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Child Neuropsychology: A Journal on
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Cognitive contributions to theory
of mind ability in children with a
traumatic head injury
Naomi Kahana Levy
a
& Noach Milgram
a
a
The Department of Behavioural Sciences, Ariel University, Ariel,
Israel
Published online: 12 Dec 2014.
To cite this article: Naomi Kahana Levy & Noach Milgram (2014): Cognitive contributions
to theory of mind ability in children with a traumatic head injury, Child Neuropsychology:
A Journal on Normal and Abnormal Development in Childhood and Adolescence, DOI:
10.1080/09297049.2014.985642
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Downloadedby[NaomiKahanaLevy]at19:3615December2014
Cognitive contributions to theory of mind ability in
children with a traumatic head injury
Naomi Kahana Levy and Noach Milgram
The Department of Behavioural Sciences, Ariel University, Ariel, Israel
The objective of the current study is to examine the contribution of intellectual abilities, executive
functions (EF), and facial emotion recognition to difficulties in Theory of Mind (ToM) abilities in
children with a traumatic head injury. Israeli children with a traumatic head injury were compared
with their non-injured counterparts. Each group included 18 children (12 males) ages 7–13.
Measurements included reading the mind in the eyes, facial emotion recognition, reasoning the
other’s characteristics based on motive and outcome, Raven’s Coloured Progressive Matrices, simila-
rities and digit span (Wechsler Intelligence Scale for Children – Revised 95 subscales), verbal fluency,
and the Behaviour Rating Inventory of Executive Functions. Non-injured children performed sig-
nificantly better on ToM, abstract reasoning, and EF measures compared with children with a
traumatic head injury. However, differences in ToM abilities between the groups were no longer
significant after controlling for abstract reasoning, working memory, verbal fluency, or facial emotion
recognition. Impaired ToM recognition and reasoning abilities after a head injury may result from
other cognitive impairments. In children with mild and moderate head injury, poorer performance on
ToM tasks may reflect poorer abstract reasoning, a general tendency to concretize stimuli, working
memory and verbal fluency deficits, and difficulties in facial emotion recognition, rather than deficits
in the ability to understand the other’s thoughts and emotions. ToM impairments may be secondary to
a range of cognitive deficits in determining social outcomes in this population.
Keywords: Theory of mind; Cognitive; Traumatic head injury; Executive functions; Israel.
It is estimated that in the United States approximately 475,000 children ages 0–14 are
hospitalized each year as a result of head injuries, and of the 435,000 children who arrive
to an emergency room, 85% are defined as suffering from a mild head injury (Langlois,
Rutland-Brown, & Thomas, 2005). In recent years, an increasing number of studies have
examined the neuropsychological, behavioral, and psychosocial effects of children’s
traumatic brain injuries (TBIs) of varying degrees (Belanger, Curtiss, Demery,
Lebowitz, & Vanderploeg, 2005; Tonks, Williams, Frampton, Yates, & Slater, 2007;
Tonks, Yates, Williams, Frampton, & Slater, 2010). In a systematic review of 28 studies,
The authors would like to thank ALYN hospital in Jerusalem for their help and cooperation, and to
Mr. Yoni Shimoni, the neuropsychologist who accompanied the study on behalf of the ALYN hospital. This
article is in memory of Prof. Noach Milgram, who passed away before its publication.
The authors report no declarations of interest.
Address correspondence to Naomi Kahana Levy, M.B. 87, Nehusha, 99833, Israel.
E-mail: Naomile11@gmail.com
Child Neuropsychology, 2014
http://dx.doi.org/10.1080/09297049.2014.985642
© 2014 Taylor & Francis
Downloadedby[NaomiKahanaLevy]at19:3615December2014
it was concluded that children and adolescents with TBI consistently manifest social
adjustment and social cognition difficulties (Rosema, Crowe, & Anderson, 2012).
The term “Theory of Mind” (ToM) ability (Premack & Woodruff, 1978) refers to a
multidimensional ability that enables understanding the mental state of one’s peers including
their expectations, feelings, and thoughts, as well as the development of empathy towards
others. Thus, ToM ability relates to essential components of mutual social relationships.
ToM ability may be divided into two main elements (Sabbagh, 2004; Tager-Flusberg,
2001): (a) immediate recognition of the other’s emotional or cognitive state, based on
accessible visual or auditory information and (b) reasoning about the other’s emotional or
cognitive state. The cooperation of these two elements, recognition and reasoning, is needed
in order produce a reliable judgment on the other’s mental state. A successful recognition of
mental states based on nonverbal cues (e.g., identifying one’s center of attention by one’s
eye gaze, emotional facial recognition) emerges among infants as young as 4 months
(Montague & Walker-Andrews, 2001; Serrano, Iglesias, & Loeches, 1992) and enables
the development of social evaluation skills, such as judging social behavior (Hamlin, Wynn,
& Bloom, 2007), predicting other’s preferences (Repacholi & Gopnik, 1997), and inferring
the social relationships of others (Liberman, Kinzler, & Woodward, 2014). The reasoning
ability includes perspective-taking abilities and more complex aspects of cognition, such as
reasoning about causes and consequences of mental states and about complex social
behaviors. Perspective-taking ability is acquired at approximately age 3–5 and is manifested
in understanding that some information in social interactions may be available to one but
not to another, which may lead to a different, correct or false, reasoning on reality (Wellman,
Cross, & Watson, 2001). The more complex reasoning abilities (e.g., being able to
distinguish between genuine and apparent emotion) rely on acquired social knowledge
and develop at a later age (Wellman & Liu, 2004). Overall, ToM ability begins to take
shape at ages 2–3 and matures around age 7 (Wellman & Liu, 2004). Indeed, numerous
studies have associated ToM abilities with various forms of social behavior. Children who
lack ToM skills may act in a socially inadequate manner. For example, they may not
apologize for hurting another person’s feelings and may have difficulties understanding
humor, difficulties in social participation, and difficulties responding to indirect and non-
verbal cues (Pettersen, 1991; see Hughes & Leekam, 2004, for a review).
Impairments in both recognition and reasoning elements of ToM abilities among
children with a head injury have been reported. For example, children with head injury
show reduced facial emotion recognition (Schmidt, Hanten, Li, Orsten, & Levin, 2010;
Tlustos et al., 2011; Tonks et al., 2007), as well as poorer performance on social cognition
tasks such as ToM tasks and mental state attribution tasks (Dennis et al., 2012; Levin
et al., 2011; Snodgrass & Knott, 2006; Turkstra, Dixon, & Baker, 2004; Walz, Yeates,
Taylor, Terry, & Shari, 2010). Consequently, some have concluded that impaired ToM
skills contribute to in-practice difficulties in social functioning (Levin et al., 2011;
Pettersen, 1991; Tonks et al., 2007; Walz et al., 2010; Yeates et al., 2004). However, it
may be that social functioning difficulties in children with a head injury can be attributed
not only to deficits in ToM skills but also to potential cognitive contributors to ToM
ability, specifically, to impairments in Executive Functions (EF) and abstract reasoning.
Children with TBI suffer from impairments in EF (Levin & Hanten, 2005), which may
contribute to their social difficulties. Indeed, in a study of children aged 6–12 with TBI,
EF was a significant predictor of poor social outcomes after controlling for background
variables and IQ at approximately 4-year follow-up (Yeates et al., 2004). In addition,
studies of the relationship between ToM impairments and social difficulties did not
2 N. K. LEVY & N. MILGRAM
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examine the impact of abstract reasoning (Snodgrass & Knott, 2006; Tonks et al., 2007;
Turkstra et al., 2004; Yeates et al., 2004). Thus, there are gaps in the knowledge on
potential contributors to ToM abilities and their associated social deficits in children.
Finally, studies that specifically examined ToM ability often focus on a single ToM ability,
either recognition or reasoning (Levin et al., 2011; Tonks et al., 2007; Walz et al., 2010;
Warschausky, Argento, Hurvitz, & Berg, 2003).
The term EF refers to interconnected abilities that mediate between one’s perception
and cognitive processing and one’s actual performance. These abilities enable one to maintain
problem-solving-oriented behavior and to achieve future goals and include planning, impulse
regulation, and thought and action flexibility (Baron, 2004; Catroppa & Anderson, 2006). The
relationship between EF and ToM reasoning abilities is a matter of ongoing debate (Carlson,
Claxton, & Moses, 2013; Carlson, Moses, & Breton, 2002; Hughes & Ensor, 2007; Mutter,
Alcorn, & Welsh, 2006). Findings on the relationship between EF and ToM ability (both
recognition and reasoning abilities) in persons with TBI are inconclusive (Henry, Phillips,
Crawford, Ietswaart, & Summers, 2006; Milders, Ietswaart, Crawford, & Currie, 2006;
Snodgrass & Knott, 2006; Tonks et al., 2007). For example, Tonks et al. compared 18
children with varying degrees of head injury to 67 noninjured controls. They found reduced
ToM recognition ability among the former compared to the latter, a difference that persisted
after controlling for EF, inhibition, and planning and organization measures. Thus, emotion
recognition skills were generally unrelated to cognitive abilities (Tonks et al., 2007).
Conversely, in a study of adults with TBI, ToM recognition abilities were significantly
associated with an EF measure of phonemic fluency among those with TBI but not in controls
(Henry et al., 2006). With regards to social reasoning abilities, associations between social
reasoning ability and EF have been reported among of adults with TBI (Milders et al., 2006).
However, in a study of 15 adults with severe TBI, no associations were found between ToM
social reasoning tasks and EF measures (Muller et al., 2010). A satisfactory resolution of the
contrasting evidence on the relation between EF and ToM ability is yet to be established.
Intelligence may affect the quality of social interaction and the performance on
various cognitive tasks, including ToM tasks (Turkstra, 2008; Walz et al., 2010). While
studies on social cognition among children suffering from a head injury have focused on
verbal aspects of understanding and abstraction abilities, the effect of nonverbal reason-
ing, to our knowledge, has not been examined (e.g., Levin et al., 2011; Walz et al., 2010).
This gap in the literature warrants further investigation particularly due to the relationship
between the ability for abstract reasoning, both verbal and nonverbal, and general
intelligence (Kaufman & Lichtenberger, 1999), and evidence suggesting a reduction of
children with TBIs nonverbal reasoning and abstraction abilities that grows with the
severity of the injury (Donders & Warschausky, 1997; Fay et al., 2009).
The objective of the current study is to examine what are the contributors to ToM
impairments in children with a traumatic head injury in an exploratory manner.
Accordingly, we examined the contribution of abstract reasoning, EF, and facial emotion
recognition to differences in ToM recognition and reasoning abilities among children with
a traumatic head injury compared to noninjured children. This examination was facilitated
by the use of two measures of ToM recognition, enhancing its convergent validity. We
hypothesize that noninjured controls would show a higher performance in measures of EF
(Levin & Hanten, 2005), abstract reasoning (Turkstra, 2008), and ToM recognition
(Schmidt et al., 2010) and reasoning (Walz et al., 2010) abilities compared to children
with a head injury. If differences in ToM recognition and reasoning abilities will be found,
the contribution of abstract reasoning, EF, and facial emotion recognition to these ToM
COGNITIVE CONTRIBUTIONS TO THEORY OF MIND 3
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differences will be examined. Given the inconclusive findings on the relationship between
EF and ToM recognition and reasoning ability, and the lack of findings on the effect of
nonverbal reasoning on ToM, no hypothesis regarding the direction of these relationships
was raised. In line with previously reported associations between emotion recognition and
social reasoning (McDonald & Flanagan, 2004), we expected facial emotion recognition
to contribute to social reasoning.
