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COGNITIVE STRUCTURE OF EXECUTIVE DEFICITS IN
FRONTALLY LESIONED HEAD TRAUMA PATIENTS
PERFORMING ACTIVITIES OF DAILY LIVING
Sandra Fortin1, Lucie Godbout2and Claude M.J. Braun1
(1Université du Québec à Montréal, Département de Psychologie, Centre de Neuroscience
de la Cognition; 2Université du Québec à Trois-Rivières, Département de Psychologie,
Laboratoire de Neuropsychologie Expérimentale et Comparée)
A
BSTRACT
Objective: Executive functions in activities of daily living (ADL) were investigated in
10 patients with frontal lobe lesions after a mild to severe closed head injury (CHI). Method:
The CHI patients were compared to 12 normal controls with a neuropsychological test
battery, a script recitation task and a realistic simulation of complex multitask ADL
(planning and preparing a meal). Results: Though the CHI patients were significantly slow
on one test and subject to interference on an attention test with parametric testing, the
groups did not differ on any neuropsychological test with non parametric testing. However,
the CHI patients manifested marked anomalies in the meal preparation task. While small
sequences of actions were easily produced, large action sets could not be correctly executed.
Conclusion: An outstanding deficit in strategic planning and prospective memory appears
to be an important underpinning of the impairment of ADL observed in CHI patients with
frontal lobe lesions.
Key words: closed head injury, activity of daily living, scripts, frontal lobe, executive
function, memory
C
OGNITIVE
S
TRUCTURE OF
E
XECUTIVE
D
EFICITS IN
F
RONTALLY
L
ESIONED
H
EAD
T
RAUMA
P
ATIENTS
P
ERFORMING
A
CTIVITIES OF
D
AILY
L
IVING
Head trauma typically damages the temporal and frontal lobes (Levin and
Kraus, 1994). Cognitive operations of the frontal lobes have often been
represented under the generic label of “executive” functions (Fuster, 1989; Kolb
and Whishaw, 1989; Tranel et al., 1994). It is well established that head trauma
impairs several aspects of executive function (Levin, 1995; Stuss et al., 1985)
and activities of daily living or ADL (Crépeau et al., 1997; Mayer et al., 1990;
Schwartz et al., 1993; Schwartz et al., 1998; Schwartz et al., 1995; Shallice and
Burgess, 1991) and there is evidence that these two impairment domains are
intimately linked (Mazaux et al., 1997). Focal frontal lesions also impair ADL
(Eslinger and Damasio, 1985; Goel et al., 1997; Goldstein et al., 1993; Schwartz
et al., 1991). It has thus been argued that executive impairment may be the main
component of deficits of ADL in brain lesioned patients (Godbout and Doyon,
1995; Grafman et al., 1993; Shallice and Burgess, 1991). In particular, planning,
self correction, decision making and judgment have been believed critical for
ADL (Acker, 1990). However, past and current representation of the cognitive
structure and brain basis of critical executive function contributing to impairment
Cortex, (2003) 39, 273-291
of ADL remains extremely vague and controversial. For example, Schwartz and
colleagues (1998) concluded that the impairment of ADL observed in their
cohort of head trauma patients did not resemble a frontal dysexecutive syndrome
as much as a globally limited attentional capacity. ADL are typically
investigated by means of spousal ratings or patient self-ratings of daily
adaptation (i.e., questionnaires or semi-structured interviews) and the actual
cognitive abilities critical for ADL are not outlined nor tested. Likewise,
executive function is a wide ranging term typically used eclectically such that
this functional domain is assessed with very different tests from one study to the
other, without unifying concepts of critical cognitive components. There have
been a few recent attempts to investigate ADL impairment from the vantage
point of highly constrained and elegant cognitive models. Within the general
domain of executive function, three such approaches appear promising, a first
focussing on prospective memory, a second on script generation and a third on
the central executive system.
Prospective memory consists of remembering, in the future, to execute a
specific action (Meacham and Singer, 1977). Prospective memory has been
demonstrated to be frontal lobe based (Cockburn, 1995; Okuda et al., 1998), to
relate to several higher order executive functions (Bisiacchi, 1996; McDaniel et
al., 1999) and to be very important in ADL (Marsh et al., 1998; Van den Broek
et al., 2000). It is impaired in head trauma patients (Kinsella et al., 1996; Shum
et al., 1999).
Script generation was first theorized neuropsychologically by Shallice (1982,
1988) and then by Grafman (1989). Shallice proposed that ADL consist of
action sequences, which to be implemented require mental schemata (scripts) in
which the ordering of individual actions is highly constrained and involves
numerous steps. Shallice’s model proposes that mental scripts are hierarchically
organized: the top level component (Supervisory Attentional System or SAS),
dealing with novel situations, is more frontal lobe dependent, whereas the lower
level component (Contention Programmer or CP), dealing with routine action
sequences and subsequences, may be more tributary to subcortical areas (e.g.,
the basal ganglia). Script tasks have since been operationalized in paper-pencil
versions (invention and recitation of scripts) and have been shown to be highly
sensitive to frontal lobe lesions (Godbout and Doyon, 1995; Sirigu et al., 1995)
and to activate frontal cortex (Crozier et al., 1999; Partiot et al., 1996).
