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 ofCambridge 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 withlongstanding stable impairments, using a wide range of tests to explore the extent of thedissociation. MU, who has bilateral lesions of occipito-parietal cortex, shows severe spatialdisorientation with relatively well-preserved semantic knowledge. He is contrasted with JBR,who has bilateral temporal lobe damage and shows severe semantic problems and no impairmenton visuo-spatial tasks. Our findings thus demonstrate a double dissociation between theperformance of semantic and spatial tasks by MU and JBR. This pattern is consistent withUngerleider and Mishkin’s (1982) neurophysiological hypothesis of separable cortical visualpathways; one which is specialised for spatial perception and follows a dorsal route fromoccipital to parietal lobes, and the other following a more ventral route from occipital totemporal lobes, whose target is semantic information needed in specifying what an object is.

INTRODUCTION

In a seminal paper, Newcombe and Russell (1969) reported a doubledissociation between visual perceptual and spatial deficits. They investigatedbrain-injured ex-servicemen with two tasks; a perceptual task in which they hadto determine the age and sex of contrast-enhanced faces, and a visually-guidedmaze learning task. Many of the ex-servicemen with right hemisphere lesionswere 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 mostseverely impaired in face perception and those who were most severely impairedin maze learning. Instead, some ex-servicemen were very poor at the faceperception task yet were able to learn the visual maze without difficulty; thesewere found to have lesions involving posterior parts of the right temporal lobe.Other cases with the opposite pattern of impaired maze learning and normal faceperception had high right posterior parietal injuries. A later report on twocontrasting cases of visual perceptual and spatial impairment, with autopsyfindings, confirmed these conclusions (Newcombe, Ratcliff and Damasio, 1987).

The importance of these findings has been further enhanced by subsequentadvances in neurophysiology. It is now known that the brain contains manyvisual areas, that these extend well beyond the classical visual cortex, and thatthey can be loosely grouped into dorsal and ventral streams (Cowey, 1994;

Cortex, (1997) 33, 529-541

Horwitz, Grady, Haxby et al., 1992). All of these facts are in line with theobservations reported by Newcombe and her colleagues (Newcombe et al., 1987;Newcombe and Russell, 1969). In particular, Newcombe’s findings fitUngerleider and Mishkin’s (1982) neurophysiological hypothesis that the brainhas two cortical visual systems. Ungerleider and Mishkin (1982) proposed thatone pathway, following a dorsal route from occipital to parietal lobes, isspecialised for spatial perception, i.e. locating where an object is. The otherpathway follows a more ventral occipito-temporal route, and is specialised forobject perception, i.e. identifying what an object is.

A number of issues relating to Ungerleider and Mishkin’s (1982) hypothesisremain unresolved. These include conceptual issues, which we address later, andunresolved empirical issues. Empirically, it is desirable to demonstrate thedifference between dorsal and ventral streams, and the corresponding object-based and space-based deficits, across a wider range of tasks. This is importantbecause Newcombe’s research group has also emphasised the dangers inherentin 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 theventral pathway was temporal lobe association areas in which knowledge aboutfamiliar objects is represented. These representations of object knowledge willinclude both visual representations of the appearance of known objects, andmore abstract representations of their functions and other attributes. The term‘semantic memory’ (Tulving, 1972) is widely used to denote such knowledge; itwas introduced by Tulving (1972), who drew a distinction between episodicmemories, which are dependent on the recall of particular incidents (such asremembering dropping a hammer on your toe last week), and semantic memories,which are for facts that have been encountered on so many different occasionsthat they effectively become decontextualised (remembering that hammers arefor knocking in nails). Following the observations of Warrington (1975),impairments of semantic memory have often been described in neuropsychologicalpatients.

One of the conditions associated with impaired semantic memory is nowknown as semantic dementia; this involves a degenerative disease whose focus isin the infero-lateral temporal lobes, causing severe impairments of both visualand 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 strikinglypreserved in cases of semantic dementia (Hodges et al., 1992a; Hodges et al.,1994). Hence, a single dissociation between impaired semantic memory andpreserved spatial abilities has been demonstrated in this progressivelydegenerative condition.

Our aim here is to report a double dissociation between spatial abilities andsemantic memory, in two brain-injured people with longstanding stableimpairment, 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 disorientationwith relatively intact semantic knowledge. He is contrasted with another person,JBR, who has severely impaired semantic memory and preserved spatial skills.

