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Knowing where and Knowing What: A Double Dissociation
KNOWING WHERE AND KNOWING WHAT: A DOUBLE DISSOCIATION Barbara A. Wilsonl, Linda Clarel, Andrew W. Youngl and John R. Hodges2 (lMedical Research Council Applied Psychology Unit, Cambridge, England; 2University of Cambridge Neurology Unit, Addenbrooke’s Hospital, Hills Road, Cambridge, England)
ABSTRACT We report a double dissociation between visuo-spatial abilities and semantic knowledge (knowledge of the names and attributes of objects and people), in two brain-injured people with longstanding stable impairments, using a wide range of tests to explore the extent of the dissociation. MU, who has bilateral lesions of occipito-parietal cortex, shows severe spatial disorientation with relatively well-preserved semantic knowledge. He is contrasted with JBR, who has bilateral temporal lobe damage and shows severe semantic problems and no impairment on visuo-spatial tasks. Our findings thus demonstrate a double dissociation between the performance of semantic and spatial tasks by MU and JBR. This pattern is consistent with Ungerleider and Mishkin’s (1982) neurophysiological hypothesis of separable cortical visual pathways; one which is specialised for spatial perception and follows a dorsal route from occipital to parietal lobes, and the other following a more ventral route from occipital to temporal lobes, whose target is semantic information needed in specifying what an object is.
INTRODUCTION In a seminal paper, Newcombe and Russell (1969) reported a double dissociation between visual perceptual and spatial deficits. They investigated brain-injured ex-servicemen with two tasks; a perceptual task in which they had to determine the age and sex of contrast-enhanced faces, and a visually-guided maze learning task. Many of the ex-servicemen with right hemisphere lesions were found to be impaired on these tasks, yet Newcombe and Russell (1969) noted that there was no overlap between the scores of the men who were most severely impaired in face perception and those who were most severely impaired in maze learning. Instead, some ex-servicemen were very poor at the face perception task yet were able to learn the visual maze without difficulty; these were found to have lesions involving posterior parts of the right temporal lobe. Other cases with the opposite pattern of impaired maze learning and normal face perception had high right posterior parietal injuries. A later report on two contrasting cases of visual perceptual and spatial impairment, with autopsy findings, confirmed these conclusions (Newcombe, Ratcliff and Damasio, 1987). The importance of these findings has been further enhanced by subsequent advances in neurophysiology. It is now known that the brain contains many visual areas, that these extend well beyond the classical visual cortex, and that they can be loosely grouped into dorsal and ventral streams (Cowey, 1994; Cortex, (1997) 33, 529-541
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Horwitz, Grady, Haxby et al., 1992). All of these facts are in line with the observations reported by Newcombe and her colleagues (Newcombe et al., 1987; Newcombe and Russell, 1969). In particular, Newcombe’s findings fit Ungerleider and Mishkin’s (1982) neurophysiological hypothesis that the brain has two cortical visual systems. Ungerleider and Mishkin (1982) proposed that one pathway, following a dorsal route from occipital to parietal lobes, is specialised for spatial perception, i.e. locating where an object is. The other pathway follows a more ventral occipito-temporal route, and is specialised for object perception, i.e. identifying what an object is. A number of issues relating to Ungerleider and Mishkin’s (1982) hypothesis remain unresolved. These include conceptual issues, which we address later, and unresolved empirical issues. Empirically, it is desirable to demonstrate the difference between dorsal and ventral streams, and the corresponding objectbased and space-based deficits, across a wider range of tasks. This is important because Newcombe’s research group has also emphasised the dangers inherent in inferring the nature of a functional deficit from performance of a single test (Young, Newcombe, de Haan et al., 1993). In Ungerleider and Mishkin’s (1982) original formulation, the target of the ventral pathway was temporal lobe association areas in which knowledge about familiar objects is represented. These representations of object knowledge will include both visual representations of the appearance of known objects, and more abstract representations of their functions and other attributes. The term ‘semantic memory’ (Tulving, 1972) is widely used to denote such knowledge; it was introduced by Tulving (1972), who drew a distinction between episodic memories, which are dependent on the recall of particular incidents (such as remembering dropping a hammer on your toe last week), and semantic memories, which are for facts that have been encountered on so many different occasions that they effectively become decontextualised (remembering that hammers are for knocking in nails). Following the observations of Warrington (1975), impairments of semantic memory have often been described in neuropsychological patients. One of the conditions associated with impaired semantic memory is now known as semantic dementia; this involves a degenerative disease whose focus is in the infero-lateral temporal lobes, causing severe impairments of both visual and non-visual semantic knowledge (Hodges, Patterson, Oxbury et al., 1992a; Hodges, Patterson and Tyler, 1994). Consistent with Ungerleider and Mishkin’s (1982) claim, it has been reported that visuospatial abilities may remain strikingly preserved in cases of semantic dementia (Hodges et al., 1992a; Hodges et al., 1994). Hence, a single dissociation between impaired semantic memory and preserved spatial abilities has been demonstrated in this progressively degenerative condition. Our aim here is to report a double dissociation between spatial abilities and semantic memory, in two brain-injured people with longstanding stable impairment, using a wide range of tests to explore the extent of the dissociation. To this end, we describe a person, MU, who shows severe spatial disorientation with relatively intact semantic knowledge. He is contrasted with another person, JBR, who has severely impaired semantic memory and preserved spatial skills.
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For each person, background details and descriptions of their performance on neuropsychological testing will be given, following which the contrasting patterns of impairment are highlighted by additional tests of spatial abilities and semantic memory. MU: BACKGROUND INFORMATION MU is a 27 year old man who was an inpatient on acute hospital wards for 11 years following an overdose of dextromoramide (Palfium) in a probable suicide attempt in 1981; he had been prescribed the drug for pain relief. He was noted to be deeply unconscious on admission, and suffered repeated cardiac arrests and spinal infarcts. He was described as having gross bilateral hemisphere damage; however, there are no records of any brain scans at the time. MU’s hospital notes indicate a history of behavioural problems in childhood, although an EEG carried out at when he was 10 years old showed no abnormalities. As a young adult, MU was seen on several occasions following episodes of self-injury and substance abuse, and on one occasion was admitted following a diving accident, unconscious and suffering from hypothermia. However, there were no known cognitive deficits prior to the overdose. A CT scan in 1995 revealed extensive bilateral occipito-parietal low density lesions with involvement of both grey and white matter, extending from the level of the third ventricle to the upper parietal regions, with the left side being more severely affected. Of note was the sparing of primary visual cortex and the medial occipital lobe. These changes are characteristic of infarctions seen in the ‘watershed’ between posterior and middle cerebral artery territories as a result of prolonged hypotension. There was also evidence of more diffuse ischaemic damage to periventricular white matter, particularly involving the right frontal region. The temporal lobes, in contrast, appeared normal. Early attempts at rehabilitation were unsuccessful, but for the past three years MU has lived in his own flat in a staffed accommodation complex. He has limited mobility in a wheelchair and attends a local day centre where he participates in a programme of rehabilitation and social activities.
MU: Neuropsychological Assessment The details of MU’s neuropsychological assessment, which revealed a range of strengths and problem areas, are summarised in Table I. All tests reported here were carried out in the period 1992-1995. (a) General Cognitive Functioning MU has a verbal IQ at the low end of the average range (92 on the WAISR). This is consistent with his probable pre-morbid functioning as indicated by his performance on an oral version of the Spot-the-Word Test (Baddeley, Emslie and Nimmo Smith, 1992). However, he was unable to complete any of the performance subtests of the WAIS-R. He had a digit span of 7 forwards, 4 backwards. He scored poorly on frontal tests of memory, with a screening score of 2 on the Rivermead Behavioural Memory Test (RBMT) (Wilson, Cockburn and Baddeley, 1985).