However, attempts to dissociate neuropsychologically the SAS and CP with
script recitation tasks have failed to date. For example, Godbout and Doyon
(1995) found that frontally lesioned patients were equally impaired in routine
and non-routine script generation. Grafman (1989) also recognized a hierarchy
of mental representation in mental scripts: some processing, located at a more
abstract level, involves representation of the entire script, at least in terms of a
beginning, a body and an end (Grafman, 1989). On the other hand, some
processing, located at a concrete level, only requires the identification and
enactment, by habit, of the appropriate node in a sequence (Grafman, 1989).
However, unlike Shallice, Grafman proposed that both these levels are located in
the frontal cortex primarily. A few attempts have now been made to
operationalize script generation tasks as ADL (Schwartz et al., 1995, 1991).
274 Sandra Fortin and Others
Shallice and Burgess (1991) found that three head injured patients with frontal
lobe damage were impaired in an ADL formatted as a requirement for
generation and execution of a script (i.e., careful attention was paid to the
patient’s sequencing of relatively long chains of everyday routine actions toward
a goal provided by the experimenter). They interpreted this impairment as a
deficit of executive function. Schwartz and colleagues (1998) found that a large
cohort of head injured patients was impaired in an ADL similarly formatted as a
script task. They set up their investigation to test various frontal lobe functions
purported to underlie ADL. For example, their ADL required a moderate level
of multitasking. They proposed that ADL seem to be supported by a variety of
frontal lobe dependent attentional functions.
The central executive system (CES) is a high order cognitive frontal lobe
module which manages multiple complex mental operations under time pressure,
and which is subserved by hemispherically specialized slave systems, namely a
left hemisphere phonological loop system and a right hemisphere visuospatial
scratchpad (Baddeley, 1986; D’Esposito et al., 1995; Smith and Jonides, 1997).
The central executive system is a clear and elegant operationalization of working
memory: tasks purported to solicit one or the other slave system are considered
CES tasks when they are required to be carried out simultaneously under time
pressure (dual-task paradigm) (Baddeley and Della Sala, 1996; Baddeley et al.,
1997). Head injured patients have been found to be outstandingly impaired at the
level of the CES (McDowell et al., 1997; Leclercq et al., 2000). Although we have
not been able to locate any reports of research on the link between the CES and
ADL in brain damaged patients, the idea certainly has been articulated (Stablum et
al., 2000). Burgess and colleagues (2000) recently reported a major investigation
of effects of focal lesions on a multitask laboratory activity. The multitask
procedure was not structured in the manner of Baddeley’s dual-task paradigm, and
thus the authors’ conceptual framework was not expressed in terms of Baddeley’s
CES, but we propose that this important report is very informative for our thinking
about components of frontal lobe function underlying ADL, including the CES.
S
TATEMENT OF
P
URPOSE
The present investigation was designed to more heavily solicit prospective
memory, strategic planning and working memory than previous investigations, and
to thus attempt to substantiate the existence of a hierarchy of mental processing
(SAS versus CP, c.f., Shallice, or an abstract versus a concrete level, cf., Grafman)
in ADL formatted as a script task. We also aimed to achieve this dissociation
neuropsychologically, which is why we recruited a sample of head trauma patients
with confirmed or suspected frontal lobe lesions, so as to demonstrate a specific
impairment of the SAS and not the CP in the context of a clear impairment of
ADL. The ADL investigated by Schwartz and colleagues (1991, 1995) were very
simple (e.g., making a cup of coffee). In our opinion, these script generation tasks
do not solicit prospective memory at all. Those developed by Shallice and Burgess
(1991) do so, but still not enough. Furthermore, these tasks only minimally solicit
frontal lobe working memory in that they are so unidimensionally linear, slavishly
Executive deficits in ADL following CHI 275
sequential and routine that they do not approach the limits of the central executive
system (as indexed by low or inexistent error rates in normals). We reasoned that
by imposing a far more complex and long lasting multitask ADL, we could (1)
heavily solicit prospective memory (which we associate with the SAS) among
other things, (2) impose strategic sequence planning, (3) tax working memory (the
CES), and (4) thus better isolate routine action sequences and sub-sequences
(which we associate with the CP).
M
ETHOD
Participants
Ten subjects had mild to severe closed head injury (CHI) with radiologically
confirmed (n = 9) or suspected (n = 1) damage to the frontal lobes and 12
controls were age, gender and education matched (see Table I). The severity of
the head trauma was estimated with the Glasgow Coma Scale (GCS) (GCS score
≤8 = severe, GCS score 9-12 = moderate, GCS 13-15 = mild [Teasdale and
Jennett, 1974]). The GCS score of each patient was the rating determined upon
hospitalization at the emergency room. However, since some participants with a
GCS score between 13 and 15 also had a confirmed cerebral lesion, the severity
of their head trauma could have been underestimated. Frontal lobe damage
corresponded to the presence of a lesion in this area as identified by CT scan
obtained within a post trauma interval of 24 hours. One patient (CG) was
suspected of having frontal lobe damage on the basis of neuropsychological
evaluation. Only one of the patients (JL) underwent neurosurgery (right frontal
craniotomy with evacuation of an epidural hematoma) resulting from the head
trauma. None of the participants had a major motor problem and only one
presented a major sensory deficit (blindness of the left eye). All patients were
living independently at the time of the study. Exclusion criteria included
neurological or psychiatric history or past substance abuse. The CHI patients
were recruited in hospitals and rehabilitation centers. Table II presents the
clinical characteristics of the CHI group.
