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Neuropsychologia 43 (2005) 99–114

Theory of mind after traumatic brain injury夽


Helen Bibby, Skye McDonald∗
School of Psychology, University of New South Wales (UNSW), Sydney, NSW 2052, Australia
Received 13 May 2003; accepted 28 April 2004

Abstract
This study investigated whether people with severe traumatic brain injury (TBI) demonstrate a specific impairment on tasks requiring
them to make inferences about others’ mental states (theory of mind tasks). Participants with severe TBI were compared to a healthy group
on verbal first-order and second-order theory of mind (ToM) tasks, non-verbal ToM tasks and on verbal and non-verbal tasks requiring them
to make general (non-mental) inferences (NMIs). The clinical group performed more poorly than controls on both ToM and NMI tasks.
This performance was not completely accounted for by the working memory or implicit language demands of the tasks. Multiple regression
analyses suggested that patients with TBI have a general weakness in inference-making that, combined with linguistic and working memory
limitations, impairs their performance on both non-verbal and second-order ToM tasks. However, a specific ToM impairment may underlie
their poor performance on verbal first-order tasks. Implications of this finding for the possibility of a separate cognitive module of ToM
are discussed, as well as for the rehabilitation of social deficits after TBI.
© 2004 Published by Elsevier Ltd.
Keywords: Mental-state; Inference; Lesion; Brain-damage; Cognitive; Module

1. Introduction 1.1. Theory of mind as a separate cognitive module

Human beings are social animals (Adolphs, 1999), and Despite its potential importance, the concept of social
social interaction requires complex, flexible behaviour cognition tends to be rather loosely defined (Adolphs,
(Adolphs, 2001; Baron-Cohen et al., 1999). In order to man- 2001). Perhaps for this reason, much of the research in
ifest this behaviour, social cognition is required (Adolphs, the area has focussed on one aspect of social intelligence,
2001). Social cognition (or social intelligence) has been namely “theory of mind” (ToM) (Happe, Brownell, &
defined as the ability to interpret others’ behaviour in terms Winner, 1999). ToM refers to the ability to think about other
of mental states, to conceptualise relationships between people’s mental states (e.g. thoughts, beliefs, intentions and
oneself and others, and to use these concepts to guide one’s desires) and use them to understand and predict others’
own behaviour and predict that of others (Adolphs, 2001; behaviour (Baron-Cohen et al., 1994; Mazza, De Risio,
Baron-Cohen et al., 1999). It has been suggested that this Sudan, Roncone, & Casacchia, 2001; Rowe, Bullock,
ability may be independent from general intelligence, with Polkey, & Morris, 2001). It has been suggested that ToM
different information processing demands (Adolphs, 2001; is a separate cognitive module, with an innate neural basis
Baron-Cohen et al., 1999). (Happe et al., 1999; Happe, Malhi, & Checkley, 2001).
However, the specific mechanism and neural pathways of
ToM are not well understood (Happe et al., 2001) and its
identity as an innate module remains controversial (e.g.
Garfield, Peterson, & Perry, 2001).
夽 Data collection for this research was facilitated by a Discovery Grant According to Fodor’s original conceptualisation (1983)
from the Australian Research Council. We gratefully acknowledge the a cognitive module is a domain specific inference-making
Liverpool Brain Injury Rehabilitation Unit, especially Anne Pfaff, the system that has a distinct neuroanatomical location, only has
Royal Ryde Rehabilitation Unit, especially Dr. Clayton King, and the access to information that is relevant to its computations,
Westmead Hospital Brain Injury Unit, especially Dr. Joe Gurka, for access
to patients.
and is independent of the diffuse central systems that govern
∗ Corresponding author. Tel.: +61-2-9385-3029; fax: +61-2-9385-3641. higher cognitive functions. Consequently, if ToM is modular
E-mail address: s.mcdonald@unsw.edu.au (S. McDonald). it should be possible to have specific ToM impairment with

0028-3932/$ – see front matter © 2004 Published by Elsevier Ltd.


doi:10.1016/j.neuropsychologia.2004.04.027
100 H. Bibby, S. McDonald / Neuropsychologia 43 (2005) 99–114

intact functioning in other areas (c.f. aphasias) (Foder, 1985) all have demonstrated a specific impairment that is disso-
or for ToM to remain intact in spite of severe intellectual ciable from general inferential ability. For example, while
impairment (Moscovitch & Umilta, 1991). Stuss, Gallup, and Alexander (2001) found that frontal lobe
Claims concerning the cognitive independence of ToM lesions resulted in impaired performance on visual perspec-
are based upon a range of findings. Firstly, there are recent tive taking and deception tasks, they did not incorporate
findings of specific, acquired ToM impairments in patients NMI tasks. Similarly, Channon and Crawford (2000) found
who have had a right hemisphere stroke (Happe et al., 1999), that patients with left anterior lesions showed impaired
frontal lobe surgery (Happe et al., 2001) and fronto-temporal comprehension on ToM stories relative to those with other
dementia (Lough, Gregory, & Hodges, 2001). Secondly, lesions, but again, no NMI stories were used. Nevertheless,
ToM ability has been shown to develop during childhood in a small number of researchers have reported a clear and
a series of increasingly complex stages that are thought to dissociable ToM impairment in patients with frontal lobe
be universal across cultures and to occur within a narrow damage. Rowe et al. (2001) studied neurosurgical patients
time frame (Happe et al., 2001; Lough et al., 2001). Also, with unilateral frontal lobe lesions and found a specific im-
the rate of development has been found to be relatively in- pairment on ToM tasks following both left and right hemi-
dependent of level of intelligence (Fletcher et al., 1995) and sphere damage, and Happe et al. (2001) found a deficit in
to have a genetic component that is independent of verbal ToM stories and cartoons compared to NMI tasks in a single
development (Hughes & Cutting, 1999). patient who had undergone a bilateral surgical procedure
Thirdly, research has demonstrated a selective impair- to cut the neuronal connections between the orbito-frontal
ment of ToM while other functioning is relatively intact in cortex and the mid-line thalamic nuclei. Therefore, some
developmental disorders such as autism (Happe et al., 1999; evidence from lesion studies is consistent with imag-
Stone, Baron-Cohen, & Knight, 1998). Conversely, there is ing research suggesting the role of the frontal lobes in
evidence of a selective sparing of ToM ability in some indi- ToM.
viduals with impaired general intellectual functioning, such Another line of evidence has implicated the right hemi-
as William’s syndrome and Down’s syndrome (Happe et al., sphere in ToM tasks. For example, Winner, Brownell, Happe,
2001; Lough et al., 2001). It should be noted, however, Blum, and Pincus (1998) found that right-hemisphere
that this evidence has not gone unchallenged. Ozonoff, brain-damaged (RHD) patients’ performance on more
Pennington, and Rogers (1991) claimed that deficits in ToM difficult (second-order) ToM tasks was fragile and vari-
in autistic individuals are caused by general impairments able compared to a control group, while left-hemisphere
in reasoning and strategy application. Furthermore, Zelazo, brain-damaged (LHD) patients’ performance on less ver-
Burack, Benedetto, and Frye (1996) found that low- bally demanding ToM tasks was not impaired. Given this
functioning adults with Down’s Syndrome performed worse mixture of findings implicating both the frontal lobes and
than normal children on several ToM tasks, and that their the right hemisphere, it is possible that the most important
performance was correlated with a test of mental flexibility. brain region for ToM is in fact the right frontal region. This
In accordance with Fodor’s conceptualisation, neuro possibility is supported by the recent findings by Tranel,
anatomical specificity is another requirement for modu- Bechara, and Denburg (2002) that the right ventromedial
larity. Indeed, a considerable amount of evidence from prefrontal cortex is related to social and emotional process-
imaging studies has suggested that the frontal lobes are nec- ing impairments, while the left ventromedial prefrontal cor-
essary for this ability (Adolphs, 2001). Baron-Cohen et al. tex is not. Also, Stuss et al.’s study (2001, discussed above)
(1994) found increased blood flow in the right orbito-frontal suggested that the right frontal lobe was particularly impor-
cortex during recognition of mental state words and Goel, tant. Despite these findings there is not universal agreement
Grafman, Sadato, and Hallett (1995) found activation of the concerning a right frontal focus. Some of the research out-
left temporal and left medial frontal lobe during a task re- lined above implicated the left frontal region rather than the
quiring mental state inferences. Fletcher et al. (1995) found right (Channon & Crawford, 2000; Fletcher et al., 1995;
increased activation in the left medial prefrontal gyrus and Goel et al., 1995), and while Surian and Siegal (2001) also
the posterior cingulate cortex when they compared normal found that RHD patients performed worse on ToM tasks
subjects’ performance on ToM stories to that on general compared to LHD patients, this only applied when the tasks
(non-mental) inference (NMI) stories and Gallagher et al. placed a demand on visuo-spatial processing.
(2000) found a similar activation pattern when they com- In sum, while there is some evidence that is sugges-
pared normal subjects’ performance on ToM and NMI tive of a separate cognitive module for ToM, the issue re-
cartoons. This evidence provides considerable support for mains controversial and more research is needed. While it
the role of the frontal lobes in ToM. appears that ToM can be differentially impaired in devel-
Localisation evidence via functional imaging studies is opmental and acquired neurological disorders this requires
strengthened considerably by the presence of convergent further clarification. Similarly, there is some evidence that
findings from neuropsychological lesion studies (Happe the frontal lobes are necessary for ToM ability, but the ex-
et al., 2001). A number of studies have investigated ac- act region of these lobes that is involved is still a matter of
quired ToM deficits after frontal lobe damage, although not debate.
H. Bibby, S. McDonald / Neuropsychologia 43 (2005) 99–114 101