METHODS
Participants
Thirty-six children from the Jerusalem and south regions of Israel participated in the
study. The research group included children with a mild-to-moderate blunt head injury
and the control group included children with a healthy development. The groups were
matched by gender and age, each including 18 children (12 males, 6 females) ages 7–13
each (M = 10.37, SD = 2.18; M = 10.36, SD = 2.23, respectively). Inclusion criteria were:
(a) age 7 and above; (b) hospitalization due to a mild or moderate blunt head injury; (c)
the head injury occurred at least a year prior to study participation; and (d) native Hebrew
speaker. Due to a low number of participants, children with a possible severe head injury
were included. Exclusion criteria were premorbid educational, developmental, psychiatric,
or other medical difficulties, an additional head injury, or no Hebrew reading proficiency.
Participants’ injury profiles are presented in Table 1.
Recruitment and Assessment
The study was approved by the Ethical Committee of Herzog Hospital in Jerusalem,
Israel, on January 2009, and was held between March 2009 and March 2010. Children with
a head injury were identified from a list of persons scheduled for periodical medical
examinations at the ALYN Hospital outpatient clinic for children with acquired and devel-
opmental head injuries in Jerusalem, Israel. The list included approximately 300 children,
32 of whom met inclusion criteria. The researcher contacted the parents of potential
participants via phone and invited them to participate in the study. Twenty parents accepted
the offer. Subsequently, letters detailing the study were sent to future participants and their
parents. Two participants withdrew their participation at this stage. Control participants were
recruited via advertisements in the ALYN Hospital and in the Jerusalem region. Of
approximately 40 persons who responded to these advertisements, 18 parents had children
who matched the research group participants in terms of age and gender. These parents were
contacted by the researcher via phone and their consent for participation was gained.
Subsequently, letters detailing the study were sent to the parents and children of the control
group. The assessments took place at participants’ homes and were scheduled at partici-
pants’ convenience. Assessment duration per participant was approximately 3 hours. Each
parent filled out and signed an informed consent form prior to assessment.
Measurements
ToM Abilities.
Recognition. Reading the mind in the eyes, children’s version (Baron-Cohen,
Wheelwright, Spong, Scahill, & Lawson, 2001; Hebrew translation in Burg-Malki,
4 N. K. LEVY & N. MILGRAM
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Table1InjuryProfilesofParticipantswithTraumaticBrainInjury(n=18).
Years(months)
GenderAgeInjuryage
Yearssince
injuryCauseofinjury
Lossof
consciousnessGCSPTALocationofinjury
Degree(asdescribed
onthechild’sfile)
Male6(11)3(3)3(8)RoadaccidentYes5a
YesLightintraventricularhemorrhageontheleft,
andsignsoflightposteriorsubarachnoid
hemorrhage
Severe
Male7(2)2(5)4(9)FallingfromahighspotYes09-OctnsDAIModerate
Female7(10)5(8)2(3)RoadaccidentYes4a
nsOccipital,frontalSevere
Male7(10)6(10)1RoadaccidentNo15nsMinimalfrontalhaemorrhageontheleftMild
Male8(10)6(3)2(7)RoadaccidentYesnsYesTemporalskullfracturesModerate
Female9(9)7(5)2(4)FallingfromahighspotForseveralminutesnsnsHeadCTyieldednofindingsModerate
Male9(9)7(9)2InjuredduringplayNonsYesFrontalontheleft.Lightepidural
hemorrhageontheleft
Mild
Female9(10)36(10)RoadaccidentYesnsnsFrontalontheright.Possiblehemorrhage
fociontherightfrontalarea
Moderate
Female10(10)3(10)7RoadaccidentYesnsnsHemiparesis.Leftsideneglect(Lt.)Moderate
Female116(1)4(11)RoadaccidentYes10nsLittlehypodensefociinthebasalgangliaModerate
Male11(2)8(10)2(4)FallingfromahighspotVague11-DecYesOccipitalModerate
Male11(3)7(8)3(7)FallNonsnsFrontalleftfractureMild
Male11(10)8(10)3FallingfromahighspotYesnsnsSubduralhemorrhageModerate
Male12(4)8(10)3(6)BlowfromaheavyobjectVaguensnsFrontalandoccipitalfracturesMild
Male12(11)11(2)1(8)RoadaccidentVague13-14nsFronto-temporalfracturesMild
Male13(3)8(2)5(1)RoadaccidentYes5a
nsFrontalfracture.Ontherightoftheorbit,a
generalcerebraledemawithopencisterns
andasmalltemporalbraincontusionon
theright.Lightsubarachnoidhemorrhage
ontheleft
Severe
Male13(7)3(6)11(1)RoadaccidentYes3a
nsFrontalcontusionanddiffusionchangesSevere
(Continued)
COGNITIVE CONTRIBUTIONS TO THEORY OF MIND 5
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Table1(Continued).
Years(months)
GenderAgeInjuryage
Yearssince
injuryCauseofinjury
Lossof
consciousnessGCSPTALocationofinjury
Degree(asdescribed
onthechild’sfile)
Female13(7)9(8)3(11)RoadaccidentYes3a
nsRightoccipitalhematomaandparietalright
hematoma.Subduralhematomaonthe
right.Fracturesontheparietalboneand
occipitalboneontheright.Spiralparietal-
temporalfractureontheright
Severe
Note.GCS=GlasgowComaScale,PTA=Posttraumaticamnesia,ns.=Notspecified,DAI=Diffuseaxonalinjury.ThedurationofPTAwasnotspecifiedformostoftheparticipants.
Theterm“Vague”underlossofconsciousnessreferstotheperson’sstateofconsciousness.
a
GCSmeasuredonevacuation.
6 N. K. LEVY & N. MILGRAM
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2009). This is a computer-administered measure, designed for ages 6 and above. The child
is presented with 28 colorless images of the eye area on a human face. The child is
requested to choose the word that best captures the image-person’s thought or feeling (out
of four possibilities). Each response is rated as correct or incorrect recognition. The total
score is the sum of correct responses. This instrument has been used in adult (Turkstra,
2008) and child (Snodgrass & Knott, 2006; Tonks et al., 2007) populations with a head
injury.
Facial emotion recognition (Burg-Malki, 2009). The task includes 48 items,
presented via a PowerPoint presentation on a computer: 24 recognition items and 24
matching items. Participants watched a short video showing a man or a woman expressing
a basic emotion (happiness, sadness, fear, anger, surprise, and disgust; 4 items per
emotion) for several seconds, were given four possibilities (four of the above basic six
emotions) and were asked to identify the emotion. Subsequently, a matching item that
refers to the same video is presented. Each matching item includes presenting a target-
video in which an emotion is expressed. The participant is then presented with three
additional videos presenting an emotional expression and is to choose which of the three
expresses the same emotion as the target-video. That is, of the three additional videos, one
matches the target-video (e.g., great fear), and the other two do not match; one presenting
an emotion that matches in its direction (negative or positive) but not in its potency (e.g.,
some anger), and the other matches in potency, but not in its direction (e.g., great
happiness). There are four matching items for each of the above six emotions. The task
includes two practice items of each type (recognition, matching). All the videos presented
have been previously validated for their potency, direction, and emotional label in a
sample of 20 adult Israelis. In the current study, four items (5, 26, 36, and 38) that had
an error-rate over 55% (in the two groups combined) were excluded from analysis. The
total score was the sum number of correct responses on both tasks (range: 0–48).
Social Reasoning. Reasoning the other’s characteristics based on motive and
outcome. Participants are presented with four stories based on the study of Heyman and
Gelman (1998) in their Hebrew version (Geller, 2006). Each story is presented in an
animated cartoon (duration: 10 seconds) on the computer (see Figure 1 for an example
story and illustrations). This is the first use of the tasks using videos on the computer
rather than cards. The use of video was in order to make the task more attractive,
accessible, and experiential. Each story involves two characters. One character (hence-
forth: agent of action) performs a behavior, which leads to a positive or negative response
by the other character. Either a positive motivation for the behavior (e.g., to make
someone happy) or a negative one (e.g., to upset someone) is presented. The agent
behaviors and story outcomes were presented both in a verbal manner and by video.
The agent motives were presented in a verbal manner. Four combinations of motive and
outcome are presented to each participant: a positive motive with a negative outcome, a
positive motive with a positive outcome, a negative motive with a positive outcome, and a
negative motive with a negative outcome. After the presentation of the video with the
agent of action’s behavior, the participant is presented with an outcome image (one of two
possible outcomes: negative or positive) and is asked, “Can you tell why the character
(agent of action) did this?,” and then the researcher provides the motive and repeats the
outcome of the behavior. This verbal presentation of motive and outcome renders emotion
recognition abilities unnecessary. Reasoning the agent’s qualities based on the motive that
COGNITIVE CONTRIBUTIONS TO THEORY OF MIND 7
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“Let me tell you a story about a boy named Shahar. Shahar brought Noam a videotape
and suggested he should watch it”
“Noam watched the tape and was very upset because the movie was very boring”
(negative outcome)
“Noam watched the tape and enjoyed it a lot, the movie was to his liking”
(positive outcome)
Experimenter: “Do you know why Shahar asked Noam to watch the video?”
Positive motive - “He wanted to make Noam happy”
Negative motive - “He wanted to upset Noam”
Figure 1 Drawings used for Story A in the reasoning task, showing the agent’s action and both the positive and
negative outcomes for the other character.
8 N. K. LEVY & N. MILGRAM
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matches the outcome indicates relying on the overt behavior, while reasoning based on the
motive that stands in contrast to the outcome indicates relying on internal states.
Accordingly, all of the following items tap reasoning abilities. First, the participant is
asked to rate the agent of action’s emotion on a scale of 5 faces, expressing great sadness
(1) to great happiness (5). For example, if the agent of action intended to upset the other
character and did not succeed, reasoning that the agent of action is sad would be adequate.
Subsequently, the participant is asked three types of questions tapping reasoning abilities.
The first relates to emotional reaction (a single question: “In your opinion, how would X
[agent of action] feel about what happened to X’s friend?), the second relates to one’s
evaluation of the agent of action and his or her behavior (three items: [a] “Do you think X
is good or bad? Is X very good? Or very bad?; [b] “Do you think X did a good or bad
thing?’ [Items 1 and 2 rated on a scale from 1 {very bad} to 5 {very good}]; and (c)
“Would you like to be a friend of X? [no, don’t know, yes]), and the third relates to
predicting the agent of action’s behavior and aims (four items: [a] “Suppose X saw a child
falling in the yard and asked for help. In your opinion, would X approach the child and
help or keep walking without offering help? [rated on a scale of 1–3; 1 = will offer help,
2 = don’t know, 3 = walk away without helping]; [b] “Suppose X has 10 shekels. If
another child needed money, how much of the 10 shekels would X give him or her?”; [c]
“Suppose that on the next day, a child from kindergarten worked on a painting for a long
time. Do you think X would like that painting to be pretty or ugly; and [d] “Suppose that
on the next day, Y [i.e., X’s friend] were to paint a painting, would X like him or her to
have a pretty painting or an ugly painting? [Items 3 and 4 both rated on a 1 {very ugly} to
5 {very pretty} scale]). This task has not been previously used in samples of children with
a head injury. A low correlation was found between the fourth item (out of the four items
predicting behavior and aims) and the rest of the items on the subscale of negative motive
and outcome, and thus it was excluded from analysis. Cronbach’s alpha was .77. Three
measures were computed: (a) reasoning on qualities when the motive stands in contrast to
the outcome (i.e., positive motive and negative outcome or negative motive and positive
outcome); (b) reasoning on qualities when the motive matches the outcome (i.e., positive
motive and outcome, or negative motive and outcome); and (c) a total score comprised of
the sum of the above. For Measures 1 and 2, scores of the negative motive were reversed,
and the score is the mean of all of the responses. For all three measures, a high score
indicates successful performance.
Executive Functioning.
