Neuropsychologia 41 (2003) 688701

Social cognition in frontotemporal dementia and Huntingtons disease

J.S. Snowden a, , Z.C. Gibbons a , A. Blackshaw a , E. Doubleday a , J. Thompson a,b ,
D. Craufurd b , J. Foster c , F. Happ d , D. Neary a
a

Cerebral Function Unit, Greater Manchester Neuroscience Centre, Hope Hospital, Salford M6 8HD, UK
b University Department of Medical Genetics, St. Marys Hospital, Manchester M13, UK
c Department of Psychology, University of Western Australia, Crawley, Perth, WA 6009, Australia
Social Genetic and Developmental Psychiatry Research Centre, Institute of Psychiatry, Kings College, London, UK
Received 19 February 2002; received in revised form 2 October 2002; accepted 2 October 2002

Abstract
Frontotemporal dementia (FTD) and Huntingtons disease (HD) are degenerative disorders, with predominant involvement, respectively
of frontal neocortex and striatum. Both conditions give rise to altered social conduct and breakdown in interpersonal relationships,
although the factors underlying these changes remain poorly defined. The study used tests of theory of mind (interpretation of cartoons
and stories and judgement of preference based on eye gaze) to explore the ability of patients with FTD and HD to interpret social situations
and ascribe mental states to others. Performance in the FTD group was severely impaired on all tasks, regardless of whether the test
condition required attribution of a mental state. The HD group showed a milder impairment in cartoon and story interpretation, and normal
preference judgements. Qualitative differences in performance were demonstrated between groups. FTD patients made more concrete,
literal interpretations, whereas HD patients were more likely to misconstrue situations. The findings are interpreted as demonstrating
impaired theory of mind in FTD, as one component of widespread executive deficits. In HD the evidence does not suggest a fundamental
loss of theory of mind, but rather a tendency to draw faulty inferences from social situations. It is concluded that social breakdown in FTD
and HD may have a different underlying basis and that the frontal neocortex and striatum have distinct contributions to social behaviour.
2002 Elsevier Science Ltd. All rights reserved.
Keywords: Frontotemporal dementia; Huntingtons disease; Social cognition, theory of mind; Behaviour

1. Introduction
Frontotemporal dementia (FTD) and Huntingtons disease
(HD) are degenerative brain disorders that affect frontostriatal systems. FTD is a predominantly neocortical disorder,
characterised by radical alterations in personality, emotions,
and social, interpersonal conduct [12,25,35,44,46,47,56].
Behavioural changes include disinhibition, tactlessness, and
loss of social proprieties [12,37,44,45,47]. Cognitive assessment typically shows deficits predominantly in frontal executive functions [47,57], indicating deficits in abstraction,
problem solving, attention, mental set shifting, sequencing,
and mental generation of information. Patients are not clinically amnesic, although formal memory test performance
is often inefficient, attributed to executive impairments.
Neuroimaging [48,62] and pathological studies [41]
of FTD demonstrate severe frontal and anterior temporal
Corresponding author. Tel.: +44-161-787-2561;
fax: +44-161-787-2993.
E-mail address: [email protected] (J.S. Snowden).

neocortical atrophy, which may be largely confined to orbital regions, or (particularly with progression of disease)
more widespread extending into anterior cingulate and dorsolateral frontal cortex. Modest pathological changes in the
striatum reflect the emergence of striatal neurological signs
usually relatively late in the disease course.
Huntingtons disease (HD) is a predominantly subcortical disorder, distinguished clinically by its characteristic
involuntary movements [30]. Patients social conduct is
altered, albeit less profoundly than in FTD, and there is
frequently severe breakdown in interpersonal relationships.
Patients are often described as self-centred, lacking in sympathy and empathy, and mentally inflexible, sometimes with
fixed ideas, which may not be consistent with the prevailing
view or available evidence. As in FTD deficits have been
reported in the processing of emotions [23,32,59]. Cognitive changes are predominantly in the realm of frontal
executive function [14], although generally less marked in
degree than in FTD, and memory impairment is ascribed
to inefficient encoding and retrieval strategies rather than a
primary failure of retention.

0028-3932/02/$ see front matter 2002 Elsevier Science Ltd. All rights reserved.
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J.S. Snowden et al. / Neuropsychologia 41 (2003) 688701

Pathological [40,63] and structural neuroimaging [6,38]

studies of HD have demonstrated marked atrophy of caudate and putamen, which form the dorsal part of the striatum or neostriatum. This is present even in the early stages
of disease [4], and has been reported in some studies in
pre-symptomatic individuals who carry the HD mutation [5].
Some frontal neocortical atrophy may also occur later in the
disease course [7], assumed to be at least partly (although
not necessarily exclusively) secondary to striatal differentiation [40].
Thus, FTD and HD represent complementary disorders
in which there is a virtual, although not exclusive, double
dissociation with respect to the distribution of degenerative
change within the frontal neocortex and striatum. FTD and
HD thus provide ideal models for the study of frontal-striatal
function. The striatum has traditionally been recognised for
its importance in the domain of motor functioning, in the
execution of learned motor plans [42]. Conditions such as
HD attest to its crucial role also in cognition. The identification of parallel and segregated frontal-subcortical circuits,
distinguished by their areas of origin in the frontal cortex
[3,43], has led to the notion that the striatum is intimately
linked functionally to the cerebral cortex. The assumption
is that analogous cognitive deficits may arise from disruption at different levels (i.e. frontal cortical or striatal) of the
circuit.
Commonalities between FTD and HD with respect to the
prominence of behavioural changes and pattern of cognitive
deficits are thus unsurprising. Nevertheless, it cannot be inferred that deficits underlying FTD and HD are identical.
Executive tasks make multiple demands, so that test scores
may mask fundamental differences in the reason for failure. Similarly, disordered social behaviour might have different underlying substrates. Comparative studies of FTD
and HD ought to clarify the nature of change in each condition. Moreover, in view of the predominance of frontal
neocortical changes in FTD and of striatal changes in HD,
such studies provide the potential for improving knowledge
of the relative contributions of the frontal lobes and striatum
in behaviour and cognition.
Traditional executive tasks do not capture the full range of
abnormalities in FTD and HD and may be a relatively poor
predictor of the patients functioning in daily life. Indeed,
some patients with FTD, in whom the pathology is confined
to the orbital regions of the frontal lobes, perform relatively
well on conventional executive tasks, despite impaired
judgement and gross breakdown in their social conduct in
daily life [39,57]. Such a finding is consistent with reports
that lesions of the orbital frontal lobes may give rise to
severe breakdown in social behaviour in the context of normal executive functioning [15,16,54]. In HD, disorganised
behaviour and breakdown in interpersonal relationships in
daily life are often prominent clinical features, outweighing
changes in neuropsychological test performance. There are
at least two factors that are likely to contribute to the relative
insensitivity of traditional tests to some of the changes in

