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Child Neuropsychology: A Journal on


Normal and Abnormal Development in
Childhood and Adolescence
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Planning and Problem Solving Skills


Following Focal Frontal Brain Lesions
in Childhood: Analysis Using the Tower
of London
Rani Jacobs & Vicki Anderson
Published online: 09 Aug 2010.

To cite this article: Rani Jacobs & Vicki Anderson (2002) Planning and Problem Solving Skills
Following Focal Frontal Brain Lesions in Childhood: Analysis Using the Tower of London, Child
Neuropsychology: A Journal on Normal and Abnormal Development in Childhood and Adolescence,
8:2, 93-106, DOI: 10.1076/chin.8.2.93.8726

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Child Neuropsychology 0929-7049/02/0802-093$16.00
2002, Vol. 8, No. 2, pp. 93–106 # Swets & Zeitlinger

Planning and Problem Solving Skills Following


Focal Frontal Brain Lesions in Childhood:
Analysis Using the Tower of London
Rani Jacobs1,2,3 and Vicki Anderson2,3
1
Royal Children’s Hospital, Melbourne, Australia, 2Murdoch Childrens Research Institute, Melbourne, Australia,
and 3University of Melbourne, Australia
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ABSTRACT

Problem solving skills were investigated in children with focal lesions using the Tower of London test (TOL;
Shallice, 1982). The scoring procedure was elaborated from previous studies to delineate separate processes
contributing to overall performance in children. Thirty-one children with focal frontal pathology, 18 children
with focal pathology in other brain regions (extra-frontal), 17 children with generalized pathology and 38
healthy children participated in the study. Results suggest a distributed network for problem solving skills,
particularly cognitive flexibility and goal setting skills. Within the frontal group, children with lesions
involving the right pre-frontal cortex had greatest problems with self-regulation, with rule breaks most
common among this group. As these skills develop relatively early in comparison to other aspects of
executive function, right pre-frontal regions may play a particularly important role in the development
of executive skills in childhood, with damage to these regions rendering children vulnerable to a range of
cognitive and social deficits.

Adult lesion studies have shown that specific pre- frontal lobe damage, and the relative immaturity
frontal regions play a greater role in mediating of these skills in childhood.
particular aspects of executive function. For
example, right pre-frontal regions are implicated Executive Function
in attention, planning, spatial working memory, Executive skills are generally considered to be
self-regulation and monitoring, while left pre- mediated by the pre-frontal cortex, as damage to
frontal regions are associated with verbal proces- this region often leads to impairments in self-
sing and verbal fluency, initiation of task activities regulation, attentional capacity, reasoning and
and verbal working memory (Alexander & Stuss, emotional control (Luria, 1980; Stuss & Benson,
2000; Eslinger & Biddle, 2000; Eslinger, Biddle 1986; Walsh, 1978). These problems have
& Grattan, 1997; Grattan, Bloomer, Archambault, significant functional implications impacting on
& Eslinger, 1994; Grattan & Eslinger, 1992; Stuss a child’s quality of life, impeding academic
et al., 1998, 1999). In contrast, relatively little is progress, limiting their capacity to acquire and
known about the localization and lateralization of sustain meaningful employment or to develop and
executive skills in children, due to the difficulty in maintain appropriate social relationships. In
obtaining a large sample of children with focal severe cases, sociopathic behavior may also be

Address correspondence to: Rani Jacobs, Department of Psychology, Royal Children’s Hospital, Parkville, Vic.
3052, Australia. Tel.: þ61 3 9345 5511. Fax: þ61 3 9345 6002. E-mail: jacobsr@cryptic.rch.unimelb.edu.au
Accepted for publication: September 20, 2002.
94 RANI JACOBS & VICKI ANDERSON

