routine clinical examination and that he suffered a number of subtle sensory impairments which likewise had not hitherto been apparent. Evoked potential recording to grating patterns showed a complex pattern of brain responses involving interactions between spatial frequency, orientation and hemisphere recorded from. The data suggested that the agnosia was caused by sensory impairments rather than a deficit in apperception. We proposed that the impairments were caused by loss of certain spatial frequency and orientation information but rejected an interpretation based on the concept of processing channels in favour of one based on object contour masking by a peppery field defect caused by disseminated lesions. This interpretation received some support from fine grain static perimetry, contrast sensitivity function measurement and orientation discrimination in the two hemifields. Qualitatively similar results were obtained in normal subjects whose field was artificially masked. The results have implications for theories of visual agnosia and for theories of vision based on the concept of processing channels.

INTRODUCTION

This paper describes research carried out over a number of years on a patient diagnosed as having a classical apperceptive agnosia 1'5. It ad- dresses two issues: the nature of deficits underlying visual agnosia, and the existence of spatial frequency and orientation processing channels in the visual system.

Visual agnosia is defined as a deficit in perception in the absence of any concomitant sensory impairment 7. It is implicit in this definition that a

sensory deficit may be present but if it is, this is unrelated to the agnosia. The major thrust of this paper is towards defining a sensory deficit, estab- lishing its existence and demonstrating its relationship with the agnosia. Many varieties of agnosia have been described ~2 arising from damage to portions of prestriate cortex and pos- terior cortex of the parietal and temporal lobes. These structures are collectively referred to as visual association cortex. A broad division of agnosias into apperceptive and associative types was made by Lissauer in 188915 and this division

* Presented at the European Brain and Behaviour Society Workshop on The Effect of Hypoxia on Brain and Behaviour, Rotterdam, April 1984.

Correspondence: J. Campion, Department of Psychology, University of Liverpool, Liverpool, U.K.

0166-4328/85/$03.30 © 1985 Elsevier Science Publishers B.V. (Biomedical Division)

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is still regarded as useful today (e.g. ref. 13). Ap- perceptive agnosia is held to be a low-level disorder resulting from a failure in 'apperception' (the formation of a percept) whereas associative agnosia is held to be a higher-level disorder in which the percept is intact but there is an inability to assign any meaning to it. A further sub-division of these two types is usually made on the basis of observed specific perceptual deficits related to damage of specific cortical regions (e.g. prosopagnosia 17, object recognition 22 and object constancf3). Behind all of this research is an implicit model of visual processing, which is perhaps most clearly articulated by Warrington 22. She proposes that visual processing is organised into 3 hierarchical stages (sensation, postsensory perceptual categorisation and semantic categorisation) within which there are a number of parallel categorical channels. It is assumed that both stages and channels can be linked to specific anatomical structures. Running counter to this approach is the view held by some workers that agnosias can be attributed to factors such as sensory impairment 2, naming difficulties 1~ and com- binations of non-specific sensory and cognitive deficits 3. We shall call these two approaches 'perceptual' and 'sensory', respectively. We should note two features of these approaches. First, that the perceptual approach implies that agnosias can lead to a particular model of visual processing, whereas the sensory approach is entirely neutral in this respect. Second, that there is the danger of a semantic quibble because if agnosia is defined in terms of non-sensory deficits then the presence of a deficit could lead one automatically to exclude it as in instance of agnosia.

Both these approaches suffer from difficulties which stem from the same underlying problem, that is the lack of an appropriate functional model. Thus with 'perceptual approach' research we do not know if 'face recognition', 'object recognition' or 'object constancy' are real functions and with 'sensory approach' research we do not know what constitutes a sensory function. We can administer a battery of sensory or perceptual tests but we do not know if we have tested a complete set of functions, and if we do discover a deficit in test performance we have no

way of relating this with certainty to any alleged functional deficit. For these reasons, the argu- ments normally set against the sensory theory, that there is no pattern of sensory loss which can be uniquely associated with the agnosia 9'22 and that some agnosic patients can be shown to have no sensory lOSS 7, lose much of their weight. The sensory loss theory deserves serious considera- tion at least, partly because sensory deficits are nearly always discovered in agnosic patients 9-'7 and partly for reasons of parsimony. However, a major problem lies in the fact that we might be able, with subtle probing, to demonstrate that a given deficit is a necessary condition for agnosia, but be unable to demonstrate that it is sufficient. In the research we present in this paper, we have used a set of converging studies drawing on knowledge of behavioural performance, electrophysiological responses and the pathological process of the lesioning agent. We have also attempted to simulate the hypothesised agnosia-inducing process in normal subjects.