Standardized Tests
Tests selected for routine assessment of executive functions included the
Trail Making Test (Reitan and Wolfson, 1993), Porteus Mazes-Revised (Arthur,
276 Sandra Fortin and Others
TABLE I
Participant characteristics on matching variables
Gender Age (years) Education (years)
Group M F M SD M SD
Control 3 9 31.4 11.3 11.6 2.5
CHI patient 3 7 31.9 10.1 11.7 2.8
M = Male, F = Female, M = Mean, SD = Standard deviation
1947), Thurstone’s Verbal Fluency Test (Thurstone and Thurstone, 1962),
Picture Arrangement subtest of the WAIS-R (Wechsler, 1981), Stroop Test-
Revised (Chatelois, 1993) and Ruff’s 2-and-7 Selective Attention Test
(Baillargeon, 1994; Ruff and Allen, 1996). Ruff’s 2-and-7 test is a paper-pencil
test measuring selective attention for 5 minutes during which the participant
must cross out 2 and 7 digits under two conditions. Under the first condition, the
digits 2 and 7 are dispersed by chance with other digits whereas in the second
condition they are dispersed with letters. The administration and the correction is
standardized. Tests selected for routine assessment of memory included the
Figural Memory, Visual Paired Associates, Verbal Paired Associates, Logical
Memory and Visual Reproduction subtests of the Wechsler memory Scale-
Revised (Wechsler, 1987). The Cognitive Failures Questionnaire (CFQ) was
used to evaluate ADL (Broadbent et al., 1982). The CFQ is a questionnaire
which measures frequencies of failures of behavior in daily life.
Script Recitation Task
As in Godbout and Doyon (1995), subjects were asked to enumerate out loud
“10 to 20 actions, that people generally do, in proper order”, for a specific ADL.
Subjects were asked to avoid idiosyncrasies and were given two examples,
“getting up in the morning” and “putting on your coat and leaving”. They had to
repeat the instructions correctly. Finally, they were asked to create and recite
aloud a script representing “going to the restaurant” and another representing
“doing the groceries”. The semantic structure of the recited actions was
measured using criteria based on four types of action (% major, % minor, %
trivial and % relevant intrusion) as in Godbout and Doyon (1995). To be
included, an action had to be mentioned by at least 25% of the normal control
Executive deficits in ADL following CHI 277
TABLE II
Clinical description of the CHI patients
Subject Age Schooling Localization of Cause Glasgow Trauma to test
(years) contusion by of Coma Scale interval
CT scan lesion Scorea(months)
J.L. 18 11 Right Snowmobile 12 24
orbitofrontal accident
N.A. 24 16 Bilateral frontal Automobile 6 15
accident
R.L. 36 08 Left frontal Fall 14 04
S.L. 27 08 Left frontal Automobile – 10
accident
S.D. 43 09 Left frontal Fall 15 44
C.G. 35 11 – Automobile – 28
accident
P.G. 54 12 Right frontal Fall 15 16
and temporal
F.L. 27 14 Right frontal Automobile 10 22
and temporal accident
F.L. 23 14 Left frontal Automobile 8 22
and temporal accident
C.P. 32 14 Bilateral frontal Assault 12 16
aGCS score determined upon hospitalization at the emergency room.
subjects of the normative study (Godbout, 1994). Actions that met this criterion
were subsequently classified as major (mentioned by more the 65% of the
normal control subjects), minor (mentioned by 45-64% of the normal control
subjects) or trivial (mentioned by 25%-44% of the normal control subjects). A
relevant intrusion was marked when the action did not meet the inclusion criteria
but belonged to the particular script. In the “going to the restaurant” script, an
example of a major semantic selection would be “request the menu”, of a minor
selection, “looking at the menu”, of a trivial selection, “have a cup of coffee”,
of a relevant intrusion, “taking one’s fork and knife”. Sequence errors,
perseverations and irrelevant intrusions were tallied as in Godbout and Doyon
(1995). Examples of sequence errors, perseverations and irrelevant intrusions in
the restaurant script are 1) “paying the bill and then eating the dessert”, 2)
mentioning “paying the bill” twice, and 3) “admiring the mountain view”,
respectively. The neuropsychological tests, script recitation task and ADL were
completed in counterbalanced order.
The ADL Task
The assignment consisted of planning and preparing a complete meal. It was
determined that all subjects had had frequent experience with that particular
ADL in real life. Subjects were required to (1) prepare a menu (2) shop for
groceries, and (3) prepare the meal selected. Each of these tasks comprises a
sequence which is incontrovertible. For example, doing the groceries requires
taking a cart, walking the aisles, selecting items, unloading the cart onto the
counter, taking the bags, etc.
The Menu Preparing Task
The subject was seated before a table with meal suggestion cards (4 entrées,
4 main courses, 4 desserts), an envelope containing money ($10.00) and a subset
of ingredients required for each meal. The subject was required to plan a 3
course meal within the budget allotted that could be prepared within 45-60
minutes. Only one menu was feasible, canned soup as entrée, boiled potatoes
and ground beef for the main course and brownies for dessert. The task required
that the subject take cognizance of the budget, select the menu accordingly and
prepare the list of missing ingredients. The setting was a hospital kitchenette
with two experimenters, one providing the instructions and the other handling
the video camera. Subjects who prepared an inappropriate menu were requested,
afterwards, to prepare the soup-beef/potatoes-brownie menu so as to create a
more standard context for the subsequent task.