530 Barbara A. Wilson and Others

For each person, background details and descriptions of their performance onneuropsychological testing will be given, following which the contrasting patternsof impairment are highlighted by additional tests of spatial abilities and semanticmemory.

MU: BACKGROUND INFORMATION

MU is a 27 year old man who was an inpatient on acute hospital wards for 11 yearsfollowing 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 onadmission, and suffered repeated cardiac arrests and spinal infarcts. He was described ashaving gross bilateral hemisphere damage; however, there are no records of any brain scansat the time.

MU’s hospital notes indicate a history of behavioural problems in childhood, althoughan EEG carried out at when he was 10 years old showed no abnormalities. As a youngadult, MU was seen on several occasions following episodes of self-injury and substanceabuse, and on one occasion was admitted following a diving accident, unconscious andsuffering from hypothermia. However, there were no known cognitive deficits prior to theoverdose.

A CT scan in 1995 revealed extensive bilateral occipito-parietal low density lesions withinvolvement of both grey and white matter, extending from the level of the third ventricleto the upper parietal regions, with the left side being more severely affected. Of note wasthe sparing of primary visual cortex and the medial occipital lobe. These changes arecharacteristic of infarctions seen in the ‘watershed’ between posterior and middle cerebralartery territories as a result of prolonged hypotension. There was also evidence of morediffuse ischaemic damage to periventricular white matter, particularly involving the rightfrontal region. The temporal lobes, in contrast, appeared normal.

Early attempts at rehabilitation were unsuccessful, but for the past three years MU haslived in his own flat in a staffed accommodation complex. He has limited mobility in awheelchair and attends a local day centre where he participates in a programme ofrehabilitation and social activities.

MU: Neuropsychological Assessment

The details of MU’s neuropsychological assessment, which revealed a rangeof strengths and problem areas, are summarised in Table I. All tests reportedhere 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 WAIS-R). This is consistent with his probable pre-morbid functioning as indicated byhis performance on an oral version of the Spot-the-Word Test (Baddeley, Emslieand Nimmo Smith, 1992). However, he was unable to complete any of theperformance subtests of the WAIS-R. He had a digit span of 7 forwards, 4backwards. He scored poorly on frontal tests of memory, with a screening scoreof 2 on the Rivermead Behavioural Memory Test (RBMT) (Wilson, Cockburnand Baddeley, 1985).

Spatial abilities and semantic memory 531

(b) Reading

MU was able to read single letters, both upper and lower case, with almost100 per cent accuracy, making only 2 errors to 208 presentations of single lowercase or upper case letters at sizes of 2 mm, 4.5 mm, 6 mm, and 7 mm (theerrors 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 only2 mm in height, MU had difficulties with single word reading and spelling, wasunable to read sentences, and was unable to write.

(c) Semantic Memory

MU’s relatively good knowledge of word meanings was shown by hisperformance on the verbal subtests of the WAIS-R and by his score of 50/60 onthe Spot-the-Word test (Baddeley et al., 1992), equivalent to an age scaled scoreof 10. He also demonstrated good knowledge of famous personalities, givingcorrect descriptions of what each person was known for to 48 out of 50 famousnames presented; some examples are listed in Table II.

(d) Visuo-spatial Abilities

As we noted above, MU was unable to complete any of the performancesubtests of the WAIS-R. Other areas of difficulty in visuo-spatial tasks included


TABLE I

Summary of Main Neuropsychological Assessment Results for MU and JBR

Test Score type Score

MU JBR

WAIS-R verbal subtests:Information Age scaled score 12 5Digit Span Age scaled score 8 7Vocabulary Age scaled score 8 7Arithmetic Age scaled score 8 9Comprehension Age scaled score 9 6Similarities Age scaled score 9 8Verbal IQ Age scaled score 92 82

Digit span forwards Span length 7 5Digit span backwards Span length 4 4Spot-the-Word Test (oral presentation) Age scaled score 10 <3RBMT Screening score 2 2Reading single letters – upper case Raw score 99% 100%Reading single letters – lower case Raw score 99% 100%Reading single words Raw score 32/50 41/50Spelling single words Raw score 46/82 37/82Behavioural Inattention Test