The Behavior Rating Inventory of Executive Functions (BRIEF; Gioia,
Isquith, Guy, & Kenworthy, 2000). The BRIEF is used to assess executive malfunc-
tions in various populations including children with a head injury (Mangeot, Armstrong,
Colvin, Yeates, & Taylor, 2002), as manifested in one’s everyday behavior at school and
at home (e.g., “repeatedly trying the same approach to solve a problem despite it being
unsuccessful”). It is completed by the child’s parents. The BRIEF has 86 items that
include eight subscales of various EFs: inhibition, flexibility of thought, emotional
control, working memory, planning and organization, arranging objects, initiation, and
control. Two indexes were calculated based on parental ratings on these subscales: (a)
behavioral regulation index (α = .88), which includes the subscales of inhibition, flex-
ibility of thought, and emotional control, and (b) meta-cognitive index (α = .96), which
includes the remaining subscales. Items are rated on a scale of 1–3 (1 = never,
COGNITIVE CONTRIBUTIONS TO THEORY OF MIND 9
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2 = sometimes, 3 = often). Eleven scores were calculated for each participant, based on
the sum scores of each of the eight subscales, two indexes, and a total score (the sum of all
ratings) (Gioia et al., 2000). Interitem reliability was .96.
Digit Span. A verbal subscale of the Wechsler Intelligence Scale for Children –
Revised 95 (WISC-R95) for children (Cahan, 1998; Hebrew adaptation), tapping verbal
working memory and focused attention. The participant is presented with a series of
numbers and is asked to repeat this series immediately, either in the same order (forward
digit-span task; 14 items) or in a reversed order (backward digit-span task; 14 items).
Items are presented in increasing level of difficulty. The total score is the sum of correct
responses (range = 0–28).
Verbal Fluency. Verbal Fluency was assessed by a fluency task (Kavé, 2005). The
participant is requested to generate as many words as possible that belong to a specific
semantic category (e.g., fruits and vegetables) or that begin in a certain letter (e.g., gimel [/g/
]) in 1 minute. The former task measured semantic fluency and the latter task measured
phonemic fluency. On each of these tasks, the total score was the sum of correct responses.
A total verbal fluency score was calculated as the sum of the two tasks’ total scores.
Abstract Reasoning.
Raven’s Coloured Progressive Matrices (RCPM), Parts A and B (Raven,
1956). This measure is designed to assess children’s abstract perceptual reasoning
abilities using nonverbal stimuli. The participant is presented with cards with images of
colorful matrices that are to be completed by one of six possibilities at the bottom of the
card. The task is divided into three parts, each involving the presentation of 12 cards. This
measure taps attention to visual details (Part A), pattern recognition (Part AB), and
analysis and reasoning based on visual stimulus (Part B). The total score is the sum of
correct responses (range: 0–36). In addition, participants’ scores were converted to
percentiles based on external US norms of this measure (Raven, Court, & Raven, 1978).
Similarities. A verbal subscale of the WISC-R95 for children (Cahan, 1998;
Hebrew adaptation), tapping classification ability, abstraction, and verbal reasoning, was
used. The subscale is comprised of 16 items, rated on a scale of 0–2 where 0 = wrong
response, 1 = concrete response, and 2 = good abstract response. The total score is the
sum of ratings (range = 0–32).
The Head Injury Degree of Severity. This score was determined by three
measures: (a) the Glasgow Coma Scale (GCS), administered on admission (McDonald
et al., 1994). The assessment is based on three indicators of consciousness: opening one’s
eyes, verbal response, and motor response. The total score ranges 3–15, where 3–8 = severe
head injury, 9–12 = moderate head injury, 13–15 = mild injury; (b) duration of loss of
consciousness (McDonald et al., 1994) categorized as mild (temporary loss of conscious-
ness, if any), moderate (over 20 minutes), and severe (over 30 minutes); and (c) duration
of Post Traumatic Amnesia (PTA; Prigatano & Gray, 2007) categorized as mild (up to 1
hour following the injury), moderate (1 hour to a single day), and severe (over a day). A
complex mild head injury was defined as a mild head injury that may include skull
fractures and a subdural or epidural bleeding.
10 N. K. LEVY & N. MILGRAM
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Statistical Analysis
Statistical analysis was conducted using SPSS 16. In order to compare the research
group and the control group on background variables (age, grade, number of siblings), a
discriminant analysis was conducted. The research hypothesis was examined via a set of
analyses of variance (ANOVAs) and t comparisons for independent samples. In a sub-
sequent analysis, two-tailed analyses of covariance (ANCOVAs) examining ToM differ-
ences between the research group and the control group were conducted, with measures of
abstract reasoning, EF (BRIEF total score, digit span, verbal fluency), and facial emotion
recognition entered as covariates, each on a separate analysis.
RESULTS
In each group, two thirds were male and one third was female. The bulk of the
families (83.8%) had married parents. Most of the participants (89%) had a mild, com-
plex-mild, or moderate head injury. Four participants had a potentially severe head injury
(GCS = 3–5 at the time of the injury or a clinical description including multiple fractures
and hemorrhages; Table 1). No differences were found on background variables (age,
grade, number of siblings) between children with a blunt head injury and noninjured
children. Comparisons of ToM, EF, and abstract reasoning between the research group
and the control group are presented next.
ToM
Recognition.
Reading the Mind in the Eyes. Children with a traumatic head injury had a
significantly poorer performance on recognizing negative facial expressions compared to
noninjured children (M = 11.94, SD = 3.20; M = 15.00, SD = 3.92, respectively),
t(34) = 2.55, p < .05, two-tailed. No significant differences were found between the
groups for positive stimuli or for the total score.
Facial emotion recognition. Noninjured children scored significantly higher
than children with a traumatic head injury on this task (M = 40.00, SD = 4.47;
M = 36.56, SD = 5.93, respectively), t(20) = 2.20, two-tailed, p < .05.
Social Reasoning.
Reasoning the Other’s Characteristics Based on Motive and Outcome.
Total score comparisons showed that children with a traumatic head injury had a
significantly lower level of performance when compared to noninjured children,
F(1, 34) = 4.37, p < .05, η2
= .11. This persisted when the motive matched the outcome
(M = 4.28, SD = 0.56; M = 4.53, SD = 0.43, respectively) and when the motive stood in
contrast to the outcome (M = 3.56, SD = 0.84; M = 4.02, SD = 0.71, respectively). An
analysis of the results of the item tapping emotional reaction showed a significant
interaction between Group and Motive by Outcome, F(1, 34) = 6.12, p < .05, η2
= .15.
In case of a negative motive with a positive outcome, children with head injury’s rating of
the agent of action’s emotion was significantly more positive when compared to non-
injured children, t(24.17) = 2.71, p < .05 (M = 2.56, SD = 1.65; M = 1.39, SD = 0.77,
COGNITIVE CONTRIBUTIONS TO THEORY OF MIND 11
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respectively). No significant differences between the groups were found for the other
combinations of Motive and Outcome (i.e., positive-positive, positive-negative, and
negative-negative). An analysis of the evaluation items showed a significant interaction
between Group and Motive by Outcome, F(1, 34) = 4.90, p < .05, η2
= .12. The two
groups had similar ratings when the motive matched the outcome, but, when they were in
contrast, an interaction between the ratings emerged: When the motive was positive and
the outcome negative, children with a head injury had lower ratings than that of non-
injured children. In contrast, when the motive was negative, noninjured children had
lower ratings, compared to the children with a head injury (see Table 2). These differences
in emotional reaction and evaluation items of social reasoning were also found in a
subsequent ANOVA analysis (see below). In addition, the ANOVA analysis showed a
significant difference of Motive by Outcome in emotional reaction, F(3, 102) = 54.09,
p < .001, and in evaluation, F(3, 102) = 62.67, p < .001. No differences were found in
predicting the future behavior of the agent of action.
Executive Functioning
A comparison of the BRIEF total scores showed that children with a traumatic head
injury had significantly higher scores compared to noninjured children, t(1, 34) = 18.25,
p < .001, two-tailed (M = 162.67, SD = 38.24; M = 118, SD = 22.45, respectively).
Children with a traumatic head injury had significantly higher scores on each of the EFs
(excluding the arranging objects subscale), on the metacognitive index, and on the
behavioral index, when compared to noninjured children (see Table 3).
Children with a traumatic head injury had a significantly lower level of perfor-
mance on the digit-span task and had lower verbal fluency total scores when compared
to noninjured children, F(1, 34) = 9.26, p < .01, η2
= .21, F(1, 34) = 7.74, p < .01,
η2
= .18, respectively (TBI children digit span: M = 8.72, SD = 2.52; noninjured
children digit span: M = 11.89, SD = 3.58; verbal fluency TBI children: M = 54.56,
SD = 20.24; verbal fluency noninjured children: M = 74.94, SD = 23.58).
Abstract Reasoning
Children with a traumatic head injury had significantly lower levels of performance
on the similarities task, t(34) = 2.73, p < .05, two tailed (M = 13.89, SD = 4.43; M = 18.22,
SD = 5.05, respectively), and on the RCPM, t(34) = 3.13, p < .01, two-tailed (M = 24.44,
SD = 8.50; M = 31.72, SD = 4.95, respectively), when compared to noninjured children.
Table 2 A Comparison of ToM Reasoning Scores by Motive and Outcome (n = 36).
Outcome M (SD)
Children with a traumatic head
injury Noninjured children
Positive Negative Positive Negative
Motive
Positive 4.15 (0.96) 2.84 (0.81) 4.16 (0.38) 3.72 (0.75)
Negative 2.36 (0.26) 1.76 (0.54) 1.69 (0.43) 1.32 (0.28)
12 N. K. LEVY & N. MILGRAM
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The Contribution of Abstract Reasoning, Executive Functioning, and
Facial Emotion Recognition to ToM Differences—Two-Tailed ANCOVA
Analysis
Recognition. After controlling for EF, as measured by the BRIEF, children with a
traumatic head injury had significantly lower scores in recognizing negative facial expres-
sions on the Reading the Mind in the Eyes task when compared to noninjured children,
F(1, 33) = 7.68, p < .01, η2
= .18. On four separate analyses, no significant differences in
recognizing negative facial expressions were found between the groups after controlling
for working memory (digit-span task), verbal fluency, abstract reasoning, and facial
emotion recognition, respectively. Thus, ANCOVA analyses showed that ToM differences
in the Reading the Mind in the Eyes task persisted when EF BRIEF scores were controlled
but not when controlling for working memory, verbal fluency, abstract reasoning, or for
facial emotion recognition.
Social Reasoning. The ANOVA and ANCOVA results for Questions 1–4 in the
element of social reasoning are presented in Table 4.
Emotional Reaction. After controlling for EF as measured by the BRIEF, the
interaction effect of Group and Outcome by Motive persisted, that is, children with a
traumatic head injury showed a significantly poorer social reasoning performance com-
pared to noninjured children, F(3, 99) = 3.23, p < .05, η2
= .08. After controlling for
working memory and verbal fluency, in two separate analyses, the significant effect of
motive by outcome persisted, F(3, 99) = 3.17, p < .05, η2
= .08, F(3, 99) = 4.00, p < .05,
η2
= .10, respectively. After controlling for facial emotion recognition, abstract reasoning,
working memory, and verbal fluency (in four separate analyses), no significant differences
in social reasoning between injured and noninjured participants were found (see Table 4).
Evaluation of the Agent of Action and his Behavior. After controlling for
EF, as measured by the BRIEF, children with a traumatic head injury had a significantly
Table 3 A Comparison of BRIEF Scores by Index, Subscale, and Group (n = 36).