689

FTD and HD. Traditional neuropsychological tests are structured and typically require a constrained set of responses.
By contrast, everyday life situations are open-ended, and
require self-generated structure and organisation. Secondly,
traditional tests are impersonal, whereas everyday life involves social interaction. Neuropsychological tasks that are
both open-ended and involve interpretation of social scenarios are likely to be particularly informative in FTD and HD
because they mirror the daily life situations in which FTD
and HD patients so dramatically fail. They may also have
the potential to reveal fundamental differences between FTD
and HD.
Recent years have seen an accumulation of literature on
social cognition [1,2]. A core component of social functioning is the capacity to attribute independent mental states to
others and to predict other peoples behaviour on the basis of their mental states, a capacity known as theory of
mind [9,36,51]. There is a growing body of evidence from
both neuroimaging [10,18,20,21,27] and brain lesion studies
[24,29,53,60,61] that the frontal lobes have a pivotal role in
theory of mind. However, to date there have been no direct
comparisons in performance on tests of social cognition between patients with predominantly frontal neocortical and
predominantly striatal pathology.
Clinical observation of patients with FTD and HD leads
to the prediction that performance on tests that require interpretation of event scenarios is likely to differ. FTD patients
typically lack insight into the change in their own behaviour
and appear oblivious of the effects that their behaviour has
on others, leading to the prediction that such patients show
a genuine loss of theory of mind. By contrast, at clinical interview HD patients may make pertinent and insightful remarks about the effects of their illness on a close relative
(e.g. It is hard on my husband having to do everything for
me. He must get very fed up). Such apparent cognisance
of others mental states leads to the prediction that social
breakdown in HD arises for reasons other than a primary
inability to ascribe mental states to others. In FTD, a purported problem in theory of mind is unlikely to be exclusive.
FTD patients commonly show concreteness of thought. A
concrete interpretation of events would be expected to be
manifest in a general difficulty in the interpretation of social
scenarios, even when they do not depend on attribution of
mental states.
The present study investigates the ability of FTD and
HD patients to interpret social situations and explores by
means of error analysis possible differences between the
two groups. The study involved four tasks drawn from the
literature on social cognition that have been used to address
theory of mind. The tasks differ with respect to their level
of difficulty. The cartoon and story tasks (tasks 13) make
relatively great mental demands on the patient raising the
possibility that they may exceed the capabilities of some patients for reasons that have little to do with social cognition
per se. The judgement of preference task (task 4) examines
the capacity for mental state attribution while minimising

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J.S. Snowden et al. / Neuropsychologia 41 (2003) 688701

executive demands. It was predicted that FTD patients

would show a general impairment, compared to normal, in
their ability to interpret situations, but that this should be
particularly pronounced when attribution of mental states
is required. It was anticipated that HD patients would show
impaired performance relative to normal, but to a lesser extent than FTD. It was predicted, however, that HD patients
would not show a disproportionate impairment in tasks
dependent upon mental state attribution compared to tasks
involving interpretation of non-social scenarios. The pattern of performance ought to clarify the nature of patients
deficits more precisely and may help to identify factors that
contribute to the breakdown in social functioning in FTD
and HD.

2. Methods
2.1. Participants
Two patient groups and a normal control group took part
in the study. Informed written consent was obtained from
participants and/or their next of kin. The study was granted
approval by the local Ethics Committee.
2.1.1. Frontotemporal dementia (FTD)
The FTD group comprised 13 consecutive patients, 9 men
and 4 women, referred to a Neurology Department Specialist Dementia Clinic who met clinical criteria for FTD [46].
Diagnosis was based on historical information, neurological examination and neuropsychological assessment, and
supported by structural (magnetic resonance) and functional
(single photon emission computerised tomography) brain
imaging. The presenting feature in all cases was personality change and all patients had demonstrable frontal executive impairments on cognitive evaluation. Patients were in
the mild to moderate stages of the disease, and were physically well. Neurological examination was entirely normal
in 10 patients. The remaining three patients showed a mild
degree of limb rigidity. Neuroimaging showed changes predominantly in orbital frontal cortex in nine patients, and
widespread frontal lobe changes in the remaining four patients. Demographic information and clinical features are
shown in Table 1. The patients had a mean Mini Mental
State Examination (MMSE) [19] score of 22. The table also
shows scores on category and letter fluency tests [58] (total

number of animals and words beginning with F generated in

1 min) and the number of categories achieved in the modified version of the Wisconsin Card Sorting test [49]. The low
scores highlight the presence of frontal executive deficits in
the FTD group.
2.1.2. Huntingtons disease (HD)
The HD group consisted of 13 consecutive patients, 5
males and 8 females, attending a regional HD clinic. In all,
the presence of HD had been confirmed by genetic testing
and all showed the characteristic choreiform movement disorder, and cognitive changes associated with the disorder.
Patients had a mean Total Functional Capacity score [55] of
9.5 indicating that they were in the mild to moderate stages
of disease. They had a mean motor deficit score of 26/124,
range 555, as measured by the Unified Huntingtons Disease Rating Scale (UHDRS) [31], consistent with mild to
moderate disease. Six patients were taking prescribed medications for the treatment of mood changes, particularly
irritability. The remaining seven patients were on no medication. No imaging data were available. A definitive diagnosis of HD can be made on the basis of the clinical features
and genetic test, so that neuroimaging was not clinically
justified.
Patient demographics and clinical data are shown in
Table 1. They were younger than the FTD patients (t =
3.5, P < 0.002), commensurate with the younger onset
age of HD, and they had been clinically symptomatic for
longer (t = 2.2, P = 0.04), consistent with the more protracted course of HD. The HD group did not differ from
the FTD group with respect to MMSE or category and
letter fluency scores. However, performance was less impaired on the Wisconsin Card Sorting test, as measured
by the greater number of categories achieved (t = 10.7,
P < 0.0001).
2.1.3. Controls
The control group consisted of 18 people who were
spouses of participants in the patient groups. All were
healthy individuals who had no history of neurological
disease, head injury or alcohol abuse. The control group
covered a wider distribution of ages than the two patient
groups (Table 1), reflecting the fact that they were drawn
from the spouses of both groups. The mean difference in
age between controls and the two patient groups did not
reach statistical significance.

