Non-verbal semantic impairment in semantic dementia.
- PubMed: 10865096
Abstract
The clinical presentation of patients with semantic dementia is dominated by anomia and poor verbal comprehension. Although a number of researchers have argued that these patients have impaired comprehension of non-verbal as well as verbal stimuli, the evidence for semantic deterioration is mainly derived from tasks that include some form of verbal input or output. Few studies have investigated semantic impairment using entirely non-verbal assessments and the few exceptions have been based on results from single cases (3: Breedin SD, Saffran EM, Coslett HB. Reversal of the concreteness effect in a patient with semantic dementia. Cognitive Neuropsychology 1994;11:617-660, 12: Graham KS, Becker JT, Patterson K, Hodges JR. Lost for words: a case of primary progressive aphasia? In: Parkin A, editor. Case studies in the neuropsychology of memory, East Sussex: Lawrence Erlbaum, 1997. pp. 83-110, 21: Lambon Ralph MA, Howard D. Gogi aphasia or semantic dementia? Simulating and assessing poor verbal comprehension in a case of progressive fluent aphasia. Cognitive Neuropsychology, (in-press). This study employed sound recognition and semantic association tasks to investigate the nature of the verbal and non-verbal comprehension deficit in 10 patients with semantic dementia. The patients were impaired on both verbal and non-verbal conditions of the assessments, and their accuracy on these tasks was directly related to their scores on a range of other tests requiring access to semantic memory. Further analyses revealed that performance was graded by concept and sound familiarity and, in addition, identified significant item consistency across the different conditions of the tasks. These results support the notion that the patients' deficits across all modalities were due to degradation within a single, central network of conceptual knowledge. There were also reliable differences between conditions. The sound-picture matching task proved to be more sensitive to semantic impairment than the word-picture matching equivalent, and the patients performed significantly better on the picture than word version of a semantic association test. We propose that these differences arise directly from the nature of the mapping between input modality and semantic memory. Words and sounds have an arbitrary relationship with meaning while pictures benefit from a degree of systematicity with conceptual knowledge about the object.
Author-supplied keywords
Non-verbal semantic impairment in semantic dementia.
Sasha Bozeat
a
, Matthew A. Lambon Ralph
a,
*, Karalyn Patterson
a
, Peter Garrard
b
,
John R. Hodges
a, b
a
MRC Cognition and Brain Sciences Unit, 15 Chaucer Road, Cambridge CB2 2EF, UK
b
University Neurology Unit, Addenbrooke’s Hospital, Cambridge, UK
Received 11 October 1999; received in revised form 8 February 2000; accepted 14 February 2000
Abstract
The clinical presentation of patients with semantic dementia is dominated by anomia and poor verbal comprehension.
Although a number of researchers have argued that these patients have impaired comprehension of non-verbal as well as verbal
stimuli, the evidence for semantic deterioration is mainly derived from tasks that include some form of verbal input or output.
Few studies have investigated semantic impairment using entirely non-verbal assessments and the few exceptions have been
based on results from single cases ([3]: Breedin SD, Saran EM, Coslett HB. Reversal of the concreteness eect in a patient with
semantic dementia. Cognitive Neuropsychology 1994;11:617–660, [12]: Graham KS, Becker JT, Patterson K, Hodges JR. Lost
for words: a case of primary progressive aphasia? In: Parkin A, editor. Case studies in the neuropsychology of memory, East
Sussex: Lawrence Erlbaum, 1997. pp. 83–110, [21]: Lambon Ralph MA, Howard D. Gogi aphasia or semantic dementia?
Simulating and assessing poor verbal comprehension in a case of progressive fluent aphasia. Cognitive Neuropsychology, (in-
press).