THE PATIENT

R.C. worked as a foreman in an iron foundry until 1975 when he suffered carbon monoxide poisoning resulting from an accident which left him with a severe visual impairment. We examined the patient on a number of occasions between 1979 and 1983. A full ophthalmological and neuropsychological assessment is presented else- where ~ in which R.C. is reported by a number of clinicians as suffering from a severe agnosia with intact sensory functions, apart from a small field defect and diminished low spatial frequency sensitivity. Cognitive functioning was reported nor- real apart from some early evidence of slight lan- guage and memory disturbance which later disap- peared. A CAT scan (Fig. 1) indicated a diffuse lesion most prominent above the calcarine sulcus of the left hemisphere extending into striate and prestriate cortex. There was some involvement of the prestriate cortex of the right hemisphere. A dynamic field plot (Fig. 2) revealed a right inferior defect consistent with the CAT scan. The same defect was reported by other workers but we had no knowledge of this at the time we performed our

229

20 deg/div Dynamic Target

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Fig. 1. CT scan of R.C.'s brain recorded on 26.4.78. The section is immediately above the calcarine sulcus. Note the low density (dark) area in the left occipital lobe involving striate and prestriate regions. Also the smaller low density patch in the prestriate region of the right hemisphere.

Fig. 2. R.C.'s visual fields plotted dynamically using a Goldman perimeter on 17.12.79. The target was 64mm 2 intensity 'e'. The solid lines indicate the plot for an inward moving target and the broken lines for an outward moving target. Left and right eyes are superimposed. The outward moving target produced a great deal of variance in responding, so the line indicated represents the 'modal' response.

examination. We obtained very different field plots depending on whether an inward or outward moving target was used. An outward moving target produced, not only a much contracted field, but a greater degree of uncertainty in responding. We initially attributed this to the patient simply

having difficulty in setting a stable criterion with this type of task, but it assumed greater significance later on in the research.

BEHAVIOURAE TESTING

Casual observation indeed supported the notion that R.C. had a severe agnosia. He appeared cognitively normal but was unable to recognise simple geometric shapes, the orientation of lines or grating patterns or even the number of such items (one or two) presented together. He was unable to name any item, describe its function or make same/different judgements between them when presented as pairs together or sequentially. His agnosia would be classified as apperceptive on the grounds that he was unable to copy any item or even trace it with his finger. He could not even trace a straight line with any accuracy. In contrast to this severely impoverished perceptual discrimination, R.C. could clearly see, in that he could negotiate obstacles in the room, reach out to manipulate objects, name objects by touch or sound and could comment on the 'sensory' quali- ties of objects such as their colour or texture. A peculiar feature of his performance was that he was very sensitive to fine repetitive patterning

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such as the graticules on drawing instruments and graph paper which he readily identified. The first indication we had that R.C.'s disorder was not as simple as it first appeared was that when closely questioned and encouraged to guess about objects shown to him, he could often make accu- rate estimates of the nature of the object. For example, he would say 'is it a tool?' when shown a pair of scissors.