Picture scanning subtest Raw score 2/9 6/9Benton Visual Retention Test

(forced-choice version) Raw score 5/16 14/16Visual Short Term Memory

(Phillips, 1983) Raw score 3/24 23/24Spatial imagery (mannikin) test

(derived from Ratcliff, 1979) Raw score 14/32 26/32Corsi Blocks Forward span 0 6

spatial imagery, picture scanning, picture matching, and visual short-termmemory. These are all documented in Table I. For spatial imagery, MU’sperforrnance was at chance level on a test involving mental rotation of amannikin, derived from Ratcliff (1979). For picture scanning, he only achieveda 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 of5/16 on the forced-choice version of the Benton Visual Retention Test (Benton,Hamsher, Varney and Spreens, 1983); this test involves matching a referencepattem to one of four possible choices that vary both in their constituent elementsand the relative positions of these elements. Visual short-term memory wasseverely 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 a4 × 4 matrix.

Visuo-motor problems were also evident. MU’s performance on Corsi blockswas strikingly poor, to the extent that he was unable to touch a single blockindicated by the tester (span 0). However, when asked to touch parts of hisbody, MU could do this without error. Whilst not entirely normal, MU’s body-directed movements were much more fluent than his movements whenperforming the Corsi blocks task, showing that his problems with this task didnot simply reflect defective motor control.

MU’s gross eye movements, for example when requested to direct his gazeto different corners of the room, appeared to be normal. However, detailed testsof eye movement revealed major difficulties. An attempt to record eyemovements to complex visual displays had to be abandoned when MU provedunable to carry out the calibration routine of scanning a 3 × 3 matrix of locationsin a fixed (top left to bottom right) order. Records of saccades to simple targetsshowed that MU found it almost impossible to maintain accurate central fixationduring 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 simplexvirus encephalitis at the age of 23. He was studying electronics at the time. He remains


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 The man who brought in the NHS.Ian Botham A batsman – entrepreneur. The best all-round cricketer England’s

had in years.Dwight Eisenhower An American general in the Second World War. He became

president after the war.Ayatollah Khomeini He’s a muslim. The bloke who put a death warrant on Salman

Rushdie and then snuffed it himself. Neil Kinnock Labour party leader. Stood down at the last election.Esther Rantzen A TV presenter. Her with the teeth. That’s Life.

densely amnesic, living in hospital and attending a sheltered workshop during the week.JBR was first described by Warrington and Shallice (1984) and subsequently investigatedby Wilson (1997) as one of a group of brain-injured people with non-progressiveimpairments of semantic memory. The CT scan presented by Warrington and Shallice(1984) showed that although damage was widespread, the area of maximal damage was inthe 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, andhis full scale IQ 84. Although these are all within the low normal range, JBRwas probably of above average ability prior to his illness, given that he wasstudying for a degree. JBR had a forward digit span of 5. Like MU, he scoredpoorly 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). Performanceof the same tests as used for MU is shown in Table I. Like MU, JBR was ableto read single letters accurately, but his word reading showed that he haddifficulty with irregularly spelled words. His spelling was also impaired.

(c) Semantic Memory

JBR showed semantic memory problems, which had been the focus ofWarrington and Shallice’s (1984) previous study. For example, he recognisednone of the items in the Graded Naming Test (McKenna and Warrington, 1983),and was poor at recognising the same items from their names. His semanticmemory problems also led him to score very poorly on an oral version of theSpot-the-Word Test (Baddeley et al., 1992). When asked to give descriptions of50 famous people, JBR stated that he had not heard of most of them; this heldfor 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 forced-choice version of the Benton Visual Retention Test (Benton et al., 1983), andmade only 1 error in a test of visual short-term memory (Phillips, 1983). He alsoscored reasonably well on the mannikin test of spatial imagery (Ratcliff, 1979),and in the normal range on the picture scanning subtest of the BehaviouralInattention Test (Wilson et al., 1988). His Corsi blocks span was normal.


MU AND JBR: CONTRASTING PATTERNS OF IMPAIRMENT

Our assessment of MU and JBR showed that whilst both had readingdifficulties, there was a striking dissociation between their visuospatial abilities(normal in JBR, but severely impaired in MU) and semantic memory (severelyimpaired in JBR, but apparently normal in MU).