1.2. Theory of mind in traumatic brain injury explicitly excluding TBI patients (e.g. Mazza et al., 2001).
In one of the few published reports that included subjects
Given that ToM is an aspect of social cognition, it is with TBI, Stone et al., 1998 demonstrated a specific (i.e.
not surprising that a range of social deficits have been as- dissociable) impairment on more difficult ToM tasks (“faux
sociated with ToM impairment. Specifically, a ToM deficit pas” tasks) in five TBI patients with bilateral damage to the
has been linked to difficulties using gestures to affect how orbito-frontal cortex. However, Bach, Happe, Fleminger, and
others feel as well as taking account of others’ interests in Powell (2000) did not find evidence of a ToM deficit in a
conversation (Fletcher et al., 1995), withdrawal from social TBI subject with acquired orbito-frontal damage and social
contact (Happe et al., 2001), insensitivity to social cues, problems.
indifference to others’ opinions, poor foresight, egocen- Santoro and Spiers (1994) assessed 10 adults after a
trism, lack of restraint and inappropriate affect (Rowe et al., closed-head-injury and found that they had more difficulty
2001), pedantic speech, inappropriate non-verbal commu- than non-head-injured adults on a video-based perspective
nication and inability to follow social rules (Bowler, 1992), taking task, and Dennis et al. (2001) found that children
and difficulty applying theoretical social knowledge to the with severe closed head injury cannot answer questions
real situation (Stone et al., 1998). Furthermore, research has about the intentions of speakers who use non-literal lan-
suggested that impaired ToM may also be associated with guage. However, it is unclear from these latter studies that
communication difficulties. In particular, it has been linked TBI results in a specific impairment of ToM because nei-
to problems comprehending non-literal speech, such as sar- ther of them compared performance on these tasks to that
casm, irony, humour and deceit (e.g. Channon & Crawford, on tasks requiring non-mental (e.g. physical) inferences
2000; Happe, 1993). (NMI). Thus, the impaired performance might be due to
One group that has been found to demonstrate many of a more general impairment in inferential ability. A small
the social and communication difficulties outlined above are number of other studies found impaired ToM in subject
people who have sustained a severe traumatic brain injury groups that included, but were not limited to TBI patients
(TBI). Subjects with TBI have been shown to have impaired (e.g. Channon & Crawford, 2000; Dimitrov et al., 1996),
social competence (Spatt, Zebenholzer, & Oder, 1997); to be but again these did not measure general inferential ability.
socially isolated (Lezak, 1995); and to have difficulties with It is clear that further research is merited to examine the
non-literal language (Dennis, Purvis, Barnes, Wilkinson, possibility of a specific ToM deficit after TBI. Therefore, the
& Winner, 2001; McDonald & Pearce, 1996; Winner et al., present study aimed to address two main questions: (1) Do
1998). They have also been described as having poor in- people with a severe traumatic brain injury (TBI) demon-
sight, talkativeness and inappropriate expressions of affec- strate impairment on tasks requiring them to make inferences
tion (Santoro & Spiers, 1994); reduced empathy (Eslinger, about others’ mental states (theory of mind tasks) compared
1998); lack of foresight, tact and concern (Lishman, 2001); to healthy controls? (2) Is this impairment independent of
egocentrism and inappropriate levels of social interaction the ability of people with TBI to make general (non-mental)
(McDonald & Pearce, 1996); impaired understanding of inferences?.
non-verbal signals (Lezak, 1995); and difficulty applying
social knowledge (Dimitrov, Grafman, & Hollnagel, 1996). 1.3. Alternative explanations of ToM task performance
The overlap between these observations and the social dif-
ficulties thought to be associated with ToM deficits raises It has been pointed out that performance on any cognitive
the question of whether patients with severe TBI have im- task reflects competence in the ability required to solve the
pairment in ToM. Furthermore, TBI often results in damage problem (in this case, ToM) and the possession of other cog-
to frontal areas in the brain (as well as temporal dam- nitive skills that are necessary but not sufficient for the task
age and diffuse axonal injury) (Adams et al., 1985, 1989; (e.g. the ability to remember information, focus attention,
Levin et al., 1987). Given these two lines of evidence, i.e. understand and answer questions, etc.) (Wellman, Cross, &
(1) poor social behaviour; (2) frontal lobe involvement, Watson, 2001). In terms of Fodor’s concept of modularity,
the possibility that many people with TBI have impaired a ToM task may well tap into a separate cognitive module
ToM merits examination. The finding of a specific ToM of ToM, but also require the involvement of other cognitive
impairment in TBI would provide further evidence for the modules and central systems.
modular nature of ToM. It would also have important im- It has been suggested that a deficit in one of these other
plications for the rehabilitation of social difficulties in this systems may underlie the impaired performance on ToM
group. Strategies to address a ToM deficit have been devel- tasks in young children (Foder, 1992), people with autism
oped for people with Asperger’s syndrome (Attwood, 1998) (Bowler, 1992), people with schizophrenia (Langdon et al.,
and schizophrenia (Sarfati, Passerieux, & Hardy-Bayle, 1997) and patients with frontal lobe damage (Channon &
2000), and these might be adapted for patients with Crawford, 2000). This question must also be considered
TBI. in relation to TBI given that the disorder is heterogeneous
Existing research on ToM deficits in TBI is very lim- and associated with a range of cognitive deficits including
ited, with many studies on acquired impairment of ToM difficulties with pragmatic language (McDonald & Pearce,
102 H. Bibby, S. McDonald / Neuropsychologia 43 (2005) 99–114

