cortex 44 (2008) 746–752
available at www.sciencedirect.com
journal homepage: www.elsevier.com/locate/cortex
Note
Naming of objects, faces and buildings in mild cognitive
impairment
Samrah Ahmeda,*, Robert Arnolda, Sian A. Thompsonb, Kim S. Grahama and
John R. Hodgesa,b
a
Medical Research Council, Cognition and Brain Sciences Unit, Cambridge, UK
University Neurology Unit, Addenbrooke’s Hospital, University of Cambridge, Cambridge, UK
b
article info
abstract
Article history:
Accruing evidence suggests that the cognitive deficits in very early Alzheimer’s Disease
Received 19 October 2006
(AD) are not confined to episodic memory, with a number of studies documenting semantic
Reviewed 29 November 2006
memory deficits, especially for knowledge of people. To investigate whether this difficulty
Revised 21 December 2006
in naming famous people extends to other proper names based information, three naming
Accepted 8 February 2007
tasks – the Graded Naming Test (GNT), which uses objects and animals, the Graded Faces
Action editor Stefan Schweinberger
Test (GFT) and the newly designed Graded Buildings Test (GBT) – were administered to 69
Published online 23 December 2007
participants (32 patients in the early prodromal stage of AD, so-called Mild Cognitive Impairment (MCI), and 37 normal control participants). Patients were found to be impaired
Keywords:
on all three tests compared to controls, although naming of objects was significantly better
Alzheimer’s disease
than naming of faces and buildings. Discriminant analysis successfully predicted group
Episodic memory
membership for 100% controls and 78.1% of patients. The results suggest that even in cases
Semantic memory
that do not yet fulfil criteria for AD naming of famous people and buildings is impaired, and
Early diagnosis
that both these semantic domains show greater vulnerability than general semantic
knowledge. A semantic deficit together with the hallmark episodic deficit may be common
in MCI, and that the use of graded tasks tapping semantic memory may be useful for the
early identification of patients with MCI.
ª 2007 Elsevier Masson Srl. All rights reserved.
1.
Introduction
Impairment of episodic memory is the hallmark of Alzheimer’s Disease (AD), at least in the vast majority of cases (Welsh
et al., 1992). It is now well established, however, that semantic
memory breakdown is also a consistent finding in patients,
even in the early stages of the disease (Chertkow and Bub,
1990; Hodges and Patterson, 1995; Dudas et al., 2005), with
studies indicating that knowledge for famous people appears
to be particularly vulnerable (Greene and Hodges, 1996). Before
reaching full-blown dementia, patients with AD pass through
a stage of more subtle cognitive impairment that can last for
several years. A number of terms have been used to describe
this pre-dementia phase. The most popular term is Mild
Cognitive Impairment (MCI). Patients with MCI present with
complaints of memory problems and perform poorly on neuropsychological tests of memory, but do not meet diagnostic
criteria for AD as judged by performance on global screening
* Corresponding author. MRC Cognition and Brain Sciences Unit, 15 Chaucer Road, Cambridge CB2 2EF, UK.
E-mail address: [email protected] (S. Ahmed).
0010-9452/$ – see front matter ª 2007 Elsevier Masson Srl. All rights reserved.
doi:10.1016/j.cortex.2007.02.002
747
cortex 44 (2008) 746–752
instruments such as the Mini Mental State Examination
(MMSE), and preservation of activities of daily living. Conversion rates from MCI to frank dementia of 15–25% over 2 years
have been reported (Petersen et al., 2001; Bozoki et al., 2001;
Albert et al., 2001; De Jager et al., 2003).
Although MCI was originally conceptualised as a purely episodic disorder, more recently studies have documented additional deficits in semantic memory (De Jager et al., 2003;
Bozoki et al., 2001; Dudas et al., 2005; Clague et al., 2005). For
example, Thompson et al. (2002) reported disproportionate
deficits across semantic categories in a comparison of a novel
Graded Faces Naming Test (GFT) and the more commonly
used Graded Naming Test (GNT; McKenna and Warrington,
1980). Patients with questionable dementia – equivalent to
cases now given a diagnosis of MCI – showed significantly
greater impairment at baseline on the GFT compared to controls. Of the participants with questionable dementia who
performed within the normal range on the GFT, only 6% progressed to AD properly compared to 86% of those who initially
showed deficits on the GFT. Similarly, Estevez-Gonzalez et al.