M (SD)
Children with traumatic head injury Noninjured children F(1, 34) η2
Index
Meta-cognitive 84.17 (20.27) 63.44 (13.88) 12.80** 0.43
Behavioral regulation 54.89 (13.11) 37.17 (6.87) 25.79*** 0.27
Subscale
Inhibition 18.44 (5.74) 12.22 (2.48) 17.80** 0.34
Flexibility of response 15.56 (4.27) 11.50 (3.01) 10.82** 0.24
Emotional regulation 20.89 (5.18) 13.44 (2.72) 29.02*** 0.46
Initiation 15.44 (4.38) 11.94 (2.68) 8.34** 0.19
Working memory 19.17 (5.37) 13.56 (3.74) 13.21** 0.28
Planning and organization 22.39 (5.92) 16.78 (4.47) 10.27** 0.23
Arranging objects 11.94 (3.6) 10.22 (3.07) 2.37 0.06
Control 15.22 (4.06) 10.94 (3.07) 12.66** 0.27
Note. *p < .05. **p < .01. ***p < .001, two tailed level of significance.
COGNITIVE CONTRIBUTIONS TO THEORY OF MIND 13
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lower level of performance when the motive stood in contrast to the outcome, when
compared to their noninjured counterparts, F(2.273, 75.14) = 3.41, p < .05, η2
= .09. After
controlling for facial emotion recognition, working memory, and verbal fluency, in three
separate analyses, the significant effect of Motive by Outcome persisted, F(3, 99) = 5.53,
p < .01, η2
= .14; F (2.25, 74.29) = 3.22, p < .05, η2
= .09; F(2.35, 77.56) = 5.01, p < .01,
η2
= .13, respectively, and there were no significant differences between the Groups based
on Motive by Outcome. After controlling for abstract reasoning, no significant effects
were found. Thus, ANCOVA analyses showed that ToM differences in social reasoning
between children with a traumatic head injury and noninjured children persisted after
controlling for EF as measured by the BRIEF and did not persist after controlling for
abstract reasoning, working memory, verbal fluency, or facial emotion recognition (see
Table 4).
DISCUSSION
This study examined differences in ToM abilities, abstract reasoning, and EF in a
sample of 36 Israeli children. Half the sample experienced traumatic head injury (mostly
mild or moderate) and the other half did not. Noninjured children performed significantly
better on ToM recognition and social reasoning, abstract reasoning, and EF measures
when compared with children with a head injury. Differences in ToM recognition and
social reasoning between the groups were no longer significant after controlling for
abstract reasoning, working memory, verbal fluency, or facial emotion recognition.
Children with a head injury scored significantly lower on measures of verbal and
nonverbal abstract reasoning compared to noninjured children. Specifically, children with
Table 4 A Comparison of Analyses on the Social Reasoning Task (n = 36).
ANOVA
Mixed-Model ANCOVA
Controlling
for facial
emotion
recognitiona
Controlling
for
intellectual
abilitiesb
Controlling
for working
memoryc
Controlling
for verbal
fluencyd
Controlling
for BRIEF
total score
F(3, 102) F(3, 99) F(3, 96) F(3, 99) F(3, 99) F(3, 99)
Emotional reaction
(Item 1)
Motive by outcome 54.09*** 0.60 1.97 3.17* 4.00* 0.76
Group 1.10 1.11 0.29 1.49 0.97 0.80
Motive by outcome by
group
2.69* 1.39 1.06 1.52 1.42 3.23*
Evaluation (Items 2–4)
Motive by outcome 62.67*** 5.53** 7.87 3.22* 5.01** 2.39
Group 0.08 0.40 0.08 0.01 0.04 0.07
Motive by outcome by
group
3.65* 0.50 0.47 0.75 0.28 3.41*
a
Measured by the facial emotion recognition task. b
Measured by the Raven Coloured Progressive Matrices,
and similarities. c
Measured by the Digit-Span task total score. d
Measured by the Verbal Fluency task (Semantic
and Phonemic total score).
*p < .05. **p < .01. ***p < .001, two tailed level of significance.
14 N. K. LEVY & N. MILGRAM
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a head injury had difficulties in abstraction and tended to concretize verbal and nonverbal
stimuli, including social stimuli. This finding contributes to the understanding of abstract
reasoning abilities in this population and extends previous findings (Donders &
Warschausky, 1997; Rosenthal, Griffith, Bond, & Miller, 1990). For example, a tendency
towards concrete thinking in both children and adults with a frontal head injury has been
reported (Rosenthal et al., 1990). It is noteworthy that multiple studies have reported
comparable performance on measures of verbal intellectual functioning among children
with TBI and controls (Levin et al., 2011; Snodgrass & Knott, 2006; Walz et al., 2010).
Accordingly, it may be that among children with TBI, abstract reasoning abilities are
particularly vulnerable while language skills are maintained. Such a differential impact on
specific intelligence components may not negatively affect the development of general
intellectual abilities (Nisbett et al., 2012). This should be examined in future longitudinal
studies. Also, studies of larger samples of children with a head injury tapping the different
domains of intellectual abilities are needed.
After controlling for abstract reasoning, no significant differences were found
between children with a head injury and controls in ToM recognition and social reasoning
abilities. Thus, it may be that children with a mild or moderate head injury have decreased
abstraction ability that contributes to their difficulties in performing ToM recognition and
social reasoning tasks. Previous studies of children with a head injury did not control for
abstract reasoning, and more severe head injuries than in the current sample were studied
(Snodgrass & Knott, 2006; Tonks et al., 2007; Turkstra et al., 2004; Turkstra, McDonald,
& DePompei, 2001; Warschausky et al., 2003; Yeates et al., 2004). Furthermore, among
children with autism spectrum disorders, ToM performance has been associated with
intellectual and language skills (Frith, 1994). Whereas verbal abilities have been reported
to predict ToM performance in children with TBI (Walz et al., 2010), to our knowledge,
this is the first report of nonverbal abstraction abilities as contributors of performance on
ToM recognition and social reasoning tasks in children with a head injury.
Children with a mild-to-moderate head injury had more difficulties in recognizing
facial expressions and facial emotion compared to controls. This finding corroborates
previous evidence from multiple studies of children with TBI (Pettersen, 1991; Schmidt
et al., 2010; Snodgrass & Knott, 2006; Tonks et al., 2007). For example, children with
moderate-to-severe TBI showed more difficulties in facial emotion recognition when
compared to children who sustained orthopedic injury (Schmidt et al., 2010). After
controlling for facial emotion recognition in the current study, differences between the
groups in ToM recognition and social reasoning ability did not persist. Thus, findings
extend previous reports, suggesting that among children with a mild or moderate head
injury, poor facial emotion recognition contributes to poorer performance in ToM recog-
nition and social reasoning tasks. In line with this, the ability to recognize facial and vocal
emotional expressions has been previously associated with subtle social reasoning skills
such as recognizing sarcasm in others (McDonald & Flanagan, 2004). Interestingly, in the
same study, emotion recognition was not associated with more complex social judgements
such as diplomatic lies (McDonald & Flanagan, 2004). Considering this alongside the
above finding, it may be that ToM recognition ability underlies ToM reasoning deficits to
an extent that depends on reasoning skills’ complexity. The effect of ToM recognition on
different social reasoning tasks should be investigated in future studies.
Children with a traumatic brain injury had a lower level of performance on two EF
tasks (digit span, verbal fluency), and experienced more EF difficulties according to
parental reports when compared to noninjured children. These findings corroborate
COGNITIVE CONTRIBUTIONS TO THEORY OF MIND 15
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previous findings on diminished EF in children with TBI including memory deficits
(Levin & Hanten, 2005) and phonological deficits (Schmidt et al., 2010). Performance
on ToM tasks in the current study was affected by EF as assessed by two direct measures.
This supports the notion that ToM abilities and EF represent two dependent cognitive
paths (Carlson et al., 2013, 2002) and bears implications for understanding the develop-
ment and precursors of ToM abilities. The persistence of ToM differences between the
groups after controlling for EF as measured by parental report may be due to the lower
sensitivity of the latter in comparison to direct measures. The findings of the current study
indicate that both EF and intellectual abilities affect ToM performance in children with
traumatic head injury. Considering this alongside the fact that some EF and intellectual
abilities overlap (e.g., working memory), future research is needed in order to delineate
specific contributions of EF and intellectual abilities to ToM deficits. From a clinical
perspective, findings underscore the need to utilize ToM assessments that are character-
ized by high specificity and sensitivity and do not additionally tap other intellectual and
cognitive capacities in this population. In line with this, it has been reported that among
children with autism spectrum disorders ToM assessments may involve different informa-
tion-processing requirements other than mentalizing abilities (Brent, Rios, Happé, &
Charman, 2004). In the current study, the ToM task of reading the mind in the eyes
involved vocabulary requirements that may have resulted in lower specificity. Also,
findings suggest that among children with a head injury, social maladjustment (Tonks
et al., 2010) may be due to EF difficulties such as social initiation and emotional
regulation rather than difficulties in understanding the other’s emotions, thoughts, and
perspective. This has implications for the design of interventions aimed at promoting
social adjustment in this population.
A strength of the current study is the comprehensive examination of potential
contributors to both recognition and reasoning ToM elements in children with a traumatic
head injury including understudied predictors such as abstract reasoning. Current ToM
assessments did not tap actual social functioning, compromising ecological validity. This
limitation could be addressed by using videotaped observations (Turkstra et al., 2004) or
by correlating face-to-face test scores with a questionnaire filled out by parents regarding
children’s actual social abilities. Given the differential performance on the two recognition
tasks, it may be that the facial emotion recognition test more adequately reflects ToM
recognition abilities in comparison to the Reading the Mind in the Eyes test in children
ages 7–13. This may due to the former’s use of pictorial information in comparison to the
latter involving vocabulary requirements. We used both direct measures and parental
reports to assess EF. Future studies should use laboratory measures of EF that are
unaffected by parents’ expectations and knowledge derived from clinical assessments
about their child’s functioning. Information regarding ongoing medical issues and current
educational placement was not available. Findings may or may not generalize to other
populations, and studies of the contributors to ToM abilities targeting specific populations
that may experience ToM impairments such as children with autism spectrum disorders
(Brent et al., 2004) or ADHD (Uekermann et al., 2010) are warranted. The current study
had a small number of participants. Approximately 44% of the eligible head-injured group
did not participate. The age range was wide (7–13) and participants had different degrees
of injury. Future studies should examine larger samples of children with a head injury and
focus on a specific injury degree in order to enable comparisons of injured participants by
factors such as age of injury and injury severity.
16 N. K. LEVY & N. MILGRAM
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Notwithstanding these limitations, the current study provides important evidence on
the difficulties experienced in abstract reasoning, EF, and ToM domains among children
who suffered mild or moderate head injuries. Current evidence suggests that impaired
ToM recognition and reasoning abilities after a head injury may result from other
cognitive impairments. The poorer performance on ToM tasks seen among children
with a head injury may reflect poorer abstract reasoning, a general tendency to concretize
stimuli, working memory and verbal fluency deficits, and difficulties in facial emotion
recognition, rather than deficits in the ability to understand the other’s thoughts and
emotions. In other words, ToM impairments may be secondary to a range of cognitive
deficits in determining social outcomes in this population. From a practical perspective,
findings support a greater focus on cognitive impairments in abstract reasoning, working
memory, verbal fluency, and facial emotion recognition rather than on ToM deficits in
providing care for children with a head injury. If cognitive impairments affect ToM
abilities in children with a mild-to-moderate head injury, as found in the current study,
it may be that this pattern is manifested more robustly among children with a severe head
injuries. This should be examined in future investigations. A better understanding of
intellectual, EF, abstract reasoning, and emotion recognition impairments following head
injury is needed in order to promote more efficacious rehabilitative efforts and a more
favorable psychosocial prognosis among children with a head injury.
