Aging & Mental Health, May 2004; 8(3): 222–232

ORIGINAL ARTICLE

Emotion processing in Alzheimer’s disease

R. S. BUCKS1 & S. A. RADFORD2

1
Department of Psychology, University of Southampton & 2Clinical Psychology Department, Bristol University,
Bristol, UK

Abstract
To date, there have been few studies of emotion processing in those suffering from Alzheimer’s disease, yet this may have an
important effect on the quality of life of both sufferers and their families. This paper describes an investigation of the relative
changes in cognition and in recognition and identification of non-verbal communicative signals of emotion in those suffering
from Alzheimer’s disease, and seeks to address the implications for clinical practice. Twelve adults with a diagnosis of
‘probable’ Alzheimer’s disease and 12 matched older adult healthy comparison participants undertook a series of tasks
involving face and prosody discrimination. Facial stimuli were presented on cards, and prosodic stimuli on audiotape. Scores
were compared with a measure of general cognitive ability. There was a significant difference between the Alzheimer’s
disease group and healthy older adult group on emotion and cognition tasks respectively. However, the ability to recognize
and identify non-verbal affect cues in emotional facial expression and emotional prosody was preserved relative to general
cognitive ability in those suffering from Alzheimer’s disease. In addition, there were no differences found in the recognition
of different emotions (happiness, sadness, anger, fear or neutral). This relative sparing of non-verbal emotional processing
skills has implications for provision of assessment and interventions based on the creation of effective forms of
communication that are less reliant on cognitive ability.

Introduction recently, a number of models of emotion and

For many caregivers of individuals with dementia,
it is the behavioural or non-cognitive features that
are most distressing (Donaldson, Tarrier & Burns,
1998). Many of these features can be seen as a
response to the individual’s emotional state (Woods,
2001), or as a means of communicating an unmet
need (Stokes, 1996), such as feelings of insecurity
(Magai & Cohen, 1998). None-the-less, behavioural
difficulties are commonly seen as a feature of the
dementia, rather than as a result of the interaction of
the person and their social environment. Woods
(2001) has argued that negative emotional feedback
from caregivers can exacerbate ‘challenging’ behav-
iour. This assumes that the individual with demen-
tia, despite their declining cognitive skills, retains
sensitivity to the emotional responses of others.
Yet, despite growing evidence of the influence
of emotional aspects of dementia on both the individ-
ual and wider social networks, research has been
concerned, largely, with the cognitive and functional
symptoms, ignoring the emotional or affective abil-
ities of those with dementia (O’Neill, 1997). More
emotion-cognition interaction have been elaborated
in the literature ( James, 2001; Woods, 1999) and it
has become increasingly clear that there is a close
connection between affect, cognition and behav-
ioural adaptation. Thus, research into care and
treatment of individuals with dementia has begun
to consider emotional as well as cognitive and
functional aspects of their conditions. However,
despite the finding that emotion expression is largely
intact in Alzheimer’s disease (AD) (Magai et al.,
1996), very few systematic studies have concentrated
on the individual with dementia’s ability to compre-
hend the emotions of others, and fewer still have
specifically studied AD.
Early studies of emotion processing recruited
participants with general organic brain disease.
For example, Kurucz, Feldmar & Werner (1979)
demonstrated deficits in recognition of facial emo-
tional expressions in patients with organic brain
disease, including AD, schizophrenia and major
affective disorders. These deficits were not explained
by prosopagnosia (Kurucz & Feldmar, 1979).
Deficits in emotion processing comprehension have

Correspondence to: Dr Romola S. Bucks, Senior Lecturer in Clinical Psychology, Department of Psychology, University of
Southampton, Building 44 (Shackleton), Highfield, Southampton, SO17 1BJ, UK. Tel: þ44 (0) 23 8059 2633. Fax: þ44
(0) 23 8059 2588. E-mail: romola.bucks@soton.ac.uk

Received for publication 3rd August 2002. Accepted 9th June 2003.