This study employed sound recognition and semantic association tasks to investigate the nature of the verbal and non-verbal
comprehension deficit in 10 patients with semantic dementia. The patients were impaired on both verbal and non-verbal
conditions of the assessments, and their accuracy on these tasks was directly related to their scores on a range of other tests
requiring access to semantic memory. Further analyses revealed that performance was graded by concept and sound familiarity
and, in addition, identified significant item consistency across the dierent conditions of the tasks. These results support the
notion that the patients’ deficits across all modalities were due to degradation within a single, central network of conceptual
knowledge. There were also reliable dierences between conditions. The sound-picture matching task proved to be more
sensitive to semantic impairment than the word-picture matching equivalent, and the patients performed significantly better on
the picture than word version of a semantic association test. We propose that these dierences arise directly from the nature of
the mapping between input modality and semantic memory. Words and sounds have an arbitrary relationship with meaning
while pictures benefit from a degree of systematicity with conceptual knowledge about the object. 7 2000 Elsevier Science Ltd.
All rights reserved.
Keywords: Semantic dementia; Progressive fluent aphasia; Frontotemporal dementia; Non-verbal comprehension; Conceptual knowledge
1. Introduction
The syndrome of semantic dementia is associated
with circumscribed temporal lobe atrophy, most
severely aecting the temporal pole and the infero-lat-
eral temporal lobe, typically bilaterally but often asym-
metrically [14,33]. The ventromedial frontal cortex
bilaterally and the amygdaloid complex are also often
aected [25,26]. The term semantic dementia was pro-
posed because the cases have a selective and progress-
ive deterioration of conceptual knowledge. The
selective nature of the semantic impairment was first
described by Warrington [35], who reported three
Neuropsychologia 38 (2000) 1207–1215
0028-3932/00/$ - see front matter 7 2000 Elsevier Science Ltd. All rights reserved.
PII: S0028-3932(00 )00034 -8
www.elsevier.com/locate/neuropsychologia
* Corresponding author. Tel.: +44-1223-355294.
E-mail address: matt.lambon-ralph@mrc-cbu.cam.ac.uk (M.A.
Lambon Ralph).
comprehension. More recent studies have highlighted
the patients’ progressive loss of knowledge about the
meanings of words, objects and concepts [13,33]. The
selective nature of the semantic deficit in these patients
has been confirmed by their good performance on
assessments of current day-to-day memory, short-term
verbal memory, visuospatial skills, non-verbal reason-
ing, phonology and syntax until very late in the course
of the disease [14].
The clinical presentation of semantic dementia is
dominated by anomia and poor verbal comprehension,
to the extent that the term ‘Gogi’, or word meaning
aphasia, is sometimes used to describe these patients in
Japan [17,30]. Imura et al. [18] and Tanabe et al. [34]
emphasised that the impairment in Gogi aphasia is
limited to the domain of language. In this regard,
Tanabe et al. noted comments from the wife of a
patient who was surprised that her husband could no
longer understand the names of objects that he still
used eciently everyday [34]. Although it has been
argued that patients with semantic dementia have
degraded knowledge for non-verbal as well as verbal
stimuli [14,33], the evidence for a non-verbal semantic
impairment has tended to rely upon tasks that include
verbal input (e.g., word-to-picture matching and draw-
ing of objects to dictation of their names) or output
(e.g., picture naming, definitions of pictured concepts,
descriptions of famous people from face stimuli, etc).
The existing literature contains limited examples of
entirely non-verbal assessment of comprehension, the
vast majority of which rely on pictures to probe
knowledge. A number of researchers have reported
impairment on the picture version of the Pyramid and
Palm Trees test [15], which is a non-verbal assessment
of semantic associations [3,20,23,31]. Breedin et al. [3]
assessed a patient on colouring of black and white line
drawings of objects and animals that have a specific
known colour. The patient showed severe impairment
on this task, being able to select the correct colour for
only 10 out of 28 items. Using similar colouring tasks,
both Graham et al. [12] and also Lambon Ralph,
Howard, Nightingale and Ellis [22] demonstrated non-
verbal semantic impairments in single case studies of
patients with semantic dementia.