In order to explore this double dissociation, MU and JBR were both givenfurther tests of semantic knowledge and spatial abilities. Semantic knowledgewas assessed using sub-tests from Hodges’s Semantic Memory Test Battery(Hodges et al., 1992a; Hodges, Salmon and Butters, 1992b), spatial abilitieswith the space perception subtests of the Visual Object and Space PerceptionBattery (VOSP) (Warrington and James, 1991).

First, then, we consider semantic knowledge. Hodges’ Semantic Memory TestBattery (Hodges et al., 1992a; Hodges et al., 1992b) uses one set of stimulusitems to assess input to and output from central representational knowledge viadifferent sensory modalities. The battery contains 48 stimulus items, representingthree categories of living items (land animals, sea creatures, and birds) and threecategories of manufactured items (household items, vehicles, and musicalinstruments), matched for prototypicality and word frequency. Knowledge ofthese items is assessed in terms of category fluency, picture naming, picturesorting, word-picture matching, naming to description, and generation of verbaldefinitions to the spoken item.

From this battery, we selected picture naming and category fluency subteststo examine MU and JBR’s semantic knowledge. Picture naming was chosen asa sensitive measure of semantic memory that involves all functional componentsof contemporary models of object recognition (Ellis and Young, 1988); requiringhigh-level visual analysis, access to stored visual knowledge (structuraldescriptions) and semantic knowledge, and name retrieval. As such, picturenaming is sensitive to deficits in any component, and therefore gives a good testof the integrity of Ungerleider and Mishkin’s (1982) ventral pathway. Categoryfluency was used to provide converging evidence of a genuinely semanticdeficit, since it involves no visual component per se.

Picture naming scores are shown in Table III. Individual scores for MU andJBR are presented together with mean scores for a small group of young controlsubjects, comprising 5 men with a mean age of 36.2 years (SD 3.2 years). Meansare 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 groupsdid not differ. MU made only one error (‘organ – hand-held – harpsichord’ for‘accordion’), though this was enough to bring him outside the perfect performanceof the young controls for musical instruments and man-made items in general. Inall other categories, MU’s performance was perfect. In contrast, JBR fellconsistently well below the range of control subjects’ scores for nearly everycategory; the exception was vehicles, for which his score was near-normal. It isnoteworthy that JBR performed worse overall than the DAT group.


Category fluency scores are shown in Table IV. MU mostly performed at thelevel 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 therange of control subjects’ scores in all categories except ‘vehicles’, where hewas near the lower limit of the normal range (JBR 11 items, range for youngcontrols 10-19). As with picture naming, JBR also performed worse overall thanthe DAT group on category fluency.

Taken together, these findings support observations of normal or near-normalsemantic memory for MU, and very impaired semantic memory for JBR. Thereare only two caveats affecting this pattern. First, normal controls performed atceiling level on these tasks, a problem which often affects studies of semanticmemory. Therefore, we cannot conclude that MU’s semantic memory is entirelynormal; however, the data presented suffice to show that MU’s semantic memoryabilities are much better than JBR’s. Second, JBR showed a discrepancy in


TABLE III

Scores on the Picture Naming Sub-test of the Hodges Semantic Memory Test Battery

Mean scores Individual scores

YC EC DAT BI JBR MU

Total correct (max = 48) 47.0 46.5 35.4 20.9 19 47Living (max = 24) 23.0 23.3 17.1 8.8 5 24

Land animals (max = 12) 11.8 11.6 8.3 6.1 3 12Sea creatures (max = 6) 5.8 5.9 4.1 1.1 1 6Birds (max = 6) 5.4 5.8 4.7 1.6 1 6

Man-made (max = 24) 24.0 23.2 18.3 12.1 14 23Household items (max = 12) 12.0 11.9 9.7 6.6 8 12Vehicles (max = 6) 6.0 6.0 4.9 3.3 5 6Musical instruments (max = 6) 6.0 5.1 3.7 2.3 1 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.