1996), recall of information, working memory, attention and (Stone et al., 1998). A number of studies have shown that
executive functioning (Lezak, 1995). young children’s performances on ToM tasks are influenced
by working memory capacity (Butler, 1997; Gordon &
1.3.1. Implicit language demands Olson, 1998; Hughes, 1998; Keenan, 1998, 2000), although
One possibility for the poor performance of young chil- the evidence suggests that it is not the sole contributing
dren on ToM tasks may be due to difficulties in under- factor (Artuso, 2000; Tager-Flusberg, Sullivan, & Boshart,
standing the purpose of the questions (Siegal, Carrington, & 1997). Notably, Davis and Pratt (1995) found that back-
Radel, 1996). This has led researchers to re-phrase the ques- wards, but not forwards, digit span was significantly related
tions used (e.g. “where will John look for his kitten?” be- to performance on false-belief tasks, even when age and
comes “where will John look for his kitten first?” or “where language ability were controlled. Subjects with TBI often
does John think his kitten is?” (Siegal et al., 1996; Wellman have impairments in working memory (Lezak, 1995), so the
et al., 2001). Siegal and coworkers (Siegal et al., 1996; possibility that this underlies observed impairments in ToM
Surian & Siegal, 2001) argued that the impaired perfor- tasks is important to address. Indeed, it has been proposed
mance of RHD patients on ToM tasks was attributable to the that a weakness in working memory may underlie a broad
pragmatic demands of the questions, and showed that using range of frontal lobe deficits (Kimberg & Farah, 1993), and
more explicit questions enables this group to make correct Stone et al. (1998) found that patients with dorsolateral
false-belief predictions. Similarly, Varley, Siegal, and Want frontal lesions only had difficulty on those theory of mind
(2001) were able to show that a patient with severe apha- tasks that placed demands on working memory.
sia retained theory of mind reasoning when they used a task Therefore, the current study took alternative hypotheses
with significantly reduced verbal demands. Given that pa- for impaired performance on ToM tasks into account by
tients with TBI are known to have difficulties with pragmatic incorporating both implicit and explicit questions, leaving
language (McDonald & Pearce, 1996), it is important to ex- the test material in front of the subject while these questions
amine their responses to both implicit and explicit questions were asked, and examining how performance on ToM tasks
about mental states. An example of the kind of questions relates to working memory capacity.
used is shown below:
1.4. Measuring theory of mind
John puts his kitten in a box, and then leaves the room
while the kitten escapes and hides under a chair. When
A wide range of different approaches have been used to
he returns, he looks for his kitten in the box.
assess ToM. These approaches have varied in terms of fac-
The implicit question would be “Why did John look for his tors such as the subjects they were designed for (ranging
kitten in the box?” A more explicit question would be: “Why from normal adults to children with autism) and their capac-
did John think his kitten was in the box?” Each question ity to distinguish between different developmental levels of
requires the same level of reasoning about mental states, but ToM (e.g. first-order, second-order and applied uses of ToM
one explicitly indicates that a response referring to mental inferences).
states is required.
1.4.1. False-belief stories
1.3.2. Memory demands ToM ability is usually measured using false-belief tasks
ToM tasks would be expected to place a considerable load (Fine, Lumsden, & Blair, 2001; Keenan, 1998), which mea-
on the memory of brain-injured participants. Researchers sure the ability to understand that other people’s beliefs may
have attempted to eliminate the possibility that memory not match the true state of affairs (Stone et al., 1998). This
problems could account for an observed deficit in several understanding normally develops at around 4 years of age
ways. Some have included a measure of prose recall in their (Hughes & Cutting, 1999). A typical false-belief story de-
studies as a covariate (Rowe et al., 2001) and others have scribes an object being moved from one location to another
incorporated a memory question after each task (Surian & without a key character’s knowledge. The subject is then
Siegal, 2001). An alternative approach is to leave the test asked to predict where that character will search for the ob-
material in front of the subject while all questions are asked ject (Tager-Flusberg et al., 1997). Other studies have used
(Channon & Crawford, 2000; Dennis et al., 2001). It has a story where the main character has acted on a false-belief
been suggested that, in addition to reducing memory load, and the subject is asked to explain his or her actions (e.g.
the practice of providing test material in written as well Channon & Crawford, 2000; Mazza et al., 2001). The latter
as verbal form increases participants’ attention to and en- may be more appropriate for adult subjects, as it has been
gagement with the activity (Kaplan, Brownell, Jacobs, & suggested that the simplest false-belief tasks designed for
Gardner, 1990). children may confuse adults because they expect more dif-
ficult questions (Siegal et al., 1996). Hughes et al. (2000)
1.3.3. Working memory demands found that most standard false-belief tasks have good reli-
It has also been claimed that impaired performance on ability, and Wellman et al., 2001 found that, despite varia-
ToM tasks may be attributable to working memory demands tions, false-belief tasks are “essentially equivalent” (p. 679).
H. Bibby, S. McDonald / Neuropsychologia 43 (2005) 99–114 103

1.4.2. Second-order stories story (e.g. Bowler, 1992; Hughes & Cutting, 1999; Lough
In addition to the first-order false-belief stories described et al., 2001) but these are not adequate as they do not require
above, a number of studies have included second-order ToM inferences to be made (Stone et al., 1998).
stories (e.g. Lough et al., 2001; Rowe et al., 2001; Santoro Therefore, the current study used stories and cartoons
& Spiers, 1994; Stone et al., 1998). Second-order stories re- to examine ToM ability in adults with and without TBI in
quire the subject to demonstrate understanding of what one verbal and non-verbal domains. It included first-order sto-
person thinks another person believes (“Mary thinks that ries in which the main character has acted on a false-belief,
John thinks. . . ”) (Bishop, 1993; Mazza et al., 2001). This second-order stories in which the main character has acted
understanding normally develops at around 6 or 7 years of on a belief about a belief, and mental state cartoons that re-
age, and is claimed to underlie the ability to distinguish a quired an understanding of false-belief to be understood. Per-
lie from a joke (Leekam & Prior, 1994; Sullivan, Winner, & formance on these ToM tasks was also compared to that on
Hopfield, 1995). It has been suggested that performance on NMI tasks (that required inferences to be drawn about things
more developmentally advanced ToM tasks provides an in- other than mental states, such as physical causation, physi-
dex of the severity of the deficit (with milder deficits picked cal anomaly or breaking social norms) to examine whether
up by more challenging tasks) (Stone et al., 1998). Studies any impairment was specific to social reasoning. All tasks
haye found that some high functioning people with autism were pilot-tested on normal adults to screen for errors, check
can pass first-order tasks but will fail second-order ones comprehensibility and to ensure the scoring criteria were
(Happe, 1993) and others have found that RHD patients’ unambiguous.
ToM impairment is restricted to second-order tasks (Happe
et al., 1999; Winner et al., 1998). Hughes et al. (2000) re- 1.5. Summary of aims
ported that second-order false-belief tasks have good relia-
bility. The present study aimed to address the following ques-
tions:
1.4.3. Mental-state cartoons
While the majority of ToM research has focussed on story (1) Do people with a traumatic brain injury (TBI) demon-
tasks of the kinds outlined above, a small number of stud- strate an impairment on tasks requiring them to make
ies have also incorporated tasks with a non-verbal compo- inferences about others’ mental states (theory of mind
nent (e.g. Bihrle, Brownell, & Powelson, 1986; Gallagher tasks) that is independent of their performance on tasks
et al., 2000; Hughes & Cutting, 1999; Sarfati et al., 2000). requiring them to make general (non-mental) infer-
Frequently these studies use mental-state cartoons, where ences?
to understand the cartoon you need an understanding of (2) At what level of inference does this impairment mani-
a character’s false-belief (Fine et al., 2001; Happe et al., fest? (first-order or second-order)
1999). Happe et al. (1999, 2001) reported that both RHD (3) Does this impairment apply to non-verbal tasks (car-
patients and a patient treated with stereotactic anterior cap- toons) as well as verbal ones (stories)?
sulotomy showed consistent ToM deficits across story and (4) Is this impairment independent of working memory
cartoon tasks, and Gallagher et al. (2000) found selective deficits that may impact on the performance of such
activation of the same brain region when they compared tasks?
normal subjects’ performance on ToM stories and cartoons. (5) Is this impairment independent of the nature of questions
However, to date there does not appear to have been an ex- (implicit or explicit) that are used to assess this ability?
amination of the performance of TBI subjects on non-verbal
ToM tasks.
2. Method
1.4.4. Non-mental inference tasks
As discussed above, the current study was interested in 2.1. Participants
examining whether subjects with TBI show impairment on
ToM that is dissociable from a more general difficulty with Fifteen outpatients (11 male, 4 female) with a mean age of
making inferences. A number of previous studies have in- 40.5 years (S.D. = 10.6) were recruited from three neurolog-
corporated stories and cartoons that require inferences to be ical rehabilitation centres. All participants had suffered a se-
drawn about things other than mental states, such as phys- vere head injury resulting in posttraumatic amnesia (PTA) of
ical causation, physical anomaly or breaking social norms an average of 94.5 days (S.D. = 81.2). A chi-square analysis
(Happe et al., 1999, 2001). Such tasks have been used in indicated that the injury had significantly effected the distri-
a number of imaging studies (e.g. Fletcher et al., 1995; bution among occupational categories of the patient group
Gallagher et al., 2000; Happe et al., 1996) and some le- (Cramer’s V = 0.838, P < 0.01), with the majority working
sion studies (Happe et al., 2001; Stone et al., 1998). Other in skilled trade or sales/clerical positions before their injury,
researchers have incorporated control questions into their and being unemployed or in volunteer positions afterwards.
mental state tasks assessing understanding and recall of the Almost all patients had CT or MRI scans which showed
104 H. Bibby, S. McDonald / Neuropsychologia 43 (2005) 99–114