(2004) used a task of famous face identification and reported
that MCI patients performed significantly worse than a control
group. The current study addresses the question of whether
the semantic impairment in MCI is specific to people or
whether it extends to other proper name based information.
To explore this issue we investigated the knowledge of
famous buildings. Unlike faces, buildings are not perceptually
homogenous but share the feature of being semantically
unique with associated proper names. Studies on testing
knowledge and/or naming for buildings are few. Milders
(2000) tested normal controls and patients with closed head
injury on two tests of retrieval: retrieval of people names and
retrieval of buildings’ names. Milders reported no significant
difference in retrieval of famous buildings or famous names.
Similarly, Brennen et al. (1990) showed that in normal participants the mean percentage error for naming of faces and buildings was similar, reporting 20% and 15% error, respectively.
Our study used the established GNT and GFT and the newly
designed matched Graded Buildings Test (GBT), which incorporates famous buildings, to investigate naming in a large
group of individuals with MCI. We predicted that performance
on the GFT and GBT would be similar, with scores on both being consistently worse than those obtained on the GNT. At
a theoretical level we wished to address the issue of whether
patients with amnestic MCI also have deficits in semantic
memory extending to person and building knowledge, and
clinically whether test performance might discriminate MCI
and controls. Our aim was to look into nature of impairment
in the memory domain. Hence this paper accepts that episodic
memory is the most salient impairment in aMCI, above other
domains, but also suggests semantic memory is similarly
a salient impairment in aMCI. A battery which includes tests
of semantic and episodic memories may be valuable for
diagnosis.
1.1.
Method
1.1.1.
Participants
A total of 69 participants took part in the study, 32 MCI
patients (14 males, 18 females, mean age 69.5 8.2) and 37
normal controls (19 males, 18 females, mean age 66.8 5.5).
Equal group sizes were initially recruited (n ¼ 40) but 8 MCI
patients were subsequently excluded because of changes in
diagnosis. Three controls were excluded because of doubts
about their cognitive status on the basis of screening questions about memory. Control participants were recruited
from the Medical Research Council Cognition and Brain
Sciences Unit Volunteer Panel in Cambridge, UK deemed cognitively normal by MMSE score >24 and no complaints of
memory problems with no history of neurological or psychiatric illness. MCI patients were recruited from the Memory
Disorders Clinic at Addenbrooke’s Hospital in Cambridge.
Diagnosis of MCI was made by a senior neurologist based on
the criteria outlined by Grundman and Petersen (2004) and
Petersen et al. (2001), namely: (1) memory complaints corroborated by an informant; (2) evidence of memory impairment
(>1.5 standard deviations (SDs) below control mean for
delayed recall) based on the Rey Auditory Verbal Learning
Test (RAVLT); (3) preserved activities of daily living (ADL);
and (4) no evidence of dementia as judged by an MMSE score
>24 and clinical judgement. MCI patients did not present
with any significant psychiatric disorder or concomitant neurological disease (such as epilepsy, alcoholism or head injury).
Patients taking medication to maintain cognitive function
were excluded. t-Tests showed no significant difference
between the two groups on age (t ¼ 1.7, df ¼ 67, p ¼ .102) and
education (t ¼ 1.6, df ¼ 67, p ¼ .120). There was a significant
difference in MMSE scores (t ¼ 3.8, df ¼ 66, p ¼ .000).
1.1.2.
Neuropsychological tests
All MCI patients were administered a general neuropsychological battery assessing global cognition, memory and fluency
(Table 1). MCI patients were impaired on all components of
the RAVLT, recall of the Rey-Osterrieth figure and on the
Addenbrooke’s Cognitive Examination (ACE; Mathuranath
Table 1 – Means and SDs of demographics and general
neuropsychological testing and graded tasks
Control (n ¼ 37) MCI (n ¼ 32)
Age (years)
Education (years)
Gender (male:female)
Global cognition
MMSE
ACE
Memory
Rey figure copy
Rey figure delayed recall
RAVLT total
RAVLT recall after interference
RAVLT 30 min delayed recall
RAVLT recognition
Graded tasks
GNT
GBT
GFT
66.8 (5.5)
13.8 (2.2)
19:18
69.5 (8.2)
12.8 (2.9)
14:18
28.8 (1.3)
94.5 (2.8)
27.2 (2.0)
82.9 (6.9)a
–
–
–
–
–
–
33.1 (3.2)a
7.8 (6.7)a
30.3 (6.9)a
3.3 (2.2)a
2.8 (2.2)a
10.8 (2.7)a
26.1 (1.8)
24.7 (2.6)
22.2 (3.1)
19.7 (4.9)
15.9 (5.0)
14.0 (5.1)
a Scores suggest impairment (1.5 SD below mean) relative to internally established mean scores obtained form matched controls.