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Summary of Main Neuropsychological Assessment Results for MU and JBR Test
WAIS-R verbal subtests: Information Digit Span Vocabulary Arithmetic Comprehension Similarities Verbal IQ Digit span forwards Digit span backwards Spot-the-Word Test (oral presentation) RBMT Reading single letters – upper case Reading single letters – lower case Reading single words Spelling single words Behavioural Inattention Test Picture scanning subtest Benton Visual Retention Test (forced-choice version) Visual Short Term Memory (Phillips, 1983) Spatial imagery (mannikin) test (derived from Ratcliff, 1979) Corsi Blocks
Score type
Score MU
JBR
12 8 8 8 9 9 92 7 4 10 2 99% 99% 32/50 46/82
5 7 7 9 6 8 82 5 4 <3 2 100% 100% 41/50 37/82
Raw score
2/9
6/9
Raw score
5/16
14/16
Raw score
3/24
23/24
Raw score Forward span
14/32 0
26/32 6
Age scaled score Age scaled score Age scaled score Age scaled score Age scaled score Age scaled score Age scaled score Span length Span length Age scaled score Screening score Raw score Raw score Raw score Raw score
(b) Reading MU was able to read single letters, both upper and lower case, with almost 100 per cent accuracy, making only 2 errors to 208 presentations of single lower case or upper case letters at sizes of 2 mm, 4.5 mm, 6 mm, and 7 mm (the errors were to the lower case ‘o’ at 4.5 mm, and the upper case ‘J’ at 6 mm). However, despite this good reading of single letters, even when these were only 2 mm in height, MU had difficulties with single word reading and spelling, was unable to read sentences, and was unable to write. (c) Semantic Memory MU’s relatively good knowledge of word meanings was shown by his performance on the verbal subtests of the WAIS-R and by his score of 50/60 on the Spot-the-Word test (Baddeley et al., 1992), equivalent to an age scaled score of 10. He also demonstrated good knowledge of famous personalities, giving correct descriptions of what each person was known for to 48 out of 50 famous names presented; some examples are listed in Table II. (d) Visuo-spatial Abilities As we noted above, MU was unable to complete any of the performance subtests of the WAIS-R. Other areas of difficulty in visuo-spatial tasks included
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TABLE II
Descriptions of Famous Personalities Given by MU (He was presented with the name of each person, and asked to describe what they were known for. JBR could not give any information about these people) Famous person
MU’s description
Nye Bevan Ian Botham
The man who brought in the NHS. A batsman – entrepreneur. The best all-round cricketer England’s had in years. An American general in the Second World War. He became president after the war. He’s a muslim. The bloke who put a death warrant on Salman Rushdie and then snuffed it himself. Labour party leader. Stood down at the last election. A TV presenter. Her with the teeth. That’s Life.
Dwight Eisenhower Ayatollah Khomeini Neil Kinnock Esther Rantzen
spatial imagery, picture scanning, picture matching, and visual short-term memory. These are all documented in Table I. For spatial imagery, MU’s perforrnance was at chance level on a test involving mental rotation of a mannikin, derived from Ratcliff (1979). For picture scanning, he only achieved a score of 2/9 on this subtest of the Behavioural Inattention Test (Wilson, Cockburn and Halligan, 1988). Picture matching was also poor, with a score of 5/16 on the forced-choice version of the Benton Visual Retention Test (Benton, Hamsher, Varney and Spreens, 1983); this test involves matching a reference pattem to one of four possible choices that vary both in their constituent elements and the relative positions of these elements. Visual short-term memory was severely defective, with MU scoring 3/24 on the test devised by Phillips (1983); this task requires remembering the pattern of positions of filled squares in a 4 × 4 matrix. Visuo-motor problems were also evident. MU’s performance on Corsi blocks was strikingly poor, to the extent that he was unable to touch a single block indicated by the tester (span 0). However, when asked to touch parts of his body, MU could do this without error. Whilst not entirely normal, MU’s bodydirected movements were much more fluent than his movements when performing the Corsi blocks task, showing that his problems with this task did not simply reflect defective motor control. MU’s gross eye movements, for example when requested to direct his gaze to different corners of the room, appeared to be normal. However, detailed tests of eye movement revealed major difficulties. An attempt to record eye movements to complex visual displays had to be abandoned when MU proved unable to carry out the calibration routine of scanning a 3 × 3 matrix of locations in a fixed (top left to bottom right) order. Records of saccades to simple targets showed that MU found it almost impossible to maintain accurate central fixation during the 1500 ms before target presentation. JBR: BACKGROUND INFORMATION JBR is a 37 year old man who sustained brain damage as a result of herpes simplex virus encephalitis at the age of 23. He was studying electronics at the time. He remains
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densely amnesic, living in hospital and attending a sheltered workshop during the week. JBR was first described by Warrington and Shallice (1984) and subsequently investigated by Wilson (1997) as one of a group of brain-injured people with non-progressive impairments of semantic memory. The CT scan presented by Warrington and Shallice (1984) showed that although damage was widespread, the area of maximal damage was in the temporal lobes, as is typical of herpes simplex encephalitis cases.
JBR: Neuropsychological Assessment All tests reported here were carried out in the period 1994-1995. (a) General Cognitive Functioning On the WAIS-R, JBR’s verbal IQ was 82, his performance IQ was 87, and his full scale IQ 84. Although these are all within the low normal range, JBR was probably of above average ability prior to his illness, given that he was studying for a degree. JBR had a forward digit span of 5. Like MU, he scored poorly on tests of memory, with a screening score of 2 on the RBMT. (b) Reading JBR’s reading and spelling is described fully by Wilson (1994). Performance of the same tests as used for MU is shown in Table I. Like MU, JBR was able to read single letters accurately, but his word reading showed that he had difficulty with irregularly spelled words. His spelling was also impaired. (c) Semantic Memory JBR showed semantic memory problems, which had been the focus of Warrington and Shallice’s (1984) previous study. For example, he recognised none of the items in the Graded Naming Test (McKenna and Warrington, 1983), and was poor at recognising the same items from their names. His semantic memory problems also led him to score very poorly on an oral version of the Spot-the-Word Test (Baddeley et al., 1992). When asked to give descriptions of 50 famous people, JBR stated that he had not heard of most of them; this held for all the examples listed in Table II, which MU described with ease. (d) Visuo-spatial Abilities JBR showed no evidence of visuo-spatial problems. His performance IQ (87) was in line with his verbal IQ (82). He performed satisfactorily on the forcedchoice version of the Benton Visual Retention Test (Benton et al., 1983), and made only 1 error in a test of visual short-term memory (Phillips, 1983). He also scored reasonably well on the mannikin test of spatial imagery (Ratcliff, 1979), and in the normal range on the picture scanning subtest of the Behavioural Inattention Test (Wilson et al., 1988). His Corsi blocks span was normal.
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MU
AND
JBR: CONTRASTING PATTERNS
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OF IMPAIRMENT
Our assessment of MU and JBR showed that whilst both had reading difficulties, there was a striking dissociation between their visuospatial abilities (normal in JBR, but severely impaired in MU) and semantic memory (severely impaired in JBR, but apparently normal in MU). In order to explore this double dissociation, MU and JBR were both given further tests of semantic knowledge and spatial abilities. Semantic knowledge was assessed using sub-tests from Hodges’s Semantic Memory Test Battery (Hodges et al., 1992a; Hodges, Salmon and Butters, 1992b), spatial abilities with the space perception subtests of the Visual Object and Space Perception Battery (VOSP) (Warrington and James, 1991). First, then, we consider semantic knowledge. Hodges’ Semantic Memory Test Battery (Hodges et al., 1992a; Hodges et al., 1992b) uses one set of stimulus items to assess input to and output from central representational knowledge via different sensory modalities. The battery contains 48 stimulus items, representing three categories of living items (land animals, sea creatures, and birds) and three categories of manufactured items (household items, vehicles, and musical instruments), matched for prototypicality and word frequency. Knowledge of these items is assessed in terms of category fluency, picture naming, picture sorting, word-picture matching, naming to description, and generation of verbal definitions to the spoken item. From this battery, we selected picture naming and category fluency subtests to examine MU and JBR’s semantic knowledge. Picture naming was chosen as a sensitive measure of semantic memory that involves all functional components of contemporary models of object recognition (Ellis and Young, 1988); requiring high-level visual analysis, access to stored visual knowledge (structural descriptions) and semantic knowledge, and name retrieval. As such, picture naming is sensitive to deficits in any component, and therefore gives a good test of the integrity of Ungerleider and Mishkin’s (1982) ventral pathway. Category fluency was used to provide converging evidence of a genuinely semantic deficit, since it involves no visual component per se. Picture naming scores are shown in Table III. Individual scores for MU and JBR are presented together with mean scores for a small group of young control subjects, comprising 5 men with a mean age of 36.2 years (SD 3.2 years). Means are also shown for elderly controls and people with dementia of Alzheimer type (DAT) from Hodges et al. (1992b), and mean scores for a group of brain-injured (BI) people with semantic deficits (Wilson, 1995). As Table III shows, the performance of the younger and elderly control groups did not differ. MU made only one error (‘organ – hand-held – harpsichord’ for ‘accordion’), though this was enough to bring him outside the perfect performance of the young controls for musical instruments and man-made items in general. In all other categories, MU’s performance was perfect. In contrast, JBR fell consistently well below the range of control subjects’ scores for nearly every category; the exception was vehicles, for which his score was near-normal. It is noteworthy that JBR performed worse overall than the DAT group.