The Grocery Shopping Task
Once the menu was planned, the participant was required to go to the
grocery and purchase the missing ingredients having been instructed to select the
smallest quantities of the essential ingredients only, and to stay within the
budget. The grocery was a 5-minute car drive from the hospital. The
experimenters accompanied the participant and took note of the behavior.
278 Sandra Fortin and Others
The Meal Preparation Task
Once back at the kitchenette, the participant was required to prepare the
meal as if for a guest arriving in an hour -including setting the table for two.
To respect this constraint, the participant gained to realize that the dessert had
to be prepared first (30 minutes preparation time). The subject was filmed and
the experimenters limited their interactions with the participant to a strict
minimum.
Scoring System of the ADL Tasks
Scoring of the ADL comprised two levels, a first dealing with “ability to
achieve the goal”, and a second dealing with a variety of specific types of errors
and behaviors. Examples of “inability to achieve the goal”, for the menu
preparation task, are choosing the wrong menu or omitting ingredients in the
grocery shopping list, for the grocery shopping task, purchasing wrong quantities
or the wrong items, for the meal preparation task, serving the meal or a course
too late, or a course cold, deviating from the recipe or from the alloted time.
More than 12 minutes between two courses was the criterion for desynchrony of
courses, based on the fact that none of the controls of the present study or 10
controls of another study (Grenier, 2000) had surpassed 11 minutes. A second
level of scoring resembled that of the script recitation task: sequence errors (ex:
putting the brownie mix in the oven before turning the oven on) and irrelevant
intrusions (ex: selecting an ingredient not on any card). In addition however, we
tallied omission errors (ex: forgetting an ingredient). During the meal
preparation task, we also tallied alternation behavior (verification of, or
intervention in, one course, during the execution of another). Requests for a
repetition of the instructions were also tallied. Time on task was noted in
minutes.
Macrostructure and Microstructure of ADL
In a complex multitask ADL such as this one, we have proposed (Godbout et
al., 2000) that mental operations can be conceptualized and operationalized in
terms of a macrostructure and a microstructure. The macrostructure is the
representation and implementation of the script as a whole (i.e., the actual plan
towards a goal). This is a relatively abstract level of representation, which in our
opinion is germaine to the SAS, strategic planning and prospective memory. The
microstructure is the representation of the highly routine (overlearned and
relatively short) sub-sequences of the script in which individual actions are
termed “nodes” (ex: greasing the pan, putting the ground beef in the pan, turning
off the burner). This is a relatively concrete level of representation, which we
relate to the CP (see Godbout et al., 2000). These macro and microstructures
cannot be drawn quantitatively from recited scripts, or even from the menu
preparation or grocery shopping tasks. Only the meal preparation task lent itself
to an operationalization of this particular construct. We propose that the script’s
macrostructure is reflected in the first node and the last. Regarding the first
Executive deficits in ADL following CHI 279
node, there is an impairment of the macrostructure if the subject does not select
to prepare the strategic course first (because the dessert takes longer to cook, it
must be prepared first). In that case, a starting error is scored and represents a
difficulty of planning. Regarding the last node, there is also an impairment of
the macrostructure if the courses do not arrive on time or in fast enough
sequence. In that case, an end point timing error is scored, indicating failure to
engage prospective memory during the task. For the microstructure, three types
of errors were scored, namely intrusion, omission and sequencing errors. Cooper
and colleagues (1995, 1997) simulated the PC in a virtual ADL task and the
resultant model associated omission errors with the CP.
This scoring system has been developed in the course of several previous
research projects on normal aging (Godbout et al., 2000) and frontally lesioned
patients (Grenier, 2000) as well as normal control groups in each of these
studies. Scoring was done from the videotapes and notes by two independent
raters. None of the scores presented in the upcoming results section suffered an
inter-rater concordance of less than 95%.
R
ESULTS
Matching of the Experimental and Control Groups
T-tests revealed no difference in age [t (20) = 0.10, n.s.] or education [t (20)
= 0.10, n.s.] between the head injured and normal groups.
280 Sandra Fortin and Others
TABLE III
Comparison of the CHI patient and control groups with t-tests on measures of executive function
Group
Measures of
executive function CHI patient Control
(N = 10) (N = 12)
M SD M SD t (20)
Trail Making Test
Part A (sec) 28.10 8.96 28.08 11.35 0.004
Part B (sec) 65.40 25.95 63.08 22.57 0.22
Porteus Mazes Test 14.20 1.74 15.58 1.93 – 1.75
Verbal Fluency Test
Lexical 30.10 7.16 37.33 11.28 – 1.75
Semantic 35.00 10.64 41.08 7.89 – 1.54
Picture Arrangement 10.50 1.27 10.83 1.70 – 0.51
Stroop Test
Color (sec) 68.60 8.59 63.50 18.43 0.85a
Interference (sec) 125.20 27.42 100.50 21.13 2.39*
Flexibility (sec) 142.60 30.86 118.75 37.92 1.60
Ruff’s 2 and 7 Test
Speed 245.70 55.97 320.42 76.25 – 2.57*†
Accuracy 95.57 4.30 95.78 1.89 – 0.14a
Processing 1.13 0.14 1.20 0.14 – 1.09
M = Mean, SD = Standard deviation
aA t-test was adjusted for unequal within variance for these contrasts.