TABLE IV

Scores on the Category Fluency Sub-test of the Hodges Semantic Memory Test Battery

Mean scores Individual scores

YC EC DAT BI JBR MU

Living Land animals 21.2 19.7 9.9 9.4 7 21Sea creatures l5.0 13.0 4.4 2.7 0 8Birds 16.8 14.1 5.4 4.0 0 14

Man-madeHousehold items 21.2 19.8 9.1 8.8 7 22Vehicles 14.2 13.9 6.9 7.2 11 17Musical instruments 17.6 14.0 6.5 6.1 2 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.

performance between living and non-living items, scoring somewhat better(though still clearly impaired overall) on non-living items, as has beenpreviously reported (Warrington and Shallice, 1984). In particular, we noted thatJBR’s scores were best for the ‘vehicles’ category, though this was a topic inwhich he had been particularly interested prior to his illness.

We turn now to spatial abilities. Scores obtained by MU and JBR on thespace perception subtests of the Visual Object and Space Perception Battery(VOSP) (Warrington and James, 1991) are shown in Table V. The VOSPcontains four such subtests. For Dot Counting, subjects are asked to count groupsof 5 to 9 randomly positioned dots. For Position Discrimination, there are twohorizontally 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 closestto the exact centre of its respective square. For Number Location, two verticallypositioned squares are used, there is a dot in the lower square, and the uppersquare contains a number of response digits, one of which corresponds exactlyto the location of the dot in the lower square; the subject’s task is to report thisdigit. For Cube Analysis, the number of cubes in drawings of small stacks ofcubes must be counted; the test stimuli are graded in difficulty by increasing thenumber of cubes from 3 up to 10 and by including ‘hidden’ bricks that must bededuced to lie behind those immediately visible.

The VOSP thus provides a good range of spatial tasks, and the results shownin Table I highlight the other dimension of this contrasting pattern of semanticand spatial impairment. Both MU and JBR passed the VOSP’s shape detectionscreening 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, adifferent pattern emerged with the four space perception subtests; MU failed allof 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 moredetail at the Number Location subtest. For each of the 10 items, we measuredthe distance between the position of the correct digit and the digit chosen byMU. His mean error was 2.3 cm. This size of error corresponds to 40% of thewidth of the reference square, and is readily visible to any normal observer.MU’s choices did not differ from an estimate of random performance (meanerror = 2.5 cm) derived by measuring the distance between the position of thecorrect digit and the digit which would have been the correct choice on thepreceding trial. Effectively, then, MU was performing at chance level.


TABLE V

Scores on the Space Perception Subtests of Warrington and James’ VOSP Battery

JBR MU

Dot Counting (10; 8) 10 Pass 3FailPosition Discrimination (20; 18) 19 Pass 12 FailNumber Location (10; 7) 10 Pass 0 FailCube Analysis (10; 6) l0 Pass 2 Fail

Figures in brackets represent (a) maximum possible score and (b) 5% cut-off score for people aged below 50, from thetest’s norms.

DISCUSSION

Our findings show a striking double dissociation between the performanceof semantic and spatial tasks by MU and JBR. This dissociation held across awide range of such tasks, which implies that the semantic versus spatialdistinction is at least a useful first approximation to the nature of the underlyingfunctions.

In our Introduction, we noted that one half of this double dissociation hadalready been reported in cases of semantic dementia. As described by Hodgeset al. (1992a, 1994), key features of semantic dementia include selectiveimpairment of semantic memory, leading to severe anomia, impaired single-word comprehension, diminished general knowledge, and reduced ability togenerate examples in category fluency tasks. These deficits are found in thecontext of unimpaired perceptual and non-verbal problem-solving skills, relativesparing of other aspects of speech production such as syntax and phonology,and relatively preserved episodic memory. JBR shows a similar picture after anon-progressive illness, although this occurs with concurrent severe amnesia.

MU, in contrast, has severely impaired visuo-spatial skills but relatively intactsemantic memory. The pattern of MU’s strengths and difficulties rules out pooreyesight or visual agnosia as explanations of his difficulties, since his ability torecognise seen objects was good. It is true that his reading was poor, but thismight well reflect the severe problems in the spatial control of eye movementsnoted when we attempted formally to record them. Similarly, his ability to scanpictures systematically was defective, even though he could identify items in thescene. Neither did MU seem to have a straightforward motor disorder; he wasable to touch parts of his body without difficulty. It was visually-directedmovements to external space that caused MU particular problems.