In addition to picture based tests, sound recognition
tasks can also provide a straightforward, non-verbal
assessment of comprehension. Sound recognition has
been assessed in one case with herpes simplex virus
encephalitis (HSVE) but it has been used most often
to test patients with pure word deafness [1,6]. Rather
than requiring a subject to identify an object or animal
by naming it in response to its characteristic sound,
Lambon Ralph and Howard [21] formulated a non-
verbal assessment by asking the patient to match the
sound to a picture of the target concept. The semantic
dementia patient IW was impaired on both this sound-
to-picture test and a corresponding sound-to-word ver-
sion thereby confirming the presence of a non-verbal
semantic impairment [21].
The aim of this cross-sectional study was to provide
further evidence for the non-verbal conceptual impair-
ment in semantic dementia based on a larger set of
patients and a more extended investigation than in pre-
vious studies. In addition to a battery of standard
assessments of comprehension, including the Pyramids
and Palm Trees test, recognition of environmental
sounds and a new semantic association task were used
to test the patients’ semantic memory non-verbally.
2. Method
2.1. Participants
Ten patients were identified through the Memory
and Cognitive Disorders Clinic at Addenbrooke’s Hos-
pital, Cambridge, UK, where they were seen by a
senior neurologist (JRH), a senior psychiatrist and a
clinical neuropsychologist. In addition to a clinical
assessment, all patients were given a number of stan-
dard psychiatric rating scales to exclude major func-
tional psychiatric disorders such as depression and
schizophrenia. They all underwent CT or MRI scan-
ning together with the usual battery of screening blood
tests to exclude treatable causes of dementia.
All patients presented with a progressive loss of
vocabulary aecting expressive and receptive language
in the context of fluent speech production. They all
fulfilled the criteria for semantic dementia previously
reported: anomia, impairment in single word compre-
hension and impoverished semantic knowledge with
relative preservation of phonology, syntax, visuospatial
abilities and day-to-day memory [13,14]. Structural
brain imaging by MRI showed focal atrophy involving
the polar and inferolateral regions of one or both of
the temporal lobes.
To compare the performance of the patients with
that of age and education matched controls, we
selected normal participants from the Medical
Research Council Cognition and Brain Sciences Unit’s
participant panel.
2.2. Assessments
2.2.1. General neuropsychology
The following battery of neuropsychological tests
was administered: the Mini-Mental State Examination
as a general measure of cognitive impairment [8], the
digit span subtest of the Wechsler Memory Scale-
Revised (WMS-R) [38] to assess auditory-verbal short
term memory; verbal fluency for the letters F, A, S to
S. Bozeat et al. / Neuropsychologia 38 (2000) 1207–12151208
coloured matrices to assess non-verbal problem solving
[27,28]; copy and immediate recall of the Rey Complex
Figure to test visuospatial skills and episodic memory
[29]. Various subtests from the Visual Object and
Space Perception battery were also used to assess
visuospatial function in more detail [36].
2.2.2. Semantic tests
2.2.2.1. General semantic assessment. The patients were
given a selection of tasks from a semantic battery,
which is a collection of tests that use the same set of
stimulus items to assess semantic knowledge systemati-
cally across dierent input and output modalities. It
contains 64 items, chosen from the corpus of line
drawings by Snodgrass and Vanderwart [32], represent-
ing three categories of living things (animals, birds and
fruit) and three categories of artefacts (household
items, tools and vehicles). The following subtests from
the semantic battery were administered: category flu-
ency, in which the subject is asked to produce as many
exemplars as possible in one minute for each of the six
categories; naming of the 64 line drawings; spoken
word-to-picture matching using picture arrays contain-
ing the target plus nine within-category foils.