In order to test his residual capacities more systematically, we asked him to name 30 line drawings of objects from the Boston Naming Test and 27 common objects equivalent to the drawings. In each case he was told if he was correct and given the correct name if he was wrong. Near misses such as the response 'flower' for 'tree' were counted as correct. Each item was presented once per testing session. There were 4 sessions over 4 days. Each session contained some new items and some he had failed to recognise previously. The testing protocol was varied slightly both within sessions and across sessions to maximise the patient's performance, since the aim was to 'draw out' as much residual capacity as possible. Thus, some items were repeated more than once and the number of repeated and new items varied as did the amount of information provided in response to the patient's questions. Despite the lack of experimental rigour, it was clear that objects were identified more easily than pictures and that repetition improved his performance. initially R.C. scored 17 out of 27 for objects but only 5 out of 30 for pictures. Of all the items presented on more than one occasion he scored 16 out of 17 for objects and 8 out of 12 for pictures. There were two features of his performance which should be stressed: First, successful performance did not indicate normal recognition. All identifications were very difficult and there was a great deal of uncertainty. Second, his subjective report and verbal responses suggested strongly that he was using partial cues to make inferences about the items, rather than recognising any of them in the normal sense of the word. However, the fact that R.C. could perform well above chance on outline drawings, difficult though these were, indicates that he was unlikely just to have been using crude physical features such as colour,

reflectance and so on, but retained some limited degree of pattern perception.

The next study was designed to determine the limits of his residual capacity by using simple stimuli and a sensitive performance measure. We also examined his responses to small luminance differences and desaturated colours. Pairs of stimuli were presented in random sequence and a forced choice response was required with feedback. Fig. 3 shows the results. It was clear that with training, R.C. could learn to discriminate between simple stimuli differing only in some spatial dimension, also that colour and brightness discrimination were substantially impaired. Neither of these perceptual attributes was detect- ed by clinical examination. Again, R.C. reported that he was not recognising the stimuli for what they were, and it was only the feedback which enabled him to attach a verbal label to what was to him a quite novel stimulus. All discriminations were trivially easy for normal subjects.

EVOKED POTENTIAL RECORDING

In order to see if R.C.'s brain responses could be related to his discrimination performance or to the site of the lesion, visual evoked potentials (VEPs) were recorded over left and right occipital lobes to flashed grating patterns of varying spatial frequency and orientation (Fig. 4.). The compo- nents which appear to be of most interest are N140 and P160 of the ON response and P170 of the OFF response. The P170 shows the typical OFF response behaviour, being largest in amplitude at low spatial frequencies and tailing off towards higher frequencies. It is symmetrical across hemispheres. In contrast the N140-P160 complex of the ON response is sensitive to both spatial frequency and orientation and shows marked assymetries. Since the OFF response is the product of luminance transience only ~4, we can conclude that the behaviour of N 140-P 160 is reflecting the brain's response to pattern. VEPs were small because of the stimulus conditions (Fig. 4.) but were reliable because of the high quality of the amplifiers and the off-line rejection of artefact. Individual VEP epochs were stored on computer disc and the amplitudes

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Fig. 3. A to E: percentage correct forced choice judgements between pairs of stimuli. The number within each bar shows the number of trials in which stimuli were presented and the horizontal line indicates chance performance. Stimulus parameters: A: red vs blue plain field using Kodak filters CC30R and CC30B. Bright vs dim plain field using no filter (luminance 300cd/m 2) and Kodak Neutral Density filter (N.D. 0.3). Fields were 22 ° high and 15 ° wide. B: horizontal vs vertical bar (8 x 2 °) and horizontal vs vertical square wave gratings (3 cycles/deg., 15 ° circular field). C: vertical vs slanting (45 °) gratings and left vs right slanting gratings, parameters as above. D: proportion of left and right slanting gratings correct. The asymmetry could have been due to a response bias but RC seemed much surer of the right gratings, saying that they were more 'prominent'. E: triangle vs circle. F: triangle vs circle vs square. For E and F, each bar represents performance in consecutive blocks of trials. All stimuli were 15 ° across the largest dimension, and were solid bright figures (300 cd/m 2) projected onto a dark ground (25 cd/mZ). In A stimuli were presented for 100 ms. In all other conditions stimuli were presented until RC made his response.

printed out during the averaging process. The amplitude of N140 and P160 was taken for each