ISSN 1360-7863 print/ISSN 1364-6915 online/04/030222-11 ß Taylor & Francis Ltd

DOI: 10.1080/13607860410001669750

also been found in patients with: Huntingdon’s
disease and unilateral stroke (Speedie et al., 1990);
Parkinson’s disease (Breitenstein et al., 2001); right
hemisphere focal lesions (Adolphs, Jansari & Tranel,
2001a;); temporal lobectomy (Adolphs, Tranel &
Damasio, 2001b), fronto-temporal dementia (Keane
et al., 2002) and, schizophrenia (Kohler et al., 2000).
In studies in AD, researchers have generally
demonstrated deficits in facial emotional recogni-
tion. However, these findings have often been com-
plicated by the severity of cognitive deficit or the
strong verbal or memory requirements of the tasks
used (Cadieux & Greve, 1997; Roudier et al., 1998).
Indeed, a number of researchers have argued that
these impairments in emotional facial recognition are
secondary to general cognitive deficits (Koff et al.,
1999).
In their study, Roudier et al. (1998) found
evidence for impairment in discrimination of facial
identity in AD but not in discrimination of emo-
tional facial expression, arguing for a dissociation of
the processing of facial identity and facial emotion;
a proposal supported by Bowers and colleagues
(Bowers, Blonder & Heilman, 1991; Bowers, Bauer
& Heilman, 1993). Further evidence supports an
additional distinction between affective facial and
prosodic processing (Borod et al., 1998; Richardson
et al., 1992). Despite this distinction, only one previous
study has assessed affective facial and prosodic
processing separately in AD. All other studies have
considered only facial emotional expression. Cadieux
and Greve (1997) found deficits in individuals with
AD in the discrimination of facial affect and on
selecting a facial affect in response to a verbal label.
They did not find deficits in emotional prosody
performance. They argued that language-related
difficulties, particularly in understanding task
demands, may have affected performance, but that
changes in facial affect perception may relate to the
early pathology affecting the temporal neocortex,
hippocampi and amygdala in AD (Braak & Braak,
1991; van Hoesen, 1997). They were unsure whether
performance on emotional prosody tasks was unim-
paired because it was somehow differentially affected
in AD by comparison with facial affect performance,
or because the prosodic stimuli, being tape-recorded,
were ‘richer’ than the facial photographs and therefore
helped to improve performance. Given that in healthy
individuals recognizing emotions from prosody alone
is thought to be more difficult than recognizing
emotions from facial expressions (Adolphs, 2002),
this explanation seems unlikely.
TABLE 1. Age, years of education and MMSE scores for healthy older adults and participants with Alzheimer’s disease
Mean (SD), range n Age
Healthy older adult participants 12 74.4 (7.1), 62–85
Participants with Alzheimer’s disease 12 75.5 (7.5), 60–89
Emotion processing in Alzheimer’s disease 223
Finally, the authors did not consider emotion-
processing deficits in terms of the different emotions
being assessed. There is accumulating evidence that
temporal lobe damage (especially to the amygdala)
may result in problems with processing fear and
anger stimuli, particularly for faces (Adolphs et al.,
2001b; Adolphs, 2002), and that the medial pre-
frontal cortex may play a role in the appraisal/
identification of emotion (Luan Phan et al., 2002).
Thus, the aim of this study was to repeat the
assessment of emotion processing as used by
Cadieux and Greve (1997), both to see if the same
pattern of facial affect and emotional prosody
performance would be found, and to examine the
ability of individuals with mild-to-moderate AD to
identify the meaning of non-verbal communicative
signals of different emotions.
Methods
Participants
Two groups of 12 older adults were recruited and
matched for age, gender, handedness and years
of education. The AD group (eight females, four
males) were recruited through a local memory dis-
orders clinic, where they underwent thorough medical,
psychiatric and psychological screening, in order to
rule out any other treatable pathology. They met
diagnostic criteria for probable Alzheimer’s disease
according to NINCDS/ADRDA criteria (McKhann
et al., 1984), and had a Mini-Mental State Exami-
nation (MMSE; Folstein, Folstein & McHugh, 1975)
scores of 12–22. All were right-handed and were
identified by the clinic as having no significant visual
or hearing impairments.
The healthy older adult (HOA) group (five females,
seven males) were recruited from the carers of those
in the AD group and from volunteers. They were all
right-handed, and had no significant visual or hearing
deficits. They had no history of physiological or
psychological difficulties of note and were taking no
medications likely to affect cognition. Table 1
contains descriptive details for these groups.
Measures
Assessment of emotional processing was based on
The Florida Affect Battery (FAB; Bowers et al.,
1991). The battery assesses visual (facial expres-
sion), auditory (prosody), and visual-auditory
Years of education MMSE
10.2 (1.0), 9–12 28.0 (1.0), 27–29
10.5 (1.0), 9–12 18.8 (2.9), 12–22
224 R. S. Bucks & S. A. Radford
(cross-modal) emotion processing. Five different
emotions (happiness, sadness, anger, fear, neutral)
were used across these subtests. Black and white
photographs of four different women were used in the
facial affect tasks. Subtest 1 assessed the ability to
discriminate ‘same’ and ‘different’ neutral faces. This
task acted as a perceptual control for the facial affect
tasks. Subtest 2 assessed the ability to discriminate
between ‘same’ or ‘different’ emotional faces. Subtest
3 assessed participants’ ability to name the affect
shown in a series of emotional faces. Subtest 4 req-
uired participants to select from five alternatives the
facial affect that matched a verbal label given by the
examiner (e.g. ‘point to the angry face’). Subtest 5
required participants to match the facial affect shown