Table 1
Demographic, clinical and neuropsychological characteristics
Group

Number

Male:female

Age (years)

Duration
illness

MMSE

Animals
per minute

F words
per minute

WCST
categories

FTD
HD
Control

13
13
18

9:4
5:8
8:10

60 (7)
50 (7)
49 (23)

3 (2)
6 (3)
n/a (n/a)

22 (6)
25 (3)
n/a (n/a)

12 (4)
14 (4)
n/a (n/a)

6 (5)
8 (4)
n/a (n/a)

1.4 (1.9)
5.5 (0.9)
n/a (n/a)

The data represent mean (S.D.).

J.S. Snowden et al. / Neuropsychologia 41 (2003) 688701

2.2. Task 1: single cartoon abstraction

2.2.1. Materials
The materials, taken from Happ et al. [28], consisted of
12 humorous cartoons. In six, designated mental cartoons,
the humour related to a cartoon characters mistaken belief
or deception, so that humour appreciation required inference
of a persons mental state. In one cartoon, for example, a
man is shown cuddling a young woman who is sitting on
his lap, while, with his free hand, he is tapping a ping-pong
ball with a bat. The humour lies in the fact that an older
woman sitting in the adjacent room, within earshot but out
of view of the couple, is deceived into believing that the man
is playing table tennis, whereas in reality he is otherwise
occupied. In six cartoons, designated physical and matched
for difficulty with the mental cartoons, the humour related
to physical properties or anomalies in the cartoon and did not
require inference of a persons mental state. For example, in
one cartoon, a line of musicians is shown entering the stage
door, each carrying a musical instrument case. One man
has no head, but is carrying a head-shaped instrument case.
Illustrative examples of cartoons are given by Happ [28].
2.2.2. Procedure
The cartoons were presented in randomised order, in accordance with Happ et al. [28], and subjects were asked to
describe what was funny about each. Responses were transcribed verbatim and the time taken to respond was recorded.
Subjects were prompted with anything else? to encourage as full a response as possible. Cartoons remained in full
view until their response was complete.
2.2.3. Scoring
Performance accuracy was measured using the scoring
system devised by Happ et al. [28]. Three points were
awarded for a full and explicit explanation, two points for
a partial or implicit explanation, one point for reference to
relevant parts of the cartoon, but without further explanation
and zero for patently incorrect responses including omissions. Examples of the marking criteria are given in Happ
et al. [28]. Scores for each test item were summated, yielding a total maximum score of 18 (6 3) for each of the two
cartoon types.
Errors, defined as responses yielding a less than perfect score, were further classified as follows: (i) omissions
(dont know responses), (ii) concrete responses (itemisation of elements without integration), (iii) descriptions (responses limited to a description of the cartoon, involving
integration of elements but no inferences that go beyond
the cartoons content), (iv) misconstructions (responses that
go beyond a description of the cartoons contents but involve drawing faulty inferences) and (v) partial responses
(responses that involve correct inferences but are incomplete
or implicit rather than explicitly stated). Accuracy measures
and error classification were rated independently by four
raters, who were blinded to clinical diagnosis. The ratings

691

used in the analyses were based on a consensus from the

four raters.
In addition to accuracy measures and error classification,
the total number of words contained in each response, and
the number of action verbs (e.g. walking, pushing) and mental state verbs (e.g. thinking, expecting) were calculated.
Word and verb counts were calculated by a single author
(ZG), and verified by two others. Calculations were made
blind to diagnosis.
2.3. Task 2: cartoon pairs
2.3.1. Materials
The materials, taken from Happ et al. [28], consisted of
10 cartoon pairs, one of which was humorous and the other
was not, having had the key humorous element replaced.
Five of the humorous cartoons were of a mental type, in
that appreciation of the humour depended on understanding
of a cartoon characters ignorance, false belief or act of
deception. Five humorous cartoons were of a physical type,
in that the humour was based on physical properties of the
cartoon and did not require inferences about a characters
mental state. Illustrative examples of cartoon pairs are given
by Happ [28].
2.3.2. Procedure
Cartoon pairs were presented side by side in accordance
with Happ et al [28], with the leftright order being
counter-balanced across items. Subjects were asked to select which cartoon of the pair they considered to be the
funny one. Accuracy of selection and time to respond were
recorded. Subjects were then asked to describe why the
cartoon was funny. As in the previous task, subjects were
cued with anything else? to elicit as full a response as
possible. Cartoons remained in full view until the response
was complete. Responses were scored as for task 1, in terms
of accuracy measure, error types and word and verb count.
2.4. Task 3: story comprehension
2.4.1. Materials
The materials were drawn from Happ et al. [28] and had
originally been adapted from a study of theory of mind in
autism [26]. They consisted of 16 short passages, 8 of which
were of a mental-type and 8 physical. The mental stories involved false belief, acts of deception, bluff and double
bluff and were followed by questions that required an inference about a characters thoughts, feelings or intentions.
The physical stories involved logical or practical situations,
and although the stories also contained people, questions required inferences about physical causation or logical consequence and not about a characters mental state.
2.4.2. Procedure
Participants were asked to read each passage silently, as
described by Happ [28], and to inform the examiner when