Original manuscript received August 19, 2013
Revised manuscript accepted November 1, 2014
First published online December 8, 2014
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Cognitive-contributions-to-theory-of-mind-ability-in-children-with-a-traumatic-head-injury

  • 2. This article was downloaded by: [Naomi Kahana Levy] On: 15 December 2014, At: 19:36 Publisher: Routledge Informa Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK Click for updates Child Neuropsychology: A Journal on Normal and Abnormal Development in Childhood and Adolescence Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/ncny20 Cognitive contributions to theory of mind ability in children with a traumatic head injury Naomi Kahana Levy a & Noach Milgram a a The Department of Behavioural Sciences, Ariel University, Ariel, Israel Published online: 12 Dec 2014. To cite this article: Naomi Kahana Levy & Noach Milgram (2014): Cognitive contributions to theory of mind ability in children with a traumatic head injury, Child Neuropsychology: A Journal on Normal and Abnormal Development in Childhood and Adolescence, DOI: 10.1080/09297049.2014.985642 To link to this article: http://dx.doi.org/10.1080/09297049.2014.985642 PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content. This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms &
  • 3. Conditions of access and use can be found at http://www.tandfonline.com/page/terms- and-conditions Downloadedby[NaomiKahanaLevy]at19:3615December2014
  • 4. Cognitive contributions to theory of mind ability in children with a traumatic head injury Naomi Kahana Levy and Noach Milgram The Department of Behavioural Sciences, Ariel University, Ariel, Israel The objective of the current study is to examine the contribution of intellectual abilities, executive functions (EF), and facial emotion recognition to difficulties in Theory of Mind (ToM) abilities in children with a traumatic head injury. Israeli children with a traumatic head injury were compared with their non-injured counterparts. Each group included 18 children (12 males) ages 7–13. Measurements included reading the mind in the eyes, facial emotion recognition, reasoning the other’s characteristics based on motive and outcome, Raven’s Coloured Progressive Matrices, simila- rities and digit span (Wechsler Intelligence Scale for Children – Revised 95 subscales), verbal fluency, and the Behaviour Rating Inventory of Executive Functions. Non-injured children performed sig- nificantly better on ToM, abstract reasoning, and EF measures compared with children with a traumatic head injury. However, differences in ToM abilities between the groups were no longer significant after controlling for abstract reasoning, working memory, verbal fluency, or facial emotion recognition. Impaired ToM recognition and reasoning abilities after a head injury may result from other cognitive impairments. In children with mild and moderate head injury, poorer performance on ToM tasks may reflect poorer abstract reasoning, a general tendency to concretize stimuli, working memory and verbal fluency deficits, and difficulties in facial emotion recognition, rather than deficits in the ability to understand the other’s thoughts and emotions. ToM impairments may be secondary to a range of cognitive deficits in determining social outcomes in this population. Keywords: Theory of mind; Cognitive; Traumatic head injury; Executive functions; Israel. It is estimated that in the United States approximately 475,000 children ages 0–14 are hospitalized each year as a result of head injuries, and of the 435,000 children who arrive to an emergency room, 85% are defined as suffering from a mild head injury (Langlois, Rutland-Brown, & Thomas, 2005). In recent years, an increasing number of studies have examined the neuropsychological, behavioral, and psychosocial effects of children’s traumatic brain injuries (TBIs) of varying degrees (Belanger, Curtiss, Demery, Lebowitz, & Vanderploeg, 2005; Tonks, Williams, Frampton, Yates, & Slater, 2007; Tonks, Yates, Williams, Frampton, & Slater, 2010). In a systematic review of 28 studies, The authors would like to thank ALYN hospital in Jerusalem for their help and cooperation, and to Mr. Yoni Shimoni, the neuropsychologist who accompanied the study on behalf of the ALYN hospital. This article is in memory of Prof. Noach Milgram, who passed away before its publication. The authors report no declarations of interest. Address correspondence to Naomi Kahana Levy, M.B. 87, Nehusha, 99833, Israel. E-mail: Naomile11@gmail.com Child Neuropsychology, 2014 http://dx.doi.org/10.1080/09297049.2014.985642 © 2014 Taylor & Francis Downloadedby[NaomiKahanaLevy]at19:3615December2014
  • 5. it was concluded that children and adolescents with TBI consistently manifest social adjustment and social cognition difficulties (Rosema, Crowe, & Anderson, 2012). The term “Theory of Mind” (ToM) ability (Premack & Woodruff, 1978) refers to a multidimensional ability that enables understanding the mental state of one’s peers including their expectations, feelings, and thoughts, as well as the development of empathy towards others. Thus, ToM ability relates to essential components of mutual social relationships. ToM ability may be divided into two main elements (Sabbagh, 2004; Tager-Flusberg, 2001): (a) immediate recognition of the other’s emotional or cognitive state, based on accessible visual or auditory information and (b) reasoning about the other’s emotional or cognitive state. The cooperation of these two elements, recognition and reasoning, is needed in order produce a reliable judgment on the other’s mental state. A successful recognition of mental states based on nonverbal cues (e.g., identifying one’s center of attention by one’s eye gaze, emotional facial recognition) emerges among infants as young as 4 months (Montague & Walker-Andrews, 2001; Serrano, Iglesias, & Loeches, 1992) and enables the development of social evaluation skills, such as judging social behavior (Hamlin, Wynn, & Bloom, 2007), predicting other’s preferences (Repacholi & Gopnik, 1997), and inferring the social relationships of others (Liberman, Kinzler, & Woodward, 2014). The reasoning ability includes perspective-taking abilities and more complex aspects of cognition, such as reasoning about causes and consequences of mental states and about complex social behaviors. Perspective-taking ability is acquired at approximately age 3–5 and is manifested in understanding that some information in social interactions may be available to one but not to another, which may lead to a different, correct or false, reasoning on reality (Wellman, Cross, & Watson, 2001). The more complex reasoning abilities (e.g., being able to distinguish between genuine and apparent emotion) rely on acquired social knowledge and develop at a later age (Wellman & Liu, 2004). Overall, ToM ability begins to take shape at ages 2–3 and matures around age 7 (Wellman & Liu, 2004). Indeed, numerous studies have associated ToM abilities with various forms of social behavior. Children who lack ToM skills may act in a socially inadequate manner. For example, they may not apologize for hurting another person’s feelings and may have difficulties understanding humor, difficulties in social participation, and difficulties responding to indirect and non- verbal cues (Pettersen, 1991; see Hughes & Leekam, 2004, for a review). Impairments in both recognition and reasoning elements of ToM abilities among children with a head injury have been reported. For example, children with head injury show reduced facial emotion recognition (Schmidt, Hanten, Li, Orsten, & Levin, 2010; Tlustos et al., 2011; Tonks et al., 2007), as well as poorer performance on social cognition tasks such as ToM tasks and mental state attribution tasks (Dennis et al., 2012; Levin et al., 2011; Snodgrass & Knott, 2006; Turkstra, Dixon, & Baker, 2004; Walz, Yeates, Taylor, Terry, & Shari, 2010). Consequently, some have concluded that impaired ToM skills contribute to in-practice difficulties in social functioning (Levin et al., 2011; Pettersen, 1991; Tonks et al., 2007; Walz et al., 2010; Yeates et al., 2004). However, it may be that social functioning difficulties in children with a head injury can be attributed not only to deficits in ToM skills but also to potential cognitive contributors to ToM ability, specifically, to impairments in Executive Functions (EF) and abstract reasoning. Children with TBI suffer from impairments in EF (Levin & Hanten, 2005), which may contribute to their social difficulties. Indeed, in a study of children aged 6–12 with TBI, EF was a significant predictor of poor social outcomes after controlling for background variables and IQ at approximately 4-year follow-up (Yeates et al., 2004). In addition, studies of the relationship between ToM impairments and social difficulties did not 2 N. K. LEVY & N. MILGRAM Downloadedby[NaomiKahanaLevy]at19:3615December2014
  • 6. examine the impact of abstract reasoning (Snodgrass & Knott, 2006; Tonks et al., 2007; Turkstra et al., 2004; Yeates et al., 2004). Thus, there are gaps in the knowledge on potential contributors to ToM abilities and their associated social deficits in children. Finally, studies that specifically examined ToM ability often focus on a single ToM ability, either recognition or reasoning (Levin et al., 2011; Tonks et al., 2007; Walz et al., 2010; Warschausky, Argento, Hurvitz, & Berg, 2003). The term EF refers to interconnected abilities that mediate between one’s perception and cognitive processing and one’s actual performance. These abilities enable one to maintain problem-solving-oriented behavior and to achieve future goals and include planning, impulse regulation, and thought and action flexibility (Baron, 2004; Catroppa & Anderson, 2006). The relationship between EF and ToM reasoning abilities is a matter of ongoing debate (Carlson, Claxton, & Moses, 2013; Carlson, Moses, & Breton, 2002; Hughes & Ensor, 2007; Mutter, Alcorn, & Welsh, 2006). Findings on the relationship between EF and ToM ability (both recognition and reasoning abilities) in persons with TBI are inconclusive (Henry, Phillips, Crawford, Ietswaart, & Summers, 2006; Milders, Ietswaart, Crawford, & Currie, 2006; Snodgrass & Knott, 2006; Tonks et al., 2007). For example, Tonks et al. compared 18 children with varying degrees of head injury to 67 noninjured controls. They found reduced ToM recognition ability among the former compared to the latter, a difference that persisted after controlling for EF, inhibition, and planning and organization measures. Thus, emotion recognition skills were generally unrelated to cognitive abilities (Tonks et al., 2007). Conversely, in a study of adults with TBI, ToM recognition abilities were significantly associated with an EF measure of phonemic fluency among those with TBI but not in controls (Henry et al., 2006). With regards to social reasoning abilities, associations between social reasoning ability and EF have been reported among of adults with TBI (Milders et al., 2006). However, in a study of 15 adults with severe TBI, no associations were found between ToM social reasoning tasks and EF measures (Muller et al., 2010). A satisfactory resolution of the contrasting evidence on the relation between EF and ToM ability is yet to be established. Intelligence may affect the quality of social interaction and the performance on various cognitive tasks, including ToM tasks (Turkstra, 2008; Walz et al., 2010). While studies on social cognition among children suffering from a head injury have focused on verbal aspects of understanding and abstraction abilities, the effect of nonverbal reason- ing, to our knowledge, has not been examined (e.g., Levin et al., 2011; Walz et al., 2010). This gap in the literature warrants further investigation particularly due to the relationship between the ability for abstract reasoning, both verbal and nonverbal, and general intelligence (Kaufman & Lichtenberger, 1999), and evidence suggesting a reduction of children with TBIs nonverbal reasoning and abstraction abilities that grows with the severity of the injury (Donders & Warschausky, 1997; Fay et al., 2009). The objective of the current study is to examine what are the contributors to ToM impairments in children with a traumatic head injury in an exploratory manner. Accordingly, we examined the contribution of abstract reasoning, EF, and facial emotion recognition to differences in ToM recognition and reasoning abilities among children with a traumatic head injury compared to noninjured children. This examination was facilitated by the use of two measures of ToM recognition, enhancing its convergent validity. We hypothesize that noninjured controls would show a higher performance in measures of EF (Levin & Hanten, 2005), abstract reasoning (Turkstra, 2008), and ToM recognition (Schmidt et al., 2010) and reasoning (Walz et al., 2010) abilities compared to children with a head injury. If differences in ToM recognition and reasoning abilities will be found, the contribution of abstract reasoning, EF, and facial emotion recognition to these ToM COGNITIVE CONTRIBUTIONS TO THEORY OF MIND 3 Downloadedby[NaomiKahanaLevy]at19:3615December2014