on a target face with one of five different emotional
expressions. Auditory stimuli for the prosody subtests
consisted of a tape-recorded female voice. Subtest 6
assessed the ability to process propositional prosody
and served as a control for the affective prosody tasks.
Participants were asked to discriminate between
‘same’ and ‘different’ non-emotional prosody in neu-
tral sentences (e.g., ‘fish jump out of water’ spoken
in an interrogative tone (?), or a declarative tone (!)).
Subtest 7 assessed the ability to judge whether
affective prosody was the ‘same’ or ‘different’ in
semantically neutral sentences spoken in an emo-
tional tone of voice. Subtest 8a required participants
to name the emotional prosody of a series of
sentences. Subtest 8b required participants to listen
to affectively intoned sentences in which the semantic
content either differed (i.e., was incongruent with; ‘all
the puppies are dead’ said in a happy tone of voice) or
paralleled (i.e., was congruent with; ‘all the puppies
are dead’ said in a sad tone of voice) the message.
Finally, in the cross-modal tasks, participants were
required to match the facial expression with one of
three corresponding prosodic stimuli (Subtest 9) or
vice versa (Subtest 10). The FAB has good test-retest
reliability (Subtest r values range from 0.89 to 0.97)
and good construct validity, as established by factor
analysis and greater than 80% agreement on the rating
of each stimulus by 70 healthy adults (Bowers et al.,
1991). Participants were provided with a cue sheet
explaining the task (e.g., ‘match face to voice’) and
a sheet of the target emotions (happiness, sadness,
anger, fear, neutral). They were also prompted and
task instructions were repeated, as required.
Participants were allowed to change their response
and to ask for clarification about each task.
Analysis
Data were analyzed using SPSS 11.0 for Windows
(2001). The Florida Affect Battery scores were
expressed as percentage correct response. Error
scores were also calculated for each emotion and
for each ‘same’ or ‘different’ stimulus type. Repeated
measures ANOVA was used to explore Group,
Trial Type (‘same’/’different’) and Condition (Facial
Affect/Emotional Prosody) effects. An alpha level of
0.05 was employed throughout.
Results
There were no significant group differences in age
(t [22] ¼ 0.4, p ¼ 0.721), years of education (t [22] ¼
0.8, U ¼ 0.435), or gender (2 [1, n ¼ 24] ¼ 1.5,
p ¼ 0.291). As expected, there was a significant
difference in MMSE scores (t [13.4, equal variances
not assumed] ¼
10.5, p ¼ 0.000). There was no
significant difference between the means for the
general population of older adults taken from norms
(Bowers et al., 1991; Crum et al., 1993) and the HOA
group on either FAB (t [23] ¼ 1.3, p ¼ 0.223) or
MMSE (t [576] ¼ 1.1, p ¼ 0.212). A repeated mea-
sures ANOVA of Group (HOA/AD) by Test (FAB/
MMSE) using percentage correct scores was con-
ducted to evaluate the group by score type interaction.
The FAB scores held up well relative to MMSE
scores in the AD group by comparison with the HOA
group as revealed by the significant interaction term
(Group by Test; F [1,22] ¼ 67.9, p ¼ 0.000). Unsur-
prisingly, there were also significant main effects
of Group (F [1,22] ¼ 15.3, p ¼ 0.000) and of Test
(F [1,22] ¼ 15.2, p ¼ 0.001).
Group comparisons
There was a significant difference between AD and
HOA groups on total FAB scores (t [22] ¼
5.2,
p ¼ 0.000). With alpha set at 0.05, power calculated
from total FAB scores was 0.98, suggesting that,
despite small sample sizes, the study was adequately
powered to find a true Group difference. Indepen-
dent samples t-tests for each subtest and for facial,
prosody and cross-modal subtotals revealed signifi-
cant differences between individuals with AD and
HOA in Facial Affect Mean Total performance, in
Facial Affect Selection and in all prosodic tasks apart
from Non-Emotional Prosody. No other facial affect
tasks produced significantly different performance.
There were also individual subtest and overall score
differences between the groups in cross-modal tasks.
Table 2 gives mean, SD, range, and significance
values for all independent samples t-tests for all
measures.
Facial and prosodic task differences
A two factor ANOVA of Task Type (Facial Affect
Mean Total/Prosody Mean Total) by group (AD/
HOA) for mean percentage correct performance
revealed that both healthy participants and those with
AD found Prosody tasks more difficult than Facial
 Emotion processing in Alzheimer’s disease 225
TABLE 2. Descriptive statistics for FAB scores expressed as percentage correct, for each participant group with
significance values
Mean (SD), range HOA n ¼ 12 AD n ¼ 12 Sig.
Facial Tasks
1. Facial Identity Discrimination 93.8 (6.4), 85.0–100 91.7 (4.9), 85.0–100 0.383
2. Facial Affect Discrimination 90.8 (5.1), 85.0–100 88.8 (4.3), 85.0–95.0 0.295
3. Facial Affect Naming 87.9 (4.5), 80.0–95.0 85.8 (6.0), 75.0–95.0 0.345
4. Facial Affect Selection 92.5 (6.2), 80.0–100 85.8 (5.6), 75.0–95.0 0.011
5. Facial Affect Matching 88.3 (6.2), 75.0–95.0 84.6 (5.8), 75.0–90.0 0.139
Facial Affect Mean Total 90.7 (3.1), 86.0–97.0 87.3 (3.4), 80.0–91.0 0.020
Prosody Tasks
6. Non-Emotional Prosody Discrimination 87.3 (8.5), 75.0–100 84.2 (4.3), 81.0–94.0 0.262
7. Emotional Prosody Discrimination 95.0 (4.3), 90.0–100 87.5 (8.4), 75.0–100 0.011
8a. Name Emotional Prosody 87.3 (6.3), 70.0–95.0 80.0 (3.7), 75.0–85.0 0.002
8b-C. Conflicting Emotional Prosody (congruent) 87.8 (8.8), 72.0–100 69.9 (12.1), 50.0–89.0 0.000
8b-I. Conflicting Emotional Prosody (incongruent) 70.8 (11.6), 55.0–89.0 42.5 (12.7), 22.0–67.0 0.000
Prosody Mean Total 85.6 (3.9), 79.0–91.2 72.8 (5.2), 66.0–83.8 0.000
Cross modal Tasks
9. Match Emotional Prosody to Emotional Face 86.7 (4.4), 80.0–95.0 78.3 (5.8), 70.0–85.0 0.001
10. Match Emotional Face to Emotional Prosody 84.6 (3.3), 80.0–90.0 74.2 (7.6), 60.0–90.0 0.001
Cross Modal Mean Total 85.6 (2.6), 82.5–92.5 76.3 (6.1), 65.0–87.5 0.000
FAB Total 87.3 (2.6), 82.5–91.9 79.3 (4.7), 72.5–88.0 0.000