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Barbara A. Wilson and Others TABLE III
Scores on the Picture Naming Sub-test of the Hodges Semantic Memory Test Battery Mean scores
Total correct (max = 48) Living (max = 24) Land animals (max = 12) Sea creatures (max = 6) Birds (max = 6) Man-made (max = 24) Household items (max = 12) Vehicles (max = 6) Musical instruments (max = 6)
Individual scores
YC
EC
DAT
BI
JBR
MU
47.0 23.0 11.8 5.8 5.4 24.0 12.0 6.0 6.0
46.5 23.3 11.6 5.9 5.8 23.2 11.9 6.0 5.1
35.4 17.1 8.3 4.1 4.7 18.3 9.7 4.9 3.7
20.9 8.8 6.1 1.1 1.6 12.1 6.6 3.3 2.3
19 5 3 1 1 14 8 5 1
47 24 12 6 6 23 12 6 5
Young control (YC) subjects: mean age 36 years. Elderly control (EC) subjects: Hodges et al. (1992b), mean age 72 years. People with Alzheimer’s disease (DAT): Hodges et al. (1992b), mean age 69 years. Brain-injured (BI) people with impaired semantic memory: Wilson (1995), mean age 35 years.
Category fluency scores are shown in Table IV. MU mostly performed at the level of controls, with the exception of the ‘sea creatures’ category (MU 8 items, range for young controls 10-20). JBR again fell consistently well below the range of control subjects’ scores in all categories except ‘vehicles’, where he was near the lower limit of the normal range (JBR 11 items, range for young controls 10-19). As with picture naming, JBR also performed worse overall than the DAT group on category fluency. TABLE IV
Scores on the Category Fluency Sub-test of the Hodges Semantic Memory Test Battery Mean scores
Living Land animals Sea creatures Birds Man-made Household items Vehicles Musical instruments
Individual scores
YC
EC
DAT
BI
JBR
MU
21.2 l5.0 16.8
19.7 13.0 14.1
9.9 4.4 5.4
9.4 2.7 4.0
7 0 0
21 8 14
21.2 14.2 17.6
19.8 13.9 14.0
9.1 6.9 6.5
8.8 7.2 6.1
7 11 2
22 17 14
Young control (YC) subjects: mean age 36 years. Elderly control (EC) subjects: Hodges et al. (1992b), mean age 72 years. People with Alzheimer’s disease (DAT): Hodges et al. (1992b), mean age 69 years. Brain-injured (BI) people with impaired semantic memory: Wilson (1995), mean age 35 years.
Taken together, these findings support observations of normal or near-normal semantic memory for MU, and very impaired semantic memory for JBR. There are only two caveats affecting this pattern. First, normal controls performed at ceiling level on these tasks, a problem which often affects studies of semantic memory. Therefore, we cannot conclude that MU’s semantic memory is entirely normal; however, the data presented suffice to show that MU’s semantic memory abilities are much better than JBR’s. Second, JBR showed a discrepancy in
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TABLE V
Scores on the Space Perception Subtests of Warrington and James’ VOSP Battery
Dot Counting (10; 8) Position Discrimination (20; 18) Number Location (10; 7) Cube Analysis (10; 6)
JBR
MU
10 Pass 19 Pass 10 Pass l0 Pass
3Fail 12 Fail 0 Fail 2 Fail
Figures in brackets represent (a) maximum possible score and (b) 5% cut-off score for people aged below 50, from the test’s norms.
performance between living and non-living items, scoring somewhat better (though still clearly impaired overall) on non-living items, as has been previously reported (Warrington and Shallice, 1984). In particular, we noted that JBR’s scores were best for the ‘vehicles’ category, though this was a topic in which he had been particularly interested prior to his illness. We turn now to spatial abilities. Scores obtained by MU and JBR on the space perception subtests of the Visual Object and Space Perception Battery (VOSP) (Warrington and James, 1991) are shown in Table V. The VOSP contains four such subtests. For Dot Counting, subjects are asked to count groups of 5 to 9 randomly positioned dots. For Position Discrimination, there are two horizontally adjacent squares, one with a dot positioned exactly in the centre, one with a dot slightly off-centre; the task requires deciding which dot is closest to the exact centre of its respective square. For Number Location, two vertically positioned squares are used, there is a dot in the lower square, and the upper square contains a number of response digits, one of which corresponds exactly to the location of the dot in the lower square; the subject’s task is to report this digit. For Cube Analysis, the number of cubes in drawings of small stacks of cubes must be counted; the test stimuli are graded in difficulty by increasing the number of cubes from 3 up to 10 and by including ‘hidden’ bricks that must be deduced to lie behind those immediately visible. The VOSP thus provides a good range of spatial tasks, and the results shown in Table I highlight the other dimension of this contrasting pattern of semantic and spatial impairment. Both MU and JBR passed the VOSP’s shape detection screening test, which requires detecting the presence of a fragmented letter ‘X’ against a noisy visual background, and is taken by Warrington and James (1991) to indicate that there is no gross deficit of visual sensory processing. However, a different pattern emerged with the four space perception subtests; MU failed all of them, with exceptionally low scores, whereas JBR passed all of them with ease. To give an indication of the severity of MU’s errors, we looked in more detail at the Number Location subtest. For each of the 10 items, we measured the distance between the position of the correct digit and the digit chosen by MU. His mean error was 2.3 cm. This size of error corresponds to 40% of the width of the reference square, and is readily visible to any normal observer. MU’s choices did not differ from an estimate of random performance (mean error = 2.5 cm) derived by measuring the distance between the position of the correct digit and the digit which would have been the correct choice on the preceding trial. Effectively, then, MU was performing at chance level.
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DISCUSSION Our findings show a striking double dissociation between the performance of semantic and spatial tasks by MU and JBR. This dissociation held across a wide range of such tasks, which implies that the semantic versus spatial distinction is at least a useful first approximation to the nature of the underlying functions. In our Introduction, we noted that one half of this double dissociation had already been reported in cases of semantic dementia. As described by Hodges et al. (1992a, 1994), key features of semantic dementia include selective impairment of semantic memory, leading to severe anomia, impaired singleword comprehension, diminished general knowledge, and reduced ability to generate examples in category fluency tasks. These deficits are found in the context of unimpaired perceptual and non-verbal problem-solving skills, relative sparing of other aspects of speech production such as syntax and phonology, and relatively preserved episodic memory. JBR shows a similar picture after a non-progressive illness, although this occurs with concurrent severe amnesia. MU, in contrast, has severely impaired visuo-spatial skills but relatively intact semantic memory. The pattern of MU’s strengths and difficulties rules out poor eyesight or visual agnosia as explanations of his difficulties, since his ability to recognise seen objects was good. It is true that his reading was poor, but this might well reflect the severe problems in the spatial control of eye movements noted when we attempted formally to record them. Similarly, his ability to scan pictures systematically was defective, even though he could identify items in the scene. Neither did MU seem to have a straightforward motor disorder; he was able to touch parts of his body without difficulty. It was visually-directed movements to external space that caused MU particular problems. Structurally, both MU and JBR had widespread damage. For JBR this was most marked in the temporal lobes, consistent with the view that damage to the temporal neocortex is critical for semantic memory loss. In the case of MU the pathology involved extensive damage to grey and white matter in the occipitoparietal region, with the CT scan showing relative sparing of the primary visual (calcarine) cortex and the temporal lobes. These findings are consistent with Ungerleider and Mishkin’s (1982) neurophysiological proposals, in which the target of the ventral pathway is temporal lobe association areas in which knowledge about familiar objects is represented, and the target of the dorsal pathway is spatial analysis carried out by parietal lobes. On this basis, a double dissociation between loss of semantic knowledge after temporal lobe damage and loss of spatial abilities with parietal involvement is exactly as would be predicted. However, more recently the nature of the functions served by the occipitoparietal pathway has been debated. This debate has centred on whether objectperception versus space-perception, or what versus where, are the correct contrasts. In particular, Goodale and Milner (1992) suggested that functional specialisation may be based not only on input qualities but also on the kind of output required, with separate processing modules evolving to mediate the different uses to which vision can be put. In this respect, they suggest that there