Table 1
Clinical features of the TBI patients
Subject number Cause of injury Injury site (CT or MRI scan) Time in PTA (days) Time post-injury (years)

1 MVA Right frontal 186 9.5


2 Assault Left temporal 120 9.5
3 MVA Bilateral fronto-temporal 16 5
4 Assault Bilateral fronto-temporal and parietal 196 14
5 MVA Left fronto-temporal and parietal 38 4
6 Fall Left temporal, parietal and occipital 10 1
7 Fall Bilateral frontal 11 3.5
8 MVA Right frontal and occipital 27 4
9 MVA – 140 14.5
10 MVA Right fronto-temporal 90 16
11 Assault Left frontal – 0.5
12 MVA Right frontal 140 3
13 Assault Right parietal 240 8.5
14 MVA Left frontal 14 2.5
15 MVA Right temporal – 8
Note: MVA = motor vehicle accident.

damage to a wide variety of brain regions. The majority had (Bihrle et al., 1986; Fletcher et al., 1995; Gallagher et al.,
frontal and/or temporal involvement. Clinical features taken 2000; Happe et al., 1999; Hughes et al., 2000; Mazza et al.,
from the patients’ medical records are shown in Table 1. 2001; Rowe et al., 2001; Sullivan et al., 1995). Some were
At the time of testing, all patients were out of PTA. adapted to ensure they were of roughly equivalent length. All
Their stage of injury was at least 6 months post, but the NMI stories were of approximately equivalent length and
in most cases was much longer, with the average time complexity to the ToM stories. Two were used by Gallagher
post-injury being 7.4 years (S.D. = 4.9). As a result of et al. (2000) and two were designed specifically for the cur-
the long average duration post-injury, the available neu- rent study. Each story was 1–2 paragraphs long and de-
ropsychological data was sketchy for some patients, but scribed characters involved in a range of activities, such as
clinical records revealed that they did not have severe household chores, organising a wedding, committing a rob-
amnesia, aphasia or agnosia, and that basic cognitive pro- bery or buying an ice-cream. The first-order ToM stories
cesses were grossly intact. Their performances on standard related to a character’s lack of knowledge about a physi-
neuropsychological tests (where available) are shown in cal situation (e.g. a stolen cigarette, a practical joke). The
Table 2. second-order ToM stories related to a character’s knowledge
Fifteen control subjects (10 male, 5 female) with a mean (or lack of knowledge) about another character’s beliefs or
age of 35.9 years (S.D. = 12.3) were recruited from the rel- intentions (e.g. that a character had received a phone mes-
atives of brain-injured participants, the general community sage, a double bluff scenario). The non-mental inference
and from advertisements placed at local social clubs and stories involved reasoning about physical cause and effect
job centres. They had no history of neurological problems (e.g. ice melting, driving around in circles).
or severe head injury, and were chosen to be similar to the Each story was individually presented to subjects in large
brain-injured subjects in demographic characteristics. The (16 point) font on A4 paper in a protective sheet. At the
results of Student’s t-tests indicated that there were no sig- same time, the story was read aloud. The story remained in
nificant differences between control and traumatic brain in- front of the subjects while four questions were asked. In the
jury (TBI) groups for age (P = 0.372) or education level (P case of the ToM stories the questions were:
= 0.711). Chi-square analyses indicated that there were also (1) A general question implicitly requiring an inference to
no significant differences for gender (P = 0.5) or pre-morbid be made about a character’s mental state. Subjects were
occupation (P = 0.508). The demographic characteristics of asked to explain the character’s words or actions, al-
all participants are shown in Table 3. though the reason behind these actions had not been di-
rectly stated in the story.
2.2. Materials (2) A follow-up question explicitly asking about mental
states.
2.2.1. Story tasks (3) Two further follow-up questions. These also explicitly
Three types of stories were used, namely first-order the- referred to mental states, but were presented in forced
ory of mind (ToM) stories, second-order ToM stories and choice format (yes or no). For each story, the correct
general (non-mental) inference (NMI) stories. A total of 12 answer to one of the questions was yes and the other
stories were given to all subjects—four of each type. Most no, so that the possibility of response bias could be
of the stories were drawn from previously published studies excluded.
H. Bibby, S. McDonald / Neuropsychologia 43 (2005) 99–114 105

Table 2
Performance on standard neuropsychological tests
Test Subject scores

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15

WAIS-III
Subtest ASS
Information 9 12 6 – 4 8 11 9 8 12 – 9 15 9
Similarities 6 9 7 – 6 1 11 4 11 10 – 4 12 7 8
Digit span 11 9 7 7 8 5 9 10 6 9 11 6 9 8 9
LNS 10 8 9 – – 6 12 5 – 8 – – 14 5 6
DS-C 7 7 4 – 4 5 13 – – 6 – 4 5 5 4
SS 6 7 5 – – 6 12 3 2 9 – 1 6 – 6
WTAR 116 101 101 – 119 – 104 110 87 92 – 102 121 100 113
WMS-III
Subtest ASS
LM1 5 7 8 – – 8 10 8 7 10 – 1 9 7 12
LM2 9 9 8 – – 9 12 8 9 9 – 2 10 9 12
Faces 1 8 10 6 – – 9 10 7 7 7 – 4 8 6 12
Faces 2 9 7 9 – – 7 10 9 5 8 – 3 10 10 12
VPA1 10 11 6 – – 10 14 5 9 5 – 2 12 6 9
VPA2 9 11 8 – – 11 13 4 8 5 – 3 11 5 10
REY CFT
Copy 21 26 23 – 28 31 30 12 – 26 – 22 34 – 23
Recall 5 14 4 – 7 22 18 2 2 19 – – 19 – 17
COWAT 29 35 21 27 11 24 56 39 25 40 35 16 37 28 29
WCST
Categories 2 – 0 – – 4 3 0 0 6 – 5 6 – 3
PE 46 – 10 – – – 26 72 11 – 20 9 – 5
CANTAB
Circ 0 0 0 – 0 – 0 0 0 2 – 2 0 – 2
Dim. total 68 68 94 – 96 – – – 127 72 – 96 68 – 87
Errors 30 13 25 – 24 – 12 32 43 13 – 30 11 – 21
Note: WAIS-III, Wechsler adult intelligence scale (3rd ed.); ASS, age scaled scores (X = 10; S.D. = 3); LNS, letter number sequencing; DS-C, digit
symbol coding; SS, symbol search; WTAR, Wechsler test of adult reading, estimated WAIS-III full intelligence quotient; WMS-III, Wechsler memory
scale (3rd ed.); LM, logical memory; VPA, verbal paired associates; CFT, complex figure test; COWAT, controlled oral word association test; WCST,
Wisconsin card sorting test (scoring criteria taken from manual); PE, perseverative errors; CANTAB, Cambridge neuropsychological test automated
battery; Circ, big/little circles; Dim., intra/extra dimensional shift.