748
cortex 44 (2008) 746–752
et al., 2000). Controls could not be tested with additional neuropsychological testing in this particular case due to limited
time and manpower.
When developing the GFT and GBT, 60 faces and 60 buildings were administered to 28 controls (a different group
from that reported in the experimental section of this study,
mean age 66.9 7.5; mean education 14.7 2.5) for naming
and identification. These results were used to select 30 items
of graded difficulty, with naming for the items ranging from
100% to 20% of participants (the same range used in the
GNT). Items were then matched on a three-way basis across
all three tests, in order that each task contained a similar
number of items that were similarly named by controls. Overall, this matching process resulted in the following mean
naming accuracy (SDs in parentheses): GFT (21.5 4.2) and
GBT (22.4 3.8), with the published figures given for the GNT
being 20.4 4.1 (Warrington, 1997). More specific details for
each test are provided below (stimuli lists are provided in
Appendix) (Fig. 1).
GNT (McKenna and Warrington, 1980): participants named
30 black and white line drawings of objects, starting with
highly familiar objects (e.g., a kangaroo and scarecrow) and
ending with more difficult and unusual exemplars (e.g.,
a cowl and retort). One mark was awarded for each correct
name provided.
GFT: participants were asked to provide the full name for 30
famous faces presented using black and white greyscale images. The stimuli covered the last 50 years (1950–2000) with
six items presented per decade. As for the GNT, as the test progressed, the famous faces become more difficult to name, as
measured by the pilot naming data. One mark was awarded
for each full name correctly produced.
GBT: participants were shown colour pictures of 30
famous buildings from across the world, for example, Buckingham Palace and Taj Mahal, and asked to provide the
name of the building. A mark was given for each correct
full name.
2.
Results
The mean number of correct responses on each of the three
tests can be seen in Fig. 2. In both groups the pattern of naming
accuracy was the same: GNT > GBT > GFT. MCI patients made
Fig. 2 – Comparison of the total correctly named items on
the GNT, GFT and GBT (maximum score [ 30). All
differences between the control group and MCI patients
were significant. Error bars represent the standard error of
the mean; s – significant group difference, * – significant
task difference in control group, y – significant task
difference in MCI group.
significantly fewer correct responses to faces, buildings and
objects in comparison to controls. A 2 3 ANOVA (group test)
revealed a significant main effect of group (F(1,67) ¼ 107.68,
p < .001), significant main effect of test (F(2,134) ¼ 49.22,
p < .001) and a significant interaction between group and test
(F(2,134) ¼ 3.40, p < .05). Pairwise post hoc comparisons
between groups confirmed a significant difference between
MCI and controls on all three tests (GNT: t ¼ 7.0, df ¼ 67,
p < .001; GFT: t ¼ 7.9, df ¼ 67, p < .001; GBT: t ¼ 8.9, df ¼ 67,
p < .001).
A components of interaction test showed that differential
impairment was significantly greater for GFT and GBT than
GNT (F(1,67) ¼ 7.661, p < .01), suggesting that unique exemplars were significantly more difficult to retrieve than
Fig. 1 – Examples from the (a) GNT; (b) GFT; (c) GBT.
cortex 44 (2008) 746–752
common exemplars. There was no significant group effect for
GFT versus GBT (F(1,67)¼0.468, p > .05), suggesting that differential impairment was the same for unique exemplars of
different categories.
Pairwise post hoc comparisons confirmed the pattern evident in Fig. 2 that performance in the control participants
was significantly different across all tests (GNT vs GBT
(t ¼ 2.7, df ¼ 36, p < .01), GNT vs GFT (t ¼ 6.6, df ¼ 36, p < .001)
and GBT vs GFT (t ¼ 5.0, df ¼ 36, p < .001)). While the MCI
participants showed a significance difference between the
GNT vs GBT (t ¼ 5.9, df ¼ 31, p < .001) and GNT vs GFT (t ¼ 6.7,
df ¼ 31, p < .001) tests, their performance on the GBT and
GFT was similar (t ¼ 1.9, df ¼ 31, p ¼ .067). This pattern suggests equivalent impairment on the GBT and GFT in the MCI
group.
2.1.
Individual scores
Impairment was defined as 1.5 SDs below the control mean.