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is a difference between perception for conscious reflection and perception for action. This claim is supported by neuropsychological studies showing compelling dissociations between the ability to report perceptual properties and the ability to act on those properties (Goodale, Meenan, Bülthoff et al., 1994; Goodale, Milner, Jakobson et al., 1991). Goodale and Milner (1992) thus proposed that what versus how may be closer to the correct contrast. There is thus a difference between Ungerleider and Mishkin’s (1982) original hypothesis of a role of occipito-parietal projections in the analysis of space and Goodale and Milner’s (1992) emphasis on their role in visuo-motor behaviours. Our observations with MU do not allow us to rule decisively in favour of one suggestion or the other, but they are relevant. As Harvey and Milner (1995) note, the debate goes back to the classic papers on consequences of bilateral parietal lesions by Bálint (1909) and Holmes (1918; 1919). Although Bálint’s and Holmes’ cases were in many respects similar, they arrived at different interpretations (Harvey and Milner, l995). Holmes (1918; 1919) emphasised the visuo-spatial aspects of the problems, concluding that they reflected a disorder in localising objects in space. In contrast, Bálint (1909) has pointed out the visuo-motor and attentional nature of his patient’s difficulties. MU’s presentation conforms in some degree to the characteristics of Bálint’s syndrome, since he shows deficits in directing gaze, a limited field of attention when describing complex scenes, and impairment of some object-directed movements of the hand performed under visual guidance, while movements that do not require visual guidance, such as those directed to the body, are executed correctly. Holmes (1918; 1919) emphasised the visuo-spatial rather than visuo-motor aspects of this disorder because the same errors were made with movement or with verbal report. For example, having described a case where a brain-injured soldier could only pick up a matchbox from his locker after repeated gropings, Holmes (1918) noted that he found it just as difficult to report verbally the locations of objects, and even their relative positions. Our observations with MU are just the same. Although MU was very poor at visuo-motor tasks, such as the Corsi blocks, spatial deficits were equally evident when a purely verbal report was required, as in the VOSP subtests (Warrington and James, 1991). We can therefore state unequivocally that MU’s problems were not just visuomotor if by visuo-motor we mean involving limb movements. In making this point, we do not seek to deny the importance of the highly compelling dissociations noted by Goodale, Milner and their colleagues (Goodale et al., 1994; Goodale and Milner, 1992; Goodale et al., 1991; Milner and Goodale, 1993), and neither do we seek to deny that the dorsal visual pathway is involved in such visuo-motor functions. Our point is only that this cannot be all that the dorsal pathway is doing. However, there is a further visuo-motor element to perceptual tasks in that many realistic tasks require eye movements. Like Bálint’s (1909) and Holmes’ (1918) cases, MU’s eye movement control was markedly poor. Defective visuo-motor control of eye movements is therefore much harder to disentangle from spatial impairments, and one is left with what looks like a chicken and egg question; do spatial problems lead to poor eye movements, or do defects of eye movement control create insuperable difficulties in spatial
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tasks? We think it is too early to say whether this will prove empirically tractable. Acknowledgements. We are very grateful to Dr. Robin Walker for recording MU’s eye movements, and to Jenny Yiend for testing control subjects. REFERENCES BADDELEY, A., EMSLIE, H., and NIMMO SMITH, I. The Speed and Capacity of Language-Processing Test. Bury St. Edmunds: Thames Valley Test Company, 1992. BÁLINT, R. Seelenlähmung des “Schauens”, optische Ataxie, räumliche Störung der Aufmerksamkeit. Monatsschrift für Psychiatrie und Neurologie, 25: 51-81, l909. BENTON, A.L., HAMSHER, K. de S., VARNEY, N., and SPREEN, O. Contributions to Neuropsychological Assessment: A Clinical Manual. Oxford: Oxford University Press, 1983. COWEY, A. Cortical visual areas and the neurobiology of higher visual processes. In M.J. Farah and G. Ratcliff (Eds.), The Neuropsychology of High-level Vision: Collected Tutorial Essays. Hillsdale, New Jersey: Lawrence Erlbaum, 1994, pp. 3-31. ELLIS, A.W., and YOUNG, A.W. Human Cognitive Neuropsychology. London: Lawrence Erlbaum, 1988. GOODALE, M.A., MEENAN, J.P., BÜLTHOFF, H.H., NICOLLE, D.A., MURPHY, K.J., and RACICOT, C.I. Separate neural pathways for the visual analysis of object shape in perception and prehension. Current Biology, 4: 604-610, 1994. GOODALE, M.A., and MILNER, A.D. Separate visual pathways for perception and action. Trends in Neurosciences, 15: 20-25, 1992. GOODALE, M.A., MILNER, A.D., JAKOBSON, L.S., and CAREY, D.P. A neurological dissociation between perceiving objects and grasping them. Nature, 349: 154-156, 1991. HARVEY, M., and MILNER, A.D. Bálint’s patient. Cognitive Neuropsychology, 12: 261-281, 1995. HoDGES, J.R., PATTERSON, K., OXBURY, S., and FUNNELL, E. Semantic dementia: progressive fluent aphasia with temporal lobe atrophy. Brain, 115: 1783-1806, 1992a. HoDGES, J.R., PATTERSON, K., and TYLER, L.K. Loss of semantic memory: implications for the modularity of mind. Cognitive Neuropsychology, 11: 505-542, 1994. HoDGES, J.R., SALMON, D.P., and BUTTERS, N. Semantic memory impairment in Alzheimer’s disease: failure of access or degraded knowledge? Neuropsychologia, 30: 301-314, 1992b. HOLMES, G. Disturbances of visual orientation. British Journal of Ophthalmology, 2: 449-468, 506-516, 1918. HOLMES, G. Disturbances of visual space perception. British Medical Journal, 2: 230-233, 1919. HORWITZ, B., GRADY, C.L., HAXBY, J.V., SCHAPIRO, M.B., RAPOPORT, S.I., UNGERLEIDER, L.G., and MISHKIN, M. Functional associations among human posterior extrastriate brain regions during object and spatial vision. Journal of Cognitive Neuroscience, 4: 311-322, 1992. MCKENNA, P., and WARRINGTON, E.K. Graded Naming Test. Windsor: NFER-Nelson, 1983. MILNER, A.D., and GOODALE, M.A. Visual pathways to perception and action. In T.P. Hicks, S. Molotchnikoff and T. Ono (Eds.), Progress in Brain Research, vol. 95. Amsterdam: Elsevier, 1993, pp. 317-337. NEWCOMBE, F., RATCLIFF, G., and DAMASIO, H. Dissociable visual and spatial impairments following right posterior cerebral lesions: clinical, neuropsychological and anatomical evidence. Neuropsychologia, 25: 149-161, 1987. NEWCOMBE, F., and RUSSELL, W.R. Dissociated visual perceptual and spatial deficits in focal lesions of the right hemisphere. Journal of Neurology, Neurosurgery and Psychiatry, 32: 73-81, 1969. PHILLIPS, W.A. Short-term visual memory. Philosophical Transactions of the Royal Society, B302: 295309, 1983. RATCLIFF, G. Spatial thought, mental rotation and the right cerebral hemisphere. Neuropsychologia, 17: 49-54, 1979. TULVING, E. Episodic and semantic memory. In E. Tulving and W. Donaldson (Eds.), Organization of Memory. New York: Academic Press, 1972, pp. 381-403. UNGERLEIDER, L.G., and MISHKIN, M. Two cortical visual systems. In D.J. Ingle, M.A. Goodale and R.J.W. Mansfield (Eds.), Analysis of Visual Behavior. Cambridge, Massachusetts: MIT Press, 1982, pp. 549-586. WARRINGTON, E.K. The selective impairment of semantic memory. Quarterly Journal of Experimental Psychology, 27: 635-657, 1975. WARRINGTON, E.K., and JAMES, M. VOSP: The Visual Object and Space Perception Battery. Bury St. Edmunds, Suffolk: Thames Valley Test Company, 1991. WARRINGTON, E.K., and SHALLICE, T. Category specific semantic impairments. Brain, 107: 829-854, 1984.
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WILSON, B., COCKBURN, J., and BADDELEY, A.D. The Rivermead Behavioural Memory Test (First edition). Bury St. Edmunds, Suffolk: Thames Valley Test Company, 1985. WILSON, B., COCKBURN, J., and HALLIGAN, P. Behavioural Inattention Test. Bury St. Edmunds, Suffolk: Thames Valley Test Company, 1988. WILSON, B.A. Syndromes of acquired dyslexia and patterns of recovery: a 6- to 10-years follow-up study of seven brain-injured people. Journal of Clinical and Experimental Neuropsychology, 16: 354-371, 1994. WILSON, B.A. Semantic memory impairments following non-progressive brain injury: a study of four cases. Brain Injury, 11: 259-269, 1997. YOUNG, A.W., NEWCOMBE, F., DE HAAN, E.H.F., SMALL, M., and HAY, D.C. Face perception after brain injury: selective impairments affecting identity and expression. Brain, 116: 941-959, 1993. Dr. Barbara Wilson, Medical Research Council Applied Psychology Unit, 15 Chaucer Road, Cambridge CB2 2EF, England.