Two other semantic assessments were also adminis-
tered: the concrete and abstract word synonym test
which requires the subject to choose one of two words
that is similar in meaning to the target word [37] and
the Pyramids and Palm Trees test [15] of associative
semantic knowledge. In this later assessment, subjects
are asked to choose one of two items that is most clo-
sely associated with the target (e.g., for the target pyra-
mid, the choice is between palm tree and pine tree ).
The stimuli are presented as either pictures or written
words.
2.2.2.2. Camel and Cactus test. Two new semantic
assessments were designed specifically for this study.
The first was a test of semantic association based on
the principle of the Pyramids and Palm Trees test [15].
Subjects were asked to choose one of four same-cat-
egory items that has an associative relationship with
the target. For example, in one of the trials the subject
was asked to match a camel to one of four types of
vegetation: cactus (the target), tree, sunflower or rose.
The target items for this test were the same 64 items as
those included in the battery of semantic tests
described above. The assessment was administered in
two forms: in one, all items (targets and response
choices) were presented as pictures; in the other form,
all stimuli were words. Concept familiarity ratings
from a previous study [10] were already available for
the 64 target items included in the Camel and Cactus
test.
2.2.2.3. Environmental Sounds test. This test was based
on the sound matching assessment used by Lambon
Ralph and Howard [21]. It contained 48 sounds from
six categories (domestic animals, foreign animals,
human sounds, household items, vehicles and musical
instruments). Some less familiar sounds were included
in an attempt to create a more sensitive measure of
early semantic impairment. There were three con-
ditions: matching sounds to pictures, sounds to written
words and spoken words to picture. Subjects were
asked to listen on each trial to a sound or a spoken
word and match it to the target stimulus (picture or
written word) from an array of 10 within-category
items.
Familiarity with the items was established by asking
20 normal participants to rate both their overall famili-
arity with each item and how often they hear each
sound on a scale of 0 (never) to 6 (every hour), leading
to a measure for familiarity with both the concept in
general and the sound specifically.
3. Results
3.1. General neuropsychology
The 10 patients covered a broad spectrum of impair-
ment as indicated by their performance on the Mini-
Mental State Examination (see Table 1). They all
showed intact working memory as measured by for-
ward and backward digit span. Although DC per-
formed worse than expected on the backward digit
span, this was probably due to a failure to compre-
hend the task. All patients exhibited some impairment
on the letter fluency test. There was general preser-
vation of non-verbal problem-solving skills as
measured by Raven’s matrices. It should be noted that
as two versions of the Raven’s matrices were used, the
advanced and the coloured, the scores are given as per-
centiles. The two patients, JC and WM, who per-
formed below the level of the other patients were both
given the advanced version of the test which is particu-
larly dicult. All patients had preserved visuospatial
skills as indicated by their copying of the Rey Figure
and performance on the various subtests of the Visual
Object and Space Perception battery. Recall of the
Rey Figure was good in all cases revealing preser-
vation of non-verbal episodic memory.
3.2. Semantic tests
3.2.1. General semantic assessment
As shown in Table 2, the patients included in this
study also covered a wide range of semantic decline
from the mildly impaired patients such as JP through
to IF. All showed reduced category fluency and some
S. Bozeat et al. / Neuropsychologia 38 (2000) 1207–1215 1209
the naming test. All patients, except for WM and JP
were impaired on comprehension as measured by the
word-to-picture matching (N.B. the patients in Tables
1 and 2 are ordered as best as possible to reflect
decreasing naming and comprehension scores). The
patients performed very poorly on the concrete and
abstract word synonym test. Apart from WM, the
synonym scores were no better than expected by
chance, revealing this assessment to be a highly sensi-
tive measure of semantic impairment. The patients
were impaired on both conditions of the Pyramids and
Palm trees test, except for JP and WM who performed
within the normal range on the picture version. Before
considering the results of the Camel and Cactus test
and the Environmental Sounds test, we note that the
patients tended to achieve similar scores for both the
non-verbal and verbal versions of the Pyramids and
Palm Trees test, supporting the view that they have a
generalised semantic impairment aecting all modal-
ities of input. In this regard it is important to note
that significant correlations were found between the
patients’ scores for all the semantic tasks (r between
0.75 and 0.94, all p
one-tailed
< 0:05 except for the con-
crete and abstract word synonyms, which is not sur-
prising given the almost uniformly chance level of
performance on this test.