Affect tasks (Main effect of task; F [1,22] ¼ 137.9,
p ¼ 0.000). Overall, HOA participants performed
better across all tasks than AD participants (Main
effect of Group; F [1,22] ¼ 14534.2, p ¼ 0.000).
However, there was also a Group by Task Type
interaction (F [1,22] ¼ 32.3, p ¼ 0.000) indicating
that AD participants found Prosody tasks relatively
more difficult than Facial Affect tasks and this
difference was greater than that found in HOA
participants. Analysis of covariance indicated that
this Task Type effect may relate to the severity of
cognitive deficit, since the Main effect disappeared
when MMSE performance was covaried out (F < 1),
as did the Main effect of Group (F < 2). But the
interaction of Task and Group remained significant
(F [1,21] ¼ 10.4, p ¼ 0.004), suggesting that differ-
ences in response to the facial and prosodic tasks
were not solely secondary to cognitive deficits.
Facial and prosody identity discrimination (subtests
1 and 6)
No significant Group differences (F < 1) and no
significant Trial Type (‘same’/different’) by Group
interactions (F < 1) were found in Facial Identity
Discrimination. However, there was a significant
difference across both groups in discriminating
‘same’ and ‘different’ faces (‘same’: AD: M ¼ 1.3,
SD ¼ 1.0; HOA: M ¼ 0.9, SD ¼ 1.2; ‘different’: AD:
M ¼ 0.4, SD ¼ 0.5; HOA: M ¼ 0.3, SD ¼ 0.9; Main
effect of Trial Type; F [1,22] ¼ 5.94, p ¼ 0.023). This
same pattern of no Group differences (F < 2) and
no interaction (F < 1), but a significant difference
between ‘same’ and ‘different’ identity discrimination
across both groups was also found in Non-Emotional
Prosody Discrimination (‘same’: AD: M ¼ 2.2,
SD ¼ 0.9; HOA: M ¼ 1.6, SD ¼ 1.4; ‘different’: AD:
M ¼ 0.3, SD ¼ 0.9; HOA: M ¼ 0.4, SD ¼ 0.9; Trial
Type; F [1,22] ¼ 15.77, p ¼ 0.001). In a three way
analysis of Group (HOA/AD) by Condition (Facial
Identity/Prosody Identity Discrimination) by Trial
Type (‘same’/different’), there was no significant
main effect of Group nor any significant interaction
terms with Group (all F < 1). There were, however,
significant main effects of Trial Type (F [1,22] ¼ 9.8,
p ¼ 0.005) and of Condition (F [1,22] ¼ 13.8,
p ¼ 0.001), as well as a significant interaction term
(F [1,22] ¼ 6.3, p ¼ 0.020). Overall, these results
revealed that HOA and AD participants were equally
good at the perceptual discrimination of neutral faces
and neutral voices, and that both found ‘same’ faces
or voices more difficult to discriminate than ‘different’
faces or voices. There were, however, no Group
differences in the ability to discriminate between faces
and voices, suggesting that any deficits found in the
ability to identify emotions were unlikely to be a result
of perceptual dysfunction.
Facial and prosody emotion discrimination (subtests
2 and 7)
No significant Group differences (F < 2) and no
significant Trial Type differences were found in
Facial Affect Discrimination (‘same’/different’;
F < 1). That is, overall both groups made similar
proportions of errors. However, there was a just
significant interaction of Group and Trial Type
(F [1,22] ¼ 4.7, p ¼ 0.041) indicating that, on aver-
age, AD participants found ‘different’ trials slightly
harder than ‘same’ trials, whilst the reverse was true
for HOA participants. For Emotional Prosody
Discrimination, an analysis of Trial Type (‘same’/
different’) by Group (AD/HOA) showed that AD
participants made significantly more errors, overall,
226 R. S. Bucks & S. A. Radford
than HOA participants (F [1,22] ¼ 7.6, p ¼ 0.011),
that both groups made significantly more ‘same’ than
‘different’ errors (F [1,22] ¼ 8.0, p ¼ 0.010) and, that
this ‘same’/’different’ trial distinction was somewhat
more marked in AD than in HOA participants as
revealed by a significant interaction (F [1,22] ¼ 8.0,
p ¼ 0.010). In a three way analysis of Group by
Condition (Facial Affect/Emotional Prosody
Discrimination) by Trial Type (‘same’/’different’),
there was a significant main effect of Group
(F [1,22] ¼ 6.9, p ¼ 0.015) and a significant three
way interaction (F [1,22] ¼ 11.3, p ¼ 0.003). How-
ever, the two-way interactions of Group by Condition
and Group by Trial Type were non-significant (both
F < 1). There was also a significant main effect of
Condition (F [1,22] ¼ 6.0, p ¼ 0.023) but not of Trial
Type (F < 1). The interaction terms of Trial Type
by Condition and Trial Type by Group both failed
to reach significance at the 5% level (Trial Type
by Condition; F [1,22] ¼ 3.9, p ¼ 0.060: Trial Type
by Group; F [1,22] ¼ 3.2, p ¼ 0.086). Post hoc com-
parisons revealed significant group differences only
for ‘different’ emotional face discrimination (AD:
M ¼ 1.4, SD ¼ 1.1; HOA: M ¼ 0.6, SD ¼ 0.8;
t [22] ¼ 2.2, p ¼ 0.043) and for ‘same’ emotional
voices (AD: M ¼ 2.3, SD ¼ 1.9; HOA: M ¼ 0.5,
SD ¼ 0.7; t [13.8] ¼ 3.1, p ¼ 0.009, equal variances
not assumed). No significant Group differences were
found for ‘same’ emotional faces (AD: M ¼ 0.8,
SD ¼ 0.7; HOA: M ¼ 1.3, SD ¼ 0.8; t [22] ¼
1.4,
p ¼ 0.179) or ‘different’ emotional voices (AD:
M ¼ 0.3, SD ¼ 0.5; HOA: M ¼ 0.5, SD ¼ 0.8;
t [22] ¼
0.9, p ¼ 0.355).
These results suggest that both groups found
emotional voice discrimination tasks more difficult
than emotional face discrimination, and that this
pattern was the same for all participants. However,
although, overall, ‘same’ and ‘different’ faces pro-
duced no significant differences in performance, the
two groups actually responded differently to them.
‘Same’ emotional voice discrimination was more
difficult for those with AD than HOA participants,
whereas for faces it was ‘different’ emotional faces
that were more difficult for those with AD to
discriminate.
Facial affect and emotional prosody naming (subtests
3 and 8a)
There was a significant main effect of Group (AD/
HOA; F [1,22] ¼ 8.7, p ¼ 0.007) and of Condition
(Facial Affect/Emotional Prosody Naming;
F [1,22] ¼ 5.1, p ¼ 0.034) on percentage correct
naming. The interaction term failed to reach
significance (F [1,22] ¼ 3.2, p ¼ 0.086). Separate
analyses of Group (AD/HOA) by Emotion (happi-
ness, sadness, anger, fear, or neutral) were con-
ducted for Facial Affect and Emotional Prosody
Naming. For Facial Affect Naming, there was no
significant Group difference, nor any interaction
between Group and Emotion (both F < 1). There
was, however, a significant main effect of Emotion
(F [4,22] ¼ 3.4, p ¼ 0.013). By contrast, for
Emotional Prosody Naming, despite no significant
main effect of Emotion (F [4,22] ¼ 2.2, p ¼ 0.075)
and no interaction of Group and Emotion (F < 1),
there was a significant main effect of Group (F
[1,22] ¼ 11.6, p ¼ 0.003). A three way analysis of
Group (AD/HOA) by Condition (Facial Affect/
Emotional Prosody Naming) by Emotion (happi-
ness/sadness/anger/fear/neutral) for percentage
correct naming, demonstrated significant Group
differences (AD/HOA; F [1,22] ¼ 8.6, p ¼ 0.008),
and a significant main effect of Emotion (F [4,22] ¼
5.1, p ¼ 0.001), but no significant interaction terms
(all F < 2). Despite significant Group differences,
however, post hoc comparisons of Group perfor-
mance on each of the emotions revealed no
significant differences (Facial Affect Naming:
Happiness, t [22] ¼ 1.5, p ¼ 0.166, equal variances
not assumed; Sadness, t [22] ¼ 1.4, p ¼ 0.171; Anger,
t [22] ¼
1.1, p ¼ 0.264; Fear, t [22] ¼ 0.5, p ¼
0.618; Neutral, t [22] ¼ 0.2, p ¼ 0.807; Emotional
Prosody Naming: Happiness, t [22] ¼ 1.7, p ¼ 0.111,
equal variances not assumed; Sadness, t ¼ 0; Anger,
t [22] ¼ 0.3, p ¼ 0.784; Fear t [22] ¼ 1.5, p ¼ 0.155;
Neutral, t [22] ¼ 1.1, p ¼ 0.303). These results indi-
cate that, overall, AD performance was worse than
HOA performance and that Emotional Prosody
Naming was more difficult than Facial Affect
Naming for both groups. However, there was no
interaction between the two and no significant
differences in the naming of different emotions in
either condition. Figure 1, shows the mean scores
graphically.
Facial affect selection and facial affect matching
(subtests 4 and 5)
Group comparison of percentage correct perfor-
mance on Facial Affect Selection and Facial Affect
Matching tasks revealed a significant difference only
on Affect Selection (t [22] ¼
2.8, p ¼ 0.011: Facial
Affect Matching; t [22] ¼
1.5, p ¼ 0.139), which
was removed by covarying out MMSE performance
(F < 1), but not by covarying out Facial Identification
Discrimination performance (F [1,21] ¼ 6.8, p ¼
0.016). These results suggest that AD participants
found Selection more difficult than Matching of
Facial Affect stimuli, but this may have been a
feature of the cognitive load of the tasks rather than
of the ability, perceptually, to identify the faces.
Comparison of performance between the two
Groups on the different Emotions (happiness, sad-
ness, anger, fear, neutral), revealed a significant
main effect of Group (F [1,22] ¼ 7.7, p ¼ 0.011) and
of Emotion (F [4,22] ¼ 4.1, p ¼ 0.004) for Facial
Affect Selection, but no interaction (F < 2). By
 Emotion processing in Alzheimer’s disease 227
1.5