(Received 14 May 1996; accepted 20 November 1996)
ABSTRACT We report a double dissociation between visuo-spatial abilities and semantic knowledge (knowledge of the names and attributes of objects and people), in two brain-injured people with longstanding stable impairments, using a wide range of tests to explore the extent of the dissociation. MU, who has bilateral lesions of occipito-parietal cortex, shows severe spatial disorientation with relatively well-preserved semantic knowledge. He is contrasted with JBR, who has bilateral temporal lobe damage and shows severe semantic problems and no impairment on visuo-spatial tasks. Our findings thus demonstrate a double dissociation between the performance of semantic and spatial tasks by MU and JBR. This pattern is consistent with Ungerleider and Mishkin’s (1982) neurophysiological hypothesis of separable cortical visual pathways; one which is specialised for spatial perception and follows a dorsal route from occipital to parietal lobes, and the other following a more ventral route from occipital to temporal lobes, whose target is semantic information needed in specifying what an object is.
INTRODUCTION In a seminal paper, Newcombe and Russell (1969) reported a double dissociation between visual perceptual and spatial deficits. They investigated brain-injured ex-servicemen with two tasks; a perceptual task in which they had to determine the age and sex of contrast-enhanced faces, and a visually-guided maze learning task. Many of the ex-servicemen with right hemisphere lesions were found to be impaired on these tasks, yet Newcombe and Russell (1969) noted that there was no overlap between the scores of the men who were most severely impaired in face perception and those who were most severely impaired in maze learning. Instead, some ex-servicemen were very poor at the face perception task yet were able to learn the visual maze without difficulty; these were found to have lesions involving posterior parts of the right temporal lobe. Other cases with the opposite pattern of impaired maze learning and normal face perception had high right posterior parietal injuries. A later report on two contrasting cases of visual perceptual and spatial impairment, with autopsy findings, confirmed these conclusions (Newcombe, Ratcliff and Damasio, 1987). The importance of these findings has been further enhanced by subsequent advances in neurophysiology. It is now known that the brain contains many visual areas, that these extend well beyond the classical visual cortex, and that they can be loosely grouped into dorsal and ventral streams (Cowey, 1994; Cortex, (1997) 33, 529-541
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Horwitz, Grady, Haxby et al., 1992). All of these facts are in line with the observations reported by Newcombe and her colleagues (Newcombe et al., 1987; Newcombe and Russell, 1969). In particular, Newcombe’s findings fit Ungerleider and Mishkin’s (1982) neurophysiological hypothesis that the brain has two cortical visual systems. Ungerleider and Mishkin (1982) proposed that one pathway, following a dorsal route from occipital to parietal lobes, is specialised for spatial perception, i.e. locating where an object is. The other pathway follows a more ventral occipito-temporal route, and is specialised for object perception, i.e. identifying what an object is. A number of issues relating to Ungerleider and Mishkin’s (1982) hypothesis remain unresolved. These include conceptual issues, which we address later, and unresolved empirical issues. Empirically, it is desirable to demonstrate the difference between dorsal and ventral streams, and the corresponding objectbased and space-based deficits, across a wider range of tasks. This is important because Newcombe’s research group has also emphasised the dangers inherent in inferring the nature of a functional deficit from performance of a single test (Young, Newcombe, de Haan et al., 1993). In Ungerleider and Mishkin’s (1982) original formulation, the target of the ventral pathway was temporal lobe association areas in which knowledge about familiar objects is represented. These representations of object knowledge will include both visual representations of the appearance of known objects, and more abstract representations of their functions and other attributes. The term ‘semantic memory’ (Tulving, 1972) is widely used to denote such knowledge; it was introduced by Tulving (1972), who drew a distinction between episodic memories, which are dependent on the recall of particular incidents (such as remembering dropping a hammer on your toe last week), and semantic memories, which are for facts that have been encountered on so many different occasions that they effectively become decontextualised (remembering that hammers are for knocking in nails). Following the observations of Warrington (1975), impairments of semantic memory have often been described in neuropsychological patients. One of the conditions associated with impaired semantic memory is now known as semantic dementia; this involves a degenerative disease whose focus is in the infero-lateral temporal lobes, causing severe impairments of both visual and non-visual semantic knowledge (Hodges, Patterson, Oxbury et al., 1992a; Hodges, Patterson and Tyler, 1994). Consistent with Ungerleider and Mishkin’s (1982) claim, it has been reported that visuospatial abilities may remain strikingly preserved in cases of semantic dementia (Hodges et al., 1992a; Hodges et al., 1994). Hence, a single dissociation between impaired semantic memory and preserved spatial abilities has been demonstrated in this progressively degenerative condition. Our aim here is to report a double dissociation between spatial abilities and semantic memory, in two brain-injured people with longstanding stable impairment, using a wide range of tests to explore the extent of the dissociation. To this end, we describe a person, MU, who shows severe spatial disorientation with relatively intact semantic knowledge. He is contrasted with another person, JBR, who has severely impaired semantic memory and preserved spatial skills.
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For each person, background details and descriptions of their performance on neuropsychological testing will be given, following which the contrasting patterns of impairment are highlighted by additional tests of spatial abilities and semantic memory. MU: BACKGROUND INFORMATION MU is a 27 year old man who was an inpatient on acute hospital wards for 11 years following an overdose of dextromoramide (Palfium) in a probable suicide attempt in 1981; he had been prescribed the drug for pain relief. He was noted to be deeply unconscious on admission, and suffered repeated cardiac arrests and spinal infarcts. He was described as having gross bilateral hemisphere damage; however, there are no records of any brain scans at the time. MU’s hospital notes indicate a history of behavioural problems in childhood, although an EEG carried out at when he was 10 years old showed no abnormalities. As a young adult, MU was seen on several occasions following episodes of self-injury and substance abuse, and on one occasion was admitted following a diving accident, unconscious and suffering from hypothermia. However, there were no known cognitive deficits prior to the overdose. A CT scan in 1995 revealed extensive bilateral occipito-parietal low density lesions with involvement of both grey and white matter, extending from the level of the third ventricle to the upper parietal regions, with the left side being more severely affected. Of note was the sparing of primary visual cortex and the medial occipital lobe. These changes are characteristic of infarctions seen in the ‘watershed’ between posterior and middle cerebral artery territories as a result of prolonged hypotension. There was also evidence of more diffuse ischaemic damage to periventricular white matter, particularly involving the right frontal region. The temporal lobes, in contrast, appeared normal. Early attempts at rehabilitation were unsuccessful, but for the past three years MU has lived in his own flat in a staffed accommodation complex. He has limited mobility in a wheelchair and attends a local day centre where he participates in a programme of rehabilitation and social activities.
MU: Neuropsychological Assessment The details of MU’s neuropsychological assessment, which revealed a range of strengths and problem areas, are summarised in Table I. All tests reported here were carried out in the period 1992-1995. (a) General Cognitive Functioning MU has a verbal IQ at the low end of the average range (92 on the WAISR). This is consistent with his probable pre-morbid functioning as indicated by his performance on an oral version of the Spot-the-Word Test (Baddeley, Emslie and Nimmo Smith, 1992). However, he was unable to complete any of the performance subtests of the WAIS-R. He had a digit span of 7 forwards, 4 backwards. He scored poorly on frontal tests of memory, with a screening score of 2 on the Rivermead Behavioural Memory Test (RBMT) (Wilson, Cockburn and Baddeley, 1985).