observed (Anderson, Bechara, Damasio, Tranel, Benson, 1984). Together, these results imply that
& Damasio, 1999; Blair & Cipolotti, 2000). executive skills are subsumed by cerebral systems
Attention and self-regulation skills underpin rather than discrete unitary processes, with the
efficient executive function with impairments in pre-frontal regions acting as a ‘supervisory sys-
these abilities resulting in impulsive responses, tem’, integrating and coordinating information
poor self-control, difficulty completing tasks and from posterior and subcortical cerebral regions
multiple errors. As these skills appear to be (Alexander & Stuss, 2000; Stuss & Alexander,
mediated by right pre-frontal regions, at least in 2000; Welsh & Pennington, 1988).
adults, right pre-frontal damage in childhood may The systemic basis of executive function may
render children vulnerable to impairment in abil- be best illustrated in the developing brain. The
ities requiring these processes. Such problems frontal lobes are the last cerebral structures to
incorporate cognitive, emotional and behavioral reach maturity, with elaboration and myelination
domains, limiting a child’s capacity to acquire of pre-frontal cerebral circuitry as well as changes
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knowledge, successfully solve problems, learn in metabolic activity occurring throughout child-
from previous mistakes and to respond appropri- hood and adolescence (Hudspeth & Pribram,
ately in social situations, therefore impeding for- 1990; Huttenlocher & Dabholkar, 1997; Klinberg,
mation of lasting friendships (Eslinger, Biddle, Viadya, Gabrieli, Moseley, & Hedehus, 1999;
Pennington, & Page, 1999; Marlowe, 1992). Thatcher, 1997). These changes are consistent
Thus, children with damage to right pre-frontal with a protracted development of executive func-
brain regions may be particularly vulnerable to tion, which commences in infancy but is not
cognitive, learning and social difficulties. Despite complete until around mid-adolescence (Ander-
their importance in childhood, to our knowledge, son, this edition; Anderson, Anderson, Northam,
no controlled group studies have attempted to Jacobs, & Catroppa, 2001; Diamond & Doar,
investigate the role of the right pre-frontal brain 1989; Diamond & Taylor, 1996; Espy, Kaufman,
regions in mediating attention and regulation & Glisky, 2001; Kelly, 2000; Klenberg, Korkman,
skills in childhood. & Lahti-Nuutila, 2001; Levin, Culhane, Hartman,
Executive deficits are not specific to frontal Evankovich, & Mattson, 1991; Stuss, 1992). This
pathology, but can also occur secondary to a development does not appear to be a uniform
disruption to connections that feed into these process for all components of executive function.
cerebral regions (Eslinger & Grattan, 1993). Rather, there appears to be different developmen-
This observation may be particularly relevant to tal trajectories for specific aspects of executive
children sustaining early brain insults due to the function, with some aspects not reaching maturity
immaturity of the central nervous system at the until mid-adolescence. For example, attention,
time of insult, and the reliance of the frontal lobes self-regulation and inhibitory responses appear
on efficient transmission of information from to mature earlier than skills such as speed of
posterior and subcortical brain regions for ade- processing, planning, goal setting and cognitive
quate development. Whether the nature and sever- flexibility (see Anderson, this edition for sum-
ity of executive impairments following damage to mary; Anderson, Anderson, Northam, & Jacobs,
these ‘‘extra-frontal’’ brain regions is similar to et al., 2001; Diamond & Doar, 1989; Diamond &
that seen following frontal lobe damage, has not Taylor, 1996; Espy, 1997; Espy, Kaufman,
been systematically studied in childhood popula- McDiarmid, & Glisky, 1999; Kelly 2000; Levin
tions, possibly due to the difficulty in recruiting et al., 1991; Luciana & Nelson, 1998; Welsh &
large samples of children with focal cerebral Pennington, 1988; Welsh, Pennington, &
pathology. Grossier, 1991).
Neuroanatomical and neurophysiological stu- The protracted development of these skills and
dies have demonstrated multiple bi-directional the ‘supervisory’ role of the frontal lobes in
connections between the pre-frontal cortex and coordinating many daily activities suggests that
all other cortical and subcortical structures children may be particularly vulnerable to impair-
(Denckla & Reiss, 1997; Luria, 1980; Stuss & ment following frontal lobe damage, with the
PROBLEM SOLVING AND FOCAL FRONTAL LESIONS 95