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J.S. Snowden et al. / Neuropsychologia 41 (2003) 688701

they had done so, following which a question related to

the passage would be asked. Subjects were advised to absorb as much of the information contained in the passage
as possible, as they would be unable to refer back to the
passage later. When participants indicated that they had assimilated the story the page was turned to reveal the question, which was read aloud to them. The question, but not
the story, remained in front of the subject during their response. Mental and physical stories were blocked and presented in counter-balanced order, in accordance with Happ
et al. [28]. The examiner recorded the time taken to study
the passage and the answers given.
The standardised scoring scheme devised by Happ et al.
[28] was adopted. Answers were credited with two points
for correct answers that gave a full and explicit account,
one point for partial or implicit answers and no points for
incorrect responses. Examples of stories and of the scoring
criteria are given in Happ et al. [28].
In addition, a classification scheme was devised to characterise the nature of errors, similar to that used in the cartoon tasks. Errors were recorded as omissions (dont know
responses), concrete responses (reiterations of parts of the
passage), descriptions (responses limited to a description of
the story, without drawing inferences), and misconstructions
(bizarre or incorrect inferences). As for the cartoon tasks,
the total number of words, the number of action verbs, and
the number of mental state verbs contained in each response
were calculated.
2.5. Task 4: judgement of preference
2.5.1. Materials
The task was based on one described previously by
Baron-Cohen et al. [8] and involved the ability to judge

preference based on eye gaze. Unlike the previous tasks

it involved a structured, forced-choice, rather than an
open-ended response. The materials consisted of 48 A4-size
cards presented in landscape format, each showing the cartoon outline of a face, positioned centrally and four coloured
pictures of items belonging to a single category (e.g. apple, strawberry, banana, pineapple) one in each of the four
corners of the card. The eye gaze of the face (upper-left,
lower-left, upper-right or lower-right) was directed towards
one of the four pictures. Across the 48 items, six object categories were used: cartoon characters, fruits, bakery items,
houses, jumpers, and cars, each category having eight exemplars. For the first 24 test items (arrow condition), a heavy
black arrow was also present, which pointed to one of the
pictures other than that towards which the faces eye gaze
was directed. The remaining 24 cards (neutral condition)
were a duplicate of the first 24, with the exception that no
arrow was present. The direction of eye gaze and the arrow
position was pseudo-random, occurring in each of the four
positions an equal number of times across the stimulus set.
An example of the test stimuli is shown in Fig. 1.
2.5.2. Procedure
Each card was presented individually, using a blocked presentation, the arrow condition being presented first. Participants were instructed to point to the one of the four pictures
on the card that the central face likes best. Responses were
recorded on a score sheet by the examiner. Participants were
not given feedback about their choices. On completion of the
task, participants whose responses did not accord with the
direction of eye gaze of the cartoon face were re-presented
with the stimuli and asked to point to the picture that the
face is looking at. They were also shown the four pictures
on a card devoid of face and arrow and asked to indicate

Fig. 1. Example of stimuli used in task 4 involving judgement of preference.

J.S. Snowden et al. / Neuropsychologia 41 (2003) 688701

which one of the four was their personal favourite. Choices

were recorded. The control looking at task was not administered to all subjects. The preference task was judged to
be so easy that it was expected to present no difficulty to a
normal adult. Given that a correct judgement of preference
implied knowledge of the item being looked at it seemed
superfluous, and perhaps slightly insulting, to ask also for a
looking at judgement. Nevertheless, the looking at task
was deemed critical for those people who had difficulty on
the judgement task, to distinguish specific problems in mental state attribution from general problems in attention or
other executive function.
The arrow condition and neutral condition were scored
separately, each item being credited one point if the patients
picture selection accorded with the direction of eye gaze of
the central face. Errors in the arrow condition were coded as
arrow if the participant had incorrectly selected the picture
corresponding to the direction of the arrow, favourite if the
participant had incorrectly chosen their personal favourite,
perseveration if the participant pointed to the same item
position as their immediately preceding response, and
random if an incorrect choice did not fit into any of the
above error types. The errors made in the neutral condition
were coded as above, but without the arrow error type.

3. Results
3.1. Task 1: single cartoon abstraction
3.1.1. Time taken to respond
The patient groups did not differ significantly in terms
of the time taken to respond for either mental or physical
cartoons.

693

3.1.2. Performance accuracy

Fig. 2 illustrates the mean scores for the cartoon explanations across groups and cartoon types. A repeated measures
ANOVA showed a main effect of group (F (2, 41) = 17.3,
P < 0.0001), but no effect of cartoon type, nor group by
cartoon-type interaction. Post hoc Tukey analyses showed
that controls performed significantly better than both FTD
(P < 0.0001) and HD patients (P = 0.004). There was a
trend towards better performance in HD compared to FTD
(P = 0.09).
3.1.3. Error type
A preliminary examination of error patterns showed that
error type was not influenced by cartoon type, so analyses of errors were based on a summation from both mental and physical cartoons. FTD patients made significantly
more omissions (t = 2.7, d.f. 29, P = 0.01) and concrete
responses (t = 4.1, d.f. 29, P < 0.0001) than the control group, and more concrete responses (t = 2.7, d.f. 24,
P = 0.01) than the HD group. In contrast, the HD patients made more misconstruction errors than both the control (t = 3.9, d.f. 29, P = 0.001) and the FTD (t = 3.8,
d.f. 4, P = 0.001) groups. When they made errors, control
subjects were more likely than the HD (t = 3.7, d.f. 29,
P = 0.001) and the FTD (t = 4.0, d.f. 29, P < 0.0001)
groups to produce partially correct responses. The following are examples of responses to the ping-pong cartoon,
described in Section 2.2.1, in which a man deceives an
older woman in the adjacent room into believing that he is
playing table tennis by tapping a ping-pong ball while he
cuddles his younger female companion. An FTD patients
concrete response consisted of: Hes bouncing the ball on
the table. An HD patients misconstruction response consisted of: Theyre having a bit of nooky while the wifes

Fig. 2. Mean accuracy scores for single cartoon interpretation (task 1) as a function of cartoon type.

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J.S. Snowden et al. / Neuropsychologia 41 (2003) 688701

sat in there. Shes thinking At least hes leaving me alone.