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Summary of Main Neuropsychological Assessment Results for MU and JBR Test
WAIS-R verbal subtests: Information Digit Span Vocabulary Arithmetic Comprehension Similarities Verbal IQ Digit span forwards Digit span backwards Spot-the-Word Test (oral presentation) RBMT Reading single letters – upper case Reading single letters – lower case Reading single words Spelling single words Behavioural Inattention Test Picture scanning subtest Benton Visual Retention Test (forced-choice version) Visual Short Term Memory (Phillips, 1983) Spatial imagery (mannikin) test (derived from Ratcliff, 1979) Corsi Blocks
Score type
Score MU
JBR
12 8 8 8 9 9 92 7 4 10 2 99% 99% 32/50 46/82
5 7 7 9 6 8 82 5 4 <3 2 100% 100% 41/50 37/82
Raw score
2/9
6/9
Raw score
5/16
14/16
Raw score
3/24
23/24
Raw score Forward span
14/32 0
26/32 6
Age scaled score Age scaled score Age scaled score Age scaled score Age scaled score Age scaled score Age scaled score Span length Span length Age scaled score Screening score Raw score Raw score Raw score Raw score
(b) Reading MU was able to read single letters, both upper and lower case, with almost 100 per cent accuracy, making only 2 errors to 208 presentations of single lower case or upper case letters at sizes of 2 mm, 4.5 mm, 6 mm, and 7 mm (the errors were to the lower case ‘o’ at 4.5 mm, and the upper case ‘J’ at 6 mm). However, despite this good reading of single letters, even when these were only 2 mm in height, MU had difficulties with single word reading and spelling, was unable to read sentences, and was unable to write. (c) Semantic Memory MU’s relatively good knowledge of word meanings was shown by his performance on the verbal subtests of the WAIS-R and by his score of 50/60 on the Spot-the-Word test (Baddeley et al., 1992), equivalent to an age scaled score of 10. He also demonstrated good knowledge of famous personalities, giving correct descriptions of what each person was known for to 48 out of 50 famous names presented; some examples are listed in Table II. (d) Visuo-spatial Abilities As we noted above, MU was unable to complete any of the performance subtests of the WAIS-R. Other areas of difficulty in visuo-spatial tasks included
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TABLE II
Descriptions of Famous Personalities Given by MU (He was presented with the name of each person, and asked to describe what they were known for. JBR could not give any information about these people) Famous person
MU’s description
Nye Bevan Ian Botham
The man who brought in the NHS. A batsman – entrepreneur. The best all-round cricketer England’s had in years. An American general in the Second World War. He became president after the war. He’s a muslim. The bloke who put a death warrant on Salman Rushdie and then snuffed it himself. Labour party leader. Stood down at the last election. A TV presenter. Her with the teeth. That’s Life.
Dwight Eisenhower Ayatollah Khomeini Neil Kinnock Esther Rantzen
spatial imagery, picture scanning, picture matching, and visual short-term memory. These are all documented in Table I. For spatial imagery, MU’s perforrnance was at chance level on a test involving mental rotation of a mannikin, derived from Ratcliff (1979). For picture scanning, he only achieved a score of 2/9 on this subtest of the Behavioural Inattention Test (Wilson, Cockburn and Halligan, 1988). Picture matching was also poor, with a score of 5/16 on the forced-choice version of the Benton Visual Retention Test (Benton, Hamsher, Varney and Spreens, 1983); this test involves matching a reference pattem to one of four possible choices that vary both in their constituent elements and the relative positions of these elements. Visual short-term memory was severely defective, with MU scoring 3/24 on the test devised by Phillips (1983); this task requires remembering the pattern of positions of filled squares in a 4 × 4 matrix. Visuo-motor problems were also evident. MU’s performance on Corsi blocks was strikingly poor, to the extent that he was unable to touch a single block indicated by the tester (span 0). However, when asked to touch parts of his body, MU could do this without error. Whilst not entirely normal, MU’s bodydirected movements were much more fluent than his movements when performing the Corsi blocks task, showing that his problems with this task did not simply reflect defective motor control. MU’s gross eye movements, for example when requested to direct his gaze to different corners of the room, appeared to be normal. However, detailed tests of eye movement revealed major difficulties. An attempt to record eye movements to complex visual displays had to be abandoned when MU proved unable to carry out the calibration routine of scanning a 3 × 3 matrix of locations in a fixed (top left to bottom right) order. Records of saccades to simple targets showed that MU found it almost impossible to maintain accurate central fixation during the 1500 ms before target presentation. JBR: BACKGROUND INFORMATION JBR is a 37 year old man who sustained brain damage as a result of herpes simplex virus encephalitis at the age of 23. He was studying electronics at the time. He remains
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densely amnesic, living in hospital and attending a sheltered workshop during the week. JBR was first described by Warrington and Shallice (1984) and subsequently investigated by Wilson (1997) as one of a group of brain-injured people with non-progressive impairments of semantic memory. The CT scan presented by Warrington and Shallice (1984) showed that although damage was widespread, the area of maximal damage was in the temporal lobes, as is typical of herpes simplex encephalitis cases.
JBR: Neuropsychological Assessment All tests reported here were carried out in the period 1994-1995. (a) General Cognitive Functioning On the WAIS-R, JBR’s verbal IQ was 82, his performance IQ was 87, and his full scale IQ 84. Although these are all within the low normal range, JBR was probably of above average ability prior to his illness, given that he was studying for a degree. JBR had a forward digit span of 5. Like MU, he scored poorly on tests of memory, with a screening score of 2 on the RBMT. (b) Reading JBR’s reading and spelling is described fully by Wilson (1994). Performance of the same tests as used for MU is shown in Table I. Like MU, JBR was able to read single letters accurately, but his word reading showed that he had difficulty with irregularly spelled words. His spelling was also impaired. (c) Semantic Memory JBR showed semantic memory problems, which had been the focus of Warrington and Shallice’s (1984) previous study. For example, he recognised none of the items in the Graded Naming Test (McKenna and Warrington, 1983), and was poor at recognising the same items from their names. His semantic memory problems also led him to score very poorly on an oral version of the Spot-the-Word Test (Baddeley et al., 1992). When asked to give descriptions of 50 famous people, JBR stated that he had not heard of most of them; this held for all the examples listed in Table II, which MU described with ease. (d) Visuo-spatial Abilities JBR showed no evidence of visuo-spatial problems. His performance IQ (87) was in line with his verbal IQ (82). He performed satisfactorily on the forcedchoice version of the Benton Visual Retention Test (Benton et al., 1983), and made only 1 error in a test of visual short-term memory (Phillips, 1983). He also scored reasonably well on the mannikin test of spatial imagery (Ratcliff, 1979), and in the normal range on the picture scanning subtest of the Behavioural Inattention Test (Wilson et al., 1988). His Corsi blocks span was normal.
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MU
AND
JBR: CONTRASTING PATTERNS
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OF IMPAIRMENT
Our assessment of MU and JBR showed that whilst both had reading difficulties, there was a striking dissociation between their visuospatial abilities (normal in JBR, but severely impaired in MU) and semantic memory (severely impaired in JBR, but apparently normal in MU). In order to explore this double dissociation, MU and JBR were both given further tests of semantic knowledge and spatial abilities. Semantic knowledge was assessed using sub-tests from Hodges’s Semantic Memory Test Battery (Hodges et al., 1992a; Hodges, Salmon and Butters, 1992b), spatial abilities with the space perception subtests of the Visual Object and Space Perception Battery (VOSP) (Warrington and James, 1991). First, then, we consider semantic knowledge. Hodges’ Semantic Memory Test Battery (Hodges et al., 1992a; Hodges et al., 1992b) uses one set of stimulus items to assess input to and output from central representational knowledge via different sensory modalities. The battery contains 48 stimulus items, representing three categories of living items (land animals, sea creatures, and birds) and three categories of manufactured items (household items, vehicles, and musical instruments), matched for prototypicality and word frequency. Knowledge of these items is assessed in terms of category fluency, picture naming, picture sorting, word-picture matching, naming to description, and generation of verbal definitions to the spoken item. From this battery, we selected picture naming and category fluency subtests to examine MU and JBR’s semantic knowledge. Picture naming was chosen as a sensitive measure of semantic memory that involves all functional components of contemporary models of object recognition (Ellis and Young, 1988); requiring high-level visual analysis, access to stored visual knowledge (structural descriptions) and semantic knowledge, and name retrieval. As such, picture naming is sensitive to deficits in any component, and therefore gives a good test of the integrity of Ungerleider and Mishkin’s (1982) ventral pathway. Category fluency was used to provide converging evidence of a genuinely semantic deficit, since it involves no visual component per se. Picture naming scores are shown in Table III. Individual scores for MU and JBR are presented together with mean scores for a small group of young control subjects, comprising 5 men with a mean age of 36.2 years (SD 3.2 years). Means are also shown for elderly controls and people with dementia of Alzheimer type (DAT) from Hodges et al. (1992b), and mean scores for a group of brain-injured (BI) people with semantic deficits (Wilson, 1995). As Table III shows, the performance of the younger and elderly control groups did not differ. MU made only one error (‘organ – hand-held – harpsichord’ for ‘accordion’), though this was enough to bring him outside the perfect performance of the young controls for musical instruments and man-made items in general. In all other categories, MU’s performance was perfect. In contrast, JBR fell consistently well below the range of control subjects’ scores for nearly every category; the exception was vehicles, for which his score was near-normal. It is noteworthy that JBR performed worse overall than the DAT group.