nature and severity of problems dependent on the 2001; Anderson, Anderson, & Lajoie, 1996;
age at which the damage occurs, and the devel- Anderson, Anderson, Northam, et al., 2001;
opmental stage of cognitive skills subsumed by Anderson, Anderson, Northam, Jacobs, et al.,
these damaged regions (Anderson & Moore, 2001; Espy, 1997; Espy et al., 2001; Gioia,
1995; Dennis, 1989; Pentland, Anderson, & Isquith, Guy, & Kenworthy, 2000; Jacobs et al.,
Wrennall, 2000; Taylor, Albo, Phelps, Sachs, & 2000; Taylor et al., 1987). Such scoring ap-
Bierl, 1987). These deficits may not be restricted proaches appear to be more informative than
to the domain of executive function, but impact traditional summary scores, which give an indi-
more broadly on cognitive and social develop- cation as to whether executive skills are impaired,
ment, leading to behavioral regulation problems, but are not useful in identifying the specific
emotional dysfunction, reduced intellectual skills reasons for this impaired performance. For
and learning difficulties (Eslinger et al., 1997; example, self-regulation deficits may underpin
Marlowe, 1992). problem solving deficits following frontal pathol-
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Given the critical role of the frontal lobes in ogy, while memory or perceptual problems may
learning, skill acquisition and social development, interfere with problem solving capacity following
it is important to be able to assess these skills in damage to posterior brain regions. This ‘micro-
children. Historically, executive function mea- analysis’ of task performance is also able to
sures were developed for use with adults, when account for different developmental trajectories
these skills are considered mature, and so im- for specific aspects of executive function per-
paired performance can be assumed to reflect formance.
executive dysfunction. In children, however, this Microanalysis of task performance may also
association may be less clear, due to both the be a useful means of investigating the contribu-
relative immaturity of executive skills at the time tion of frontal and extra-frontal brain regions to
of insult and the lack of maturity of these skills at executive function performance, providing the
the time of assessment. These developmental opportunity to separate out lower order functions
issues also need to be taken into account, as (e.g., visuo-spatial skills, memory, etc), from
poor performance may reflect impairment or more strategic aspects of performance such as
developmental delay. Alternatively, a child’s per- planning and cognitive flexibility. Specifically,
formance may appear to be impaired when com- one might expect primary deficits in executive
pared with adult data, but may actually be within skills, such as regulation and attentional control,
developmental expectations when compared with following pre-frontal damage. In contrast, impair-
other children of the same age. Mapping the ments in planning, organization and problem
development of executive function has received solving may occur either as a direct consequence
much focus in recent years and led to the val- of pre-frontal injury or secondary to an interrup-
idation of executive function measures that are tion to areas that feed into frontal lobes and
appropriate for use with children, and an increased associated deficits in skills such as information
understanding of the way these skills develop in processing, memory, visuo-spatial and visuo-
healthy children (Anderson et al., 1996; motor skills.
Anderson, Anderson, & Garth, 2001; Anderson,
Anderson, Northam, & Jacobs, 2001; Anderson, The Tower of London (TOL)
Anderson, Northam, & Taylor, 2001; Espy, 1997; The Tower of London Test (TOL; Shallice, 1982)
Jacobs, Anderson, & Harvey, 2000; Klenberg is commonly employed as a measure of executive
et al., 2000). function, with a particular focus on planning,
In addition to identifying more appropriate strategic decision-making and problem solving
executive function measures for children, there (Anderson et al., 1996; Levin & Kraus, 1994;
has also been a move to design scoring systems Levin et al., 1994; Morris, Ahmed, Syed, &
that allow for quantification of specific processes Toone, 1993; Owen, Downes, Sahakian, Poleky, &
that contribute to overall performance on execu- Robbins, 1990). This test was initially devised for
tive measures (Anderson, Anderson, & Garth, use with adults, but is frequently utilized in
96 RANI JACOBS & VICKI ANDERSON

pediatric settings due to the recent availability of solving). It was expected that:
normative information for children (Anderson
(i) All children with cerebral damage (frontal,
et al.,1996; Krikorian, Bartok, & Gay, 1994).
extra-frontal and generalized pathology
Impaired performance on the TOL has been
groups) would perform more poorly than
reported in a range of pediatric disorders such as
controls on all aspects of performance on
closed head injury, hydrocephalus, meningitis
the TOL. However, children with damage to
and early-treated phenylketonuria (Dimitrov,
the pre-frontal regions would have relatively
Grafman, & Hollnagel, 1996; Fletcher,
greater impairments than children with extra-
Brookshire, Landry, & Bohan, 1996; Levin &
frontal and generalized damage on the more
Kraus, 1994; Levin et al., 1997; Welsh,
strategic aspects of performance (e.g., self-
Pennington, Ozonoff, Rouse, & McCabe, 1990).
regulation, goal setting and switching), due to
However, in these conditions damage has incor-
the direct effects of damage to the pre-frontal
porated, but has not necessarily been confined to,
cortex;
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pre-frontal cortex (Dimitrov et al., 1996; Fletcher


(ii) Within the frontal group, self-regulation
et al., 1996; Levin & Kraus, 1994; Levin et al.,
skills would be more clearly lateralized due
1997; Welsh et al.,1990), suggesting that while
to the relative maturity of these skills at the
the TOL may be sensitive in detecting brain
time of assessment. Specifically, children
impairment its utility in specifically tapping
with damage to the right pre-frontal regions
frontal lobe damage in childhood, remains
would exhibit relatively greater problems
unclear.
with self-regulation than those with left-
TOL scoring systems such as that outlined by
sided lesions. Children with bilateral lesions
Anderson et al. (1996) may assist in delineating
would perform most poorly due to the extent
executive aspects of performance from lower
of damage to pre-frontal regions.
order skills. This version of the TOL uses three
balls on three posts of differing heights and
involves 12 trials of increasing difficulty, ranging METHOD
from two moves to five moves. The child is shown
a card with the final configuration and told to Participants
match the configuration on the card in the speci- The sample comprised 107 children, aged between 7
fied number of moves. In addition to a measure of and 16 years. The clinical sample (n ¼ 69), was
overall performance, which incorporates time and ascertained via neurology and neuroradiology clinics
errors, Anderson et al. also provide developmen- at the Royal Children’s Hospital, Melbourne, Australia.
tal data for separate aspects of performance such Etiology and timing of lesion were diverse and included
a number of acquired (penetrating head injury, stroke,
as failed attempts and the number of trials suc-
hemorrhage, tumor, contusion following fall, cyst) and
cessfully solved. developmental (focal dysplasia, tuberous sclerosis,
In the current study, the scoring procedure schizencephaly) lesions.
developed by Garth, Anderson, and Wrennall
(i) Frontal lesion group: comprised 31 children with a
(1997) was further extended to include quantifi-
focal lesion to pre-frontal cortex (n ¼ 12 left, n ¼ 9
cation of a number of ‘strategic’ aspects to per- right and n ¼ 10 bilateral lesions) evident on mag-
formance. The task was administered to a group netic resonance imaging (MRI). Children with
of children with focal lesions involving the pre- frontal lesions that involved extensive posterior
frontal cortex, and their performance compared cortical regions (more than 10% of another lobe
with children with focal lesions to other cerebral affected) were not included in the frontal sample.
regions (extra-frontal), those with generalized (ii) Extra-frontal lesion group: consisted of 18 children
with a focal lesion to cortical regions excluding
pathology and healthy children. Using this proce-
the frontal lobes (parietal, temporal or occipital
dure, scores were derived for a number of separate lobe), evident on MRI. As with the frontal sample,
but integrated processes including, planning, effi- etiology of lesion was diverse and timing of
ciency, regulation, goal setting and switching, as lesion included both acquired and developmental
well as overall task performance (problem disorders.
PROBLEM SOLVING AND FOCAL FRONTAL LESIONS 97

