Professional Documents
Culture Documents
Perceptual Dysfunction, Semantic Impairment?: Topographic Amnesia: Spatial Specific
Perceptual Dysfunction, Semantic Impairment?: Topographic Amnesia: Spatial Specific
318
Table 1 SE's performance on standardised neuropsychological assessments description subtest was within the normal
Assessment Score range, although all his errors were with ani-
General intellectual: WAIS-R:
mals (SE 20/24; controls 22-4 (SD 1-3)). At
Performance IQ 101 the time the present set of experiments were
Verbal IQ 99 conducted, his picture naming (SE 32/48;
Full scale IQ 100
National adult reading test (NART) 100 controls 43-5 (SD 2 3)) and word-picture
Estimated premorbid IQ matching (SE 43/48; controls 47-1 (SD 1-1))
Perception: fell outside the normal range suggesting that
Fragmented letters (VOSPt) 20/20
Cube analysis (VOSP) 10/10 SE has a mild semantic disorder. This was
Position discrimination (VOSP) 19/20 supported by his mildly impaired performance
Benton and van Allen facial recognition test 44/54
Benton line orientation test 39/40 on the pyramids and palm trees test17 of asso-
Memory: ciative semantic knowledge. He obtained a
Wechsler memory scale-revised (index score) score of 45/52 where controls make less than
General memory index 94
Visual memory index 100 three errors. On the Snodgrass and
Visual reproduction I (immediate) 77th percentile Vanderwart corpus of 260 line drawings, SE
Verbal memory index 92
Logical memory I 44th percentile was able to name 75 of the 100 pictures of nat-
Delayed memory index 76* ural kinds (animals, fruit, and vegetables, etc)
Logical memory II 24th percentile
Visual reproduction I 2nd percentile compared with 152 of the 160 (96%) man
Warrington recognition memory test: faces 33/50* made items (vehicles, furniture, tools, cloth-
Warrington recognition memory test: words 38/50
Rey complex figure: copy 34/36 ing, etc). Further investigation showed that, in
Rey complex figure: recall 9/36* addition to his problems with buildings and
Rivermead behavioural memory test
(screening score) 10/12 places, SE has a mild, but significant, deficit in
Autobiographical memory interview his associative knowledge of animals and
Personal semantic information 61-5/63
Autobiographical incidents 27/27 details of this aspect of his case have been
Executive: described in a separate paper.'8
Wisconsin card sorting test 6 categories
Verbal fluency (FAS 60 s each) 33
Trail making test A 22 5 s
Trail making test B
Cognitive estimates test
76 s Experimental investigations
7 errors
SPATIAL LEARNING AND KNOWLEDGE
Language:
Token test 36/36 To examine the possibility that SE's topo-
Test for the reception of grammar (TROG) 76/80 graphic amnesia was the result of a primary
Boston naming test 39/60*
disorder of spatial memory, we carried out a
*Impaired performance. series of investigations of his spatial learning
tVOSP = Visual object and space perception battery (Warrington and James'-). and knowledge.
skills, with his current IQ, as measured by the Supraspan learning
Wechsler adult intelligence scale-revised'2 On a Corsi block tapping task, SE had a spa-
being no different from his predicted premor- tial short-term memory span of five. To assess
bid IQ, based on his performance on the supraspan learning, two further steps were
national adult reading test.'3 He also had satis- added and SE was able to learn the extended
factory perceptual, language, and executive span in three trials, a performance considered
functioning. His performance on memory tests to be within normal limits."'
showed satisfactory verbal, but impaired visual
memory functioning. Although he scored in Maze learning
the normal range on the Rivermead behav- SE was assessed on two maze learning tasks.
ioural memory test and his general memory One task involved learning a route through an
index on the WMS-R was normal and com- array of blocks or "stepping stones", similar in
mensurate with his IQ, SE showed impair- form to that described by Milner,20 and the
ment in delayed recall of visual information other involved discovering and remembering a
(for example, visual reproduction and Rey fig- route through a complex maze, similar in type
ure). To assess his semantic memory abilities to the Porteus mazes.2' With both tasks, once
we compared his performance on a battery of the routes had been learned, the mazes were
experimental tests previously described in systematically rotated to investigate whether
detail'9 to that of 25 age and IQ matched con- SE's learning was orientation dependent. For
trols.'t On the category fluency test, his total both tasks his performance was compared with
scores for the number of correct exemplars that of five age and sex matched controls
generated from three living and three man (mean age 64-4 (SD 2-61)).
made categories fell within the normal range Maze I (stepping stones)-This task involved
(SE living total 52 (controls 58-3 (SD 12-2)), learning a 16 step route through a 6 x 6 array
man made 51 (controls 55-5 (SD 8 5))). of blocks or "stepping stones". Subjects were
Likewise his performance on the naming to required to discover the route (involving either
Table 2 Performance (trials to criterion) of SE and controls on the stepping stone maze test
Maze I Maze 1
Maze 1 (90° rotation) (180° rotation) Maze 2
Criterion = 3 correct Criterion = 2 correct Criterion = 2 correct Criterion = 1 correct
SE 8 4 2 8
Controls (n = 5) 9-0 (4-3) 6-3 (3 3) 3 3 (2 3) 5 5 (2 4)
Values for controls are mean (SE).