  • 7. differences will be examined. Given the inconclusive findings on the relationship between EF and ToM recognition and reasoning ability, and the lack of findings on the effect of nonverbal reasoning on ToM, no hypothesis regarding the direction of these relationships was raised. In line with previously reported associations between emotion recognition and social reasoning (McDonald & Flanagan, 2004), we expected facial emotion recognition to contribute to social reasoning. METHODS Participants Thirty-six children from the Jerusalem and south regions of Israel participated in the study. The research group included children with a mild-to-moderate blunt head injury and the control group included children with a healthy development. The groups were matched by gender and age, each including 18 children (12 males, 6 females) ages 7–13 each (M = 10.37, SD = 2.18; M = 10.36, SD = 2.23, respectively). Inclusion criteria were: (a) age 7 and above; (b) hospitalization due to a mild or moderate blunt head injury; (c) the head injury occurred at least a year prior to study participation; and (d) native Hebrew speaker. Due to a low number of participants, children with a possible severe head injury were included. Exclusion criteria were premorbid educational, developmental, psychiatric, or other medical difficulties, an additional head injury, or no Hebrew reading proficiency. Participants’ injury profiles are presented in Table 1. Recruitment and Assessment The study was approved by the Ethical Committee of Herzog Hospital in Jerusalem, Israel, on January 2009, and was held between March 2009 and March 2010. Children with a head injury were identified from a list of persons scheduled for periodical medical examinations at the ALYN Hospital outpatient clinic for children with acquired and devel- opmental head injuries in Jerusalem, Israel. The list included approximately 300 children, 32 of whom met inclusion criteria. The researcher contacted the parents of potential participants via phone and invited them to participate in the study. Twenty parents accepted the offer. Subsequently, letters detailing the study were sent to future participants and their parents. Two participants withdrew their participation at this stage. Control participants were recruited via advertisements in the ALYN Hospital and in the Jerusalem region. Of approximately 40 persons who responded to these advertisements, 18 parents had children who matched the research group participants in terms of age and gender. These parents were contacted by the researcher via phone and their consent for participation was gained. Subsequently, letters detailing the study were sent to the parents and children of the control group. The assessments took place at participants’ homes and were scheduled at partici- pants’ convenience. Assessment duration per participant was approximately 3 hours. Each parent filled out and signed an informed consent form prior to assessment. Measurements ToM Abilities. Recognition. Reading the mind in the eyes, children’s version (Baron-Cohen, Wheelwright, Spong, Scahill, & Lawson, 2001; Hebrew translation in Burg-Malki, 4 N. K. LEVY & N. MILGRAM Downloadedby[NaomiKahanaLevy]at19:3615December2014
  • 8. Table1InjuryProfilesofParticipantswithTraumaticBrainInjury(n=18). Years(months) GenderAgeInjuryage Yearssince injuryCauseofinjury Lossof consciousnessGCSPTALocationofinjury Degree(asdescribed onthechild’sfile) Male6(11)3(3)3(8)RoadaccidentYes5a YesLightintraventricularhemorrhageontheleft, andsignsoflightposteriorsubarachnoid hemorrhage Severe Male7(2)2(5)4(9)FallingfromahighspotYes09-OctnsDAIModerate Female7(10)5(8)2(3)RoadaccidentYes4a nsOccipital,frontalSevere Male7(10)6(10)1RoadaccidentNo15nsMinimalfrontalhaemorrhageontheleftMild Male8(10)6(3)2(7)RoadaccidentYesnsYesTemporalskullfracturesModerate Female9(9)7(5)2(4)FallingfromahighspotForseveralminutesnsnsHeadCTyieldednofindingsModerate Male9(9)7(9)2InjuredduringplayNonsYesFrontalontheleft.Lightepidural hemorrhageontheleft Mild Female9(10)36(10)RoadaccidentYesnsnsFrontalontheright.Possiblehemorrhage fociontherightfrontalarea Moderate Female10(10)3(10)7RoadaccidentYesnsnsHemiparesis.Leftsideneglect(Lt.)Moderate Female116(1)4(11)RoadaccidentYes10nsLittlehypodensefociinthebasalgangliaModerate Male11(2)8(10)2(4)FallingfromahighspotVague11-DecYesOccipitalModerate Male11(3)7(8)3(7)FallNonsnsFrontalleftfractureMild Male11(10)8(10)3FallingfromahighspotYesnsnsSubduralhemorrhageModerate Male12(4)8(10)3(6)BlowfromaheavyobjectVaguensnsFrontalandoccipitalfracturesMild Male12(11)11(2)1(8)RoadaccidentVague13-14nsFronto-temporalfracturesMild Male13(3)8(2)5(1)RoadaccidentYes5a nsFrontalfracture.Ontherightoftheorbit,a generalcerebraledemawithopencisterns andasmalltemporalbraincontusionon theright.Lightsubarachnoidhemorrhage ontheleft Severe Male13(7)3(6)11(1)RoadaccidentYes3a nsFrontalcontusionanddiffusionchangesSevere (Continued) COGNITIVE CONTRIBUTIONS TO THEORY OF MIND 5 Downloadedby[NaomiKahanaLevy]at19:3615December2014
  • 10. 2009). This is a computer-administered measure, designed for ages 6 and above. The child is presented with 28 colorless images of the eye area on a human face. The child is requested to choose the word that best captures the image-person’s thought or feeling (out of four possibilities). Each response is rated as correct or incorrect recognition. The total score is the sum of correct responses. This instrument has been used in adult (Turkstra, 2008) and child (Snodgrass & Knott, 2006; Tonks et al., 2007) populations with a head injury. Facial emotion recognition (Burg-Malki, 2009). The task includes 48 items, presented via a PowerPoint presentation on a computer: 24 recognition items and 24 matching items. Participants watched a short video showing a man or a woman expressing a basic emotion (happiness, sadness, fear, anger, surprise, and disgust; 4 items per emotion) for several seconds, were given four possibilities (four of the above basic six emotions) and were asked to identify the emotion. Subsequently, a matching item that refers to the same video is presented. Each matching item includes presenting a target- video in which an emotion is expressed. The participant is then presented with three additional videos presenting an emotional expression and is to choose which of the three expresses the same emotion as the target-video. That is, of the three additional videos, one matches the target-video (e.g., great fear), and the other two do not match; one presenting an emotion that matches in its direction (negative or positive) but not in its potency (e.g., some anger), and the other matches in potency, but not in its direction (e.g., great happiness). There are four matching items for each of the above six emotions. The task includes two practice items of each type (recognition, matching). All the videos presented have been previously validated for their potency, direction, and emotional label in a sample of 20 adult Israelis. In the current study, four items (5, 26, 36, and 38) that had an error-rate over 55% (in the two groups combined) were excluded from analysis. The total score was the sum number of correct responses on both tasks (range: 0–48). Social Reasoning. Reasoning the other’s characteristics based on motive and outcome. Participants are presented with four stories based on the study of Heyman and Gelman (1998) in their Hebrew version (Geller, 2006). Each story is presented in an animated cartoon (duration: 10 seconds) on the computer (see Figure 1 for an example story and illustrations). This is the first use of the tasks using videos on the computer rather than cards. The use of video was in order to make the task more attractive, accessible, and experiential. Each story involves two characters. One character (hence- forth: agent of action) performs a behavior, which leads to a positive or negative response by the other character. Either a positive motivation for the behavior (e.g., to make someone happy) or a negative one (e.g., to upset someone) is presented. The agent behaviors and story outcomes were presented both in a verbal manner and by video. The agent motives were presented in a verbal manner. Four combinations of motive and outcome are presented to each participant: a positive motive with a negative outcome, a positive motive with a positive outcome, a negative motive with a positive outcome, and a negative motive with a negative outcome. After the presentation of the video with the agent of action’s behavior, the participant is presented with an outcome image (one of two possible outcomes: negative or positive) and is asked, “Can you tell why the character (agent of action) did this?,” and then the researcher provides the motive and repeats the outcome of the behavior. This verbal presentation of motive and outcome renders emotion recognition abilities unnecessary. Reasoning the agent’s qualities based on the motive that COGNITIVE CONTRIBUTIONS TO THEORY OF MIND 7 Downloadedby[NaomiKahanaLevy]at19:3615December2014
  • 11. “Let me tell you a story about a boy named Shahar. Shahar brought Noam a videotape and suggested he should watch it” “Noam watched the tape and was very upset because the movie was very boring” (negative outcome) “Noam watched the tape and enjoyed it a lot, the movie was to his liking” (positive outcome) Experimenter: “Do you know why Shahar asked Noam to watch the video?” Positive motive - “He wanted to make Noam happy” Negative motive - “He wanted to upset Noam” Figure 1 Drawings used for Story A in the reasoning task, showing the agent’s action and both the positive and negative outcomes for the other character. 8 N. K. LEVY & N. MILGRAM Downloadedby[NaomiKahanaLevy]at19:3615December2014
  • 12. matches the outcome indicates relying on the overt behavior, while reasoning based on the motive that stands in contrast to the outcome indicates relying on internal states. Accordingly, all of the following items tap reasoning abilities. First, the participant is asked to rate the agent of action’s emotion on a scale of 5 faces, expressing great sadness (1) to great happiness (5). For example, if the agent of action intended to upset the other character and did not succeed, reasoning that the agent of action is sad would be adequate. Subsequently, the participant is asked three types of questions tapping reasoning abilities. The first relates to emotional reaction (a single question: “In your opinion, how would X [agent of action] feel about what happened to X’s friend?), the second relates to one’s evaluation of the agent of action and his or her behavior (three items: [a] “Do you think X is good or bad? Is X very good? Or very bad?; [b] “Do you think X did a good or bad thing?’ [Items 1 and 2 rated on a scale from 1 {very bad} to 5 {very good}]; and (c) “Would you like to be a friend of X? [no, don’t know, yes]), and the third relates to predicting the agent of action’s behavior and aims (four items: [a] “Suppose X saw a child falling in the yard and asked for help. In your opinion, would X approach the child and help or keep walking without offering help? [rated on a scale of 1–3; 1 = will offer help, 2 = don’t know, 3 = walk away without helping]; [b] “Suppose X has 10 shekels. If another child needed money, how much of the 10 shekels would X give him or her?”; [c] “Suppose that on the next day, a child from kindergarten worked on a painting for a long time. Do you think X would like that painting to be pretty or ugly; and [d] “Suppose that on the next day, Y [i.e., X’s friend] were to paint a painting, would X like him or her to have a pretty painting or an ugly painting? [Items 3 and 4 both rated on a 1 {very ugly} to 5 {very pretty} scale]). This task has not been previously used in samples of children with a head injury. A low correlation was found between the fourth item (out of the four items predicting behavior and aims) and the rest of the items on the subscale of negative motive and outcome, and thus it was excluded from analysis. Cronbach’s alpha was .77. Three measures were computed: (a) reasoning on qualities when the motive stands in contrast to the outcome (i.e., positive motive and negative outcome or negative motive and positive outcome); (b) reasoning on qualities when the motive matches the outcome (i.e., positive motive and outcome, or negative motive and outcome); and (c) a total score comprised of the sum of the above. For Measures 1 and 2, scores of the negative motive were reversed, and the score is the mean of all of the responses. For all three measures, a high score indicates successful performance. Executive Functioning. The Behavior Rating Inventory of Executive Functions (BRIEF; Gioia, Isquith, Guy, & Kenworthy, 2000). The BRIEF is used to assess executive malfunc- tions in various populations including children with a head injury (Mangeot, Armstrong, Colvin, Yeates, & Taylor, 2002), as manifested in one’s everyday behavior at school and at home (e.g., “repeatedly trying the same approach to solve a problem despite it being unsuccessful”). It is completed by the child’s parents. The BRIEF has 86 items that include eight subscales of various EFs: inhibition, flexibility of thought, emotional control, working memory, planning and organization, arranging objects, initiation, and control. Two indexes were calculated based on parental ratings on these subscales: (a) behavioral regulation index (α = .88), which includes the subscales of inhibition, flex- ibility of thought, and emotional control, and (b) meta-cognitive index (α = .96), which includes the remaining subscales. Items are rated on a scale of 1–3 (1 = never, COGNITIVE CONTRIBUTIONS TO THEORY OF MIND 9 Downloadedby[NaomiKahanaLevy]at19:3615December2014