(iii) Generalized group: comprised 17 children with Procedure


diffuse cerebral pathology detected on MRI. Etiol- Children in the frontal and extra-frontal groups were
ogy included closed head injury, neurofibromato- recruited prospectively over a 7-year period, and
sis and developmental disorders (e.g., subcortical identified on the basis of MRI evidence of a focal
band heterotopia, polymicrogyria) incorporating cortical lesion. A neuroradiologist and pediatric
multiple brain regions. neurologist rated the scans according to site and nature
of cerebral pathology. Children in the generalized
Inclusion criteria for all participants in lesion groups group were identified either on the basis of CT or MRI
were: (i) attendance at mainstream school; (ii) cerebral evidence of a diffuse injury (e.g., diffuse axonal
MRI; (iii) no history of psychiatric disturbance or shearing), multi-focal pathology (e.g., tuberous sclero-
attention deficit disorder prior to lesion onset; (iv) sis involving all lobes) or global developmental brain
minimum of 3 months post lesion onset at time of anomaly (e.g., subcortical band heterotopia). Once
assessment. identified, permission was sought from the primary
A control group was recruited from mainstream consultant to approach families about the study.
schools for comparison purposes. Children were Following consent from the consultant, a letter was
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identified via their school, and parents contacted for sent to families describing the study and inviting them
consent. The group comprised 38 children between 7 to participate. Children in the control group did not
and 16 years, with no previous history of learning undergo MRI. Consent to approach schools for the
disability, attentional problems, and psychiatric or purpose of recruiting healthy control children was first
emotional disturbance. obtained via the Education Department for Government
All children were required to have English as a schools and via the appropriate board for Non-
primary language and a Full-Scale IQ  70 (WISC-III, Government schools. Following consent, letters were
Wechsler, 1991). Demographic data for the sample are sent to the principals of primary and secondary schools
presented in Table 1, and demographic data and lesion in the Melbourne metropolitan region, incorporating a
characteristics for the frontal group are presented in range of socio-demographic regions. Schools that
Table 2. consented to participate were then asked to randomly

Table 1. Demographic Characteristics of Each Group.

Frontal Extra-frontal Generalized Control Partial


n ¼ 31 n ¼ 18 n ¼ 17 n ¼ 38 2

Males n (%) 19 (61.3) 11 (61.1) 12 (70.6) 19 (50) n/a


Age: M(SD) 11.3 (2.8) 10.7 (3.0) 10.6 (2.6) 10.8 (2.7) .011
SESa: M(SD) 4.7 (1.4) 4.0 (0.8) 3.9 (0.9) 4.1 (1.2) .076
Full-Scale IQ: M(SD) 90.2 (10.1) 92.4 (10.4) 88.9 (10.6) 105.2 (13.6) .283
a
SES: Socio-economic status (Daniel, 1983) – low scores reflect high SES.

p < .01 (all clinical groups significantly lower Full-Scale IQ than controls).

Table 2. Demographic and Lesion Characteristics of Frontal Group.