Peace!.
3.1.4. Word and verb count
A repeated measures ANOVA comparing the number of
words per response elicited by the three groups for the two
types of cartoon revealed a main effect of cartoon type
(F (1, 39) = 12.6, P = 0.001), but no effect of group nor
group by cartoon type interaction. Mental cartoons elicited
lengthier responses than physical cartoons.
A repeated measures ANOVA comparing the number of
action verbs produced by the three groups for the two cartoon
types showed no main effect of group, but a small effect of
cartoon type (F (1, 41) = 7.0, P = 0.01). More action verbs
were produced for physical than for mental cartoons. There
was no interaction effect of group by cartoon type.
A repeated measures ANOVA comparing the number of
mental state verbs produced showed a main effect of group
(F (2, 41) = 7.9, P = 0.001), a main effect of cartoon type
(F (1, 41) = 63.0, P < 0.0001), and an interaction effect of
group by cartoon type (F (2, 41) = 9.5, P < 0.0001). Post
hoc analyses showed that FTD patients produced significantly fewer mental state verbs than controls (P = 0.001).
Other group comparisons were non-significant. As expected,
mental cartoons elicited more mental state verbs than physical cartoons. The interaction effect resulted from a smaller
disparity in number of mental state verbs for the two cartoon
types in the FTD group (t = 2.1, P = 0.06) compared to
the HD group (t = 4.9, P < 0.0001) and controls (t = 7.1,
P < 0.0001).
3.1.5. Frequency analysis
The frequency with which overall performance accuracy
scores were superior or inferior in the mental compared
to the physical cartoon condition was calculated for each
group and frequency values were submitted to a Sign
test. FTD patients were significantly more likely to perform worse in the mental than the physical condition
(two-tailed test P < 0.01), whereas other groups showed
no significant bias.
3.2. Task 2: cartoon pairs
3.2.1. Choice of cartoon pair
The number of correct choices made by the three groups
for mental and physical cartoons is shown in Table 2. A
repeated measures ANOVA comparing the number of correct
Table 2
Correct selection of forced-choice cartoons
Group

Mental cartoons

Physical cartoons

FTD
HD
Control

3.2 (1.8)
4.1 (1.2)
4.6 (0.5)

1.8 (1.3)
3.4 (1.2)
4.6 (0.7)

The data represent mean (S.D.).

choices for the two cartoon types showed a main effect of

group (F (2, 41) = 19.6, P < 0.0001), and cartoon type
(F (1, 41) = 11.9, P = 0.001), and an interaction effect of
group by cartoon type (F (2, 41) = 3.9, P = 0.03). Post
hoc analyses revealed that controls were significantly more
accurate than the FTD patients (P < 0.0001), and there was
a trend towards greater accuracy of controls compared to HD
patients (P = 0.07). HD patients made more correct choices
than FTD patients (P = 0.002). More correct choices were
made for mental than physical cartoons, particularly in the
patient groups compared to controls.
3.2.2. Time taken to respond
A repeated measures ANOVA showed no difference in
response times in the three groups and there was no effect
of cartoon type on response time.
3.2.3. Accuracy of interpretation
Fig. 3 illustrates scores for the three groups across cartoon types. A repeated measures ANOVA showed a main
effect of group (F (2, 41) = 21.4, P < 0.0001), but no
effect of cartoon type or group by cartoon-type interaction.
Post hoc analyses showed that controls performed significantly better than both FTD (P < 0.0001) and HD patients
(P = 0.007). HD patients achieved higher scores than FTD
patients (P = 0.01).
3.2.4. Error type
A preliminary examination of error patterns showed that
error type was not influenced by cartoon type, so analyses
of errors were based on a summation from both mental and
physical cartoons. FTD patients made more omission and
single element concrete responses than HD patients (t = 2.2,
d.f. 23, P = 0.04; t = 3.4, d.f. 23, P = 0.003, respectively)
and controls (t = 3.3, d.f. 28, P < 0.003; t = 3.8, d.f. 28,
P = 0.001, respectively). HD patients, by contrast, made
more misconstruction errors than FTD patients (t = 3.7, d.f.
23, P = 0.001) and controls (t = 4.2, d.f. 29, P < 0.0001).
Control subjects made significantly more partially correct
responses than both FTD (t = 4.3, d.f. 29, P < 0.0001),
and HD patients (t = 2.3, d.f. 29, P = 0.03).
3.2.5. Word and verb count
A repeated measures ANOVA showed that the groups did
not differ in terms of the number of words contained in their
responses. There was also no effect of cartoon type on length
of response and no interaction effect.
A repeated measures ANOVA comparing the number of
action verbs produced by the three groups showed a small effect of group (F (2, 41) = 4.1, P = 0.02). FTD patients produced fewer overall action words than controls (P = 0.03).
There was no main effect of cartoon type. There was however
an interaction effect of group by cartoon type (F (2, 41) =
6.9, P = 0.003), reflecting the fact that whereas control subjects tended to produce more action verbs for physical than
mental cartoons, the HD group showed the reverse effect.

J.S. Snowden et al. / Neuropsychologia 41 (2003) 688701

695

Fig. 3. Mean accuracy scores for forced-choice cartoon interpretation (task 2) as a function of cartoon type.

A repeated measures ANOVA comparing the number of

mental state verbs produced by the three groups showed
a main effect of group (F (2, 41) = 4.6, P = 0.02), and
of cartoon type (F (1, 41) = 25.0, P < 0.0001), and an
interaction effect of group by cartoon type (F (2, 41) =
3.8, P = 0.03). Post hoc analyses revealed that FTD
patients produced fewer mental state verbs than controls (P = 0.01). As expected more mental state verbs
were produced for mental than for physical cartoons, but
the difference was proportionally smaller for the FTD
group.
3.2.6. Frequency analysis
The frequency with which overall performance accuracy
scores were superior or inferior in the mental compared
to the physical cartoon condition was calculated for each
group and frequency values were submitted to a Sign test.
Control subjects were significantly more likely to perform worse in the mental than the physical condition
(two-tailed test P < 0.02), whereas the patient groups
showed no significant bias.
3.3. Task 3: story comprehension
3.3.1. Time taken to respond
A repeated measures ANOVA comparing the time to respond by the three groups for the two story types showed
a main effect of group (F (2, 27) = 4.1, P = 0.03), but no
effect of story type or interaction effect. HD patients were
slower to respond than FTD patients (P = 0.04), and tended
to be slower than control subjects (P = 0.06). No other
group comparisons were significant.