  • 13. 2 = sometimes, 3 = often). Eleven scores were calculated for each participant, based on the sum scores of each of the eight subscales, two indexes, and a total score (the sum of all ratings) (Gioia et al., 2000). Interitem reliability was .96. Digit Span. A verbal subscale of the Wechsler Intelligence Scale for Children – Revised 95 (WISC-R95) for children (Cahan, 1998; Hebrew adaptation), tapping verbal working memory and focused attention. The participant is presented with a series of numbers and is asked to repeat this series immediately, either in the same order (forward digit-span task; 14 items) or in a reversed order (backward digit-span task; 14 items). Items are presented in increasing level of difficulty. The total score is the sum of correct responses (range = 0–28). Verbal Fluency. Verbal Fluency was assessed by a fluency task (Kavé, 2005). The participant is requested to generate as many words as possible that belong to a specific semantic category (e.g., fruits and vegetables) or that begin in a certain letter (e.g., gimel [/g/ ]) in 1 minute. The former task measured semantic fluency and the latter task measured phonemic fluency. On each of these tasks, the total score was the sum of correct responses. A total verbal fluency score was calculated as the sum of the two tasks’ total scores. Abstract Reasoning. Raven’s Coloured Progressive Matrices (RCPM), Parts A and B (Raven, 1956). This measure is designed to assess children’s abstract perceptual reasoning abilities using nonverbal stimuli. The participant is presented with cards with images of colorful matrices that are to be completed by one of six possibilities at the bottom of the card. The task is divided into three parts, each involving the presentation of 12 cards. This measure taps attention to visual details (Part A), pattern recognition (Part AB), and analysis and reasoning based on visual stimulus (Part B). The total score is the sum of correct responses (range: 0–36). In addition, participants’ scores were converted to percentiles based on external US norms of this measure (Raven, Court, & Raven, 1978). Similarities. A verbal subscale of the WISC-R95 for children (Cahan, 1998; Hebrew adaptation), tapping classification ability, abstraction, and verbal reasoning, was used. The subscale is comprised of 16 items, rated on a scale of 0–2 where 0 = wrong response, 1 = concrete response, and 2 = good abstract response. The total score is the sum of ratings (range = 0–32). The Head Injury Degree of Severity. This score was determined by three measures: (a) the Glasgow Coma Scale (GCS), administered on admission (McDonald et al., 1994). The assessment is based on three indicators of consciousness: opening one’s eyes, verbal response, and motor response. The total score ranges 3–15, where 3–8 = severe head injury, 9–12 = moderate head injury, 13–15 = mild injury; (b) duration of loss of consciousness (McDonald et al., 1994) categorized as mild (temporary loss of conscious- ness, if any), moderate (over 20 minutes), and severe (over 30 minutes); and (c) duration of Post Traumatic Amnesia (PTA; Prigatano & Gray, 2007) categorized as mild (up to 1 hour following the injury), moderate (1 hour to a single day), and severe (over a day). A complex mild head injury was defined as a mild head injury that may include skull fractures and a subdural or epidural bleeding. 10 N. K. LEVY & N. MILGRAM Downloadedby[NaomiKahanaLevy]at19:3615December2014
  • 14. Statistical Analysis Statistical analysis was conducted using SPSS 16. In order to compare the research group and the control group on background variables (age, grade, number of siblings), a discriminant analysis was conducted. The research hypothesis was examined via a set of analyses of variance (ANOVAs) and t comparisons for independent samples. In a sub- sequent analysis, two-tailed analyses of covariance (ANCOVAs) examining ToM differ- ences between the research group and the control group were conducted, with measures of abstract reasoning, EF (BRIEF total score, digit span, verbal fluency), and facial emotion recognition entered as covariates, each on a separate analysis. RESULTS In each group, two thirds were male and one third was female. The bulk of the families (83.8%) had married parents. Most of the participants (89%) had a mild, com- plex-mild, or moderate head injury. Four participants had a potentially severe head injury (GCS = 3–5 at the time of the injury or a clinical description including multiple fractures and hemorrhages; Table 1). No differences were found on background variables (age, grade, number of siblings) between children with a blunt head injury and noninjured children. Comparisons of ToM, EF, and abstract reasoning between the research group and the control group are presented next. ToM Recognition. Reading the Mind in the Eyes. Children with a traumatic head injury had a significantly poorer performance on recognizing negative facial expressions compared to noninjured children (M = 11.94, SD = 3.20; M = 15.00, SD = 3.92, respectively), t(34) = 2.55, p < .05, two-tailed. No significant differences were found between the groups for positive stimuli or for the total score. Facial emotion recognition. Noninjured children scored significantly higher than children with a traumatic head injury on this task (M = 40.00, SD = 4.47; M = 36.56, SD = 5.93, respectively), t(20) = 2.20, two-tailed, p < .05. Social Reasoning. Reasoning the Other’s Characteristics Based on Motive and Outcome. Total score comparisons showed that children with a traumatic head injury had a significantly lower level of performance when compared to noninjured children, F(1, 34) = 4.37, p < .05, η2 = .11. This persisted when the motive matched the outcome (M = 4.28, SD = 0.56; M = 4.53, SD = 0.43, respectively) and when the motive stood in contrast to the outcome (M = 3.56, SD = 0.84; M = 4.02, SD = 0.71, respectively). An analysis of the results of the item tapping emotional reaction showed a significant interaction between Group and Motive by Outcome, F(1, 34) = 6.12, p < .05, η2 = .15. In case of a negative motive with a positive outcome, children with head injury’s rating of the agent of action’s emotion was significantly more positive when compared to non- injured children, t(24.17) = 2.71, p < .05 (M = 2.56, SD = 1.65; M = 1.39, SD = 0.77, COGNITIVE CONTRIBUTIONS TO THEORY OF MIND 11 Downloadedby[NaomiKahanaLevy]at19:3615December2014
  • 15. respectively). No significant differences between the groups were found for the other combinations of Motive and Outcome (i.e., positive-positive, positive-negative, and negative-negative). An analysis of the evaluation items showed a significant interaction between Group and Motive by Outcome, F(1, 34) = 4.90, p < .05, η2 = .12. The two groups had similar ratings when the motive matched the outcome, but, when they were in contrast, an interaction between the ratings emerged: When the motive was positive and the outcome negative, children with a head injury had lower ratings than that of non- injured children. In contrast, when the motive was negative, noninjured children had lower ratings, compared to the children with a head injury (see Table 2). These differences in emotional reaction and evaluation items of social reasoning were also found in a subsequent ANOVA analysis (see below). In addition, the ANOVA analysis showed a significant difference of Motive by Outcome in emotional reaction, F(3, 102) = 54.09, p < .001, and in evaluation, F(3, 102) = 62.67, p < .001. No differences were found in predicting the future behavior of the agent of action. Executive Functioning A comparison of the BRIEF total scores showed that children with a traumatic head injury had significantly higher scores compared to noninjured children, t(1, 34) = 18.25, p < .001, two-tailed (M = 162.67, SD = 38.24; M = 118, SD = 22.45, respectively). Children with a traumatic head injury had significantly higher scores on each of the EFs (excluding the arranging objects subscale), on the metacognitive index, and on the behavioral index, when compared to noninjured children (see Table 3). Children with a traumatic head injury had a significantly lower level of perfor- mance on the digit-span task and had lower verbal fluency total scores when compared to noninjured children, F(1, 34) = 9.26, p < .01, η2 = .21, F(1, 34) = 7.74, p < .01, η2 = .18, respectively (TBI children digit span: M = 8.72, SD = 2.52; noninjured children digit span: M = 11.89, SD = 3.58; verbal fluency TBI children: M = 54.56, SD = 20.24; verbal fluency noninjured children: M = 74.94, SD = 23.58). Abstract Reasoning Children with a traumatic head injury had significantly lower levels of performance on the similarities task, t(34) = 2.73, p < .05, two tailed (M = 13.89, SD = 4.43; M = 18.22, SD = 5.05, respectively), and on the RCPM, t(34) = 3.13, p < .01, two-tailed (M = 24.44, SD = 8.50; M = 31.72, SD = 4.95, respectively), when compared to noninjured children. Table 2 A Comparison of ToM Reasoning Scores by Motive and Outcome (n = 36). Outcome M (SD) Children with a traumatic head injury Noninjured children Positive Negative Positive Negative Motive Positive 4.15 (0.96) 2.84 (0.81) 4.16 (0.38) 3.72 (0.75) Negative 2.36 (0.26) 1.76 (0.54) 1.69 (0.43) 1.32 (0.28) 12 N. K. LEVY & N. MILGRAM Downloadedby[NaomiKahanaLevy]at19:3615December2014
  • 16. The Contribution of Abstract Reasoning, Executive Functioning, and Facial Emotion Recognition to ToM Differences—Two-Tailed ANCOVA Analysis Recognition. After controlling for EF, as measured by the BRIEF, children with a traumatic head injury had significantly lower scores in recognizing negative facial expres- sions on the Reading the Mind in the Eyes task when compared to noninjured children, F(1, 33) = 7.68, p < .01, η2 = .18. On four separate analyses, no significant differences in recognizing negative facial expressions were found between the groups after controlling for working memory (digit-span task), verbal fluency, abstract reasoning, and facial emotion recognition, respectively. Thus, ANCOVA analyses showed that ToM differences in the Reading the Mind in the Eyes task persisted when EF BRIEF scores were controlled but not when controlling for working memory, verbal fluency, abstract reasoning, or for facial emotion recognition. Social Reasoning. The ANOVA and ANCOVA results for Questions 1–4 in the element of social reasoning are presented in Table 4. Emotional Reaction. After controlling for EF as measured by the BRIEF, the interaction effect of Group and Outcome by Motive persisted, that is, children with a traumatic head injury showed a significantly poorer social reasoning performance com- pared to noninjured children, F(3, 99) = 3.23, p < .05, η2 = .08. After controlling for working memory and verbal fluency, in two separate analyses, the significant effect of motive by outcome persisted, F(3, 99) = 3.17, p < .05, η2 = .08, F(3, 99) = 4.00, p < .05, η2 = .10, respectively. After controlling for facial emotion recognition, abstract reasoning, working memory, and verbal fluency (in four separate analyses), no significant differences in social reasoning between injured and noninjured participants were found (see Table 4). Evaluation of the Agent of Action and his Behavior. After controlling for EF, as measured by the BRIEF, children with a traumatic head injury had a significantly Table 3 A Comparison of BRIEF Scores by Index, Subscale, and Group (n = 36). M (SD) Children with traumatic head injury Noninjured children F(1, 34) η2 Index Meta-cognitive 84.17 (20.27) 63.44 (13.88) 12.80** 0.43 Behavioral regulation 54.89 (13.11) 37.17 (6.87) 25.79*** 0.27 Subscale Inhibition 18.44 (5.74) 12.22 (2.48) 17.80** 0.34 Flexibility of response 15.56 (4.27) 11.50 (3.01) 10.82** 0.24 Emotional regulation 20.89 (5.18) 13.44 (2.72) 29.02*** 0.46 Initiation 15.44 (4.38) 11.94 (2.68) 8.34** 0.19 Working memory 19.17 (5.37) 13.56 (3.74) 13.21** 0.28 Planning and organization 22.39 (5.92) 16.78 (4.47) 10.27** 0.23 Arranging objects 11.94 (3.6) 10.22 (3.07) 2.37 0.06 Control 15.22 (4.06) 10.94 (3.07) 12.66** 0.27 Note. *p < .05. **p < .01. ***p < .001, two tailed level of significance. COGNITIVE CONTRIBUTIONS TO THEORY OF MIND 13 Downloadedby[NaomiKahanaLevy]at19:3615December2014