An example of a first-order ToM story (adapted from The questions were always asked in order from least to
Hughes et al., 2000) is shown below: most explicit, to prevent cuing. For NMI stories, a similar
set of four questions was asked, but in this case the mental
states of the characters were irrelevant and the questions
Larry really likes drinking Coke, but he hates milk concerned physical cause and effect. Examples of a NMI
and refuses to touch it. Larry has a brother, Jack, who story and a second-order ToM story are in Appendices A
likes playing tricks on people. One day, Larry was and B with some sample responses.
drinking some Coke when the phone rang. He put down
the can and went into the other room to answer the 2.2.2. Cartoon tasks
phone. Meanwhile, Jack came in. He decided to play a Two types of cartoon tasks were used, namely ToM and
trick on Larry. He poured all the Coke out of the can, NMI cartoons. A total of eight cartoons were given to
and put milk in it instead. When Larry came back from all subjects—four of each type. All cartoons were drawn
the phone he was thirsty. He went over to the can and from previously published studies (Gallagher et al., 2000;
drank from it. Happe et al., 1999). The ToM cartoons were based around
a character’s lack of knowledge about a physical situation1
(e.g. the presence of a monster, a practical joke). The NMI
Implicit question: Why did Larry drink from the can?
Explicit question: What was Larry thinking about the can?
1 None of the ToM cartoons required an understanding of one character’s
Forced choice questions:
knowledge of another character’s beliefs or intentions, that is, they were
Did he think the can had Coke in it? all first-order rather than second-order ToM tasks (Bishop, 1993; Mazza
Did he know Jack had put milk in the can? et al., 2001).
106 H. Bibby, S. McDonald / Neuropsychologia 43 (2005) 99–114

Table 3 ers (Happe, 1994; Happe et al., 1999). For both stories and
Demographics of the TBI patients and the control group cartoons, answers to implicit questions were scored out of
Continuous variable TBI patients Control subjects two. In the case of ToM tasks, subjects scored one point for
(mean (S.D.)) (mean (S.D.)) an adequate response, and a second point for the use of a
N per group 15 15 mental state term (e.g. thinks, wants, wishes, believes, etc.).
Age (years) 40.5 (10.6) 35.9 (12.3) For NMI tasks, subjects scored two points for an adequate
Education (years) 13.2 (2.5) 14.0 (2.4)
answer. All follow-up questions were allocated one point for
Categorical variable TBI patients Control subjects each correct answer.
percentage percentage
Gender 2.2.4. Working memory task
Male 73.3 66.7 All subjects were administered the Digit Span sub-
Female 26.7 33.3
test from the Wechsler adult intelligence scale (3rd ed.)
Pre-morbid occupation (WAIS-III) (Wechsler, 1997) which measures memory span
Professional/manager 28.6 26.7
for digits repeated forwards and backwards. Based on Davis
Sales/clerical 28.6 13.3
Skilled trade 35.7 40.0 and Pratt (1995), the current study used the longest span
Unskilled trade 7.1 13.3 of digits correctly repeated backwards as an absolute (un-
Unemployed 0.0 6.7 scaled) measure of subject’s ability to mentally manipulate
Post-injury occupation∗ information.
Professional/manager 6.7 N/A
Sales/clerical 13.3 2.3. Design and procedure
Skilled trade 0.0
Unskilled trade 0.0
Unemployed 46.7
The University of NSW ethics committee, as well as the
Volunteer 26.7 ethics committee of each participating rehabilitation centre
Student 6.7 approved the study. It was performed in accordance with
∗ Significant difference at P < 0.05.
the ethical standards laid down in the 1964 Declaration of
Helsinki. All subjects gave their informed consent prior to
cartoons were based around physical cause and effect (e.g. their inclusion in the study.
a shrinking potion) or a reference to a cultural concept (e.g. Subjects were each tested in a single session of 1–1.5 h.
three blind mice). Cartoons and stories were presented in randomised order.
Each cartoon was individually presented to subjects on The entire story or cartoon caption was repeated once if
A4 paper in a protective sheet. Subjects were allowed 10 s subjects requested it. No other assistance was given, and al-
to examine the cartoon. One ToM and one NMI cartoon though general encouragement was provided throughout the
included a brief caption. These were read to subjects at the session, no feedback was given about the correctness of an-
beginning of the ten-second period. The cartoons remained swers. All subjects with TBI and most controls were tested
in front of the subjects while four questions were asked. In individually, and their responses to questions were recorded
the case of the ToM cartoons the questions were: verbatim for subsequent scoring by the first author. Some
control subjects were tested in small groups of two or three
(1) A general question implicitly requiring an inference to
people. In this case, the procedure was identical, except that
be made about a character’s mental state. Based on
subjects wrote their own responses on a standard form once
Happe, Malhi, and Checkley (2001), subjects were asked
the story and questions had been read to them. After all sto-
to explain why each cartoon was funny.
ries and cartoons were presented, subjects were administered
(2) A follow-up question explicitly asking about mental
the working memory task. In the case of group administra-
states.
tions to control subjects, this task was given individually in
(3) Two further follow-up questions. These were presented
a separate room.
in the same forced choice format as the stories.
Again, the questions were always asked in order from
least to most explicit, to prevent cuing. For NMI cartoons, a 3. Results
similar set of four questions were asked, but in this case the
mental states of the characters were irrelevant and the infer- 3.1. Story tasks
ences concerned things such as physical cause and effect.
Examples of a ToM and an NMI cartoon are in Appendices A For each subject, total scores for first-order ToM,
and B with some sample responses. second-order ToM and NMI stories were calculated by sum-
mating scores across all questions. Fig. 1 presents the mean
2.2.3. Scoring total score for each type of story for subjects with and with-
The scoring system for implicit questions was adapted out TBI. A 3 (type of story) × 2 (TBI) analysis of variance
from Channon and Crawford (2000) and Happe and cowork- (ANOVA) was performed to examine the patterns of scores
H. Bibby, S. McDonald / Neuropsychologia 43 (2005) 99–114 107

the main effect of cartoon, F(1,28) = 0.452, P = 0.5). There


was also no evidence that the pattern of differences be-
tween TBI subjects and controls varied across different car-
toon types (for the interaction effect, F(1,28) = 2.04, P =
0.16).

3.3. Comparison of stories and cartoons

To examine the effect of type of material (story or car-


toon), subjects’ scores on first-order ToM and NMI sto-
ries were compared to those on ToM and NMI cartoons
(second-order ToM stories were not included, as there
Fig. 1. Mean total score in story tasks for subjects with and without TBI. were no second-order inferences required in the ToM car-
toons). A 2 (type of material) × 2 (type of inference) × 2
(TBI) ANOVA revealed that, consistent with findings when
for the two groups. Subjects with TBI received significantly
stories and cartoons were considered separately, subjects
lower scores than control subjects (a main effect of TBI),
with TBI received significantly lower scores than control
F(1,28) = 8.312, P < 0.01, and story types differed appre-
subjects (a main effect of TBI), F(1,28) = 14.568, P <
ciably in the scores that subjects obtained on them (a main
0.01. This difference was greater for cartoons than for
effect of story), F(2,56) = 7.027, P < 0.01. However, there
stories (a significant interaction), F(1,28) = 10.942, P <
was no evidence that the pattern of differences between TBI
0.01, but there was no evidence that the type of inference
subjects and controls varied across different story types (for
(ToM or NMI) influenced it (for the interaction, F(1,28)
the interaction effect, F(2,56) = 0.283, P = 0.75).
= 5.208, P = 0.385). Further, scores on cartoons were
Follow-up tests of contrasts revealed that scores on
lower than scores on stories (a main effect of type of mate-
second-order ToM stories were significantly lower than
rial), F(1,28) = 118.129, P < 0.001. No other effects were
both first-order stories, F(1,28) = 12.963, P < 0.01, and
significant.
NMI stories, F(1,28) = 4.920, P < 0.05. There was no ev-
idence of a significant difference between first-order ToM
and NMI stories (F(1,28) = 1.200, P = 0.772). 3.4. Examining the impact of working memory

3.2. Cartoon tasks 3.4.1. Story tasks


In order to determine whether working memory medi-
ated the significant findings for ToM and NMI stories, a
Fig. 2 presents the mean total score (summated across
3 (type of story) × 2 (TBI) analysis of covariance (AN-
all question types) for each type of cartoon for subjects
COVA) was performed with subjects’ longest digit span
with and without TBI. A 2 (type of cartoon) × 2 (TBI)
backwards as a covariate. The main effect of TBI was re-
ANOVA revealed that, as with the stories, subjects with TBI
duced, but remained significant, F(1,27) = 6.53, P = 0.017
received significantly lower scores than control subjects (a
(previously 0.002). In other words, when working mem-
main effect of TBI), F(1,28) = 17.833, P < 0.001. How-
ory performance was controlled, subjects with TBI still per-
ever, there was no evidence that cartoon types differed ap-
formed significantly worse than control subjects on story
preciably in the scores that subjects obtained on them (for
tasks.