Left Right Bilateral Partial


n ¼ 12 n¼9 n ¼ 10 2

Males: N (% of sample) 9 (75) 4 (44.4) 6 (60) n/a


Age: M(SD) 11.9 (2.4) 10.8 (3.4) 11.4 (2.9) .016
SES: M(SD) 4.7 (1.4) 4.8 (1.1) 4.5 (1.8) .015
Full-Scale IQ: M(SD) 92.0 (8.6) 89.3 (13.0) 88.8 (9.6) .022
Lesion Characteristics
Developmental lesion: N (% sample) 4 (33.3%) 3 (33.3%) 3 (30%) n/a
Epilepsy: N (% sample) 8 (66.7%) 4 (44.4%) 6 (60%) n/a
Age at seizure onset: M(SD) 7.3 (4.3) 5.0 (4.5) 9.0 (5.0) .108
Note. No significant differences.
98 RANI JACOBS & VICKI ANDERSON

identify a male and a female whose birth date fell in the complete each problem within 1 min. Timing com-
first and second half of the year, for each birth year mences once the card containing the configuration
specified. Letters were then sent to these families via is exposed, and ceases following successful com-
the school principal (to ensure anonymity for families pletion of the problem. Following an unsuccessful
who did not wish to be involved), outlining the study attempt, the balls are placed back in their original
and inviting them to participate. Where families did not position and the child may attempt the problem
wish to be involved, the principal was asked to send a again. This procedure may be repeated as many
letter to another family that matched the gender and times as required within the 1 min time limit.
birth date criteria of the child who declined to be
involved. The score for each trial is based on speed and
Children of families who provided written consent accuracy with a maximum score of 9 given for each
as per hospital ethics procedure, then participated in a problem. Children are penalized for each failed attempt
neuropsychological assessment incorporating a stan- or for any rule breaks they make while completing each
dardised measure of general intellectual ability and a problem. In addition to the overall score, which is
range of traditional and more experimental executive calculated by summing the time score for each
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function measures. Children in the lesion groups were individual trial, the total time taken to complete all
seen either at the hospital or at home in a single session trials, and the total number of failed attempts were also
with a break. Children in the control group were seen at calculated independently (Anderson et al., 1996). An
school, in a single session with breaks in accordance estimate of planning time was derived by recording
with timetabled recess and lunch breaks. time taken between the child seeing the problem and
moving the first ball from the post and placing it on a
Measures new post (Garth et al., 1997). This was then averaged
across the 12 trials. To investigate regulation skills, the
(i) Intellectual capacity: This was obtained using the total number of rule violations (rule breaks) was also
Wechsler Intelligence Scale for Children, III recorded. These violations included a child picking up
(WISC-III). Verbal, Performance and Full-Scale more than one ball at a time, placing two balls on the
intellectual quotients were calculated. smallest post or placing balls on the desk. When a rule
(ii) The Tower of London (Anderson et al., 1996; break occurred, the child was reminded of the rule, the
Shallice, 1982): Comprises 12 items of increasing balls were placed back to the original position, a failed
complexity. Children are required to rearrange attempt recorded, and the child was instructed to try
three coloured balls on three posts of differing again. Perseverative errors were recorded as errors
heights to match a specified configuration, in a where after making a failed attempt, the same sequence
specified number of moves. In manoeuvring the of moves was repeated on the subsequent attempt.
balls, children are told that they may only move These errors were considered to be a measure of
one ball at a time, must place each ball on a post cognitive inflexibility, reflecting impaired working
and not on the desk, and may only place two balls memory and/or the inability to modify behavior
at a time on the middle post and only one at a time following feedback. These scores are summarized in
on the last post. The task is timed and children must Table 3.

Table 3. Summary of Tower of London Variables, the Aspect of Executive Function Tapped and the Regions Shown
to Mediate These Skills in Adults.

Variable Aspect of executive function Frontal region involved


tapped

Mastery
No. items correct Problem solving Left
Total score Problem solving Left
Rate
Planning time (s) Planning Right
Total time taken Efficiency Right
Strategy
No. rule breaks Self-regulation Right
No. failed attempts Goal setting Right (spatial tasks)
Perseverative errors Switching Right, left, superior medial
PROBLEM SOLVING AND FOCAL FRONTAL LESIONS 99