Mean errors
1

0.5

0
Happiness

Sadness

Anger

Fear

Neutral

Happiness

Sadness

Anger

Fear

Neutral
Facial Affect Naming Emotional Prosody Naming

HOA AD

FIG. 1. Mean errors by participant group for Facial Affect and Emotional Prosody Naming (subtests 3 and 8a).

1.5

1
Mean errors

0.5

0
Happiness

Fear

Fear
Anger

Anger
Neutral

Neutral
Sadness

Sadness
Happiness

Facial Affect Selection HOA AD Facial Affect Matching

FIG. 2. Mean errors by participant group for Facial Affect Selection and Facial Affect Matching (subtests 4 and 5).

contrast, for Facial Affect Matching, there was only a 0.060). Pair-wise comparisons of the ‘congruent’
significant main effect of Emotion (F [4,22] ¼ 3.0, and ‘incongruent’ trials revealed significant Group
p ¼ 0.023), the main effect of Group (F [1,22] ¼ 2.7, differences in both tasks (Congruent; t [22] ¼
4.1,
p ¼ 0.116) and the interaction term (F < 1) proving p ¼ 0.000: Incongruent; t [22] ¼
5.7, p ¼ 0.000).
non-significant. These results suggest that both These results suggest that both groups found sen-
groups found some emotions more problematic tences in which the emotional tone conflicted with
than others. However, there were no significant the meaning more difficult than those where the
differences in the way the groups selected or meaning and tone were congruent, and that AD
matched different emotions. Figure 2 shows errors participants found all sentences more difficult than
on the two tasks by Emotion and by Group. HOA participants. In addition, there was a trend
towards individuals with AD finding emotional tone
‘incongruent’ with the meaning of a sentence,
Conflicting emotional prosody (congruent or relatively more problematic than HOA participants.
incongruent: subtest 8b)