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epoch and summed for each of the spatial frequencies and each of the orientations from each of the two most lateral positions (left and right). The 24 resulting sums for each peak are displayed in Fig. 5. and the data were subjected to a three factor analysis of variance (frequency × orientation x hemisphere) with repeated measures on one factor (hemisphere) to assess their reliability. Table I provides the summary of the analysis. There is a strong hemisphere effect in that overall the left hemisphere VEPs are much more positive owing to the fact that they are dominated by a P160 upon which the N140 appears to be superimposed. More interesting, though, are the interactions between spatial frequency, orientation and hemisphere. We cannot, of course, assume that N140 and P160 are reflecting independent processes, but each is capable of reflecting different aspects of the VEPs response. Perhaps the best way of characterising the data is to say that the right hemisphere is more responsive to pattern generally, particularly to horizontal gratings. The left hemisphere appears to be sharply 'tuned' (as measured by N140) to 6 cycles. The P160 to horizontal gratings follows closely the frequency response of N140, being most positive at 1 cycle and most negative at 6 cycles, but there is a marked difference in the response to vertical gratings. The maximum positivity is at 2 cycles with only slight fall off towards 12 cycles. This frequency x orientation interaction is common over both hemispheres, which suggests that it is not due to the lesion, or at least not due to any feature of it which is asymmetrical. This could indicate that the P160 of the ON response, like the P170 of the OFF response, is a response to luminance transience rather than pattern. If this is the case, then the domination of the left hemisphere response by this positivity (Figs. 4, 5) indicates that this hemisphere lacks sensitivity to pattern. These inferences are in accord with the CAT scan and field plot which indicate a greater involvement of the left hemisphere.

CONTRAST SENSITIVITY

We had evidence from the VEPs that the lesion had caused R.C.'s brain to become differentially

232

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TABLE I

Analysis of variance summary table for VEPs

233

Source NI40

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Total 671 Between 335 70.136 Orientation 1 117.360 1.75 Frequency 5 222.389 3.31 Frequ x Or 5 96.360 1.43 Error Between 324 67.236 Within 336 10.144 Hemisphere 1 1 2 1 0 . 0 2 2 189.184 Hem x Or 1 0.898 0.140 Hem x Frequ 5 22.617 3.536 Hem x Or x Frequ 5 3.719 0.581 Error Within 324 6.376

671 38.486 335 63.530

n.s. 1 0.975 0.016 n.s. < 0.01 5 147.738 2.422 < 0.05 n.s. 5 155.999 2.557 <0.05

324 60.997 336 13.518

<0.0001 1 2 4 0 8 . 4 7 1 3 9 1 . 3 7 0 <0.001 n.s. 1 0.101 0.0163 n.s. <0.005 5 20.571 3.342 <0.01 n.s. 5 7.346 1.194 n.s.

324 6.154

sensitive to cer tain spatial f requencies and orien-

tat ions. Prev ious workers ~ repor ted tha t his con- t ras t sensitivity funct ion ( C S F ) was relatively

normal . H o w e v e r we wished to invest igate this fur ther unde r cond i t ions which wou ld allow us to

measure C S F for different or ienta t ions o f grat ing and for different hemifields o f presenta t ion. O u r

intent ion was to relate our p syc hophys i c a l da t a to

bo th V E P and ana tomica l data. T o this end, con- t ras t th resholds were m e a s u r e d for each o f the

grat ing stimuli used in the V E P recording. Stimuli were f lashed for 10 ms in left, right and full fields. The threshold cri terion was the first de tec t ion o f

a pa t te rn o f any kind. C S F was de te rmined for R.C. and a no rma l subject (Fig. 6). Whe re a s the

no rma l subject exhibited a no rma l C S F with

m a x i m u m sensitivity at 2 - 3 cycles per degree,

R .C . ' s C S F was gross ly abnormal . In the normal , there were visual field differences and also orienta t ion differences in threshold , but the full field C S F was clearly a s u m m a t i o n o f the two hemi-

fields. In R.C. the C S F was flat and lower in the

left field. Hor i zon t a l stimuli p r o d u c e d cons is tent - ly higher thresholds , as they did in the normal , but

the shape o f the funct ion was quite different for

the two or ienta t ions in the case o f RC. Fur ther -

more , the full field C S F did no t appea r to derive f rom eitfier o f the two hemifields. The higher

thresholds and flatter C S F in the right field is cons is ten t with the larger lesion and reduced

pa t te rn sensitivity o f the left hemisphere , but

o therwise the da t a are no t very illuminating. The absolute th reshold values are relatively no rma l at

either end o f the f requency range but m u c h in-

c reased in the middle o f the range. It could have been that R.C. was no t actual ly r e spond ing to the

detec t ion o f pa t te rn a l though ins t ructed to do so.