3.3.2. Accuracy
Fig. 4 shows accuracy scores for the story comprehension test in the three groups for the two story types. A repeated measures ANOVA showed a main effect of group
(F (2, 30) = 19.3, P < 0.0001), but no effect of story type
or interaction effect. Control subjects performed better than
both FTD (P < 0.0001) and HD patients (P = 0.01), and
HD patients performed better than FTD patients (P = 0.01).
3.3.3. Error type
FTD patients were more likely than controls to make
omission errors (t = 2.4, d.f. 22, P = 0.03), concrete responses (t = 4.1, d.f. 22, P < 0.0001) and description responses (t = 5.2, d.f. 22, P < 0.0001). FTD patients also
made more concrete responses (t = 2.1, d.f. = 13, P =
0.05) and description responses (t = 3.0, d.f.13, P = 0.01)
than HD patients. HD patients showed a trend towards more
misconstruction errors than the control group (t = 1.9, d.f
25, P = 0.07). Control subjects were more likely than FTD
patients to make partially correct responses (t = 3.6, d.f.
22, P = 0.002).
3.3.4. Word and verb count
There was no difference in the overall number of words
per response produced by each of the three groups and length
of response was not influenced by story-type.
A repeated measures ANOVA comparing the number of
action verbs produced by the three groups showed no effect
of group, story type, or interaction effect of group by story
type.
A repeated measures ANOVA comparing the number of
mental state verbs produced by the three groups showed

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J.S. Snowden et al. / Neuropsychologia 41 (2003) 688701

Fig. 4. Mean accuracy scores for story interpretation (task 3) as a function of story type.

no main effect of group, but a main effect of story type

(F (1, 30) = 56.2, P < 0.0001), and a trend towards an
interaction effect of group by story type (F (2, 30) = 3.1,
P = 0.06). More mental state verbs were elicited for mental
than for physical stories, but this increase was smaller for
the FTD group than the other groups.
3.3.5. Frequency analysis
The frequency with which overall performance accuracy
scores were superior or inferior in the mental compared to
the physical story condition was calculated for each group
and frequency values were submitted to a Sign test. No group
showed a statistical bias towards better performance for one
or other story type.
3.4. Task 4: determining preference from eye gaze
3.4.1. Accuracy
Fig. 5 shows mean accuracy scores for each group,
when a distracting arrow was present and absent. A repeated measures ANOVA showed a main effect of group
(F (2, 39) = 5.5, P = 0.008), but no effect of condition (arrow versus no arrow), and no interaction effect of
group by condition. Post hoc analyses showed that FTD
patients made more errors than both HD patients (P =
0.03) and controls (P = 0.01). HD patients did not differ
from controls and performance in both approached ceiling
levels.
3.4.2. Error types
In view of the rarity of errors made by the HD and control groups, their responses were not subjected to analysis of
error type. In the FTD group incorrect responses were dominated by favourite errors, which accounted for 71% of all

incorrect responses (patients selected their personal favourite

picture disregarding eye gaze). Although a relatively high
number of incorrect responses (39%) accorded with the direction of the arrow, in the majority of these instances the
response also corresponded to the patients favourite picture, so that the basis for the correct choice was ambiguous.
The lack of a statistical effect of condition (arrow present
versus arrow absent), implying that the presence of the arrow had no overall effect on performance accuracy, suggests
that incorrect choices were largely being made on the basis of personal favourite and not arrow direction. One single
FTD patient appears to represent an exception to this general
rule. In the arrow condition 20 of his 22 incorrect responses
corresponded to the arrow direction. Perseverations of a single response position and random errors were rare in all
patients.
3.4.3. Judgement of eye direction
Three of the FTD patients had exhibited chance level
performance in the judgement of preference task. These
individuals were subsequently asked to indicate which of
the four items the cartoon face was looking at. Two FTD
patients had no difficulty carrying out the looking at task
and scored, respectively 100 and 92% correct, compared
with performance, respectively of 21 and 17% correct in
the preference task. These differences in performance
for the like and look at tasks were highly significant (McNemar test 2 = 17.1, P < 0.001; 2 = 16.1,
P < 0.001 for the two patients, respectively). By contrast
the third patient persisted in selecting her own personal
favourite item, disregarding the direction of eye gaze of
the cartoon face. Her accuracy score of 25% correct was
unchanged from her chance level score in the preference
task.

J.S. Snowden et al. / Neuropsychologia 41 (2003) 688701

697

Fig. 5. Mean score for judgement of preference (task 4) as a function of the presence or absence of a distractor arrow.
Table 3
Correlation between social cognition and standard executive test scores
Social task

Executive task
Category fluency (n = 12)

Letter fluency (n = 13)

WCST categories (n = 11)

(a) FTD
Task 1
Task 2
Task 3
Task 4

(single cartoons)
(forced-choice cartoons)
(stories)
(preference judgement)

0.58
0.69
0.13
0.28

0.62
0.53
0.01
0.36

0.57
0.75
0.58
0.20

(b) HD
Task 1
Task 2
Task 3
Task 4

(single cartoons)
(forced-choice cartoons)
(stories)
(preference judgement)

0.38
0.37
0.73
0.37

0.04
0.02
0.38
0.28

0.09
0.08
0.11
0.71

P < 0.05.
P < 0.001.

3.5. Relationship of performance on social cognition and

standard executive tests

3.6. Relationship of FTD performance to distribution

of frontal atrophy

For each of the four social cognition tasks a total performance accuracy score was calculated. In the case of the
cartoon and story tasks, this involved summating accuracy
scores for the mental and physical conditions. In the case of
the judgement of preference task scores for the arrow and no
arrow conditions were summated. The relationship between
total accuracy scores and performance on the category fluency (animals generated in one minute), letter fluency (F
words generated in one minute) and Wisconsin Card Sorting
test (WCST) was examined.
Table 3 shows the correlation between performance on
the experimental tasks and standard executive tests. Modest
relationships were found but these were not consistent across
tasks or for the two groups.

Nine FTD patients showed predominant orbitofrontal abnormalities on neuroimaging, whereas four patients showed
widespread frontal lobe changes, extending into dorsolateral
frontal cortex. Patients with widespread changes performed
worse that those with more circumscribed changes on the
cartoon and story tasks (P < 0.05) but not the preference
task.