Statistical Analyses (c) Strategy: Differences were identified across


(i) Demographic characteristics: Differences between
all three strategy variables. There was a sig-
the groups on demographic characteristics of age, nificant group effect for failed attempts F(3,
socio-economic status (SES) and Full-Scale IQ 100) ¼ 3.4, p < .05, 2 ¼ .09, and rule breaks,
were investigated using analysis of variance F(3, 100) ¼ 5.0, p < .01, 2 ¼ .13, with the
(ANOVA). Where significant differences were 95% confidence intervals showing that the
observed, post-hoc analysis was conducted using frontal group made more failed attempts and
Tukey’s Honestly Significant difference. Chi- more rule breaks than the control group. Of
square analyses were employed to investigate dif-
ferences between the groups with respect to gender
note, for control children, only those
distribution as well as lesion characteristics for the younger than 9 years at the time of the assess-
frontal group (% children with epilepsy, % children ment made rule breaks. Children who made
with developmental lesions). five or more rule breaks had either frontal
(ii) TOL variables: Raw scores for variables of the (n ¼ 4) or generalized (n ¼ 1) pathology.
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TOL were used in the analysis as age standardized There was also a significant group effect for
scores were not available for all variables. As the perseverative errors, F(3, 100) ¼ 4.3, p < .01,
groups were not matched for age, differences
between lesion and control groups, and between
2 ¼ .11, again with the frontal group making
laterality groups within the frontal lobe group, more perseverative errors than controls.
were investigated using analysis of covariance co-
varying for age (ANCOVA). Post-hoc analyses
were performed by investigating the 95% confi- Laterality
dence intervals for each group.
(a) Lesion characteristics: There were no differ-
ences between the left, right and bilateral
groups with respect to proportion of children
RESULTS with developmental lesions or seizures and
the age at seizure onset.
Demographic Characteristics (b) TOL performance: Lateralization of skills
There were no differences between the four within the frontal group was investigated for
groups with respect to gender, age and socio- strategic variables, as these parameters were
economic status (SES), although a significant sensitive to frontal lobe damage. These
between group difference was found for Full- results are summarized in Table 5.
Scale IQ, F(3, 100) ¼ 13.8, p < .01, 2 ¼ .29. As
expected, post hoc analysis revealed that the There was a significant group effect for failed
frontal (p < .01), extra-frontal (p < .01) and gen- attempts, F(3, 64) ¼ 3.9, p < .05, 2 ¼ .15. Al-
eralised (p < .01) groups all obtained significantly though the right and bilateral groups made more
lower scores than controls. failed attempts than the left lesion and control
Within the frontal group, there were no differ- groups, the only statistically significant difference
ences between the left, right and bilateral groups was observed between the bilateral and control
with respect to gender, age, SES and Full-Scale groups at the 95% confidence interval. As shown
IQ. in Figure 1, rule breaks were most common in
children with right (44% sample) and bilateral
(70% sample) lesions, and these groups also
Between Group Comparisons
obtained higher mean scores on this variable in
on the TOL
comparison to the left lesion and control groups.
(a) Mastery: As outlined in Table 4, all groups ANCOVA revealed a significant main effect
performed similarly with respect to total for rule breaks, F(3, 64) ¼ 6.2, p < .01, 2 ¼ .23,
number of trials correct and the overall score. with the bilateral group making significantly more
(b) Rate: There were also no differences between rule breaks than the control group. The difference
the groups with respect to the total solution between the right and control groups also
time and average planning time. approached significance at the 95% confidence
100
Table 4. Results for TOL Performance for Each Group: Adjusted Means and Standard Error.

Frontal Extra-frontal Generalized Control Partial


n ¼ 31 n ¼ 18 n ¼ 17 n ¼ 38 2
Age Adj. Age Adj. Age Adj. Age Adj.
M (95% CI) M (95% CI) M (95% CI) M (95% CI)

Mastery
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Problem solving
No. of trials correct 10.5 (10.1–10.9) 10.6 (10.0–11.1) 10.7 (10.1–11.2) 10.9 (10.6–11.3) .012
Total score 68.8 (65.9–72.2) 67.6 (63.6–71.8) 66.6 (62.3–71.1) 69.7 (67.8–73.7) .014
Rate
Planning, efficiency
Time taken (s) 271.0 (237.2–302.1) 289.5 (246.8–330.8) 292.9 (247.9–336.8) 277.0 (240.6–300) .008

RANI JACOBS & VICKI ANDERSON


Average planning time (s) 4.5 (3.7–5.5) 4.7 (3.4–5.9) 4.9 (3.7–6.0) 3.8 (3.0–4.6) .029
Strategy
Self-regulation
No. rule breaks 2.0 (1.3–2.6) 1.1 (0.2–1.9) 1.6 (0.7–2.5) 0.3 (0.3–0.9) .142
Goal Setting
No. failed attempts 9.5 (8.4–10.7) 9.2 (7.7–10.7) 10.2 (8.6–11.8) 7.3 (6.2–8.4) .107
Shifting set/switching
No. perseverative errors 2.2 (1.6–2.7) 1.8 (1.1–2.5) 1.9 (1.1–2.6) 0.9 (0.4–1.4) .103
Note. Age adjusted means.

p < .05;  p < .01.
PROBLEM SOLVING AND FOCAL FRONTAL LESIONS 101

Table 5. Performance on TOL According to Lesion Laterality for Children With Frontal Lobe Lesions.

Left Right Bilateral Control Partial


n ¼ 12 n¼9 n ¼ 10 n ¼ 38 2
Age Adj. Age Adj. Age Adj. Age Adj.
M (95% CI) M (95% CI) M (95% CI) M (95% CI)

Strategy
Self-regulation
No. rule breaks 1.1 (00–2.2) 1.9 (0.7–3.1) 2.7 (1.6–3.9) 0.2 (0.4–0.8) .227
Goal setting
No. failed attempts 7.9 (5.9–9.9) 10.1 (7.7–12.4) 11.3 (9.0–13.5) 7.2 (6.1–8.4) .171
Shifting set/switching
No. perseverative errors 1.7 (0.8–2.6) 1.9 (1.0–2.9) 2.9 (1.9–3.8) 0.8 (0.4–1.3) .215
Note. Age adjusted means.
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p < .05;  p < .001.