Analysis of Group (AD/HOA) by Task Type (con- Cross-modal tasks: Match Emotional Face to
gruent/incongruent trials) for percentage correct Emotional Prosody, Match Emotional Prosody
performance on Conflicting Emotional Prosody to Emotional Face (subtests 9 and 10)
revealed a significant Group difference in overall
performance (F [1,22] ¼ 36.1, p ¼ 0.000), and a sig- Analysis of the cross-modal tasks revealed that,
nificant difference, overall, in whether the emotional although AD participants performed worse overall
prosody was ‘congruent’ or ‘incongruent’ with the than HOA participants (F [1,22] ¼ 24.0, p ¼ 0.000),
meaning of the sentences spoken (F [1,22] ¼ 71.7, and Matching Emotional Faces to Emotional
p ¼ 0.000). The interaction, however, just failed to Prosody was slightly more difficult for both groups
reach statistical significance (F [1,22] ¼ 3.9, p ¼ than Matching Emotional Prosody to Emotional
228 R. S. Bucks & S. A. Radford
Faces (F [1,22] ¼ 6.7, p ¼ 0.016), the two Tasks were
equally difficult for both groups as revealed by a non-
significant interaction term (F < 1). Analysis of
covariance with MMSE as the covariate rendered
all effects non-significant (all F < 1), suggesting that
cognitive features of the tasks may have contributed
significantly to Group and Task differences.
Response to different emotions
To explore overall differences in emotion processing
performance for the five different emotions, the
number of errors made in emotion discrimination
for each Emotion (happiness, sadness, anger, fear,
neutral) was totalled across Facial and Prosody tasks
separately (subtests 3, 4, 5, and 8a). A three-way
analysis of Group (AD/HOA) by Task (Facial/
Prosody) by Emotion (happiness/sadness/anger/
fear/neutral) revealed a significant main effect of
Emotion (F [4,22] ¼ 13.6, p ¼ 0.000) and of Group
(F [1,22] ¼ 12.9, p ¼ 0.002), as well as a significant
interaction of Emotion and Task (F [4,22] ¼ 7.7,
p ¼ 0.000). However, there was no significant main
effect of Task (F < 1) and no other significant
interaction terms (all F < 1), suggesting that, overall,
there were no significant differences between error
rates of Facial and Prosody tasks. Post hoc, Group
comparisons revealed that only in the discrimina-
tion of happiness on Facial tasks (t [16.5] ¼ 2.4,
p ¼ 0.030, equal variances not assumed) was there a
significant Group difference. All other comparisons
failed to reach statistical significance (Facial Affect
Tasks: sadness, t [22] ¼ 0.9, p ¼ 0.339; anger,
t [22] ¼ 1.5, p ¼ 0.157; fear: t [22] ¼ 1.0, p ¼ 0.329;
neutral: t [22] ¼ 0.4, p ¼ 0.681; Emotional Prosody
Tasks: happiness t [22] t ¼ 1.7, p ¼ 0.111, equal vari-
ances not assumed; sadness, t ¼ 0; anger, t [22] ¼
0.3, p ¼ 0.784; fear, t [22] ¼ 1.5, p ¼ 0.155; neutral,
t [22] ¼ 1.1, p ¼ 0.303).
Discussion
A number of important findings have been demon-
strated by this study. The first is that individuals with
AD showed significant deficits in emotion processing
ability, by comparison with healthy older adult
controls, primarily for prosodic tasks. However,
overall, emotion-processing ability was preserved
relative to general cognitive ability in AD. This is in
marked contrast to the findings of Cadieux & Greve
(1997), in whose study individuals with AD demon-
strated preserved emotional prosody processing
relative to healthy controls but impaired facial affect
processing. They argued that this was a result of the
differences between facial and prosody tasks used in
both studies. The facial stimuli were ‘still’ photo-
graphs, and thus presented emotions as static visual
patterns. In contrast, the prosodic stimuli were
dynamic, audiotaped expressions, in which the task
was much more similar to the kind of emotional
prosody an individual would encounter in the natural
environment. In their view, deficits in facial affect
processing, therefore, might be a consequence of early
changes in visual-perceptual processing which
affected emotional processing but not identity deci-
sions. This argument may be supported by a recent
study of visual exploration of facial emotion in AD
(Ogrocki et al., 2001) which found that individuals
with AD used different processing strategies when
looking at photographs of emotional faces; fixating
less on the face and eye area and more on off-face
areas than healthy controls. These differences did not,
however, produce significantly poorer emotion iden-
tification performance in this study. Moreover,
covarying out identity performance did not remove
significant group differences in emotional prosody
performance. Cadieux and Greve (1997) have argued
that this may be due to insensitivity of the identity
tasks to early perceptual breakdown. Further investi-
gation using more ecologically valid facial stimuli,
such as standardized video images, should offer a
better contrast to taped prosodic tasks, and more
sensitive measures of perceptual function, both facial
and prosodic, might help to clarify these somewhat
inconsistent findings.
The FAB subtest performance
Analysis of the individual subtests, including com-
parisons of equivalent facial affect and prosody tasks,
and comparisons of errors in ‘same’ or ‘different’
stimuli revealed some interesting findings. When
asked to discriminate affect in faces and voices, there
were no Group differences for facial stimuli, although
Prosody Discrimination did produce poorer perfor-
mance in AD than HOA participants. Interestingly,
in Facial Affect Discrimination ‘different’ emotional
faces proved more problematic than ‘same’ faces for
those with AD. By contrast, in Prosody Discrimina-
tion, both groups found ‘same’ emotional voices
slightly harder to discriminate than ‘different’ voices
and this pattern was slightly more marked for those
with AD. This pattern of findings is difficult to
explain and the modest interactions may be a feature
of small numbers of errors rather than reflecting
some significant feature of emotion discrimination
performance in AD, per se.
Facial Affect Naming appeared to be unproblem-
atic for the AD group, whereas Emotional Prosody
Naming proved more difficult. However, both
groups found the Prosody Naming Task more
difficult than the equivalent Facial Affect Naming
task. This may reflect a general finding that prosody
tasks are simply more difficult than equivalent facial
affect tasks, perhaps reflecting the requirement for
processing in multiple structures which are distrib-
uted within both the left and right hemispheres
(Adolphs, 2002).