4. Discussion
Both FTD and HD groups were impaired relative to controls in their interpretation of humorous cartoons and story
vignettes. The FTD group was more severely affected than

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J.S. Snowden et al. / Neuropsychologia 41 (2003) 688701

the HD group, consistent with the grosser social breakdown

and executive failure demonstrable in FTD.
Previous investigations using the same cartoon and story
materials have shown a disproportionate impairment on
the mental compared to the physical conditions in patients
following right hemisphere stroke [28] and in a patient
following frontal lobe surgery [29]. The dissociation was
interpreted as demonstrating impairments in theory of mind
associated respectively with right hemisphere and frontal
lobe lesions. It was predicted that FTD patients would show
a similar disproportionate impairment for mental compared
to physical items, whereas HD patients would show no such
dissociation. The findings were not entirely in accordance
with prediction. Both patient groups were essentially comparably impaired for the two types of test material, poorer
scores for mental compared to physical material being
demonstrated in FTD only in task 1.
Analysis of error responses provides clues to the basis
for the lack of dissociation, whilst also drawing attention to
important qualitative differences between FTD and HD. In
the FTD group, the largest proportion of errors for the cartoon tasks were omissions and concrete responses. Patients
reported not knowing what was funny about cartoons and either failed to produce a response, or itemised elements without further explanation (e.g. Theres a car, theres a child).
Thus, not only did patients fail to go beyond the contents of
the cartoon and draw inferences they also failed to integrate
elements of the cartoon into a thematic narrative. Failures
occurring at this relatively low-order level of cognition inevitably applied equally to mental and physical test material.
These concrete-type responses contrasted strikingly with the
errors of control subjects, which largely constituted partial
responses: responses that were insufficiently detailed or inferences were implicit rather than explicitly stated. Controls
typically did draw inferences, going beyond the literal elements of the cartoon.
In the HD group, a large proportion of errors in the cartoon tasks were of the description type: a full and integrated commentary on the contents of each cartoon was
provided but without drawings inferences beyond the physical contents. Such errors occurred to some extent in all
groups and were of no differentiating value. Of more theoretical interest is the presence of misconstruction errors. For
a substantial proportion of items HD patients did draw inferences that went beyond the physical contents of the cartoon. They abstracted and formulated hypotheses, including
hypotheses about a characters feelings or belief. However,
those inferences deviated from the conventional interpretation. For example, the usual interpretation of the ping-pong
cartoon described in Section 2.2.1 is that the man is deceiving the older woman into thinking he is playing table tennis. The response Theyre having a bit of nooky while the
wifes sat in there. Shes thinking At least hes leaving me
alone. Peace! suggests a diametrically opposite response:
the older woman is not deceived. Such eccentric interpretations constituted a trademark of HD, in that they occurred

at least once in all but one of the HD patients, yet were

virtually absent in other groups. Group differences cannot
be explained in terms of notional differences in severity of
impairment between FTD and HD. Misconstruction errors
did not occur even in relatively high-functioning FTD patients, whose overall level of accuracy on the cartoon tests
was comparable to that of HD subjects. They cannot, moreover, be attributed to scoring bias, because responses were
evaluated blind to diagnosis. The tendency to misconstrue
cut across stimulus type, being present both for mental and
physical cartoon types.
A similar pattern of errors occurred for the story task.
FTD patients were more likely than other groups to give
concrete responses, reiterating parts of the story without
drawing inferences. By contrast, there was a trend for HD
patients to make misconstruction errors, drawing faulty
inferences from stories. Controls were more likely to give
partially correct responses. Thus, the findings suggest a
consistent pattern of performance regardless of the nature
of the stimulus material.
The cartoon and story tasks are both relatively demanding. Concrete responses in FTD patients might potentially
have arisen due to task complexity: the requirement to integrate information and draw inferences might simply have
imposed too great a mental executive demand on the patient.
General executive deficits may have masked more specific
deficits in mental state attribution. The face test is important
in that it is undemanding, requiring no active mental manipulation or integration of information and it can be achieved
by children as young as 3 years. Participants merely point
to one of four pictures that the cartoon face prefers, preference being determined by direction of eye gaze. Nevertheless, FTD patients as a group showed an impaired ability to
carry out the task, frequently disregarding eye gaze direction and basing their selection of preference on their own
personal favourite. The fact that at least some patients had
no difficulty determining which item the face was looking
at suggests that failures on preference judgement could not
be ascribed to executive deficits such as inability to attend
to the test stimuli. Moreover, all patients complied with the
task when asked for their personal preference suggesting that
failures are unlikely to be secondary to comprehension impairment. Expression of personal preference might be construed as constituting a pre-potent response that the patient
is no longer able to override or inhibit and is consistent with
the impairments in response inhibition typical of frontal lobe
dysfunction. However, the concrete mode of response, based
on their own personal preference, is compatible also with
the notion that FTD patients have an egocentric world-view
in which they fail to recognise or attribute to others a mental
state that differs from their own. Such an interpretation is
consistent with relatives reports that FTD patients are oblivious to the feelings and needs of others. FTD patients, unlike
children with autism [8], were not typically greatly influenced by the presence of an arrow, suggesting that external
environmental stimuli were a less potent factor in guiding

J.S. Snowden et al. / Neuropsychologia 41 (2003) 688701

responses than patients own internal mental state. However,

there was an exception to this general rule. Responses in one
FTD patient consistently corresponded to the arrow direction, highlighting heterogeneity within the FTD population.
HD patients had no difficulty on the preference judgement task. This is consistent with earlier findings that they
could draw inferences about another persons emotions,
thoughts or beliefs and with clinical observations that HD
patients make pertinent and insightful remarks about the
effects of their illness on a close relative. Nevertheless,
insight demonstrated at a cognitive level, is frequently not
matched by commensurately considerate, sympathetic or
empathic behaviour in the patients daily life. There is a
mismatch between what the patient says and does. HD patients show alterations in the processing of emotion [23,59]
and one possibility is that HD patients lack of sympathy
and empathy arises more at an emotional than a cognitive
level. In any event, it cannot be attributed to an inability per
se to attribute mental states. By contrast, FTD patients exist
in an egocentric world, in which they do not ascribe independent mental states to others, a factor likely to contribute
to their loss of capacity for sympathy and empathy.
If HD patients can infer mental states in others but FTD
patients cannot then this should be reflected in the number
of mental state terms used in interpreting cartoons and stories. Consistent with prediction HD patients did not differ
from controls with respect to the number of mental terms
used. Conversely, FTD patients produced significantly fewer
mental state terms, despite a comparable overall length of responses. This may partly reflect patients tendency to itemise
elements, without integration into a coherent narrative. Indeed, on the cartoon pairs task FTD patients showed a reduction in the number of action verbs as well as mental state
verbs. Nevertheless, a significant reduction in action verbs
was demonstrated on a single task only, whereas a reduction
in mental state verbs was a more pervasive finding. This disparity suggests that at least one contribution to FTD patients
poor test performance is a failure to engage in mentalising
and in the attribution of mental states to others. It is of relevance that a SPECT imaging study [10] demonstrated activation of orbitofrontal cortex in subjects required to judge
whether words represented mental state terms. All the FTD
patients in the present study had demonstrable involvement
of orbitofrontal cortex on MR and SPECT imaging.
A number of studies have demonstrated dissociations in
performance on theory of mind and traditional frontal executive tasks [11,17,24,29,34,39,52], interpreted as evidence
for the independence of theory of mind and executive skills.
Nevertheless, it is reasonable to suppose that executive impairments will have a secondary impact on performance on
theory of mind tasks, and some studies have found a relationship between performance on the two types of tasks [13,53].
In one study [13] patients with left anterior lesions, like FTD
patients in the present study, failed to make non-literal interpretations, a finding ascribed to their tendency to attend only
to the most salient aspect of the relevant information. The