Although the frontal group performed most


poorly on strategy variables, the performance
of the extra-frontal and generalised groups was
also reduced in comparison to controls, suggest-
ing that while executive dysfunction may be more
severe following frontal pathology, it is also a
feature of childhood cerebral pathology, irrespec-
tive of the site of damage.
Fig. 1. Proportion of children in the frontal group There were no differences between the groups
making rule breaks according to lesion with respect to the time taken to plan an approach
laterality.
to each problem. One explanation for this may be
that the measure of planning used in this study
interval. There was also a significant main effect was not a reliable indicator of planning ability. A
for group on the number of perseverative errors, recent adult study using a computerized version
F(3, 64) ¼ 5.7, p < .01, 2 ¼ .21, with the bilateral of the TOL would support such a notion. Owen
group once again making more of these errors et al. (1990) used a procedure where the number
than the controls. of moves to solve a problem was not specified and
found similar mean latencies between the frontal
pathology group and controls for the time taken
DISCUSSION between the problem being exposed and partici-
pants making an initial move. However, the fron-
There were no differences between the frontal, tal lobe pathology group took longer than controls
extra-frontal, generalized and control groups on to implement their second move, suggesting less
mastery and rate scores despite differences on efficient planning in the frontal pathology group,
more strategic aspects of performance, suggesting which may be masked when only looking at the
that at least in children, rate and mastery initial latency between seeing the problem and
parameters are not particularly sensitive in making the first move. This study also showed
distinguishing site specific problems associated less efficient problem solving skills in the frontal
with executive dysfunction. Differences were pathology group who required more moves to
evident on all strategy scores, with the frontal solve problems than controls. Similarly, tasks
group consistently performing more poorly, such as the Tower of Hanoi, which is purported
suggesting that strategy scores may be more to also assess planning and problem solving skills,
sensitive for detecting frontal pathology. requires children to solve each problem in the
102 RANI JACOBS & VICKI ANDERSON

smallest number of moves, rather than giving this for efficient function in these domains. There may
information to the child, as was done in this study. be different reasons for impaired executive func-
Thus, it is important to note that the nature of the tion performance depending on the site of patho-
task may vary according to the procedure logy. For example, goal setting deficits in the
adopted. For example, protocols requiring chil- frontal pathology group may in part be accounted
dren to solve a problem in the fewest number of for by impairments in self-regulation, with this
moves, may impose a greater demand on plan- group making the greatest number of rule breaks,
ning, working memory and cognitive flexibility which were also recorded as a failed attempt.
skills as children need to think about a number of While the extra-frontal group performed similarly
alternatives and choose the most efficient strategy poorly in the domain of goal setting, the severe
prior to commencing the task. self-regulation deficits observed in the frontal
The total time taken to complete the 12 trials group were not as apparent, raising the possibility
was not sensitive in detecting group differences in for different reasons for impaired goal setting
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performance. As this measure reflects global skills in these two groups.


performance, it is not helpful in detecting intra- Although the reasons for goal setting deficits
individual variation in performance on each trial. may vary according to the site of pathology, these
For example, some children were quick to com- difficulties in devising and carrying out goals have
plete some trials, approaching problems impul- similar functional implications for children in
sively but obtaining the correct solution, thereby everyday life, impacting on learning, social inter-
obtaining a high score, while on other trials, such action and cognitive development. As a result of
an impulsive approach was associated with many their impairment, children may struggle to know
errors and a longer solution time. In contrast, how to start open-ended tasks, to set realistic study
other children methodically planned their ap- goals, to organise incoming information in an
proach to each trial, made fewer errors but took efficient manner for later recall, and to generate
longer to solve each problem. appropriate solutions to problems at school, in the
Although the greatest deficits on strategy vari- workplace and in personal relationships. In addi-
ables were observed following focal frontal tion, children with frontal pathology may also be
pathology, reduced performance was also found impulsive, failing to consider the consequences of
for the other lesion groups. These findings support their actions, and may act inappropriately in social
a systemic rather than localized basis for execu- situations despite being aware of social rules,
tive skills, with deficits occurring either as a direct which may further isolate them from their peers.
consequence of damage to the pre-frontal cortex
or secondary to a disconnection between frontal Lateralization of Executive Skills
and other brain regions. These results are consis- Overall, children with bilateral lesions performed
tent with functional imaging and animal studies, most poorly on the TOL in comparison to those
which have demonstrated rich connections with unilateral lesions, possibly reflecting the
between the pre-frontal cortex and posterior and greater volume of frontal lobe pathology. Chil-
subcortical regions, with particularly strong links dren with right-sided lesions also experienced
between posterior association areas and dorsolat- relatively greater problems with self-regulation,
eral pre-frontal cortex, a region associated with goal setting and shifting set than those with left-
problem solving skills (Alexander & Stuss, 2000). sided lesions and controls. Based on the scoring
Although children with extra-frontal and gen- procedure used in this study, deficits in self-
eralized pathology were also prone to making rule regulation and goal setting lead to a lower overall
breaks and perseverative errors on the TOL rela- score on the TOL, reflecting less efficient problem
tive to controls, these problems were more severe solving skills. These findings, in conjunction with
following frontal lobe lesions. Thus, while the normative data showing that regulation skills
integrity of the frontal lobes is critical for self- develop relatively early, suggest that although
regulation and adaptive behaviour, input from many brain regions may be involved in successful
posterior and subcortical regions is also required performance on the TOL, the right pre-frontal
PROBLEM SOLVING AND FOCAL FRONTAL LESIONS 103