Looking at the overlap of impairment across the tests 13% of
controls were impaired on only one test (3% GNT, 5% GFT,
5% GBT) with the remaining 87% showing no impairment. Of
the MCI cases, 13% showed no impairment, 31% were impaired
on one test only (12% GNT, 12% GFT, 7% GBT), 28% were
impaired on two tests (19% GNT and GFT, 3% GFT and GBT,
6% GNT and GBT) and 28% were impaired on all three tests.
2.1.1.
Discriminant analysis
A combined discriminant analysis was performed with diagnosis as the dependent variable and GNT, GFT and GBT scores
as predictor variables (Table 2). All 69 cases were entered. The
correlations between predictor variables and the discriminant
function suggested that GBT (r ¼ .597), then GFT (r ¼ .468), and
then GNT (r ¼ .157) were the best predictors of diagnosis. Overall the discriminant function using all three variables successfully predicted group membership for 100% of controls and
78.1% of patients suggesting that false positives were unlikely
but false negatives (21.9%) were more common.
3.
Discussion
The findings reported here replicate earlier studies documenting deficits in MCI patients that extend beyond episodic memory. Of particular note was that 87% of the individuals
considered at high risk of developing dementia were impaired,
compared to controls, on at least one of the naming tasks. The
difficulties exhibited by the patients were particularly severe
Table 2 – Classification results of discriminant analysis
Diagnosis on entry
Predicated group membership
MCI
Count
MCI
Normal
25
0
%
MCI
Normal
78.1
.0
Normal
7
37
21.9
100.0
749
for the more unique semantic exemplars (buildings and faces).
This study, therefore, confirms Thompson et al.’s (2002)
reported finding of greater vulnerability for person’s knowledge over general semantic knowledge and extends this by
adding new evidence suggesting that famous buildings are
a similarly vulnerable category (see also Blackwell et al.,
2004; De Jager and Budge, 2005; Van Lancker and Kelin,
1990). Furthermore, the graded tests have good discriminant
capabilities. The tests are able to distinguish between normal
control performance and those with early stage dementia
although some false negatives are possible (21.9% of cases).
A combination of the graded semantic tasks may aid in earlier
and more specific diagnosis, with implications for therapeutic
intervention to delay the onset of frank dementia.
We have not addressed the question of whether the impairment in naming reflects problems with lexical access or
a breakdown in the structure of semantic knowledge concerning famous people and buildings. Earlier studies of naming
and knowledge of people in patients with very mild AD,
some of whom would now be classified as MCI, points strongly
towards a semantic disorder (Greene and Hodges, 1996; Binetti
et al., 1995; Hodges et al., 1992).
In addition there are fundamental differences in the structure of semantic knowledge about things and people. Proper
names are special because of their unique mapping and are
thought to be more difficult to retrieve than common nouns
due to the weak and arbitrary links between a proper noun
and its reference. Detailed discussion on theories of proper
name production can be found in Valentine et al. (1996).
This is consistent with the widespread notion that proper
names are essentially more difficult to retrieve, even in the
healthy aged with intact recognition and knowledge for the
famous people they are asked to name (Semenza et al., 1996,
2003; Bredart, 1993). The significant advantage in controls for
naming of buildings over faces has been reported. Hanley
and Kay (1998) noted that naming problems extended to other
types of proper names in patients with quantitatively more
severe face naming impairment (see also Fery et al., 1995).
Brennen et al. (1990) and Milders (2000) also reported numerically (albeit not significantly) higher percentage naming for
building over faces in normal participants.
Furthermore, there is evidence for anatomically distinct regions in the brain for processing of objects, people and buildings. The results of this study are in keeping with the idea that
closely related brain regions are involved with the processing
of famous people and famous building knowledge. GornoTempini and Price (2001) found that the left anterior medial
temporal cortex responded to famous faces and famous buildings. Similarly, Grabowski et al. (2001) asked normal participants to name pictures of famous faces and famous
landmarks, including buildings and natural landscapes. Both
categories produced increased activation in the left temporal
pole relative to baseline activity at rest. There was no main effect of category suggesting that the left temporal pole is associated with retrieval of unique items rather than specific
retrieval of categories of proper names. This emphasises
that semantically unique items place demands on the same
area of semantic processing as each other, and this is at least
partially separate from common name processing, although
not an absolute dichotomy (Hodges and Graham, 1998).