3.2.2. Camel and Cactus test
Looking at the patients individually, it is clear that
eight out of 10 were impaired on the Camel and Cac-
tus test when compared to controls, the exception
being WM who scored at the bottom of the normal
range on the picture version and JP who scored within
the normal range on both conditions (see Fig. 1). As
noted earlier, these two patients were in the early
stages of semantic dementia and their mild semantic
deficit was only revealed by certain assessments.
An analysis of variance was used to investigate the
dierences in performance of patients and controls for
the two dierent conditions of this test. This analysis
revealed a significant main eect of group, with the
patients performing worse than controls
F 1, 27 10:81, p < 0:01); there was no main eect
of condition F 1, 27 < 1 but a significant interaction
between group and condition F 1, 27 4:18,
p 0:05). Post hoc paired-samples t-tests revealed that
the patients performed significantly better on the pic-
ture than the word condition of this test (pictures:
mean — 40.6 (SD — 13.9), words: mean — 37 (SD —
16.25); t
7
2:93, p < 0:05).The small dierence
favouring the word condition for the control subjects
was not statistically reliable (pictures: mean — 56.9
(SD — 7.27), words: mean — 59.1 (SD — 6.3);
t
19
1:16, n.s).
Scores on the picture condition of the Camel and
Cactus test were significantly correlated with all the
semantic measures in Table 2, except the concrete and
abstract word synonym test (r between 0.88 and 0.95,
all p
one-tailed
< 0:01). Performance on the word con-
dition also correlated with the same semantic assess-
ments (r between 0.77 and 0.88, all p
one-tailed
< 0:05).
Table 1
General neuropsychology
Test (maximum score) JP WM SL JC DS AT DC JW JH IF Control
mean
(SD)
MMSE (30) 29 27 28 24 23 25 18 NT 9 11 28.8 (0.5)
Digit span
forward 6 8 6 8 6 8 7 5 6 5 6.8 (0.9)
backward 5 7 3 4 4 5 2 5 5 5 4.7 (1.2)
Letter fluency (total: FAS) 27 29 31 23 7 20 16 NT 19 16 44.2 (11.2)
Raven’s matrices (percentiles) > 95
a
50
b
NT 25
b
95
a
90
a
> 95
a
> 95
a
90
a
90
a
Rey Figure
copy (36) 35 35 30 30 35 28 32 36 36 26 34 (2.9)
immediate recall 23.5 24 15.5 NT 17.5 14 12 NT 10.5 NT 18.3 (5.2)
VOSP
incomplete letters (20) NT 19 20 20 20 NT 20 20 18 NT 19.2 (0.8)
dot counting(10) 10 10 10 10 10 10 10 10 10 10 9.9 (0.3)
position discrimination (20) NT 20 NT 20 20 NT 17 NT 20 20 19.8 (0.6)
cube analysis (10) NT 10 NT 9 10 NT 10 NT 10 6 9.7 (2.5)
number location (10) 10 9 10 10 9 10 10 NT 10 NT 8.9 (2.8)
Patients are ordered according to their performance on the naming and the category comprehension tests (see Table 2). VOSP — Visual
Object and Space Perception battery.
a
Raven’s coloured progressive matrices.
b
Raven’s advanced progressive matrices.
NT — not tested.
S. Bozeat et al. / Neuropsychologia 38 (2000) 1207–12151210
the term semantic dementia implies a selective and gra-
dual impairment to a single central system of concep-
tual knowledge, leading to impairments in all tasks
that require activation of such knowledge, whether
they involve verbal or non-verbal input or output
modalities. If this is the case, performance on dierent
semantic assessments should not only be correlated
but, where the same terms/concepts are used, patients
should exhibit significant item consistency across the
dierent modalities tested. Item consistency across the
two conditions of the Camel and Cactus test was
investigated using a series of simultaneous logistic re-
gression analyses.