3.4.2. Cartoon tasks


In order to determine whether working memory medi-
ated the significant findings for ToM and NMI cartoons, a
2 (type of cartoon) × 2 (TBI) ANCOVA was performed,
using the same covariate as for stories. The same pattern
seen with the stories emerged, i.e. the main effect of TBI
was reduced, but remained significant, F(1,27) = 16.628
(previously 168.033), P < 0.001. Interestingly, in contrast
to the story condition, when longest digit span backwards
was a covariate a significant main effect for type of car-
toon emerged, F(1,27) = 5.534, P < 0.05. This indicated
that, when the subjects’ ability to mentally manipulate in-
Fig. 2. Mean total score in cartoon tasks for subjects with and without formation was controlled, a difference between scores on
TBI. ToM and NMI cartoons was revealed, such that scores
108 H. Bibby, S. McDonald / Neuropsychologia 43 (2005) 99–114

Table 4 Table 5
Mean total score for each type of question for NMI, first order ToM and Mean total score for each type of question for NMI and ToM cartoons
second order ToM stories for subjects with and without TBI for subjects with and without TBI
Group Story Type of Mean total Group Cartoon Type of Mean total score
question score (to 1 question (to 1 decimal place)
decimal place) TBI patients NMI Implicit 2.4
TBI patients NMI Implicit 6.4 Explicit 5.1
Explicit 4.9 Forced choice 4.7
Forced choice 6.3
ToM Implicit 2.1
First order ToM Implicit 5.6 Explicit 4.0
Explicit 5.6 Forced choice 6.1
Forced choice 7.3
Control subjects NMI Implicit 5.1
Second order ToM Implicit 4.1 Explicit 6.1
Explicit 4.0 Forced choice 7.3
Forced choice 6.9
ToM Implicit 3.8
Control NMI Implicit 6.7 Explicit 5.7
subjects Forced choice 7.1
Explicit 6.1
Forced choice 7.3
Subjects’ scores on forced choice questions were re-coded
First order ToM Implicit 7.1
Explicit 6.5 using Reid’s (1977) formula2 to adjust for guessing. The
Forced choice 7.7 analyses outlined above were then repeated, with the re-
Second order ToM Implicit 5.8
sults being consistent with those obtained for the unadjusted
Explicit 5.6 scores.
Forced choice 7.3
3.5.2. Cartoon tasks
For each subject, total scores for their responses to im-
on ToM cartoons were significantly lower than on NMI plicit, explicit, and forced choice questions were calculated
cartoons. for each type of cartoon. Table 5 presents the mean total
score for each type of question for NMI and ToM cartoons
3.5. Examining the impact of language demands for TBI and control subjects. A 2 (type of cartoon) × 3
(type of question) × 2 (TBI) ANOVA revealed that, as for
3.5.1. Story tasks stories, the subjects’ scores differed significantly depending
For each subject, total scores for their responses to im- on what type of question was used (a main effect of ques-
plicit, explicit, and forced choice questions were calculated tion type), F(2,56) = 78.586, P < 0.001, and that the differ-
for each type of story. Table 4 presents the mean total score ence between scores on types of cartoons was influenced by
for each type of question for each type of story for TBI and the type of question being asked (a significant interaction),
control subjects. A 3 (type of story) × 3 (type of question) × F(2,56) = 5.137, P < 0.01. Once again there was no evi-
2 (TBI) ANOVA revealed that subjects’ scores differed sig- dence that the pattern of differences between TBI subjects
nificantly depending on what type of question was used (a and controls varied across different types of question (for
main effect of question type), F(2,56) = 39.350, P < 0.001, the interaction, F(2,56) = 1.381, P = 0.26). No other main
and that the difference between scores on types of stories effects or interactions were significant, apart from the main
was influenced by the type of question being asked (a signif- effect of TBI, which has been discussed above.
icant interaction), F(4,112) = 39.350, P < 0.001. There was Follow-up tests of contrasts revealed that scores on forced
no evidence that the pattern of differences between TBI sub- choice questions were significantly higher than on explicit
jects and controls varied across different types of question questions, F(1,28) = 19.47, P < 0.001, and scores on ex-
(for the interaction effect, F(2,56) = 1.702, P = 0.19). No plicit questions were significantly higher than on implicit
other main effects or interactions were significant, apart from questions, F(1,28) = 5.732, P < 0.05. Furthermore, for im-
the main effect of TBI, which has been discussed above. plicit and explicit questions, scores on ToM cartoons were
Follow-up tests of contrasts revealed that scores on forced lower than NMI cartoons, but for forced choice questions,
choice questions were significantly higher than on implicit scores on NMI cartoons were lower than ToM cartoons.
questions, F(1,28) = 37.597, P < 0.001, and scores on im- As with the stories, subjects’ scores on forced choice
plicit questions were significantly higher than on explicit questions were re-coded using Reid’s (1977) formula to ad-
questions, F(1,28) = 5.732, P < 0.05. Furthermore, the dif- 2 S = 1/2(n − 1)[n(R + B/n) + (n − 1)Q − Q2 /(R + B/n)] where S is
ferences between second-order ToM and other types of sto- the adjusted score, n the number of choices per question, R the number
ries were larger for implicit questions than for forced choice of correct answers, B the number of omitted questions and Q the total
questions. number of questions.
H. Bibby, S. McDonald / Neuropsychologia 43 (2005) 99–114 109

just for guessing. The analyses outlined above were then re- model (for NMI cartoons, β = 0.548, P < 0.01; for longest
peated, with the results generally being consistent with those digit span backwards, β = 0.341, P < 0.05). Thus, presence
obtained for the unadjusted scores. However, one additional of TBI did not explain a significantly greater amount of the
effect was found. Specifically, when scores on forced choice variance in ToM cartoon performance above that accounted
questions were adjusted for guessing, the pattern of differ- for by ability to mentally manipulate information and ability
ences between TBI subjects and controls was found to vary to make non-mental inferences.
across different types of question (a significant interaction),
F(1,28) = 6.981, P < 0.05. Follow-up tests of contrasts re- 3.7. Examination of the contribution of chronicity of lesion
vealed that the difference between TBI subjects and controls to performances after TBI
was greater for forced choice questions than explicit ques-
tions. To explore whether the length of time since injury im-
pacted on TBI subjects’ performances on theory of mind
3.6. Further examination of the contribution of inferential tasks, two further multiple regression analyses (MRAs) were
ability to ToM conducted.