*p < .05. † This comparison remained significant after Bonferroni-Holm correction for type 1 error.
Neuropsychological Tests
The CHI patients and controls were compared on the neuropsychological tests
with t-tests (Table III and Table IV). Only two measures of “executive function”
were indicative of a significant impairment of the CHI patients, namely the
interference condition (time-to-completion) of the Stroop test [t (20) = 2.39,
p < .05] and speed on Ruff’s 2-and-7 Test [t (20) = – 2.57, p < .05]. There were
no differences between the groups on measures of memory performance
(Memory Quotient, Verbal Memory Quotient, Non Verbal Memory Quotient) or
on the CFQ [CHI patients M = 36.30, SD = 17. 60, normal group M = 37.83,
SD = 9.60, t (20) = – 0.26, n.s.].
Script Recitation Task
Semantic Aspect
A first t-test determined that the total number of actions recited did not differ
between the two groups [t (20) = – 1.04, n.s]. A 2 ×4 repeated measures
ANOVA determined that there was no interaction between GROUP and
ACTION TYPE (major, minor, trivial or intrusive relevant [F (3, 60) = 1.10,
n.s.]. This suggests that whatever might be a cause of script generation deficits,
or of ADL, in this cohort, it will not be a result of impairment of semantic
structure, or of access to semantic memory.
Errors
Tallies of perseverations, intrusion and sequence errors, per group, were
submitted to the Fisher Exact Test (Table V). Two patients and no controls
made irrelevant intrusion errors (n.s). There were no perseverative errors at all.
However, the CHI patients committed significantly more sequence errors than
the normal control group (4/10 vs. 0/12, p = .029).
ADL Tasks
Ability to Achieve the Goal
The high performance of the normal subjects on this task supported a simple
characterization of “ability to achieve the goal” i.e., success/failure: no errors on
Executive deficits in ADL following CHI 281
TABLE IV
Comparison of the CHI patient and control groups with t-tests on memory quotient scores
Group
Quotient CHI patient Control
(N = 10) (N = 12)
M SD M SD t (20)
Memory 109.20 20.79 109.42 13.30 – 0.03
Verbal memory 104.80 23.19 104.17 11.81 0.08a
Non verbal memory 120.30 14.41 117.08 13.62 0.54
M = Mean, SD = Standard deviation
aA t-test was adjusted for unequal within variance for this contrast.
any ADL = success, one or more errors on any ADL = failure (Table VI) (note
that the errors under consideration exclude first action, end point timing,
sequence, omission and intrusion errors, see the method section). Thus
operationalized, Fisher Exact Tests indicated no significant impairment of the
CHI patients relative to the control group on the menu preparing task (5/10 vs.
7/12, p = .794). However, the CHI patients were significantly impaired on the
grocery shopping (6/10 vs. 1/12, p = .015 ) and meal preparation tasks (6/10 vs.
1/12, p = .015). On the grocery shopping task, the CHI patients did not respect
the required quantities of ingredients and on the meal preparation task the CHI
patients did not successfully complete various courses (ex: cake not cooked
enough, cold soup).
Specific types of errors
A t-test determined that the CHI patients (M = 4.1, SD = 2.56) made a
greater number of errors (starting, end point timing, sequence, intrusive, and
omissive) than did the normal controls (M = 1.5, SD = 1.83) [t (20) = 2.77, p =
.012]. The two groups were then compared for each type of error with Fisher
Exact Tests. See Table VII. With regard to the macrostructure, the CHI patients
made significantly more errors selecting the first action of the meal preparation
task (did not start with the dessert), as well as significantly more errors in
282 Sandra Fortin and Others
TABLE V
Comparison of the CHI patient and control groups with the Fisher Exact Test on errors pertaining to
the script generation task
Group
Error type CHI patient Control
(N = 10) (N = 12)
0 error ≥1 error 0 error ≥1 error p
Sequencing error 6 4 12 0 .029*
Perseveration error 10 0 12 0 –
Intrusion error 8 2 12 0 .195
* p < .05.
TABLE VI
Comparison of the CHI patient and control groups with the Fisher Exact Test on ability to achieve
the goal (ADL tasks)
Group
ADL Task CHI patient Control
(N = 10) (N = 12)
0 error ≥1 error 0 error ≥1 error p
Menu preparing task 5 5 5 7 .794
Grocery shopping task 4 6 11 1 .015*
Meal preparation task 4 6 11 1 .015*
* p < .05.
serving the meal in synchrony (< 12 minutes between courses). With regard to
the microstructure, a Fisher Exact Test of omission errors (ex: omitting an
ingredient) indicated an impairment of the CHI patients.
Other analyses
The two groups were comparable in alternations between courses during the
meal preparation task [t (20) = – 1.47, n.s.]. The number of requests for a
repetition of the instructions was comparable for the two groups (8/10 vs. 8/12,
p = .417). Though two CHI patients were confused at outset in one of the ADL
(minutes of hesitation), the effect was not significant. Time on task (TOT)
fluctuated wildly and was not normally distributed, so it was log transformed
log10 (TOT + 1). T-tests indicated that time on task did not differ for the two
groups on the menu preparing task [t (20) = – 1.13, n.s.] or the grocery
shopping task [t (20) = 1.81, n.s]. However, the CHI patients (M = 53.09,
SD = 13.63) spent more time on the task than the control group (M = 44.39,
SD = 6.96) in the meal preparation task [t (20) = 2.14, p < .05].