A
cxI
I.rLL
cz=rn]
3L
c3mrnizrnzn
AL
c~ ~ ~ ~ ~
Topographic amnesia: spatial memory disorder, perceptual dysfunction, or category specific semantic memory impairment?
-i - Ta =
error was made subjects were prompted
321
irni
LrLXIx.rxz
ri rn
r
A
tive interference).
Maze 2-On this task subjects were presented
with a complex labyrinth maze (fig 2A) and
asked to find the path through the maze from
start to finish. The time taken to do this was
r.x recorded. To assess learning, subjects were
repeatedly re-presented with the same maze.
_ WI
c..,c tM.c. WI ....'.I... _______________________
It PI
'I -
therapy sign, turn right when I see ward C2"). severely prosopagnosic patient. PHD, a 34
This approach, however, occasionally let him year old left handed man, was previously a
down; for example, on trial 1 he had used the trainee draughtsman. He sustained a severe
strategy, "go past the doors and turn left head injury at the age of 18 and has experi-
where there is a man sitting down," which enced persisting problems with face recogni-
resulted in errors at stages five and six on trial tion, recognition of animals, reading, and
2, when the man had moved! To contrast with writing (with a pattern of surface dyslexia and
the hospital route we also assessed SE on a dysgraphia) and episodic memory.
route in the city centre of Cambridge. The
route was chosen to have the same number of PEOPLE AND PLACES
decision points as the hospital route and the Famous people
same procedure was used. The result was a SE and PHD were shown photographs of 53
similar performance, SE learning the route very famous people who had been prominent
after four trials, making a total of 10 errors, over the past four decades (politicians, TV and
and successfully retracing the route after a 20 film stars, etc) and asked to provide the name
minute delay. Once again he relied on specific of the person, or if unable to name the person,
verbal strategies (usually street names) to help to provide specific identifying information. On
him navigate and his errors were almost always another occasion SE and PHD were given the
at decision points where there were no obvious names of the famous people and asked to pro-
street signs. vide as much information about them as possi-
ble. In the second condition, and when
Geographical knowledge identifying information was given by the
SE was asked to draw a map of his home town, patient rather than the name in the photo-
which he did very successfully (fig 3). graph condition, two independent raters
assessed each response. A scoring criteria was
adopted such that a response was scored as
Commnent correct if the general occupation plus at least
The results of the preceding investigations one other piece of correct information was
suggest that SE's spatial knowledge and learn- given. For example, an answer "actor" or
ing are virtually normal, although we saw "sportsman" would not be sufficient, but
some evidence of his topographical navigation "English actor" or "comedy actor" or
problems, as well as his use of compensatory "Sport-tennis player" or "football player"
strategies, on the locomotor routes. We moved were all scored as correct. Agreement between
on to investigate the possibility that SE's topo- the raters was almost 100%; any disagree-
graphic disorientation was the result of an ments were resolved by discussion. Control
agnosia for familiar places. At the same time, data were obtained from members of the
we carried out parallel investigations into his MRC Applied Psychology Unit subject panel
difficulty with familiar faces to explore the and staff of British Rail, Cambridge. In total,
potential relation between problems with faces 37 subjects (mean age 49-0 (SD 17-6), range
and places. In this set of investigations we con- 20-82 years) were given the face identification
trasted SE's performance with that of a more task and 27 (mean age 53-7 (SD 15-4), range
Topographic amnesia: spatial memory disorder, perceptual dysfunction, or category specific semantic memory impairment? 323
o 50
{D
40
*U1
*z
30
20
10
_ .....