To further explore the relative contribution of inferential 3.7.1. Story tasks


and working memory ability in explaining the variance in An MRA was conducted using the Enter method, taking
performance on theory of mind tasks, a number of multiple scores on first-order ToM, second-order ToM and NMI sto-
regression analyses (MRAs) were conducted. ries as predictor variables for the criterion variable of time
elapsed after injury. The resulting model was not significant
3.6.1. First-order ToM stories (F(3,11) = 1.22, P = 0.348). Adjusted R2 = 0.045. In other
A stepwise MRA was conducted taking presence of TBI, words, there was no evidence that chronicity of lesion im-
scores on NMI stories, and performance on the working pacted on performances on the story tasks. β and P values
memory task (longest digit span backwards) as predictor for each predictor variable are shown below:
variables for the criterion variable of scores on first-order
ToM stories. TBI was the only significant predictor, adjusted Predictor variable β P
R2 = 0.175, F(1,29) = 7.136, P < 0.05 for the model, β
= 0.366. Thus, working memory ability and ability to make Total score for first-order ToM stories 0.039 0.893
non-mental inferences about stories did not explain a sig- Total score for second-order −0.340 0.275
nificantly greater amount of the variance in first-order ToM ToM stories
story performance above that accounted for by presence of Total score for NMI stories 0.545 0.110
TBI.
3.7.2. Cartoon tasks
3.6.2. Second-order ToM stories An MRA was conducted using the Enter method, taking
A stepwise MRA was conducted taking presence of TBI, scores on ToM and NMI cartoons as predictor variables for
scores on NMI and first-order ToM stories, and perfor- the criterion variable of time elapsed after injury. The result-
mance on the working memory task as predictor variables ing model was not significant (F(2,12) = 0.556, P = 0.588).
for the criterion variable of scores on second-order ToM Adjusted R2 = −0.068. In other words, there was no evi-
stories. Scores on the working memory task and on NMI dence that chronicity of lesion impacted on performances on
stories were significant predictors, adjusted R2 = 0.326, the cartoon tasks. β and P values for each predictor variable
F(2,29) = 8.011, P < 0.01 for the model (for longest digit are shown below:
span backwards, β = 0.478, P < 0.01; for NMI stories,
β = 0.364, P < 0.05). Thus, presence of TBI and ability Predictor variable β P
to make first-order ToM inferences did not explain a sig- Total score for ToM cartoons 0.204 0.511
nificantly greater amount of the variance in second-order Total score NMI cartoons −1.013 0.311
ToM story performance above that accounted for by ability
to mentally manipulate information and ability to make
non-mental inferences.
4. Discussion
3.6.3. ToM cartoons
A stepwise MRA was conducted taking presence of TBI, 4.1. Theory of mind in traumatic brain injury
scores on NMI cartoons, and performance on the working
memory task as predictor variables for the criterion vari- The present study aimed to determine whether people
able of scores on ToM cartoons. Scores on both the working with severe TBI demonstrate impairment on tasks requir-
memory task and on NMI cartoons were significant predic- ing them to make inferences about other’s mental states
tors, adjusted R2 = 0.351, F(2,29) = 8.842, P < 0.01 for the (ToM tasks) compared to tasks requiring them to make gen-
110 H. Bibby, S. McDonald / Neuropsychologia 43 (2005) 99–114

eral (non-mental) inferences (NMIs). The performance of that of Stone et al. (1998), who found that subjects with dor-
subjects with and without TBI was compared for first and solateral frontal lesions had difficulty with only those ToM
second-order verbal ToM tasks, non-verbal ToM tasks and tasks that placed demands on working memory ability. How-
for verbal and non-verbal NMI tasks. Initial analyses re- ever, their finding only applied to patients with dorsolateral
vealed that subjects with TBI performed more poorly than damage—it did not hold for the orbito-frontal group. Thus,
control subjects on all tasks, and that the nature of the in- it is unsurprising that a similar finding was not obtained for
ference made in each task (mental state or non-mental in- the heterogenous TBI group in the current study.
ference) did not effect the size of this discrepancy. This Further information about the role of working memory in
would seem to suggest that subjects with TBI have a gen- non-verbal tasks was provided by the finding that when back-
eral impairment in the ability to make inferences, rather wards digit span was held constant, a significant difference
than a specific deficit in ToM ability. The observed deficits between types of cartoon emerged such that ToM cartoons
in inference-making are consistent with reports of impaired scored lower than NMI cartoons. This suggests that the NMI
reasoning and problem solving in this group (Lezak, 1995). cartoons were more taxing on working memory than ToM
However, follow-up multiple regression analyses (MRAs) cartoons, and that some other factor besides working mem-
suggest that the explanation of a general inference-making ory caused ToM cartoons to be performed more poorly. This
impairment in TBI subjects is not adequate to explain all factor could be the same general ToM ability thought to un-
the results. Specifically, while subjects’ performance on derlie the verbal first-order ToM task although, once again,
second-order ToM stories and ToM cartoons was signifi- the possibility that some, as yet untested cognitive domain
cantly predicted by inference-making ability (and working is responsible requires examination. For the cartoon tasks,
memory performance), these abilities were not significant additional abilities that could impact on TBI performance
predictors of subjects’ performance on first-order ToM sto- include humour comprehension and spotting visual details,
ries. This raises the possibility that people with TBI may and these could be examined in future research.
also have a specific ToM impairment underlying their poor
performance on verbal first-order tasks. This finding is con- 4.2.2. Implicit language demands
sistent with a number of previous studies that have claimed The language demands of the questions were significantly
to have identified a ToM impairment in subjects with TBI. related to performance on both ToM and NMI tasks for all
Most of these studies (Channon & Crawford, 2000; Dennis subjects. In general, subjects performed better when ques-
et al., 2001; Dimitrov et al., 1996; Santoro & Spiers, 1994) tions were more explicit.3 Furthermore, when implicit ques-
have not included an index of general inferential ability in tions were asked, all subjects performed more poorly on
their design. Thus, the current study increases confidence in non-verbal ToM and second-order verbal ToM tasks com-
their claims and illustrates the importance of including such pared to NMI tasks, but this pattern was diminished or re-
an index in future research. Evenso, despite the apparent versed when forced choice questions were asked. Thus, it
independence of first-order ToM and general inferencing, is clear that performance on ToM tasks is influenced by the
both types of tasks were performed poorly. Therefore, it language demands of the tasks. This is consistent with re-
remains unclear as to whether the first-order ToM perfor- search emphasising the importance of language for ToM de-
mance was, indeed, indicative of a specific weakness or velopment in children (e.g. Garfield et al., 2001).
continued to reflect broader deficits that were simply not Despite the relationship between language and ToM out-
tested in this study. lined above, there was little evidence that the language de-
mands of the questions influenced the size of the difference
4.2. Impact of task demands on ToM performance between the TBI and control groups. The only exception
to this was the finding that, once scores on forced choice
4.2.1. Working memory demands questions were adjusted for guessing, the difference between
As noted above, working memory ability was found to be TBI subjects and controls on cartoon tasks was greater for
a significant predictor of both non-verbal and second-order forced choice questions than for free-response explicit ques-
verbal ToM performance in all subjects. Thus, it is clear that tions. This may be due to that fact that TBI subjects guessed
many ToM tasks do involve working memory. This is gener- more frequently on the forced choice questions, thus the
ally consistent with Davis and Pratt (1995), who found that adjustment formula reduced their scores more significantly
backwards digit span was significantly related to children’s
performance on false-belief tasks. 3 Surprisingly, in the case of story tasks, implicit questions were an-
However, verbal first-order ToM performance was not sig- swered better than free-response explicit questions while forced choice
nificantly predicted by working memory ability in the current explicit questions were the easiest for subjects. This finding did not apply
study. Furthermore, the differences between control and TBI to the cartoon tasks. It was observed that many subjects’ answers to im-
subjects on both ToM and NMI tasks were found to remain plicit questions about the stories (“Why did he/she do that?”) included a
complete answer to the free-response explicit question (“What was he/she
after working memory performance was controlled. Thus, thinking?”), and it may be that some subjects were confused about what
working memory ability does not completely explain the im- was required for the second answer, believing they needed to provide
pairment seen by the TBI group. This finding differs from additional information and thus failing to give a one-point response.
H. Bibby, S. McDonald / Neuropsychologia 43 (2005) 99–114 111