Assessment of item consistency is complicated by
the fact that some items are invariably harder than
others. Specifically, performance in semantic dementia
is known to be aected by the familiarity of each con-
cept [9,19]. One would therefore expect to find some
consistency simply on the basis that unfamiliar items
will tend to be consistently inaccurate, and more fam-
iliar items consistently accurate [2,5,16,21]. Consistency
between the picture and word conditions was assessed
by predicting the former from the latter, and vice
versa, with two additional predictor variables included
in the regression equation: familiarity and patient. The
possibility that consistency may vary across individual
patients was assessed by repeating each regression
analysis with an interactive term, patient by predicting
task, included. The two patients who performed at
chance on one or both versions of the Camel and Cac-
tus test, IF and DC, were not included in the consist-
ency analysis.
These analyses revealed significant consistency
across the two conditions (Wald values 30.61 and
30.99, both p < 0:001). Performance was significantly
aected by familiarity only in the word version of the
test (Wald=11.64, p < 0:001). Accuracy varied
between patients (Wald values 20.01 and 73.18, both
p < 0:05), but there was no indication that consistency
varied across subjects (Wald values 0.83 and 1.08, n.s).
Table 2
Assessment of semantic memory
Test (maximum score) JP WM SL JC DS AT DC JW JH IF Control
mean
(SD)
Category fluency
living 42 38 23 15 3 14 6 3 5 2 60.3 (12.6)
manmade 37 29 20 21 10 18 4 4 7 5 54.8 (10.3)
Naming (64) 59 57 45 43 17 17 11 9 6 1 62.3 (1.6)
Word-picture matching (64) 64 63 60 58 58 57 36 23 18 18 63.7 (0.5)
Word synonyms
concrete (25) 13
a
21 15
a
12
a
12
a
16 14
a
NT 12
a
13
a
23.7 (1.3)
abstract (25) 14
a
18 15
a
8
a
14
a
14
a
13
a
NT 13
a
13
a
23.0 (2.1)
Pyramids and Palm Trees
words (52) 48 48 46 44 46 45 25
a
32 25
a
28
a
51.1 (1.1)
pictures (52) 49 52 48 41 46 47 36 27
a
37 22
a
51.2(1.4)
a
Score not significantly better than expected by chance.
Fig. 1. (a) Performance on the picture condition of the camel and
cactus test. The two horizontal lines denote the upper and lower
limits of normal performance. (b) Performance on the word con-
dition of the camel and cactus test. The two horizontal lines denote
the upper and lower limits of normal performance. Data are not
available for JW and JH.
S. Bozeat et al. / Neuropsychologia 38 (2000) 1207–1215 1211
Looking at the patients individually, it is clear that
they all scored outside the normal range on all con-
ditions of the Environmental Sounds test except for
WM, whose score fell below normal on sound-to-word
matching only (see Fig. 2).
Analysis of variance revealed a significant main
eect of group, with the patients performing worse
than the control subjects F 1, 24 68:01, p < 0:001);
there was a main eect of condition F 2, 48 81:36,
p < 0:001 and an interaction between group and con-
dition (F(2,48)=8.71, p < 0:01), which arose from a
larger dierence between word-to-picture matching
and the two conditions requiring sound recognition in
the patients than in the controls (patients: word–pic-
ture: mean — 33.3 (SD — 11.64), sound–picture:
mean — 21.6 (SD — 8.69), sound–word: mean —
19.8 (SD — 7.89); controls: word–picture: mean —
47.75 (SD — 0.57), sound–picture: mean — 41.18 (SD
— 2.54), sound–word: mean — 41.25 (SD — 2.74)).