Facial Affect Selection and Matching also proved
more problematic for those with AD than HOA
controls; with Selection more difficult than Match-
ing. It is possible that these differences reflect a
difference in task demands, since, in Selection, the
participant must choose a face that matches a verbal
label, whereas, in Matching, they must match two
emotional faces. Indeed, it may be argued that there
is no one-to-one correspondence of an emotion word
to a facial expression, making the selection task
considerably more difficult than the matching task.
As Russell (1995) and Ekman (1994) have both
proposed, emotion words, such as anger, are short-
hand for entire ‘scripts’ which include a collection of
events and processes, including physiological and
motor responses, memories, thoughts, images and
information processing. It is interesting, therefore,
that despite differences between the groups on the
two tasks, both groups responded similarly to the five
different emotions across both modalities. By neces-
sity, emotion-processing tasks, of the type exempli-
fied by the FAB have relied on participants
responding to verbal labels and verbal task demands.
Future research may wish to consider alternative
methods of assessing emotion processing which
obviate the need to use verbal labels. These might
include more sophisticated matching tasks in which
participants are required to match a target facial
expression with one of a number of facial expressions
each of which may vary in the intensity of the
emotion demonstrated.
In the cross-modal tasks, task complexity only
magnified the problem for those with AD. Both
groups found Matching Emotional Faces to
Emotional Prosody more difficult than the reverse
matching. However, there were task differences in
memory load that may account for this apparent
difference in performance. In the Match Emotional
Prosody to Emotional Faces task as soon as a
sentence is heard it can be matched with one of the
faces. In the Match Emotional Face to Emotional
Prosody task, the participants had to hold all three
sentences in memory before matching one of them to
the target face. This suggestion is supported by the
finding that covarying out general cognitive ability
removed the significant Group difference.
Finally, in the Conflicting Emotional Prosody task,
all participants found sentences for which the
emotional tone conflicted with the meaning more
difficult to judge than those where the meaning and
the tone were congruent. There was also a trend
towards individuals with AD finding incongruency
relatively more difficult than congruency than HOA
participants. Such incongruency may be common in
caring situations when, for example, a frustrated
caregiver says something to an individual with AD in
an angry tone of voice, the meaning of which is
meant to be pleasant. Indeed, incongruency may be
magnified since face, voice and meaning may all
conflict.
Emotion processing in Alzheimer’s disease 229
Different emotions
When comparing discrimination ability for the differ-
ent emotions, only facial tasks involving ‘happiness’
judgements gave rise to significantly more errors in
the AD than the HOA group: although, overall error
rates were very low. Indeed, total errors for ‘sadness’,
‘anger’, ‘fear’ and ‘neutral’ emotions were the same
as or greater than for ‘happiness’ in both groups. It
should be noted, however, that individuals from
both the HOA and AD groups found some of the
facial fear judgements problematic. This was reflected
in particular in comments made by individuals with
AD, for example: ‘She looks surprised, but I don’t
have that on my list’; ‘I want to say surprised, but it is
not here’.
Unfortunately, the FAB does not contain the
emotions of ‘disgust’, ‘surprise’ or ‘contempt’,
which have been considered in other emotion proc-
essing research. Given that some of the participants
with AD wanted to choose ‘surprise’ for fear stimuli,
future studies may wish to add these other emotions.
Nonetheless, there were no overall Group differences
in performance for fear stimuli either for facial or
prosodic tasks. This finding contrasts with a study
in which AD participants found facial expressions of
fear and contempt more difficult to process than
controls (Lavenu et al., 1999). These findings are also
intriguing when one considers the extensive evidence
relating amygdala and temporal lobe damage to
problems with responses to facial fear stimuli (e.g.,
Schmolck & Squire, 2001), although, damage to
temporal lobe structures, including the amygdala,
does not appear to be sufficient to produce deficits in
recognizing emotions from prosody (e.g., Adolphs
et al., 2001b). Given the known extent of histopatho-
logical and atrophic damage to the amygdala in AD
(Braak & Braak, 1991; van Hoesen, 1997) more
marked deficits in the processing of facial fear stimuli
were expected. However, the relationship between
the extent of amygdala damage and facial emotion
processing deficits is not linear (Adolphs et al., 2001a;
Shimokawa et al., 2001) and considerable variation
has been found between tasks (Schmolck & Squire,
2001). In particular, despite relatively intact proces-
sing of facial stimuli showing fear in this study,
Hamann, Monarch and Goldstein (2002) recently
found evidence of a marked impairment in fear
conditioning in individuals with AD not associated
with the MMSE scores. This is, clearly, an area for
future research.
In sum, these findings confirm that some of the
decrements in performance seen in previous studies
of emotion processing in AD may have had more to
do with general cognitive deficits, than deficits in
emotion processing per se. This finding is also
supported by the work of Roudier et al., (1998)
who found preservation in discrimination of emo-
tional facial expression. However, Roudier et al.,
(1998) also found that identity discrimination was
230 R. S. Bucks & S. A. Radford
impaired in AD; a finding not supported by this
study. Consideration of the specific tests used offers
some explanations. In the FAB all the faces used in
the Facial Identity Discrimination Task were neutral.
In Roudier et al., (1998) the faces contained the same
or a different emotion. Two possible explanations
arise from this difference. The first is that individ-