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Barbara A. Wilson and Others TABLE III
Scores on the Picture Naming Sub-test of the Hodges Semantic Memory Test Battery Mean scores
Total correct (max = 48) Living (max = 24) Land animals (max = 12) Sea creatures (max = 6) Birds (max = 6) Man-made (max = 24) Household items (max = 12) Vehicles (max = 6) Musical instruments (max = 6)
Individual scores
YC
EC
DAT
BI
JBR
MU
47.0 23.0 11.8 5.8 5.4 24.0 12.0 6.0 6.0
46.5 23.3 11.6 5.9 5.8 23.2 11.9 6.0 5.1
35.4 17.1 8.3 4.1 4.7 18.3 9.7 4.9 3.7
20.9 8.8 6.1 1.1 1.6 12.1 6.6 3.3 2.3
19 5 3 1 1 14 8 5 1
47 24 12 6 6 23 12 6 5
Young control (YC) subjects: mean age 36 years. Elderly control (EC) subjects: Hodges et al. (1992b), mean age 72 years. People with Alzheimer’s disease (DAT): Hodges et al. (1992b), mean age 69 years. Brain-injured (BI) people with impaired semantic memory: Wilson (1995), mean age 35 years.
Category fluency scores are shown in Table IV. MU mostly performed at the level of controls, with the exception of the ‘sea creatures’ category (MU 8 items, range for young controls 10-20). JBR again fell consistently well below the range of control subjects’ scores in all categories except ‘vehicles’, where he was near the lower limit of the normal range (JBR 11 items, range for young controls 10-19). As with picture naming, JBR also performed worse overall than the DAT group on category fluency. TABLE IV
Scores on the Category Fluency Sub-test of the Hodges Semantic Memory Test Battery Mean scores
Living Land animals Sea creatures Birds Man-made Household items Vehicles Musical instruments
Individual scores
YC
EC
DAT
BI
JBR
MU
21.2 l5.0 16.8
19.7 13.0 14.1
9.9 4.4 5.4
9.4 2.7 4.0
7 0 0
21 8 14
21.2 14.2 17.6
19.8 13.9 14.0
9.1 6.9 6.5
8.8 7.2 6.1
7 11 2
22 17 14
Young control (YC) subjects: mean age 36 years. Elderly control (EC) subjects: Hodges et al. (1992b), mean age 72 years. People with Alzheimer’s disease (DAT): Hodges et al. (1992b), mean age 69 years. Brain-injured (BI) people with impaired semantic memory: Wilson (1995), mean age 35 years.
Taken together, these findings support observations of normal or near-normal semantic memory for MU, and very impaired semantic memory for JBR. There are only two caveats affecting this pattern. First, normal controls performed at ceiling level on these tasks, a problem which often affects studies of semantic memory. Therefore, we cannot conclude that MU’s semantic memory is entirely normal; however, the data presented suffice to show that MU’s semantic memory abilities are much better than JBR’s. Second, JBR showed a discrepancy in
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TABLE V
Scores on the Space Perception Subtests of Warrington and James’ VOSP Battery
Dot Counting (10; 8) Position Discrimination (20; 18) Number Location (10; 7) Cube Analysis (10; 6)
JBR
MU
10 Pass 19 Pass 10 Pass l0 Pass
3Fail 12 Fail 0 Fail 2 Fail
Figures in brackets represent (a) maximum possible score and (b) 5% cut-off score for people aged below 50, from the test’s norms.
performance between living and non-living items, scoring somewhat better (though still clearly impaired overall) on non-living items, as has been previously reported (Warrington and Shallice, 1984). In particular, we noted that JBR’s scores were best for the ‘vehicles’ category, though this was a topic in which he had been particularly interested prior to his illness. We turn now to spatial abilities. Scores obtained by MU and JBR on the space perception subtests of the Visual Object and Space Perception Battery (VOSP) (Warrington and James, 1991) are shown in Table V. The VOSP contains four such subtests. For Dot Counting, subjects are asked to count groups of 5 to 9 randomly positioned dots. For Position Discrimination, there are two horizontally adjacent squares, one with a dot positioned exactly in the centre, one with a dot slightly off-centre; the task requires deciding which dot is closest to the exact centre of its respective square. For Number Location, two vertically positioned squares are used, there is a dot in the lower square, and the upper square contains a number of response digits, one of which corresponds exactly to the location of the dot in the lower square; the subject’s task is to report this digit. For Cube Analysis, the number of cubes in drawings of small stacks of cubes must be counted; the test stimuli are graded in difficulty by increasing the number of cubes from 3 up to 10 and by including ‘hidden’ bricks that must be deduced to lie behind those immediately visible. The VOSP thus provides a good range of spatial tasks, and the results shown in Table I highlight the other dimension of this contrasting pattern of semantic and spatial impairment. Both MU and JBR passed the VOSP’s shape detection screening test, which requires detecting the presence of a fragmented letter ‘X’ against a noisy visual background, and is taken by Warrington and James (1991) to indicate that there is no gross deficit of visual sensory processing. However, a different pattern emerged with the four space perception subtests; MU failed all of them, with exceptionally low scores, whereas JBR passed all of them with ease. To give an indication of the severity of MU’s errors, we looked in more detail at the Number Location subtest. For each of the 10 items, we measured the distance between the position of the correct digit and the digit chosen by MU. His mean error was 2.3 cm. This size of error corresponds to 40% of the width of the reference square, and is readily visible to any normal observer. MU’s choices did not differ from an estimate of random performance (mean error = 2.5 cm) derived by measuring the distance between the position of the correct digit and the digit which would have been the correct choice on the preceding trial. Effectively, then, MU was performing at chance level.
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DISCUSSION Our findings show a striking double dissociation between the performance of semantic and spatial tasks by MU and JBR. This dissociation held across a wide range of such tasks, which implies that the semantic versus spatial distinction is at least a useful first approximation to the nature of the underlying functions. In our Introduction, we noted that one half of this double dissociation had already been reported in cases of semantic dementia. As described by Hodges et al. (1992a, 1994), key features of semantic dementia include selective impairment of semantic memory, leading to severe anomia, impaired singleword comprehension, diminished general knowledge, and reduced ability to generate examples in category fluency tasks. These deficits are found in the context of unimpaired perceptual and non-verbal problem-solving skills, relative sparing of other aspects of speech production such as syntax and phonology, and relatively preserved episodic memory. JBR shows a similar picture after a non-progressive illness, although this occurs with concurrent severe amnesia. MU, in contrast, has severely impaired visuo-spatial skills but relatively intact semantic memory. The pattern of MU’s strengths and difficulties rules out poor eyesight or visual agnosia as explanations of his difficulties, since his ability to recognise seen objects was good. It is true that his reading was poor, but this might well reflect the severe problems in the spatial control of eye movements noted when we attempted formally to record them. Similarly, his ability to scan pictures systematically was defective, even though he could identify items in the scene. Neither did MU seem to have a straightforward motor disorder; he was able to touch parts of his body without difficulty. It was visually-directed movements to external space that caused MU particular problems. Structurally, both MU and JBR had widespread damage. For JBR this was most marked in the temporal lobes, consistent with the view that damage to the temporal neocortex is critical for semantic memory loss. In the case of MU the pathology involved extensive damage to grey and white matter in the occipitoparietal region, with the CT scan showing relative sparing of the primary visual (calcarine) cortex and the temporal lobes. These findings are consistent with Ungerleider and Mishkin’s (1982) neurophysiological proposals, in which the target of the ventral pathway is temporal lobe association areas in which knowledge about familiar objects is represented, and the target of the dorsal pathway is spatial analysis carried out by parietal lobes. On this basis, a double dissociation between loss of semantic knowledge after temporal lobe damage and loss of spatial abilities with parietal involvement is exactly as would be predicted. However, more recently the nature of the functions served by the occipitoparietal pathway has been debated. This debate has centred on whether objectperception versus space-perception, or what versus where, are the correct contrasts. In particular, Goodale and Milner (1992) suggested that functional specialisation may be based not only on input qualities but also on the kind of output required, with separate processing modules evolving to mediate the different uses to which vision can be put. In this respect, they suggest that there