Paired-samples t-tests confirmed that both the patients
and controls performed significantly better on the
word-to-picture matching condition compared to both
of the sound conditions (t values between 4.91 and
9.97, all p < 0:001). There was no significant dierence
between sound-to-picture matching and sound-to-word
matching (patients: t
9
1:57, n.s; controls:
t
17
0:92, n.s).
Significant correlations were found between the
patients’ scores for all conditions of this test, the
semantic battery tests and the Camel and Cactus test
(between 0.73 and 0.97, all p
one-tailed
< 0:05), though
not with the concrete and abstract synonym test. The
correlation between sound-to-picture matching and the
word condition of the Camel and Cactus test just
failed to reach significance r 0:59, p
one-tailed
0:06).
3.2.3.1. Item consistency. Consistency between the
three conditions of the Environmental Sounds test was
also measured by a series of simultaneous logistic re-
gression analyses. For example, consistency between
the sound-to-picture and sound-to-word conditions
was assessed by predicting the former from the latter,
and then repeated the other way around, with two ad-
ditional predictor variables included in the regression
equation: familiarity (either general familiarity or
sound familiarity) and patient. The possibility that
consistency may vary across individual patients was
tested by repeating each regression analysis with an
interactive term, patient by predicting task, included.
Performance was significantly consistent across all
possible pairings of the three conditions (Wald values
between 13.16 and 34.67, all p < 0:001). Accuracy was
aected by familiarity, whether measured as the famili-
arity with the sound (Wald values between 4.65 and
11.87, all p < 0:05 or familiarity in general (Wald
values between 4.26 and 48.26, all p < 0:05). The one
exception to this summary is that, when predicting per-
formance on the word-to-picture matching task from
performance on sound-to-picture matching, the eect
of general familiarity failed to reach significance
(Wald=2.94, p 0:08). Accuracy varied significantly
between the patients (Wald values between 18.83 and
39.45, all p < 0:001), but there was no indication that
consistency varied across subjects (Wald values
between 0.01 and 23.89, n.s).
Fig. 2. (a) Performance on the sound-to-picture matching test. The
two horizontal lines denote the upper and lower limits of normal
performance. (b) Performance on the sound-to-word matching test.
The two horizontal lines denote the upper and lower limits of normal
performance. (c) Performance on the word-to-picture matching test.
The two horizontal lines denote the upper and lower limits of normal
performance.
S. Bozeat et al. / Neuropsychologia 38 (2000) 1207–12151212
The aim of this study was to demonstrate that the
key impairment in semantic dementia is not simply a
word comprehension deficit but a generalised deterio-
ration of semantic memory that extends to the non-
verbal domain. Overall, the patients performed signifi-
cantly below the control subjects on both the picture
version of the Camel and Cactus test and the sound-
to-picture matching condition of the Environmental
Sounds test. These results provide clear evidence that
comprehension is impaired in semantic dementia even
in tasks where neither stimuli nor responses contain or
require any words. Significant correlations were found
between the patients’ scores on all the semantic tests as
well as item consistency across the dierent modalities
of the Camel and Cactus test and the Environmental
Sounds test, even after controlling for the familiarity
of the items. Altogether, this evidence provides strong
support for the notion that semantic dementia is best
characterised as a progressive impairment to central
conceptual knowledge, that supports semantic per-
formance independent of modality.
Further analysis also revealed reliable dierences
between modalities. The patients performed signifi-
cantly better on the picture than word condition of the
Camel and Cactus test, a result that was not echoed in
the control group. On the Environmental Sounds test,
both the patients and controls were more successful on
the word-to-picture matching condition than either of
the sound conditions, though the dierence was greater
in the patients than the controls. There were no dier-
ences in either group between matching sounds to pic-
tures and sounds to words.