uals with AD have difficulties with Facial Identity
Discrimination but only when faces are presented
with different emotions. The second is that the
participants in the study by Roudier et al., (1998)
were confused about the nature of the task. In the
study by Roudier et al., (1998), participants were
required to attend to facial identity whilst ignoring
emotional expression and this may have led partici-
pants to believe they must distinguish between faces
on the basis of emotion as well as identity. Our
findings suggest the latter explanation. Our findings
are consistent, however, with a study by Shimokawa
et al., (2000), in which participants with AD
performed better on a test of emotional comprehen-
sion using cartoons than participants with vascular
dementia.
Implications for care
The evidence from this study suggests that, while
those suffering from mild-to-moderate AD may be
impaired on tasks of general cognitive ability, they
retain much of their ability to recognize non-verbal
emotional cues in faces and voices. These findings
have implications both for the behavioural presenta-
tion of the individual and for clinical interventions.
In another study in AD, performance on a series of
emotional comprehension tasks was a good predictor
of an ‘interpersonal behaviour’ measure (assessing
indifference to interpersonal relationships and diffi-
culty in treatment or management) as rated by care
staff (Shimokawa, et al., 2001). By contrast, the
MMSE was not a good predictor of these behaviours.
Behavioural disturbance is often seen as a key
stressor for caregivers. It is an important considera-
tion that this disturbance may arise, not as a
consequence of the severity of the cognitive deficit
that individuals experience, but as a result of the
degree to which they can understand and, perhaps,
predict the emotions of others.
Psychological approaches to AD have an extensive
history based on ‘management’, with the aim of
ameliorating certain aspects of the disorder, decreas-
ing disability and the frequency of behavioural
difficulties (Woods & Britton, 1985), and interven-
tions have historically targeted these aspects of the
disease, to the exclusion of other concomitant
difficulties (Kitwood, 1997). Over the last 10 years,
however, there has been a growing shift of emphasis
away from managing the individual as if they are a
passive recipient of both the disease and our care of
them, to seeing them as active participants in their
own care (Downs, 1997; Post, 2001; Woods, 2001),
who retain a sense of self long into the disease
process (Mills & Coleman, 1994; Sabat & Harre,
1992). To accumulating evidence that both the self
and the expression of emotion (Magai et al., 1996)
are preserved even late into AD, can now be added
the possibility that the perception of emotions is also
relatively preserved. Understanding these factors
provides support for a large number of interventions.
On a day-to-day level, relative preservation of the
comprehension of emotions in others provides an
opportunity to improve communication. Firstly, this
substantiates the importance of emphasizing the non-
verbal (both facial and prosodic) qualities of commu-
nications in order to improve understanding in people
with AD. It also highlights the importance of keeping
content and affect congruent. Finally, carers may be
encouraged to pay more attention to the person with
AD’s own emotional expression as it may be more
reliably meaningful than their words: both because it
reflects their pre-morbid personality (Magai et al.,
1997) and because it may well be a response to
accurate perceptions of emotions in others.
Clearly, these principles can be applied in all
caring settings, through general communication to
specific interventions. For example, the relative
preservation of emotion processing and emotional
expression also supports the growing number of
psychological interventions being offered to individ-
uals with AD. In mild stages of the disease these
might include support groups (LaBarge & Trtanj,
1995; Snyder, Quayhagen & Shepherd, 1995),
psychotherapy, including grief or loss work (Bender
& Cheston, 1997), or cognitive-behavioural inter-
ventions (see Cheston, 1998 for a review; Scholey &
Woods, 2003). Viewed from such a perspective,
traditional therapies such as validation (Feil, 1993),
or reminiscence (Greene, Ingram & Johnson, 1993),
along with physical therapies such as massage and
music or sensory stimulation (Pollack & Namazi,
1992; Spaull, Leach & Frampton, 1998) gain new
legitimacy; previously a problem despite their clear
benefits ( James & Ballard, 2001). In addition, the
results published here support newer approaches
such as the Interacting Cognitive subsystems (ICS)
model ( James, 2001). The ICS model proposes that
language based, conscious awareness is only one
form of awareness, and that most cognitive informa-
tion is processed using non-language based systems.
The ICS emphasizes the importance of non-verbal
skills. Indeed, the ICS model, as applied to indi-
viduals with dementia, asserts that ‘it is often not the
content of the speech that determines the discus-
sant’s feeling about a conversation, but how the infor-
mation is conveyed (speaker’s tone, body posture,
facial expression)’ ( James, 2001a, pp. 33). Finally,
even when intervening at a more cognitive level,
clinicians may be able to devise interventions using
implicit memory, which is also relatively preserved
in AD (Backman, 1996) using retrieval cues provided

by facial expression of emotion or tone of voice
(Herlitz, Lipinska & Backman, 1992).
Acknowledgements
The authors wish to thank Professor Gordon
Wilcock (Department of Care of the Elderly,
University of Bristol) and the staff and patients of
The Bristol Memory Disorders Clinic, Blackberry
Hill Hospital for their assistance. The Bristol
Memory Disorders Clinic is part of North Bristol
NHS Healthcare Trust. Thanks are also due to
Catherine Emmerson and Reg Morris. This study
was undertaken as part of Shirley Radford’s
Doctorate of Clinical Psychology. This study was
conducted whilst Romola Bucks was working at the
Bristol Dementia Research Group, Department of
Care of the Elderly, University of Bristol.
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