Relation between the ADL Tasks, Neuropsychological Tests
and the Script Recitation Task
Each neuropsychological test measure and the global error score (sum of
sequence, irrelevant intrusion and perseverative errors) on the script recitation
task were compared to each other with the Fisher Exact Test, as well as to the
global error score on the ADL task, and to each term of the ADL
macrostructure, namely starting and end point timing errors on the meal
preparation component. Neuropsychological test measures were dichotomized at
the median, and the script generation and ADL measures were coded as pass =
no errors, and fail = one or more errors. The Stroop flexibility condition (time-
Executive deficits in ADL following CHI 283
TABLE VII
Comparison of the CHI patient and control groups with the Fisher Exact Test on errors pertaining to
the microstructure and macrostructure
Group
ADL Task CHI patient Control
(N = 10) (N = 12)
0 error ≥1 error 0 error ≥1 error p
Macrostructure
Starting error 3 7 9 3 .046*
(strategic planning)
End point timing error 4 6 12 0 .003*†
(prospective memory)
Microstructure
Sequencing error 3 7 7 5 .185
Omission error 5 5 11 1 .043*
Intrusion error 9 1 12 0 .455
* p < .05. † This comparison remains significant after a Bonferroni-Holm correction for type 1 error.
to-completion) related significantly positively to the global ADL error score
(p < .01) and Trails B time-to-completion related positively to starting errors on
the ADL task (p < .02). Within the ADL task macrostructure, starting errors did
not relate significantly to end point timing errors. The global error score on the
script recitation task related significantly positively with poor Stroop flexibility
(p < .02). The relation between the script recitation task and the ADL measures
fell short of significance. We also coded end point timing errors by
dichotomizing at the median. So operationalized, end point timing errors
co-varied significantly with Stroop flexibility (p < .01), Stroop Color naming
(p < .05), Semantic fluency (p < .05 ), QM (p < .05) and the global error score
on the script recitation task (p < .02). However, after Bonferroni-Holm
correction for type 1 error, the relation between end point timing errors
dichotomized at the median and semantic fluency and Stroop color naming were
no longer significant. All the other comparisons remained significant.
D
ISCUSSION
Is there something special about ADL in the neuropsychological context?
Though they are of obvious critical importance in the clinical setting because of
their importance for the patient, the cognitive underpinnings of ADL remain
quite mysterious. When they are tested directly, ADL can reveal residual
impairment in stabilized cases which is no longer visible in most formal
cognitive tests, as in the present investigation. Our ADL task appeared to better
identify impairment of these head injured patients with frontal damage than the
cognitive tests we had selected. This aspect of our findings supports the
literature (reviewed in the introduction) reporting substantial and longstanding
impairment of ADL in closed head injury.
The critical cognitive components in the impairment of ADL observed in the
present investigation appear not to be in the domains of declarative or semantic
memory, nor in several aspects of executive function such as visual search (Trails
Test), brief mental sequencing (Picture arrangement), or short-term planning
(Porteus Maze Test). However, it is to be stressed that four of our ten CHI
patients had undergone a neuropsychological evaluation beforehand. Thus, it is
possible that a practice effect mitigated the difference on the neuropsychological
tests between the CHI group and the control group. However, our finding of a
normal cognitive profile in this cohort of patients presenting difficulties in a
complex ADL is in agreement with clinical observations detailed in previous
reports (Ackerly and Benton, 1947; Brickner, 1936; Cripe, 1996; Eslinger and
Damasio, 1985; Shallice and Burgess, 1991). Mental slowing (Ruff’s 2-and-7 test)
and sensitivity to interference (Stroop interference condition) were observed in the
CHI cohort (parametric testing only). Thus, inattentiveness and mental slowing
may have played a role in the impairment of ADL. Regarding mental slowing, we
think this may have contributed only modestly to performance on our ADL task.
Recall the absence of significant relation between the Stroop interference
condition, Ruff’s 2-and-7 test and the end point timing error score. Moreover,
none of the CHI patients had a major motor problem such as paresis. A potential
284 Sandra Fortin and Others
problem in stating that the CHI patients were “better” on neuropsychological tests
than the ADL task is that different statistics were used for these two domains,
namely t-tests for the neuropsychological tests and Fisher Exact Tests for the
ADL task. Consequently, we submitted the neuropsychological tests to Fisher
Exact Tests (with groups split at the whole cohort median). With this more
conservative statistical approach, none of the neuropsychological tests yielded a
significant group difference.
We propose rather that prospective memory may be a key element of the
particular impairment of ADL observed here, particularly the time-based more
than the event-based component. Time-based prospective memory has been
found to be more impaired in normal aging (Einstein et al., 1995; but see
Rendell and Thomson, 1999) and in brain damage (Cockburn, 1996; Shum et al.,
1999) than event-based prospective memory. Unfortunately, no research has yet
been done, that we could find, to determine whether frontal lesions outstandingly
impair time-based more than event-based prospective memory. Though the
relationship between time-based prospective memory with executive function
remains tenuous, it is clear that it is less correlated with retrospective episodic
memory than is event-based prospective memory (Cockburn, 1996). In the
present investigation there was no relationship between script recitation or
performance in ADL and retrospective episodic memory, vaguely suggesting that
event-based prospective memory could have been intact in our CHI patients.