cortex may play a particularly important role in systemic nature of executive skills has also
early development of non-verbal problem solving been described in adult studies showing the
skills, via it’s role in regulating behavior. Some involvement of posterior cerebral regions on
caution must be applied to this statement, as the some executive function tasks (Stuss et al.,
study focussed on non-verbal problem solving. It 1998, 1999). This has significant implications
is possible that children with left pre-frontal for children who may be vulnerable to a range
lesions may demonstrate similar problems to the of executive impairments either as a direct con-
right lesion group on verbally based problem sequence of frontal lobe damage or secondary
solving measures. to damage to regions that feed into the frontal
While children with unilateral left and unilat- lobes.
eral right pre-frontal damage were prone to mak- The pattern of lateralization described in the
ing perseverative errors on the TOL, greatest adult literature was not as clearly delineated in
deficits in the ability to shift set were seen in children. Self-regulation, an aspect of executive
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children with bilateral damage. The ability to shift function which is relatively mature by mid-child-
set requires a number of skills including memory, hood, did show a pattern similar to that demon-
in particular working memory, self-monitoring strated in adults, with the right pre-frontal region
and an ability to inhibit or relinquish a previous appearing to be more important in mediating
response in order to develop an alternative these skills. The early development of regulation
approach. A deficit in any of these skills may skills is likely to reflect their importance in the
contribute to perseverative errors, with the rela- subsequent development of other aspects of
tive combination of these problems varying executive function, thus suggesting that the nature
according to the site of pathology, and resulting and severity of executive impairments may be
in reduced performance irrespective of laterality greatest in children with right pre-frontal pathol-
of damage. ogy, at least when tasks do not have a significant
Rate scores were not particularly useful in verbal component. Self-regulation problems are
delineating laterality groups. This is not surpris- likely to have broad implications for learning and
ing given that these scores tend to reflect informa- social interaction, interfering with a child’s capa-
tion processing and speed of response, skills city to persist with problems in order to achieve
believed to be linked to the integrity of white an appropriate solution, to think about many
matter structures in the brain, and are therefore possible solutions to a problem before attempting
less likely to be localized to any specific cerebral to solve the problem, or respond appropriately in
region. social situations.
Overall, the pattern of results suggests that The high rate of regulation problems in chil-
while the frontal lobes play a particularly impor- dren with bilateral pre-frontal damage suggests
tant role in mediating executive skills in child- that as with adults, the medial regions of the pre-
hood, other brain regions are also important for frontal cortex may also be important in mediating
efficient function. The frontal lobes have been these skills as bilateral damage frequently in-
suggested to be important in coordinating and volves these areas. However, as the bilateral
integrating information from other brain regions group also have a greater loss of frontal volume,
and have rich connections to posterior and sub- large group studies that incorporate children with
cortical cerebral structures (Alexander & Stuss, focal medial damage are required to investigate
2000; Eslinger & Grattan, 1993; Stuss & this relationship between specific site of da-
Alexander, 2000; Welsh & Pennington, 1988). mage (e.g., dorsolateral vs. medial) and the
Thus, damage to ‘extra-frontal’ brain regions is development of executive skills in childhood.
likely to disrupt the transmission between poster- Studies utilizing tasks that tap both verbal and
ior regions and the frontal lobes, resulting in non-verbal problem solving skills will also
functional problems as evidenced by difficulty assist in differentiating the contribution of the
planning one’s approach to problems and identi- left and right pre-frontal regions in problem sol-
fying sub-goals to achieve an overall goal. The ving skills.
104 RANI JACOBS & VICKI ANDERSON

ACKNOWLEDGEMENTS Dennis, M. (1989). Language and the young damaged


brain. In T. Boll & B. Bryant (Eds.), Clinical
This research was funded by grants from the National Neuropsychology and brain function: Research,
Health and Medical Research Council, Australia, and measurement and practice. (pp. 85–123).
the Murdoch Childrens Research Institute, Melbourne, Washington: American Psychological Association.
Australia. We are deeply indebted to the families who Diamond, A. (1985). Development of the ability to use
agreed to be involved in this research. recall to guide action, as indicated by infants’
performance on AB. Child Development, 56,
868–883.
Diamond, A., & Doar, B. (1989). The performance of
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