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cortex 44 (2008) 746–752
There is a common assumption of early and specific MTL
damage in MCI but the results of this study support the literature showing that pathology, even very early on, must extend
beyond the hippocampus. A number of studies have shown
early temporal neocortex involvement (Convit et al., 2000;
De Santi et al., 2001; Chetelat and Baron, 2003). This early temporal involvement may be relevant to the differential impairment in naming unique and non-unique entities. Moore and
Price (1999) suggested that naming faces stimulates more activation in the semantic areas in comparison to naming objects because the semantic features associated with famous
faces are unique and not applicable to other members of the
category. It should be noted that not all aMCI showed semantic impairment. This variability in impairment might be
accounted for by differences in severity of the disease process,
differences in progression of disease, or educational and autobiographical experiences. This is an important focus for future
research as it has been reported that MCI patients who convert to AD at follow up show greater atrophy in temporal areas
than those who do not progress (Convit et al., 2000; BellMcGinty et al., 2005; Hirao et al., 2005). It is important to
note here that we are not attempting to dispute the notion
of early episodic amnesia in aMCI. Our aim in this study was
to highlight, in conjunction with this consistent episodic amnesia, other points of focus for optimal diagnostic efficacy in
early stage disease. We agree that if MCI is considered to be incipient AD, as it is generally regarded, then the neuropathological features of AD will be present (Morris et al., 2001;
Price et al., 2001). Hence in addition to the hallmark initial episodic memory deficit one might also expect sensitive neuropsychological instruments to detect impairment in other
cognitive domains.
In retrospect there are a number of potential limitations,
which must be acknowledged. The stimuli used were protypical examples of objects, buildings and famous faces as far as
they could be named by normal age and education matched
controls. We matched items from the GNT, GBT and GFT
according to the percentage of controls that could correctly
name each item, with the GNT items being presented as line
drawings and the GBT and GFT as photos. We accept that
line drawings and photos may be visually processed differently. This may have added perceptual difficulty although
such difficulties are not usually reported in MCI. This study
could be replicated using photos of objects instead of drawings, where we would hypothesise the same result.
The notion that a semantic deficit together with the hallmark episodic deficit may categorise MCI merits to further
study. However, we do not mean to suggest that semantic difficulties are specific. Instead, we confirm early semantic impairment and suggest semantic impairment as a point of
emphasis in clinical testing, where the majority of clinical
tests emphasize episodic memory. There is growing evidence
that semantic memory is also a salient impairment in aMCI
(Clague et al., 2005; Dudas et al., 2005; Thompson et al.,
2002). It would be interesting to follow up performance on
the graded tasks to map the progression of MCI patients
who convert to AD and those who remain stable or revert to
normal functioning. Retrospective data could provide valuable
diagnostic information. Further study might look into using
the graded tests in conjunction with imaging to help
consolidate research into the structure and processes of semantic memory and also to delineate if the naming problem
is due to semantic degradation or lexical access.
4.
Conclusion
In conclusion, the results suggest that naming is impaired in
MCI patients relative to controls, and can be used as an early
diagnostic tool. The characteristics of proper names make
them particularly sensitive to this naming deficit. The results
confirm that impairments in generating semantic information
can be seen very early on, in the pre-clinical stages of AD. Used
together as a mini battery, the graded tests could prove useful
as a sensitive indicator of the status of semantic memory in
MCI.
Acknowledgements
This work was supported by the Alzheimer’s Research Trust
via a Joseph Pollock Alzheimer’s Research Scholarship to
Samrah Ahmed. We are grateful to Joanna Mitchell for help
with data compilation and Peter Watson for statistical advice.
Appendix
Famous buildings utilised in the Graded Buildings Test (in ascending order of difficulty):
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
19.
20.
21.
22.
23.
24.
25.
26.
27.
28.
Taj Mahal
Leaning Tower of Pisa
Stonehenge
Statue of Liberty
Great Wall of China
Eiffel Tower
Big Ben/St. Stephen’s Tower
BT/British Telecom/Post Office Tower
Tower Bridge
Windsor Castle
Stansted Airport
Buckingham Palace
Sphinx
St. Paul’s Cathedral
Millenium Dome
Cenotaph
King’s College Chapel
Nelson’s Column
Arc de Triomphe
(British Airways) London Eye
Notre Dame (Cathedral)
Golden Gate Bridge
Brandenburg Gate
Parthenon
Louvre
St. Pancras Station
Mount Rushmore
Capitol Building
cortex 44 (2008) 746–752
29. Macchu Picchu
30. El Temple Expiatori de la Sagrada Familia/Sagrada Familia/Gaudi Cathedral
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