However, in the absence of independent measures of prospective memory, the
presence of a prospective memory deficit in our cohort of CHI patients remains
an assumption.
Furthermore, we propose that prospective memory may not have been the
only important cognitive component of successful accomplishment of our
complex ADL. In the present investigation there was evidence to the effect that
both strategic planning and prospective memory were impaired in the CHI
patients on the ADL task. In fact, our macrostructure is a combination of
strategic planning, prospective memory and working memory constructs. The
first action in our meal preparation task is probably more akin to strategic
planning than to prospective memory per se (one plans to remember something
in the future, but actually remembering it is another thing). The CHI patients of
the present investigation were significantly impaired on this specific component
(p = .046). The last action of our meal preparation task (serving the courses with
good timing) is probably more akin to time-based prospective memory than to
planning. Indeed it reflects the cumulative ability to manage the timing aspect of
the task as it is unfolding. The CHI patients of the present investigation were
outstandingly impaired on this specific component (p = .003). Success on the
first element was not correlated with success on the last, suggesting again
differing underlying cognitive abilities.
It could be argued that the difficulties of the CHI patients on the ADL task in
the absence of a major deficit on the neuropsychological tests, could be due to
greater difficulty of the ADL task than the tests traditionally used in clinical
neuropsychology. Thus, the differences between the CHI patients and the control
group could be an artifact of psychometric properties of the ADL task rather than
true differences in the abilities of the two groups (see Miller et al., 1995). Our
Executive deficits in ADL following CHI 285
ADL task and the neuropsychological tests indeed have different characteristics.
As outlined by Shallice and Burgess (1991), “on neuropsychological tests, the
patient typically has a single explicit problem to tackle at any one time, the trials
tend to be very short, task initiation is strongly prompted by the examiner and what
constitutes successful trial completion is clearly characterized. Rarely are patients
required to organize or plan their behavior over long time periods, or to set
priorities in the face of two or more competing tasks”. Successful performance of
the patients on traditional paper-pencil tests could thus be explained as irrelevant
to the patients’ deficit since certain such tests may not tap strategic planning or
prospective memory, in contrast to everyday life activities such as preparing a
complex meal, which involves the “prioritization of competing demands and
creation, maintenance and activation of delayed intention” (Burgess et al., 2000).
More support for a deficit of strategic planning and prospective memory ADL
among CHI patients, would be afforded by administration of tasks specifically
designed to test these functions. For this purpose, we propose the Six Element Test
(SET) (Shallice and Burgess, 1991) or the Greenwich Test (Burgess et al., 2000).
These multitasking tests consist of 3 open-ended tasks, which the participants are
required to attempt in a fixed period of time in a way which maximizes the overall
score. Certain rules have to be respected. The Greenwich Test procedure permits
partialing out of the relative contribution of task learning and remembering,
planning, plan-following (prospective memory) and remembering one’s actions, in
a multitasking performance. An important study has shown that among measures
of intelligence, memory, language, perception and several measures of the
executive functions, only the Cube Analysis subtest from the Visual Object and
Space Perception Battery and the SET were significantly associated with
intentionality (Burgess et al., 1998). Using the Greenwich test, Burgess and
colleagues (2000) found that lesions to the left posterior cingulate and forceps
major regions gave deficits on “task learning and remembering, plan-following
(prospective memory) and remembering one’s actions”, but not “planning”.
Remembering task contingencies after a delay was also affected by lesions in the
region of the left anterior cingulate, and rule-breaking and failures of task switching
were additionally found in people with lesions affecting the medial and more polar
aspects of Brodman’s areas 8, 9 and especially 10. Planning deficits were
associated with lesions to the right dorsolateral prefrontal cortex. Thus, tasks
soliciting prospective memory and strategic planning seem sensitive to brain
damage, particularly of the frontal lobes.
Representational Hierarchy in Script Generation
Our findings obliquely support Shallice’s (1982, 1988) and Grafman’s (1989)
notions of a mental hierarchy in script generation. As expected, it was the
macrostructure of the ADL task which most outstandingly identified the plight
afflicting our subjects with head injury and frontal lobe damage, ten times more
significantly than the microstructure. The emphasis in the literature on the
neuropsychology of scripts has leaned very heavily to the action sequencing
component. The errors given most consideration have been sequence errors.
However, the present investigation suggests that sequencing per se, though
286 Sandra Fortin and Others
impaired on our paper-pencil script recitation task (in this respect, we have
replicated Godbout and Bouchard, 1999; Godbout and Doyon, 1995; Sirigu et al.,
1995, 1996), may not have been the most impaired within script generation in this
particular cohort of frontally lesioned CHI patients in an ADL setting. It was the
highest, most abstract, level of representation of the script which was the most
impaired. This very high level is not solicited in simple script recitation, nor is it
in brief routine ADL activities -and even less in presently available formal
neuropsychological tests. This is not a reason to ignore or dismiss the
microstructure in ADL however. Indeed, we did observe significant impairment,
only less marked, of the microstructure, specifically in the form of omission errors
in the ADL tasks. Schwartz and colleagues (1998) also reported significant rates
of omission errors in an ADL task in head injured patients.