W h a t e v e r the reason, the da t a do indicate the

presence o f a subtle sensory deficit which is likely to be dependen t on field o f p resen ta t ion and orientat ion. To this extent, at least, they are con-

sistent with the V E P and ana tomica l data .

Fig. 4. VEPs recorded to horizontal (A) and vertical (B) square wave gratings flashed for 500 ms. The epoch length is 2 s comprising 1 s prior to stimulus onset and 1 s after stimulus onset. The stimulus was a 14 x 7 ° rectangular field and the luminance of light bars was 50 cd/m 2 and the luminance of dark bars 15 cd/m 2. The figure above each set of 4 EPs indicates the spatial frequency of the stimulus in cycles/deg. EPs were recorded from an array of 4 silver/silver chloride electrodes placed at 2 and 4 cm to the left and right of Oz, each referred to a common Fz electrode (International 10/20 designation). Bandwidth of the recording apparatus was 0.16-30 Hz at 3 dB attenuation. Individual epochs were digitised at 256 samples/s, to 10 bit accuracy and stored on computer disk. A paper record was also kept of EEG, EOG and stimulus onset and was used to reject epochs from the averages containing eye movement of other artefact. Averages contained data from 25 to 30 epochs.

234

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ORIENTATION DISCRIMINATION

The next question we wished to address was whether the 'sensory' deficits could be related in any way to R.C.'s discrimination performance, if they could be, we might have grounds for pro- posing that his agnosia had an underlying sensory basis. We had shown that R.C. could make forced choice judgements between grating orientations (Fig. 3). Given his abnormal CSF we might expect this capacity to vary with spatial frequency and hemifield of presentation. Using the same stimuli as in the CSF and VEP studies, we deter-

mined R.C.'s ability to make forced choice judgements between horizontal and vertical gratings of each of the 6 spatial frequencies in each hemifield (Fig. 7). Stimuli were presented for 500 ms in a random sequence and R.C. was forced to judge the orientation on each trial. Feedback was always provided. Performance was poor although overall well above chance for both hemifields. Performance varied with spatial frequency and this variation varied with hemifield, although the reliability of the variation could not be assessed statistically. Performance at 6 cycles in the left hemifield was the worst case and the difference

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Fig. 7. Percentage correct orientation judgements for gratings of 6 spatial frequencies (horizontal axis) presented in the left (solid line) and right (broken line) hemifield. 48 stimuli were presented (24 of each orientation) in a random sequence at each spatial frequency. Performance was above chance overall in both the left (z = 4.2, P < 0.00005) and right (z = 22.04, P < 0.00005) fields. For a given spatial frequency, performance over 620,0 represents above chance performance for 48 trials.

between this and performance at 12 cycles in the same hemifield (the greatest difference) fell just short of statistical significance. The relationship between these data and previous data is unclear but it does again suggest that there is a hemifield difference in spatial frequency sensitivity and that this is reflected in discrimination performance. As with the discrimination performance described before (Fig. 3) R.C. never actually recognised any of the orientations but used cues such as 'promi- nence' together with the feedback to attach the appropriate verbal label.