u0U1) 0 U)
1)
O1
U1)
U)
a)
U)
ut
a) tn
a
U) U) 0
a) E C)
a-
C.) c; LL V
z aL Z Z z z CL
26-80 years) were given the name identifica- the name of each place and asked to provide as
tion task. SE and PHD are considerably differ- much information as possible about it. As with
ent in age, but because age did not correlate the famous faces task, in the second condition,
significantly with performance on either the and when identifying information was given by
face or name tasks, data from the whole con- the patient rather than the name in the photo-
trol group are included. To compare the per- graph condition, two raters rated each
formance of the two patients across tasks their response to determine if it included sufficient
raw scores were converted to z scores. information to clearly identify the famous
The results, (fig 4) show that PHD was building or landmark. Once again agreement
severely impaired (score = 16-98%, z = between the raters was almost 100%, with the
-4- 15), being well outside the range of normal few disagreements resolved by discussion.
controls in identifying famous faces, and SE is Control data were obtained from SE's wife
clearly poor (score = 39-62%, z = 264), - (who was tested on the photographs) and age
falling just below the range of normal controls and education matched control subjects from
(43T4%-98d1%). On the identification from the Applied Psychology Unit subject panel.
name task, PHD was well within the normal Twenty nine subjects (mean age 56-79 (SD
range (score = 73-58%, z = 1.51), whereas - 16-1 1)) were asked to identify the places from
SE's performance (score = 66-04%, z = photographs and a further 14 (mean age 43-79
-
2 33) fell at the bottom of the range of nor- (SD 17-76)) were asked to identify them from
mal controls (62-3%-100%). their names.
The results (fig 4) show that SE was
Famous Places severely impaired (z = -3-46) on recognising
SE and PHD were shown a set of photographs buildings or landmarks from photographs. For
of 25 famous places (for example, the Statue example, he thought that the Leaning Tower
of Liberty, Leaning Tower of Pisa, Pyramids, of Pisa was the Empire State Building, that
Eiffel Tower) and asked to provide the name Sydney Opera House was "Somewhere in
or as much identifying information as possible. Africa", and that Trafalgar Square was
On another occasion they were provided with "Somewhere like Greece." When asked to
324 McCarthy, Evans, Hodges
identify places from their names he was some- recognition impairment extends into the
what better, but still significantly poorer than anterograde domain: not only did he fail to
control subjects (z = - 300). In this condition identify previously familiar places, but he also
it was striking that he was often unable to pro- had problems in coding those aspects of the
vide any information about what a landmark environment that stand as cues to location.
looked like, even when information such as the His preserved ability to code and process spatial
location of the landmark was provided. By information provided him with some topo-
contrast, PHD was within the normal range graphic "tools". Knowledge of spatial routes
for both the photograph and the name condi- and the availability of a mental map of the
tions. environment, even one as complex as that
recalled by SE, are insufficient for normal nav-
igation; knowing where you are at any one
Discussion time and knowing when you have finished
We have described a patient with a severe dis- your journey requires the coding of places.22
order of building and place recognition. Failure at this level must be particularly dis-
Despite having normal spatial short term turbing in the context of an environment that
memory, normal maze learning, and excellent is familiar. The fact that SE could learn simple
recall of pre-morbidly acquired spatial infor- routes in the hospital and in Cambridge
mation, SE, nevertheless, had a grave disorder demonstrates that verbal cues may compen-
in finding his way around familiar places. Our sate to some extent for place recognition
investigations have established that SE's sen- impairments.
sory and higher order perceptual skills were He was impaired on tasks involving the
intact. He was normal on a range of visual recall of visual forms after a delay. However,
tests that are failed by patients with disorders an anterograde visual memory deficit is not
of visual sensory or perceptual processing and sufficient to account for his difficulties with
he performed at a normal level on tasks requir- finding his way around; many of his route
ing him to identify common objects. SE's fail- finding difficulties involved places previously
ure to name or identify familiar and famous very familiar to him. Furthermore his autobio-
places therefore seems to be a relatively iso- graphical memory for facts and events was
lated cognitive deficit, although as we have normal. Because SE showed moderate clinical
noted, and discuss in a separate paper,'8 he difficulties in recognising and identifying
had an additional mild deficit in his associative familiar faces as well as in recognising places,
knowledge of animals. SE's difficulty with we were concerned to establish whether there
buildings and places appeared to extend was a more pervasive visual information pro-
beyond the visual recognition domain; we cessing deficit that could account for both
have documented a significant deficit in his aspects of his case. Damasio and Damasio23
ability to provide semantic information about have proposed that prosopagnosia arises from
places in response to their spoken names. In impaired differentiation between visually simi-
particular, his knowledge of the appearance of lar tokens and in view of the common co-
places seemed to be substantially impover- occurrence of prosopagnosia and topographic
ished. amnesia it seems plausible to suggest that
These findings raise a number of issues places and faces are on a continuum of task
regarding the organisation of those cognitive difficulty. Our investigation of a patient with
processes required for spatial orientation and severe prosopagnosia served as a control for
navigation. Firstly, we shall consider the rela- this set of possibilities. Despite grave difficul-
tive status of place recognition and spatial ties in identifying faces (PHD's ability to iden-
memory in topographic orientation; secondly, tify famous people from their names was
we shall discuss the possibility that failure to strikingly better than his face identification, as
recognise buildings and places is part of a is the case in classic prosopagnosia), PHD was
more pervasive information-processing deficit entirely normal in recognising places and
affecting the ability to identify exemplars buildings. We would argue that these findings
within a class consisting of visually similar are inconsistent with a simple visual informa-
types. Finally, we shall discuss the implica- tion processing explanation of SE's disorder.