There is no puzzle in the pattern of correlations
between tests and consistency between items across
dierent conditions combined with dierences in per-
formance on the dierent conditions. This pattern is
easily explicable in terms of the notion that partially
degraded knowledge will have dierential eects on
overt performance depending on the nature of the
mapping between input/output modalities and concep-
tual knowledge. Information available directly from
the perception of pictures and objects provides clues to
both form and function [11]. Gibson’s notion of aor-
dance [11] has some overlap with the theories of Cara-
mazza and colleagues [4], who propose firstly, that
objects benefit from direct access to meaning from
visual input (the assumption of privileged access) and,
secondly, that knowledge about the structural aspects
of an object is closely linked to the semantic properties
that specify its function (the assumption of privileged
relationships). A similar proposal can be found in the
literature on category specific deficits [6,7]. At a com-
putational level of description, this can be cast in
terms of the systematicity of the mapping between
dierent representations. Systematicity can be thought
of in terms of how well features of the input are able
to predict output patterns. In a perfectly systematic
mapping, each output feature can be predicted by a
corresponding input feature, whereas in an arbitrary
mapping, there is no such predictability.
Lambon Ralph and Howard [21] used a simple con-
nectionist simulation to demonstrate the impact of
dierent mappings between surface form and concep-
tual knowledge. Following simulated damage to the
semantic system, comprehension performance was
always better when semantic representations were acti-
vated by picture than by word input. Furthermore,
even when the network made comprehension errors,
these nearly always involved activation of the correct
semantic region for pictures but this was much less
likely to occur for words. In this simulation only a
portion of the full distributed semantic representation
was related systematically to the picture representation.
When the quality of the two parts of the conceptual
representation was compared, both exhibited a signifi-
cant dierence, favouring picture over word input.
This would seem to suggest that even limited systema-
ticity between input modality and a minor part of the
full semantic pattern is likely to benefit comprehension
in general.
Further support for the dierential eects of sys-
tematic and arbitrary mapping comes from another
simulation reported by McGuire and Plaut [24]. They
found that task systematicity had a dramatic eect on
the rate of acquisition and the robustness of the system
to damage. For example, when just 1% of the connec-
tions were removed there was no eect on the task
supported by a systematic mapping, but, this level of
damage reduced correct performance to 78% on the
task underpinned by arbitrary mapping.
These computational models, like the patients
described here, exhibit impaired comprehension of
both word and picture stimuli as well as a significant
dierence in accuracy favouring the pictures. The net-
works demonstrate that such a dierence should be
expected following impairment to a unitary semantic
system because the arbitrary mapping underlying word
comprehension is relatively sensitive to mild levels of
damage.
Although the discussion of these networks has been
cast only in terms of picture and word comprehension,
the same argument can be applied to explain perform-
ance on the sound recognition tests. Even the two
mildest patients included in this study (JP and WM),
who did not show much impairment on the other
semantic tests, had scores outside the normal range on
one or both conditions of the sound recognition task,
suggesting that this assessment is very sensitive to
early/mild semantic impairment. We propose that
there may be two factors underlying this finding.
S. Bozeat et al. / Neuropsychologia 38 (2000) 1207–1215 1213
ship with their meaning than pictures do and this
makes them vulnerable to mild levels of semantic
impairment. Unlike words, however, we are not often
required to access meaning solely from the sound of
an object. We are more accustomed to hearing a
sound and seeing the animal or object at the same
time. Indeed we know from this and previous studies
[9,19] that familiarity is an important predictor of per-
formance in these cases, and so it is important to note
that the ratings of familiarity with the sound of an
item were significantly lower than for the concept as a
whole t
47
2:17, p < 0:05). A test involving the com-
bination of sounds and words as stimuli, therefore,
creates a particularly dicult situation for the patients
with semantic dementia because both have a largely
arbitrary mapping to meaning, and the sounds are, on
the whole, relatively unfamiliar.
Acknowledgements
We are indebted to the continuing support of the
patients included in this study. This research is sup-
ported by grants from the Medical Research Council
(UK) and the National Institutes of Health (USA).
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