The present findings partially support Grafman’s (1989) writings cognitively
and Shallice’s (1982, 1988) writings neuropsychologically. Indeed, the cognitive
difference between macrostrucuture and microstructure, as defined by us, is more
a matter of abstractness of the former and concreteness of the latter (c.f.,
Grafman) than non routineness of the former and routineness of the latter (c.f.,
Shallice). After all, preparing a meal is very routine, -it is whether we do it well
or not, and of course it is not easy at all to be a perfect chef even though we may
cook meals every day. On the other hand, our frontally damaged patients had a
clearly more marked impairment in the macrostructure than the microstructure. A
study such as the present one cannot determine definitively that it was the frontal
damage of this cohort of CHI patients which produced the pattern of results. A
comparison with a group with extra-frontal lesions would provide a more
definitive demonstration. Nevertheless, the results obtained here lead us to
suggest that two brain substrates ought perhaps be conceptualized, one for each
level (as in Shallice, 1982), rather than only one for both levels (as in Grafman,
1989). Whether the other critical brain substrate (which when lesioned would
selectively destroy the microstructure) is in the basal ganglia or elsewhere in the
frontal lobe or anywhere else, for that matter, remains to be investigated. A brain
substrate for the microstructure may not exist at all. Because the microstructure
is so basic, overlearned and simple, we propose that it is probably diffusely
distributed throughout the brain, with a slight predominance for the premotor,
prefrontal and central grey areas and their interconnections. It is well established
that procedural memory does not reside in the hippocampi, as HM and other
patients without functional hippocampi are quite normal on procedural memory
tasks (Gabrieli et al., 1993). However, even though there has been enthusiasm for
the idea (e.g. Duyckaerts et al., 1998), there really does not seem to exist a
highly localized repository, such as the basal ganglia, for overlearned material in
the brain, not even procedurally encoded acquired action sequences (Wise, 1996),
let alone explicitly declarative sequences such as solicited in script tasks. Rather,
procedural learning, in its acquisition and retention components, involves a more
distributed frontal-basal ganglia circuit (Poldrack et al., 1999). Likewise, there is
no general empirical basis for stating that the frontal lobe is the exclusive
repository of all that is action sequencing. For example, Kolb and Milner (1981)
found that imitation of a series of three brachial actions is easier for frontal
lobectomy patients than for parietal lobectomy patients. Likewise, Cloutier
Executive deficits in ADL following CHI 287
(1997) found that parietal patients have greater difficulty in script generation than
frontal patients when the scripts are spatially demanding. Though the small
sample size limits the strength of the conclusions that can be reached here, we do
feel confident that the frontal lobe is important in strategic planning and
prospective memory in complex long lasting multitask ADL. Grenier (2000)
found that the same ADL task as here yielded results very similar to our CHI
patients, with a cohort of patients with focal frontal lesions (excised tumors).
Questions of Ecological Validity
Self rating of ADL may not be a very valid index in closed head injury.
Indeed, the Cognitive Failures Questionnaire appeared insensitive in the present
study. Although the CFQ is a useful measure, it is very specific to everyday
cognitive errors rather than a measure of what the individual actually performs or
is capable of performing. The Glasgow Outcome Scale (Jennett and Bond, 1975),
the Disability Rating Scale (Rappaport et al., 1982) and the Community
Integration Questionnaire (Willer et al., 1993) are more direct measures of ADL.
Future studies of ADL might do well to include such measures. However, the
present results do show that real-life ADL tasks can be quantified and that they
can be outstandingly sensitive to brain damage. They are however unwieldy for
the typical clinical setting. We are beginning to identify critical cognitive
components of performance in complex ADL such as prospective memory and
sequence planning. Existing commercially available paper-pencil tests of these
functions are probably not adequate for the purpose of identifying impairment of
these components in for ADL. The Porteus Mazes test undoubtedly measures
sequence planning. However, the mental operation required is single-task, it is
highly structured, it involves a narrow set of action sequence options, it is of short
duration and it comprises no time pressure. That is not the sort of “strategic”
planning that seems critical for complex ADL, at least not as suggested by the
results of the present investigation. The Rivermead Behavioral Memory Test
(Wilson et al., 1991) contains a few items claiming to measure prospective
memory. The prospective memory component of that test is selectively sensitive
to the early stage of dementia (Huppert and Beardsall, 1993) and to Parkinson’s
disease (Katai, 1999) but it is probably far too rudimentary, and the task too easy
for this test to be a likely candidate for predicting impairment of complex ADL.
More research must be carried out to identify the critical cognitive components of
complex ADL, in view of implementing brief and inexpensive (paper-pencil)
desktop approaches to these components, if possible, so as to eventually develop
clinically relevant performance-based tests that will be useful for the prognosis of
performance of complex ADL in brain damaged patients.
Acknowledgments. This research was made possible in part by grants from the Fonds
Institutionnel de Recherche de l’Université du Québec à Trois-Rivières to the second author
and by a scholarship from the Natural Sciences and Engineering Research Council of Canada
to the first author. An abbreviated form of the work reported here was presented at the
annual meeting of Theoretical and Experimental Neuropsychology (TENNET), in Montreal,
in June 2001.
288 Sandra Fortin and Others
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(Received 9 April 2001; reviewed 30 Maj 2001; revised 29 April 2002; accepted 17 September
2002; Action Editor Jordan Grafman)
Executive deficits in ADL following CHI 291