tions of our findings for cognitive theories of A cross over dissociation of the type demon-
memory organisation. strated here (although not a strong double dis-
We have documented normal levels of per- sociation in view of SE's mild impairment on
formance on formal tests of short term and the famous faces test) indicates that faces and
long-term spatial memory in a patient who is places cannot lie on a single continuum of task
deficient in his recognition of landmarks. We difficulty.2425
were able to establish that SE could learn both Further evidence against the visual informa-
"stepping stone" and "labyrinth" mazes effec- tion processing hypothesis can be drawn from
tively. His learning and memory for locomotor the finding that SE's deficit extended to
space were also explored on tests conducted in include impoverished knowledge of the spoken
hospital and town environments. Although we names of famous places. To the best of our
found evidence of substantial learning, SE's knowledge, SE is the first documented case of a
learning in locomotor space did not seem to be concordant verbal and visual deficit in the
entirely normal; he was over-reliant on ver- knowledge of buildings and landmarks.
bally labelled cues and he made occasional Previous cases of "building agnosia" have typi-
errors in his selection of appropriate land- cally been assumed to have a primary failure in
marks. We suggest, therefore, that SE's place processing visual information, rather than a
Topographic amnesia: spatial memory disorder, perceptual dysfunction, or category specific semantic memory impairment? 325
disorder which affects their conceptual knowl- College, Cambridge. We would also like to thank staff of British
Rail, Cambridge, who gave their time to provide control data in
edge (indeed the very notion of an agnosic this study, and two anonymous referees for their helpful com-
contribution to topographic disorders arose in ments on earlier versions of this paper.
the context of differentiating impairments of
perceptual processing from disorders of mem- 1 Paterson A, Zangwill OL. A case of topographic disorienta-
ory).' The evidence for a "supramodal" deficit tion associated with a unilateral cerebral lesion. Brain
1945;68:188-21 1.
in SE suggests that his disorder arises cen- 2 DeRenzi E, Faglioni P, Villa P. Topographical amnesia. J7
trally, beyond information detection, parsing, Neurol Neurosurg Psychiatry 1977;40:498-505.
3 Pallis CA. Impaired identification of faces and places with
and perceptual organisation. We suggest that agnosia for colours. Report of a case due to cerebral
it implicates his semantic memory for build- embolism. J Neurol, Neurosurg Psychiatry 1955;18:
218-24.
ings and landmarks. 4 Whitely AM, Warrington EK. Selective impairment of
It is now widely recognised that disorders of topographical memory: a single case study. Jf Neurol
Neurosurg Psychiatry 1978;41:575-8.
semantic knowledge can implicate specific cat- 5 Grusser OJ, Landis T. Visual agnosias and other disturbances of
egories of information.26 Impaired knowledge visual perception and cognition. Basingstoke: Macmillan,
1991.
of "buildings" or "places" may therefore con- 6 DeHaan EHF, Young AW, Newcombe F. Faces interfere
stitute an additional example of category spe- with name classification in a prosopagnosic patient.
Cortex 1987;23:309-16.
cific semantic breakdown. Indeed, knowledge 7 DeHaan EHF, Young AW, Newcombe F. Covert and overt
of places seems to be a particularly coherent recognition in prosopagnosia. Brain 1991 ;114:2575-91.
8 Bruyer R, Leterre C, Seron X, Feyereisen P, Strypstein E,
category of knowledge-and one which may Pierrard E, Rectem D. A case of prospagnosia with some
extend to infrahuman species. In this context, preserved covert remembrance of familiar faces. Brain
Cogn 1983;2:257-84.
reports of "place sensitive" cells in the hip- 9 DeRenzi E. Current issues in prosopagnosia. In Ellis HD,
pocampus of rats and monkeys are clearly rele- Jeeves MA, Newcombe KF, Young AW, eds. Aspects offace
vant.27 If SE's deficit is to be conceptualised in processing. Dordrecht, Holland: Martinus, Nijhoff, 1986.