  • 17. lower level of performance when the motive stood in contrast to the outcome, when compared to their noninjured counterparts, F(2.273, 75.14) = 3.41, p < .05, η2 = .09. After controlling for facial emotion recognition, working memory, and verbal fluency, in three separate analyses, the significant effect of Motive by Outcome persisted, F(3, 99) = 5.53, p < .01, η2 = .14; F (2.25, 74.29) = 3.22, p < .05, η2 = .09; F(2.35, 77.56) = 5.01, p < .01, η2 = .13, respectively, and there were no significant differences between the Groups based on Motive by Outcome. After controlling for abstract reasoning, no significant effects were found. Thus, ANCOVA analyses showed that ToM differences in social reasoning between children with a traumatic head injury and noninjured children persisted after controlling for EF as measured by the BRIEF and did not persist after controlling for abstract reasoning, working memory, verbal fluency, or facial emotion recognition (see Table 4). DISCUSSION This study examined differences in ToM abilities, abstract reasoning, and EF in a sample of 36 Israeli children. Half the sample experienced traumatic head injury (mostly mild or moderate) and the other half did not. Noninjured children performed significantly better on ToM recognition and social reasoning, abstract reasoning, and EF measures when compared with children with a head injury. Differences in ToM recognition and social reasoning between the groups were no longer significant after controlling for abstract reasoning, working memory, verbal fluency, or facial emotion recognition. Children with a head injury scored significantly lower on measures of verbal and nonverbal abstract reasoning compared to noninjured children. Specifically, children with Table 4 A Comparison of Analyses on the Social Reasoning Task (n = 36). ANOVA Mixed-Model ANCOVA Controlling for facial emotion recognitiona Controlling for intellectual abilitiesb Controlling for working memoryc Controlling for verbal fluencyd Controlling for BRIEF total score F(3, 102) F(3, 99) F(3, 96) F(3, 99) F(3, 99) F(3, 99) Emotional reaction (Item 1) Motive by outcome 54.09*** 0.60 1.97 3.17* 4.00* 0.76 Group 1.10 1.11 0.29 1.49 0.97 0.80 Motive by outcome by group 2.69* 1.39 1.06 1.52 1.42 3.23* Evaluation (Items 2–4) Motive by outcome 62.67*** 5.53** 7.87 3.22* 5.01** 2.39 Group 0.08 0.40 0.08 0.01 0.04 0.07 Motive by outcome by group 3.65* 0.50 0.47 0.75 0.28 3.41* a Measured by the facial emotion recognition task. b Measured by the Raven Coloured Progressive Matrices, and similarities. c Measured by the Digit-Span task total score. d Measured by the Verbal Fluency task (Semantic and Phonemic total score). *p < .05. **p < .01. ***p < .001, two tailed level of significance. 14 N. K. LEVY & N. MILGRAM Downloadedby[NaomiKahanaLevy]at19:3615December2014
  • 18. a head injury had difficulties in abstraction and tended to concretize verbal and nonverbal stimuli, including social stimuli. This finding contributes to the understanding of abstract reasoning abilities in this population and extends previous findings (Donders & Warschausky, 1997; Rosenthal, Griffith, Bond, & Miller, 1990). For example, a tendency towards concrete thinking in both children and adults with a frontal head injury has been reported (Rosenthal et al., 1990). It is noteworthy that multiple studies have reported comparable performance on measures of verbal intellectual functioning among children with TBI and controls (Levin et al., 2011; Snodgrass & Knott, 2006; Walz et al., 2010). Accordingly, it may be that among children with TBI, abstract reasoning abilities are particularly vulnerable while language skills are maintained. Such a differential impact on specific intelligence components may not negatively affect the development of general intellectual abilities (Nisbett et al., 2012). This should be examined in future longitudinal studies. Also, studies of larger samples of children with a head injury tapping the different domains of intellectual abilities are needed. After controlling for abstract reasoning, no significant differences were found between children with a head injury and controls in ToM recognition and social reasoning abilities. Thus, it may be that children with a mild or moderate head injury have decreased abstraction ability that contributes to their difficulties in performing ToM recognition and social reasoning tasks. Previous studies of children with a head injury did not control for abstract reasoning, and more severe head injuries than in the current sample were studied (Snodgrass & Knott, 2006; Tonks et al., 2007; Turkstra et al., 2004; Turkstra, McDonald, & DePompei, 2001; Warschausky et al., 2003; Yeates et al., 2004). Furthermore, among children with autism spectrum disorders, ToM performance has been associated with intellectual and language skills (Frith, 1994). Whereas verbal abilities have been reported to predict ToM performance in children with TBI (Walz et al., 2010), to our knowledge, this is the first report of nonverbal abstraction abilities as contributors of performance on ToM recognition and social reasoning tasks in children with a head injury. Children with a mild-to-moderate head injury had more difficulties in recognizing facial expressions and facial emotion compared to controls. This finding corroborates previous evidence from multiple studies of children with TBI (Pettersen, 1991; Schmidt et al., 2010; Snodgrass & Knott, 2006; Tonks et al., 2007). For example, children with moderate-to-severe TBI showed more difficulties in facial emotion recognition when compared to children who sustained orthopedic injury (Schmidt et al., 2010). After controlling for facial emotion recognition in the current study, differences between the groups in ToM recognition and social reasoning ability did not persist. Thus, findings extend previous reports, suggesting that among children with a mild or moderate head injury, poor facial emotion recognition contributes to poorer performance in ToM recog- nition and social reasoning tasks. In line with this, the ability to recognize facial and vocal emotional expressions has been previously associated with subtle social reasoning skills such as recognizing sarcasm in others (McDonald & Flanagan, 2004). Interestingly, in the same study, emotion recognition was not associated with more complex social judgements such as diplomatic lies (McDonald & Flanagan, 2004). Considering this alongside the above finding, it may be that ToM recognition ability underlies ToM reasoning deficits to an extent that depends on reasoning skills’ complexity. The effect of ToM recognition on different social reasoning tasks should be investigated in future studies. Children with a traumatic brain injury had a lower level of performance on two EF tasks (digit span, verbal fluency), and experienced more EF difficulties according to parental reports when compared to noninjured children. These findings corroborate COGNITIVE CONTRIBUTIONS TO THEORY OF MIND 15 Downloadedby[NaomiKahanaLevy]at19:3615December2014
  • 19. previous findings on diminished EF in children with TBI including memory deficits (Levin & Hanten, 2005) and phonological deficits (Schmidt et al., 2010). Performance on ToM tasks in the current study was affected by EF as assessed by two direct measures. This supports the notion that ToM abilities and EF represent two dependent cognitive paths (Carlson et al., 2013, 2002) and bears implications for understanding the develop- ment and precursors of ToM abilities. The persistence of ToM differences between the groups after controlling for EF as measured by parental report may be due to the lower sensitivity of the latter in comparison to direct measures. The findings of the current study indicate that both EF and intellectual abilities affect ToM performance in children with traumatic head injury. Considering this alongside the fact that some EF and intellectual abilities overlap (e.g., working memory), future research is needed in order to delineate specific contributions of EF and intellectual abilities to ToM deficits. From a clinical perspective, findings underscore the need to utilize ToM assessments that are character- ized by high specificity and sensitivity and do not additionally tap other intellectual and cognitive capacities in this population. In line with this, it has been reported that among children with autism spectrum disorders ToM assessments may involve different informa- tion-processing requirements other than mentalizing abilities (Brent, Rios, Happé, & Charman, 2004). In the current study, the ToM task of reading the mind in the eyes involved vocabulary requirements that may have resulted in lower specificity. Also, findings suggest that among children with a head injury, social maladjustment (Tonks et al., 2010) may be due to EF difficulties such as social initiation and emotional regulation rather than difficulties in understanding the other’s emotions, thoughts, and perspective. This has implications for the design of interventions aimed at promoting social adjustment in this population. A strength of the current study is the comprehensive examination of potential contributors to both recognition and reasoning ToM elements in children with a traumatic head injury including understudied predictors such as abstract reasoning. Current ToM assessments did not tap actual social functioning, compromising ecological validity. This limitation could be addressed by using videotaped observations (Turkstra et al., 2004) or by correlating face-to-face test scores with a questionnaire filled out by parents regarding children’s actual social abilities. Given the differential performance on the two recognition tasks, it may be that the facial emotion recognition test more adequately reflects ToM recognition abilities in comparison to the Reading the Mind in the Eyes test in children ages 7–13. This may due to the former’s use of pictorial information in comparison to the latter involving vocabulary requirements. We used both direct measures and parental reports to assess EF. Future studies should use laboratory measures of EF that are unaffected by parents’ expectations and knowledge derived from clinical assessments about their child’s functioning. Information regarding ongoing medical issues and current educational placement was not available. Findings may or may not generalize to other populations, and studies of the contributors to ToM abilities targeting specific populations that may experience ToM impairments such as children with autism spectrum disorders (Brent et al., 2004) or ADHD (Uekermann et al., 2010) are warranted. The current study had a small number of participants. Approximately 44% of the eligible head-injured group did not participate. The age range was wide (7–13) and participants had different degrees of injury. Future studies should examine larger samples of children with a head injury and focus on a specific injury degree in order to enable comparisons of injured participants by factors such as age of injury and injury severity. 16 N. K. LEVY & N. MILGRAM Downloadedby[NaomiKahanaLevy]at19:3615December2014
  • 20. Notwithstanding these limitations, the current study provides important evidence on the difficulties experienced in abstract reasoning, EF, and ToM domains among children who suffered mild or moderate head injuries. Current evidence suggests that impaired ToM recognition and reasoning abilities after a head injury may result from other cognitive impairments. The poorer performance on ToM tasks seen among children with a head injury may reflect poorer abstract reasoning, a general tendency to concretize stimuli, working memory and verbal fluency deficits, and difficulties in facial emotion recognition, rather than deficits in the ability to understand the other’s thoughts and emotions. In other words, ToM impairments may be secondary to a range of cognitive deficits in determining social outcomes in this population. From a practical perspective, findings support a greater focus on cognitive impairments in abstract reasoning, working memory, verbal fluency, and facial emotion recognition rather than on ToM deficits in providing care for children with a head injury. If cognitive impairments affect ToM abilities in children with a mild-to-moderate head injury, as found in the current study, it may be that this pattern is manifested more robustly among children with a severe head injuries. This should be examined in future investigations. A better understanding of intellectual, EF, abstract reasoning, and emotion recognition impairments following head injury is needed in order to promote more efficacious rehabilitative efforts and a more favorable psychosocial prognosis among children with a head injury. Original manuscript received August 19, 2013 Revised manuscript accepted November 1, 2014 First published online December 8, 2014 REFERENCES Baron, I. S. (2004). Neuropsychological evaluation of the child. New York, NY: Oxford University Press. Baron-Cohen, S., Wheelwright, S., Spong, A., Scahill, V., & Lawson, J. (2001). Are intuitive physics and intuitive psychology independent? A test with children with Asperger syndrome. Journal of Developmental and Learning Disorders, 5, 47–78. Belanger, H. G., Curtiss, G., Demery, J. A., Lebowitz, B. K., & Vanderploeg, R. D. (2005). Factors moderating neuropsychological outcomes following mild traumatic brain injury: A meta- analysis. Journal of the International Neuropsychological Society, 11(3), 215–227. doi:10.1017/S1355617705050277 Brent, E., Rios, P., Happé, F., & Charman, T. (2004). Performance of children with autism spectrum disorder on advanced theory of mind tasks. Autism, 8(3), 283–299. doi:10.1177/ 1362361304045217 Burg-Malki, M. (2009). Social cognition and social behavior among children with Williams syndrome and children with Velo-cardio-facial syndrome (Doctoral Dissertation) Bar- Ilan University, Ramat Gan. (in Hebrew). Cahan, S. (1998). Manual for WISC-R 95. Jerusalem: The Israeli Ministry of Education – The Psychological and Counseling Service and the Henrietta Szold Institute for Research in Behavioural Science. (in Hebrew). Carlson, S. M., Claxton, L. J., & Moses, L. J. (2013). The relation between executive function and theory of mind is more than skin deep. Journal of Cognition and Development. Advance online publication. doi:10.1080/15248372.2013.824883 COGNITIVE CONTRIBUTIONS TO THEORY OF MIND 17 Downloadedby[NaomiKahanaLevy]at19:3615December2014
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