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is a difference between perception for conscious reflection and perception for action. This claim is supported by neuropsychological studies showing compelling dissociations between the ability to report perceptual properties and the ability to act on those properties (Goodale, Meenan, Bülthoff et al., 1994; Goodale, Milner, Jakobson et al., 1991). Goodale and Milner (1992) thus proposed that what versus how may be closer to the correct contrast. There is thus a difference between Ungerleider and Mishkin’s (1982) original hypothesis of a role of occipito-parietal projections in the analysis of space and Goodale and Milner’s (1992) emphasis on their role in visuo-motor behaviours. Our observations with MU do not allow us to rule decisively in favour of one suggestion or the other, but they are relevant. As Harvey and Milner (1995) note, the debate goes back to the classic papers on consequences of bilateral parietal lesions by Bálint (1909) and Holmes (1918; 1919). Although Bálint’s and Holmes’ cases were in many respects similar, they arrived at different interpretations (Harvey and Milner, l995). Holmes (1918; 1919) emphasised the visuo-spatial aspects of the problems, concluding that they reflected a disorder in localising objects in space. In contrast, Bálint (1909) has pointed out the visuo-motor and attentional nature of his patient’s difficulties. MU’s presentation conforms in some degree to the characteristics of Bálint’s syndrome, since he shows deficits in directing gaze, a limited field of attention when describing complex scenes, and impairment of some object-directed movements of the hand performed under visual guidance, while movements that do not require visual guidance, such as those directed to the body, are executed correctly. Holmes (1918; 1919) emphasised the visuo-spatial rather than visuo-motor aspects of this disorder because the same errors were made with movement or with verbal report. For example, having described a case where a brain-injured soldier could only pick up a matchbox from his locker after repeated gropings, Holmes (1918) noted that he found it just as difficult to report verbally the locations of objects, and even their relative positions. Our observations with MU are just the same. Although MU was very poor at visuo-motor tasks, such as the Corsi blocks, spatial deficits were equally evident when a purely verbal report was required, as in the VOSP subtests (Warrington and James, 1991). We can therefore state unequivocally that MU’s problems were not just visuomotor if by visuo-motor we mean involving limb movements. In making this point, we do not seek to deny the importance of the highly compelling dissociations noted by Goodale, Milner and their colleagues (Goodale et al., 1994; Goodale and Milner, 1992; Goodale et al., 1991; Milner and Goodale, 1993), and neither do we seek to deny that the dorsal visual pathway is involved in such visuo-motor functions. Our point is only that this cannot be all that the dorsal pathway is doing. However, there is a further visuo-motor element to perceptual tasks in that many realistic tasks require eye movements. Like Bálint’s (1909) and Holmes’ (1918) cases, MU’s eye movement control was markedly poor. Defective visuo-motor control of eye movements is therefore much harder to disentangle from spatial impairments, and one is left with what looks like a chicken and egg question; do spatial problems lead to poor eye movements, or do defects of eye movement control create insuperable difficulties in spatial
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tasks? We think it is too early to say whether this will prove empirically tractable. Acknowledgements. We are very grateful to Dr. Robin Walker for recording MU’s eye movements, and to Jenny Yiend for testing control subjects. REFERENCES BADDELEY, A., EMSLIE, H., and NIMMO SMITH, I. The Speed and Capacity of Language-Processing Test. Bury St. Edmunds: Thames Valley Test Company, 1992. BÁLINT, R. Seelenlähmung des “Schauens”, optische Ataxie, räumliche Störung der Aufmerksamkeit. Monatsschrift für Psychiatrie und Neurologie, 25: 51-81, l909. BENTON, A.L., HAMSHER, K. de S., VARNEY, N., and SPREEN, O. Contributions to Neuropsychological Assessment: A Clinical Manual. Oxford: Oxford University Press, 1983. COWEY, A. Cortical visual areas and the neurobiology of higher visual processes. In M.J. Farah and G. Ratcliff (Eds.), The Neuropsychology of High-level Vision: Collected Tutorial Essays. Hillsdale, New Jersey: Lawrence Erlbaum, 1994, pp. 3-31. ELLIS, A.W., and YOUNG, A.W. Human Cognitive Neuropsychology. London: Lawrence Erlbaum, 1988. GOODALE, M.A., MEENAN, J.P., BÜLTHOFF, H.H., NICOLLE, D.A., MURPHY, K.J., and RACICOT, C.I. Separate neural pathways for the visual analysis of object shape in perception and prehension. Current Biology, 4: 604-610, 1994. GOODALE, M.A., and MILNER, A.D. Separate visual pathways for perception and action. Trends in Neurosciences, 15: 20-25, 1992. GOODALE, M.A., MILNER, A.D., JAKOBSON, L.S., and CAREY, D.P. A neurological dissociation between perceiving objects and grasping them. Nature, 349: 154-156, 1991. HARVEY, M., and MILNER, A.D. Bálint’s patient. Cognitive Neuropsychology, 12: 261-281, 1995. HoDGES, J.R., PATTERSON, K., OXBURY, S., and FUNNELL, E. Semantic dementia: progressive fluent aphasia with temporal lobe atrophy. Brain, 115: 1783-1806, 1992a. HoDGES, J.R., PATTERSON, K., and TYLER, L.K. Loss of semantic memory: implications for the modularity of mind. Cognitive Neuropsychology, 11: 505-542, 1994. HoDGES, J.R., SALMON, D.P., and BUTTERS, N. Semantic memory impairment in Alzheimer’s disease: failure of access or degraded knowledge? Neuropsychologia, 30: 301-314, 1992b. HOLMES, G. Disturbances of visual orientation. British Journal of Ophthalmology, 2: 449-468, 506-516, 1918. HOLMES, G. Disturbances of visual space perception. British Medical Journal, 2: 230-233, 1919. HORWITZ, B., GRADY, C.L., HAXBY, J.V., SCHAPIRO, M.B., RAPOPORT, S.I., UNGERLEIDER, L.G., and MISHKIN, M. Functional associations among human posterior extrastriate brain regions during object and spatial vision. Journal of Cognitive Neuroscience, 4: 311-322, 1992. MCKENNA, P., and WARRINGTON, E.K. Graded Naming Test. Windsor: NFER-Nelson, 1983. MILNER, A.D., and GOODALE, M.A. Visual pathways to perception and action. In T.P. Hicks, S. Molotchnikoff and T. Ono (Eds.), Progress in Brain Research, vol. 95. Amsterdam: Elsevier, 1993, pp. 317-337. NEWCOMBE, F., RATCLIFF, G., and DAMASIO, H. Dissociable visual and spatial impairments following right posterior cerebral lesions: clinical, neuropsychological and anatomical evidence. Neuropsychologia, 25: 149-161, 1987. NEWCOMBE, F., and RUSSELL, W.R. Dissociated visual perceptual and spatial deficits in focal lesions of the right hemisphere. Journal of Neurology, Neurosurgery and Psychiatry, 32: 73-81, 1969. PHILLIPS, W.A. Short-term visual memory. Philosophical Transactions of the Royal Society, B302: 295309, 1983. RATCLIFF, G. Spatial thought, mental rotation and the right cerebral hemisphere. Neuropsychologia, 17: 49-54, 1979. TULVING, E. Episodic and semantic memory. In E. Tulving and W. Donaldson (Eds.), Organization of Memory. New York: Academic Press, 1972, pp. 381-403. UNGERLEIDER, L.G., and MISHKIN, M. Two cortical visual systems. In D.J. Ingle, M.A. Goodale and R.J.W. Mansfield (Eds.), Analysis of Visual Behavior. Cambridge, Massachusetts: MIT Press, 1982, pp. 549-586. WARRINGTON, E.K. The selective impairment of semantic memory. Quarterly Journal of Experimental Psychology, 27: 635-657, 1975. WARRINGTON, E.K., and JAMES, M. VOSP: The Visual Object and Space Perception Battery. Bury St. Edmunds, Suffolk: Thames Valley Test Company, 1991. WARRINGTON, E.K., and SHALLICE, T. Category specific semantic impairments. Brain, 107: 829-854, 1984.
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WILSON, B., COCKBURN, J., and BADDELEY, A.D. The Rivermead Behavioural Memory Test (First edition). Bury St. Edmunds, Suffolk: Thames Valley Test Company, 1985. WILSON, B., COCKBURN, J., and HALLIGAN, P. Behavioural Inattention Test. Bury St. Edmunds, Suffolk: Thames Valley Test Company, 1988. WILSON, B.A. Syndromes of acquired dyslexia and patterns of recovery: a 6- to 10-years follow-up study of seven brain-injured people. Journal of Clinical and Experimental Neuropsychology, 16: 354-371, 1994. WILSON, B.A. Semantic memory impairments following non-progressive brain injury: a study of four cases. Brain Injury, 11: 259-269, 1997. YOUNG, A.W., NEWCOMBE, F., DE HAAN, E.H.F., SMALL, M., and HAY, D.C. Face perception after brain injury: selective impairments affecting identity and expression. Brain, 116: 941-959, 1993. Dr. Barbara Wilson, Medical Research Council Applied Psychology Unit, 15 Chaucer Road, Cambridge CB2 2EF, England.
(Received 14 May 1996; accepted 20 November 1996)