Structurally, both MU and JBR had widespread damage. For JBR this wasmost marked in the temporal lobes, consistent with the view that damage to thetemporal neocortex is critical for semantic memory loss. In the case of MU thepathology involved extensive damage to grey and white matter in the occipito-parietal 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 istemporal lobe association areas in which knowledge about familiar objects isrepresented, and the target of the dorsal pathway is spatial analysis carried outby parietal lobes. On this basis, a double dissociation between loss of semanticknowledge after temporal lobe damage and loss of spatial abilities with parietalinvolvement is exactly as would be predicted.

However, more recently the nature of the functions served by the occipito-parietal pathway has been debated. This debate has centred on whether object-perception versus space-perception, or what versus where, are the correctcontrasts. In particular, Goodale and Milner (1992) suggested that functionalspecialisation may be based not only on input qualities but also on the kind ofoutput required, with separate processing modules evolving to mediate thedifferent uses to which vision can be put. In this respect, they suggest that there


is a difference between perception for conscious reflection and perception foraction. This claim is supported by neuropsychological studies showingcompelling dissociations between the ability to report perceptual properties andthe ability to act on those properties (Goodale, Meenan, Bülthoff et al., 1994;Goodale, Milner, Jakobson et al., 1991). Goodale and Milner (1992) thusproposed that what versus how may be closer to the correct contrast.

There is thus a difference between Ungerleider and Mishkin’s (1982) originalhypothesis of a role of occipito-parietal projections in the analysis of space andGoodale 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 onesuggestion or the other, but they are relevant.

As Harvey and Milner (1995) note, the debate goes back to the classic paperson consequences of bilateral parietal lesions by Bálint (1909) and Holmes (1918;1919). Although Bálint’s and Holmes’ cases were in many respects similar, theyarrived at different interpretations (Harvey and Milner, l995). Holmes (1918;1919) emphasised the visuo-spatial aspects of the problems, concluding that theyreflected a disorder in localising objects in space. In contrast, Bálint (1909) haspointed out the visuo-motor and attentional nature of his patient’s difficulties.

MU’s presentation conforms in some degree to the characteristics of Bálint’ssyndrome, since he shows deficits in directing gaze, a limited field of attentionwhen describing complex scenes, and impairment of some object-directedmovements of the hand performed under visual guidance, while movements thatdo not require visual guidance, such as those directed to the body, are executedcorrectly.

Holmes (1918; 1919) emphasised the visuo-spatial rather than visuo-motoraspects of this disorder because the same errors were made with movement orwith verbal report. For example, having described a case where a brain-injuredsoldier 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 thelocations of objects, and even their relative positions. Our observations with MUare just the same. Although MU was very poor at visuo-motor tasks, such as theCorsi blocks, spatial deficits were equally evident when a purely verbal reportwas required, as in the VOSP subtests (Warrington and James, 1991).

We can therefore state unequivocally that MU’s problems were not just visuo-motor if by visuo-motor we mean involving limb movements. In making thispoint, we do not seek to deny the importance of the highly compellingdissociations 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 involvedin such visuo-motor functions. Our point is only that this cannot be all that thedorsal pathway is doing. However, there is a further visuo-motor element toperceptual tasks in that many realistic tasks require eye movements. Like Bálint’s(1909) and Holmes’ (1918) cases, MU’s eye movement control was markedlypoor. Defective visuo-motor control of eye movements is therefore much harderto disentangle from spatial impairments, and one is left with what looks like achicken and egg question; do spatial problems lead to poor eye movements, ordo defects of eye movement control create insuperable difficulties in spatial


tasks? We think it is too early to say whether this will prove empiricallytractable.

Acknowledgements. We are very grateful to Dr. Robin Walker for recording MU’s eyemovements, 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 NeuropsychologicalAssessment: A Clinical Manual.Oxford: Oxford University Press, 1983.

COWEY, A. Cortical visual areas and the neurobiology of higher visual processes. In M.J. Farah andG. 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 inNeurosciences, 15: 20-25, 1992.

GOODALE, M.A., MILNER, A.D., JAKOBSON, L.S., and CAREY, D.P. A neurological dissociation betweenperceiving 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 objectand 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 followingright 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 ofthe 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: 295-309, 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 ofMemory.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 andR.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 ExperimentalPsychology, 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.


WILSON, B., COCKBURN, J., and BADDELEY, A.D. The Rivermead Behavioural Memory Test(Firstedition). 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 studyof 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 fourcases. 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 braininjury: 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)


knowing where and knowing what: a double dissociation

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