THE MASKING HYPOTHESIS

With the VEP and CSF data it would be tempting to conclude that R.C.'s agnosia derived from selective damage to one or more spatial frequency and orientation channels. Deficits of the sort reported here are offered as evidence of the functional reality of processing channels and the loss of such channels is frequently offered as an explanation of perceptual deficits ~ 8,19. We did not favour such an interpretation for a number of

reasons. First, selective discrimination loss cannot in itself constitute evidence for functional channels, and even if it did, it would not be possible to predict any particular agnosic symp- tom from such loss without a model relating processing channels to perceptual performance. Second, there is no reason for expecting certain channels to be selectively vulnerable to injury. Third, we could not predict particular channel loss from what is known of the pathological processes of CO poisoning. Fourth, we could not predict particular channel loss from what we know of the anatomical distribution of the lesion. Instead we were impressed by a number of features of R.C.'s condition. First, form perception was clearly possible but it was greatly impoverished in some as yet unspecified manner. Second, R.C. maintained that his vision was 'not clear' despite his normal acuity j and sensitivity to repetitive fine patterning. Third, his field plot was very unstable with an outward moving target, CO poisoning is known to cause disseminated multifocal (peppery) infarcts of cortical tissue due to anoxia "~. We therefore hypothesised that the en- tire visual field of the patient was 'peppered' with minute scotoma resulting simply from randomly distributed multiple infarcts. The distribution happened to be of such a density and the infarcts of such a size as to cause optimal masking of contours at certain spatial frequencies and orientations. The process could also be such that it caused optimal masking of object contours, thus producing a severe agnosia. The effect would be similar to the 'critical band masking' of Stromeyer and Julesz 21 but would be due to spatial distribution of scotoma acting as a mask or filter, rather than to the interruption of functional channels.

In order to test this hypothesis we examined the central portion of RC's visual field (Fig. 8A) in the following manner. It was divided into 8001 ~ squares and using an Aimark perimeter, a spot of light was flashed within each square for 1 s. R.C. viewed the centre of his field monocularly and rated each flash for brightness on a 4 point scale from maximally bright ('1') to unseen ('4'). To indicate the pattern of responding and provide an indication of what R.C.'s visual field might really be like, we filled each square with a spot whose

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size related to the brightness rating. If the response was '1' we left the square blank and if the response was '2' to '4' we used a spot of increasing size on the grounds that such responses indicated the presence of scotoma which were either of varying density or varying size, or indeed both. Fig. 8B shows the results of plotting the visual field in this way. It is apparent that the field is indeed peppered with scotoma as predicted and that the density and size of the scotoma varies between the two hemifields. We cannot make any quantitative prediction from these results because they provide only a crude indication of the real state of affairs. We can, however, claim that they are in agreement with our prediction and with previous results. The major question remains. Could this be an explanation of the agnosia?

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Fig. 9 shows an indication of what we are pro- posing the world looks like to R.C. It is only a rough indication because, of course, he would be unaware of the peppering but would be left with the perceptual consequences. We claim that our theory has face validity at least. It is possible that such an effect could be caused by CO poisoning and furthermore, it would be unlikely to be detect- ed by routine clinical examination. All the behavioural data we have presented seem likely to be explicable by such a process. R.C. reported always, when pressed, that his vision was 'not clear' and that he felt that if he 'blinked his eyes everything would come clear'. One should not rely too heavily on such anecdotal reports, but we suggest that a world looking something like that

Fig. 9. Photograph of a wheelbarrow leaning against a wall (top left) and a bucket (centre) covered with a random dot mask. It is proposed that the mask simulates the peppering of R.C.'s field due to multiple infarcts. It is possible that the visual agnosia is caused by this process although the size and distribution of the scotoma might vary and the patient would be unaware of the scotoma because of their cortical origin.

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produced in Fig. 9 would be likely to give rise to such subjective impressions. It is also interesting that if pictures like this are shown to normal subjects, they find it difficult to describe what they see but items are not completely obliterated. They report attributes of objects if pressed. For example, the most prominent objects in the picture are a weelbarrow propped up on end against a wall (top left) and a bucket (centre). Subjects usually cannot identify the bucket but report that the weelbarrow is a 'cart' or 'trolley' of some description. They are clearly using partial cues to make inferences just as R.C. seemed to be doing. Furthermore, although we have not tested this rigorously, normal subjects seem to be able to learn to identify objects as they become familiar with the nature of the distortion of the picture. It is this process which could underly RC's learning to identify objects and shapes (Fig. 3) and his 'recovery' reported by other workers ~.