699

authors argued that impaired executive function provided a

sufficient explanation of the impaired story comprehension
performance, without the need to invoke an additional theory of mind impairment. Nevertheless, they acknowledged
the possibility that there may be two routes to impairment
in theory of mind tasks, arising from disruption either to
broader executive processes or to specific theory of mind
ability. We would adopt such a view. The FTD group was
not disproportionately impaired for social than for physical
cartoons and stories compared to controls, and FTD patients
showed worse performance for social compared to physical
stimuli only on task 1, suggesting that general executive impairments contribute substantially to test performance. Indeed, poorer overall performance was generally seen in those
patients with widespread frontal lobe atrophy. Nevertheless,
the relationship between performance on social cognition
and standard executive tests was relatively modest and not
systematic across tasks. Moreover, on the preference judgement task some FTD patients failed to ascribe preference,
yet had no difficulty reporting direction of eye gaze. The
two tasks (Which one does he like? versus Which one
is he looking at?) make comparable demands on attention
and differ only with respect to the need for mental state
attribution. Performance differences provide evidence for a
specific impairment in theory of mind. We would argue that
FTD patients have a genuine impairment in theory of mind,
but that in many patients, in whom frontal lobe atrophy is
severe and widespread this constitutes only one of a variety
of deficits. General executive impairments will have an inevitable impact on performance on theory of mind tasks and
may mask more specific deficits in theory of mind. Deficits
in theory of mind independent of executive function might
be expected early in the course of disease when pathological change is relatively confined to orbitofrontal regions
[57]. Later in the disease course, with extension of pathology into dorsolateral regions, the picture will be increasingly
coloured by additional executive deficits. Complementary
findings and anatomical interpretation come from a study
of the relationship between empathy, which requires the capacity to appreciate anothers thoughts and feelings, and
cognitive flexibility, as measured by conventional executive
tasks [22]. Differences between findings in the present study
and another study of FTD patients [24], in which impairments were demonstrated on theory of mind but not control
tasks, are likely to be attributed to differences in severity.
The patients in the latter study had a substantially higher
mean MMSE score than the present FTD patients (27 versus 22) and performed better on the WCST (4.4 versus 1.4
categories), suggesting that they were at an earlier stages in
their illness.
HD patients in the present study showed little convincing
evidence of deficits in theory of mind. Nevertheless patients
performed abnormally on tasks requiring interpretation of
situations. Their tendency to make misconstruction errors
has a resonance with their functioning in daily life. Relatives
reports suggest that people with HD sometimes interpret

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J.S. Snowden et al. / Neuropsychologia 41 (2003) 688701

events and social interactions in ways that do not accord with

the norm. It is possible that their tendency to misconstrue
may underlie or at least contribute to the fixed ideation and
intransigence that are characteristic of some people with
HD. The relatively weak correlation between performance
on social cognition and standard executive tasks exemplifies
the fact that the problems encountered by HD patients in
open-ended tasks (and indeed normal social situations) may
not be adequately reflected in standard executive tests.
We have interpreted differences between FTD and HD as
reflecting the fact that FTD is largely a frontal neocortical
disorder and HD a disorder of the striatum. However, in disorders that affect frontostriatal circuitry a common assumption is that analogous deficits will arise regardless of the level
of the circuit at which disruption occurs. Why then should
FTD and HD be qualitatively different? If FTD and HD involve different striatofrontal circuits[3,43] then might this
explain qualitative differences? FTD is thought to progress
in an orbital-to-dorsolateral direction [57], whereas the dorsal to ventral striatal progression in HD [63] suggests the
reverse. Nevertheless, differential involvement of circuits is
an unlikely explanation. The classification of frontostriatal
circuits [50] and the extent to which they are parallel [33]
is itself not without controversy. Moreover, the FTD group
included patients both with a relatively circumscribed orbitofrontal atrophy and with widespread frontal atrophy, presumably involving each of the dorsolateral, orbitofrontal and
anterior cingulate loops, yet none showed an HD-like pattern of error response. Furthermore, poor performance on
executive tasks has characteristically been associated with
dorsolateral frontal lobe pathology [43], yet it was the FTD
patients who performed the more poorly on these tasks suggesting dorsolateral frontal dysfunction at least as great as
in HD. In FTD frontal cortical grey and white matter are
comparably affected [41], whereas in HD there is imaging
[7] and pathological [40] evidence of a disproportionate involvement of white matter. In FTD maximal loss of neurones occurs in the superficial layers II and III, resulting
primarily in loss of cortico-cortical connections, whereas in
HD pyramidal neurones in deeper layers V and VI, which
subserve cortico-subcortical projection fibres, are most involved. We would suggest that the key distinction underlying performance differences is that FTD involves primarily
frontal neocortex and its cortico-cortical afferents whereas
HD is a disorder of the striatum and its cortico-subcortical
connections.
The study highlights the value of open-ended tasks involving interpretation of social situations, in exploring deficits
arising from disorders of the frontostriatal system. The findings suggest that, despite superficial similarities in the pattern of cognitive disorder and altered social conduct in FTD
and HD, qualitative differences exist in the nature of underlying deficits. In FTD there is a loss of theory of mind
but that additional executive deficits colour patients performance on theory of mind tasks. In HD there is no convincing evidence of a loss of theory of mind. Future studies

need to address the qualitative characteristics of performance

in laboratory-based and real-life social situations to clarify
more precisely the basis for social breakdown in FTD and
HD.
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