10 Assal G, Faure C, Anderes JP. Non-reconnaissance d'ani-
these terms, then the asymmetry of his pathol- maux familiers chez un paysan: zooagnisie ou prosopag-
nosie pour les animaux. Rev Neurol (Paris) 1984;140:
ogy raises the interesting possibility that the 580-4.
processing of landmarks as meaningful entities 11 Folstein MF, Folstein SE, McHugh PR, Mini-mental
state: a practical method of grading the cognitive state of
may be mediated via the non-dominant hemi- patients for the clinician. J Psychiatric Res 1975;12:
sphere. For most documented cases of seman- 189-98.
tic impairment, the lesion locus has 12 Wechsler D. Manualfor the Wechsler adult intelligence scale-
revised. New York: Psychological Corporation, 1981.
consistently (although not exclusively) impli- 13 Nelson H. National adult reading test. 2nd ed. Windsor,
Berkshire: NFER-Nelson, 1991.
cated the dominant or left temporal lobe (for 14 Warrington EK, James M. Visual object and space perception
reviews see McCarthy and Warrington2 and battery. Flempton: Thames Valley Test Company, 1991.
Patterson and Hodges28). However, Ellis et al29 15 Hodges JR, Salmon DP, Butters N. Semantic memory
impairment in Alzheimer's disease: failure of access or
described a patient who had undergone a right degraded knowledge? Neuropsychologia 1992;30:301-14.
anterior lobectomy for long standing epilepsy 16 Hodges JR, Patterson K, Oxbury S, Funnell E. Semantic
dementia: progressive fluent aphasia with temporal lobe
and who had a semantic memory disorder atrophy. Brain 1992;115:1783-806.
affecting knowledge of buildings, people, and 17 Howard D, Patterson K. Pyramids and palm trees test.
Flempton: Thames Valley Test Company, 1992.
famous animals and, more recently, Evans et 18 Laws KR, Evans JJ, Hodges JR, McCarthy RA. Naming
al'0 described a patient with focal atrophy of without knowing and appearance without associations:
evidence for constructive processes in semantic memory.
the right temporal lobe who was initially Memory 1995;3:409-33.
prosopagnosic and progressed to have a more 19 Hodges JR, Oxbury S. Persistent memory impairment fol-
lowing transient global amnesia. J Clin Exp Neuropsychol
general loss of semantic knowledge of people. 1990;12:904-20.
Although SE's lesion primarily involved the 20 Milner B. Visually guided maze learning in man: effects of
bitemporal hippocampal, bilateral frontal and unilateral
right temporal lobe and hippocampus, his left cerebral lesions. Neuropsychologia 1965;3:317-338.
handedness complicates any interpretation of 21 Porteus SD. Porteus maze test. Fifty years application. Palo
Alto: Pacific Books, 1965.
cerebral asymmetry. It would seem plausible, 22 O'Keefe J, Nadel L. The Hippocampus as a cognitive map.
however, for the storage and processing of Oxford: Clarendon Press, 1978.
23 Damasio AR, Damasio H. Face agnosia and the neural sub-
place knowledge to be closely linked with per- strates of memory. Ann Rev Neurosci 1990;13:89-109.
ceptual and spatial skills that are dependent on 24 Shallice T. From neuropsychology to mental structure.
Cambridge: CUP, 1988.
right hemispheric function. Further case studies 25 McCarthy RA, Warrington EK. Cognitive neuropsychology: a
may help to establish whether cognitive sys- clinical introduction. London: Academic Press, 1990.
26 McCarthy RA, Warrington EK. The impairment of seman-
tems concerned with processing information tic memory. Philos Proc R Soc Biol 1995;346:89-96.
relating to environmental landmarks are 27 O'Keefe J, Speakman A. Single unit activity in rat hip-
pocampus during a spatial memory task. Exp Brain Res
unusual in their dependence on the right 1987;68: 1-27.
hemisphere. 28 Patterson K, Hodges JR. Disorders of semantic memory. In
Baddeley AD, Wilson BA, Watts FN, eds. Handbook of
memory disorders. Chichester: John Wiley, 1995:167-87.
29 Ellis AW, Young AW, Critchley EMR. Loss of memory for
We are grateful to John Pilling for making the original referral people following temporal lobe damage. Brain 1989;112:
and the patients and their families for their continuing assis- 1469-83.
tance. We also thank SE and PHD for giving us permission to 30 Evans JJ, Heggs AJ, Antoun N, Hodges JR. Progressive
use their initials in this paper. R A McC's work was partially prosopagnosia associated with selective right temporal
supported by a grant from the Leverhulme Trust to Kings lobe atrophy: a new syndrome? Brain 1995;118:1-13.