Our final approach attempted to induce agnosic performance in a normal subject using a random dot mask. One of the authors acted as subject (R.L.) and we examined both CSF and orientation discrimination. Stimuli were tachistoscopi- cally presented for 10 ms. The adaptation field was the random dot mask and this was replaced by the stimulus during presentation. Three conditions were employed; no mask, low frequency mask and high frequency mask. The spatial frequency of the mask was varied simply by varying the average density of dots without any attempt to quantify this in any way. The same grating patterns were used as with RC. The CSF was determined by a self-paced method of adjustment with 10 replications at each of the 6 spatial frequencies under the three conditions of mask. Orientation discrimination was determined using a forced choice procedure identical to that used for RC. The results of both these experiments are produced in Fig. 10. The data for the C S F were subjected to a three way analysis of variance and the summary is given in Table II.

The important aspect of the analysis is frequency by mask interaction, indicating that different spatial frequencies of mask elevate different spatial frequency thresholds. The elevation is in the direction predicted, that is the low frequency

TABLE 11

A nalysis of variance summary tableJor contrast thresholds in the normal subject

Source DF M S F P

Total 119 Stimulus 5 3.345 9.838 <0.001 Mask 1 1.875 5.515 <0.025 Stim x Mask 5 0.990 2.910 <0.025 Error 108 0.340

mask elevates low spatial frequencies and the high frequency mask elevates high spatial frequencies. Notice that the presence of the mask has a general flattening effect on the CSF as we saw in the case of R.C. The effect of the masks on orientation discrimination is less clear. There is clearly an effect of some sort. Perhaps this is best described as shifting the performance curve towards the low frequency end in the case of the high frequency mask and towards the high frequency end in the case of the low frequency mask. Both sets of data show at least a qualitatively similar result to that found in R.C.

SUMMARY AND CONCLUSIONS

R.C. presented as a classical agnosic patient. This was confirmed by clinicians and independent experimental research. Our data can be divided into 3 categories: behavioural, electrophysiological and anatomical. We have shown that R.C. has abnormal brightness and colour discrimination and a CSF which is abnormal, different in the two hemifields and sensitive to stimulus orientation. We have further shown, using 'fine-grain' static perimetry that his visual field is peppered with scotoma in an asymmetrical fashion. Although agnosic by traditional criteria, we have shown that R.C. can be trained to make a number of forced choice discriminations based on orientation and simple geometric features and that he can also learn to discriminate certain objects and line drawings. We have shown that the orientation discrimination varies with spatial frequency and hemifield of presentation. VEPs show that R.C.'s visual cortex is differentially sensitive

239

%

80

70

60

50

40

Correct N: 48 mask

7

n i i i ~

:". ""O ."" ,' . . . . . O 4

Contrast Thresho ld

oo .O...o."°"o

O~ .-"" ~o °

~ o..°"~...i~ S~

I I I I I I 3 ~ 0,5 1 2 3 6 12 0.5 t 2 3 6 12

Fig. 10. Left: percentage correct forced choice orientation judgements in a normal subject for 6 spatial frequencies (horizontal axis) under three masking conditions. Right: contrast thresholds (vertical axis, arbitrary units) for the same subject and the same stimuli under the same masking conditions. Note the flattening of the CSF under masking conditions and the interaction between spatial frequency of stimulus and mask.

to pattern and orientation depending on hemisphere of recording. We hypothesise that R.C.'s agnosic symptoms are caused by the visual field peppering caused by multifocal cortical lesions. There are 3 questions remaining. Can this peppering explain all the behavioural data? Are the behavioural data sufficient to account for the agnosia? Does our hypothesis have anything to say about agnosias in other patients? We cannot, of course prove that the peppering could explain either all the behavioural data or that it would be sufficient to cause the agnosia. However, the fact that we can demonstrate at least some of the effects in normals by the introduction of similar masking processes, suggests that the hypothesis is at least plausible. It has the benefit of parsimony in that it draws upon simple well understood prin- ciples rather than upon hypothetical processes. It should allow us, in principle at least, to develop experimental paradigms with normal subjects to simulate the various symptoms of agnosic patients in a more systematic manner.