than those of the control group. Regardless of this, there is This is more relevant to predictive false-belief tasks (“where
certainly no evidence that language ability consistently ex- will he look for the doll?”) than tasks that require explana-
plains the weaker performance of the TBI group. This find- tion (“why did he look there?”). In studies of children with
ing contrasts to those of Siegal and coworkers (Siegal et al., autism, Ozonoff et al. (1991) found that executive function-
1996; Surian & Siegal, 2001) who found that subjects with ing was related to ToM performance, while Tager-Flusberg
RHD were able to make accurate false-belief predictions if et al. (1997) failed to do so. Similarly, while researchers such
the need to infer the question’s meaning was removed. This as Channon and Crawford (2000) found a relationship be-
discrepancy may be due to the different patient groups con- tween executive functioning and ToM ability in adults with
sidered in the studies, or it could be because of the different damage to the frontal lobes, others have failed to do so (Bach
types of false-belief tasks employed (prediction versus ex- et al., 2000; Lough et al., 2001; Rowe et al., 2001; Varley
planation). Further research would be needed to determine et al., 2001). Clearly, the relationship between ToM perfor-
which of these is the case. mance and executive functioning remains controversial. In
order to further the argument that ToM is indeed modular,
4.3. Implications of results for the modularity of ToM the findings of the current study suggesting the presence of
a specific ToM deficit need to be replicated in further studies
According to Foder (1983), a cognitive module is a do- that consider the impact of executive functioning and other
main specific inference-making system that is independent cognitive skills not tested in this study.
of other modules and of the diffuse central systems that gov-
ern higher cognitive functions. The findings of the current 4.4. Conclusion and implications
study have implications for the debate about the modular
nature of ToM. Hughes (1998) claimed that correlations be- In conclusion, this study found that patients with se-
tween performance on false-belief tasks and other abilities vere TBI performed more poorly than controls on both
(such as language or working memory) suggest that ToM is NMI and ToM tasks. Further analysis of the data sug-
not a separate cognitive module (i.e. it is not independent of gests that patients with TBI have a general weakness
other modules or systems). However, this claim misses the in inference-making that impairs their performance on
distinction between a task and the conceptual ability it in- non-verbal and second-order verbal ToM tasks. However,
dexes. If some of the systematic variance in false-belief task they may also have a specific ToM deficit that impairs their
performance cannot be explained in terms of other cognitive performance on verbal first-order ToM tasks. Their weaker
skills, it may be due to an independent ToM module. performance on first-order ToM was not correlated with
Given the findings outlined in the current study, the poor general inference ability, and was not completely accounted
performance of TBI subjects on verbal first-order ToM for by working memory ability, or the language demands
tasks does not appear to be adequately accounted for by of the tasks, although there is evidence that each of these
inferential, working memory or language ability. It was not factors contributed to their performance on some of these
related to chronicity of lesion, and it is unlikely to be due tasks. None-the-less, a clear distinction between a lack of
to the general memory demands of the task, because these competence on first-order ToM tasks on the one hand and
were minimised. Further, it cannot be attributed to demo- normal general inferencing ability on the other was not
graphic differences such as gender, age or education level, found. Thus it remains to be determined whether a specific
as there were no significant group differences. Thus, a clear ToM deficit can be observed relative to other tasks with
contendor for the poor ToM performance was not found, comparable (non-mentalising) processing demands. The
other than poor ToM itself. Nevertheless, the case for mod- findings of the current study have implications for the de-
ularity could have been more strongly made had a clear bate about the modular nature of ToM, and, if replicated in
distinction been observed between (impaired) first-order further studies that consider the impact of other cognitive
ToM ability and (intact) general inference ability. This was skills such as executive functioning, would add support for
not the case. Nor did this study address all cognitive skills the claim that ToM ability is a separate cognitive module.
that may potentially impact upon performance on ToM and Finally, the findings of the current study have implications
other inferencing tasks. In particular, there was no index for the rehabilitation of social impairments after TBI. The
of attention or executive functioning—other than working study suggests that a range of factors may impact on TBI
memory—despite the fact that both areas are commonly patients’ social performance, including inferential ability,
disturbed in patients with severe TBI (Lezak, 1995). language comprehension, working memory capacity, ToM
Importantly, the role of executive function in ToM has ability and possibly an understanding of humour. This sug-
been examined in a variety of populations although with gests that, rather than simply applying an existing reha-
mixed results. Some researchers have found that executive bilitation program to train ToM ability (such as those that
functioning is associated with ToM development in children have been developed for people with Asperger’s syndrome
(Hughes, 1998; Wellman et al., 2001). In such cases the in- (Attwood, 1998) and schizophrenia (Sarfati et al., 2000), re-
hibitory control aspect of executive functioning was specifi- habilitation of social deficits after TBI requires a compre-
cally related to children’s ToM performance (Hughes, 1998). hensive individual assessment to determine which factors are
112 H. Bibby, S. McDonald / Neuropsychologia 43 (2005) 99–114

impacting on that individual’s difficulties. Treatment should the ceremony the reception centre calls Betty to warn her
be tailored to address and/or compensate for those factors that the air-conditioning unit has broken down, but they are
that are identified. installing fans to cool off her guests when they arrive.
The ceremony goes smoothly, and everyone drives to the
reception in good spirits. When they arrive, the room looks
Appendix A. Examples of stories and responses beautiful and everyone praises Betty’s taste. But when she
goes to sit down at the head table, the table-cloth is soaking
A.1. Second-order ToM task (adapted from Sullivan et al., and all the napkins are soggy. There is a big puddle on tile
1995) floor.
Implicit question: Why is there so much water on the head
John and Mary are in the park when they see an ice-cream table?
truck. Mary would like to buy an ice-cream but has no money Sample 2-point response: “Because the heat melted the
with her. The ice-cream man tells her to go home and get her ice sculpture of the swan”.
money because he will be staying in the park all day. Mary Sample 0-point response: “Must have been because ev-
goes home and John stays in the park. Then the ice-cream eryone was sweating so much”.
man tells John he is moving to the church. He drives off and
John goes home. On his way to the church the ice-cream man Explicit question: What effect would the broken
meets Mary and tells her where he is going. They arrange air-conditioner have had?
to meet at the church so Mary can buy her ice-cream. Later Sample correct response: “Made the room hot so the swan
John goes to Mary’s house. Her sister says she has gone to melted”.
buy ice-cream. John goes to look for her in the park. Sample incorrect response: “It might have leaked on the
Implicit question: Why does John look for Mary in the table”.
park?
Forced choice questions: Did the air-conditioner leak on
Sample 2-point response: “Because he does not know the table?
she met the ice-cream man who told her to go to the
church“. Correct response: No.
Sample 1-point response: “Because the ice-cream man Did the heat melt the swan?
moved after she left the park”.
Sample 0-point response: “He does not really want to find Correct response: Yes.
her”.
Explicit question: What was John thinking when he Appendix B. Examples of cartoon and responses
looked for her in the park?
Sample correct response: “That she did not know the B.1. ToM cartoon (adapted from Gallagher et al., 2000):
ice-cream man moved”.
Sample incorrect response: “He must have decided to play
at the park instead”.
Forced choice questions: Does he think Mary will be at
the park?
Correct response: Yes.
Does he know that Mary knows where the ice-cream
truck is?
Correct response: No.

A.2. NMI story (developed for this study)

Betty has been making arrangements for her wedding. She Implicit question: Why is this cartoon funny?
is very happy about the sculpture she has organised for the
head table at the reception—a big, glittering swan carved Sample 2-point response: “Because he does not know the
out of ice. piano is about to fall on his head”.
On the morning of the wedding the weather looks perfect. Sample 1-point response: “He is looking at the stool, but
But as the day continues it gets hotter and hotter, and people the piano is about to fall”.
in the church look sweaty and uncomfortable. Just before Sample 0-point response: “It is not funny”.
H. Bibby, S. McDonald / Neuropsychologia 43 (2005) 99–114 113

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