The generality of our findings is open to question. Agnosias are a heterogeneous set of visual disorders and it seems unlikely that the underlying causes would be either simple or unita- ry. It could be that R.C. is typical of only one very small group of apperceptive agnosics. Effron's patient S 8 shared many common features with R.C. and also suffered from CO poisoning. He and several other cases of apperceptive agnosia suffered from some condition leading to anoxia. It is possible that this type of lesion results in a particular type of agnosia generated by the masking process we have described. If this is true then we should be able to develop a procedure for defining the syndrome in behavioural terms. Our findings should at least alert us to the possibility of undetected sensory dysfunction contributing to other agnosias.

Our findings also have implications for channel theories of visual processing. Selective spatial frequency and orientation sensitivity in patients are often used as evidence for the functional reality of

240

the respective channels. We have shown that such loss of sensitivity may be brought about by processes other than damage to the relevant channels. For example, in MS patients, CSF abnor- malities specific to orientation j 9 and VEP delays also specific to orientation 4 have been reported and are usually interpreted as channel loss 19. However, careful static perimetry in such patients ~' has revealed the presence of patchy relative scotoma which could equally well account for the channel loss in terms of our masking hypothesis. The fact that orientation specificity is found with checkerboards 6 as well as gratings suggests that perhaps an interpretation in terms of masking is more parsimonious. As with sensory losses we certainly need to consider more careful- ly the spatial distribution of lesions, their qualita- tive nature rather than merely their gross location and the effects that such factors could have on perceptual performance and electrophysiological responses.

ACKNOWLEDGEMENTS

We are deeply indebted to the patient R.C. who tolerated our tedious and taxing procedures with diligence, stoicism and good humour. We thank Dr. Neary and his staff at Manchester Royal In- firmary, England, for introducing us to R.C. and providing facilities for the early part of the study. We also thank Drs. Abadi and Kulikowski of the Ophthalmic Optics Department, University of Manchester Institute of Science and Technology and Dr. Meudell of the Psychology Department, University of Manchester, for access to their data. We are grateful to Dr. Mayes of the same Depart- ment who has spent many hours discussing the case with us and has made a number of useful comments and suggestions.

REFERENCES

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2 Bay, E., Disturbances of visual perception and their examination, Brain, 76 (1953) 516-550.

3 Bender, M.B. and Feldman, M., The so-caUed 'visual agnosias'. Brain, 95 (1972) 173-186.

4 Calnisa, J., Mylin, L.H. and Bodis-Wollner, I., l'he effect of stimulus orientation on the visual evoked potential in multiple sclerosis, Ann. Neurol., 10 ( 1981 ) 532-539.

5 Campion, J., Evoked potentials and discriminative capacities in a case of visual agnosia. In R.H. Nodar and C. Barber (Eds.), Evoked Potentials lI: The Second Inter- national Evoked Potentials Symposium, Butterworths, 1984.

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15 Lissauer, H., Ein Fall yon Seelenblindheit nebst einem Beitrage zur Theorie derselben, Arch. Psychiat. Nerv- krankh., 21 (1889) 222-270.

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17 Meadows, J.C., The anatomical basis of prosopagnosia, J. Neurol. Neurosurg. Psychiat., 37 (1974) 489-501.

18 Regan, D., Visual psychophysical tests in multiple sclerosis as an aid to diagnosis, localisation of pathology and assessment of experimental therapy. In L.M. Proenza, J.M. Enoch and A. Jampolsky (Eds.), ClinicalApplications of Visual Psychophysics, Cambridge University' Press, 1981, pp. 234-272.

19 Regan, D., Visual information chaneling in normal and disordered vision, Psychol. Rev., 89 (1982) 407-444.

20 Rubens, A.B., Agnosia. In K.M. Heilman and E. Valenstein (Eds.), Clinical Neuropsychology, Oxford Uni- versity Press, 1979, pp. 233-267.

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15 (1985) 227-240 elsevier 227 bbr00441 - university of liverpool

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