AN ECOLOGICAL APPROACH TO PLANNINGDYSFUNCTION: SCRIPT EXECUTION
Mathilde Chevignard1, Bernard Pillon2, Pascale Pradat-Diehl1, Chantal Taillefer1,Sylvie Rousseau1, Catherine Le Bras2 and Bruno Dubois2
(1Service de Rducation Neurologique, 2INSERM EPI 007 and Fdration de Neurologie,Hpital de la Salptrire, Paris, France)
Planning, which concerns many activities in everyday life, is a two-stage process. Thefirst one predetermines a course of actions aimed at achieving some specific goals. It isfounded on managerial knowledge or overlearned sequences of events and may be testedby script generation. The second stage entails monitoring and guiding the execution of theplan to a successful conclusion. It must take into account environmental contingencies andmay be tested by script execution. If the frontal lobes intervene not only in managerialknowledge (Grafman, 1989) but also in binding the plan with contextual environment(Damasio, Tranel and Damasio, 1991; Shallice and Burgess, 1991), script execution wouldbe more sensitive than script generation to planning deficits. To test this hypothesis, scriptexecution and script generation were compared in 11 patients with a dysexecutive syndromeand 10 matched controls, using three scripts of daily life activities: (1) shopping forgroceries; (2) cooking; (3) answering a letter and finding the way to post the reply.Two way ANOVAs showed more errors in execution than in generation, more errors inpatients than in controls, and a greater difference between execution and generation inpatients than in controls. Furthermore, context neglect and environmental adherencewere the two types of errors that best differentiated patients from controls. Finally, the totalnumber of errors in execution correlated with the score on behavioral questionnairesanswered by occupational therapists. These results confirm our hypothesis and suggest thatscript execution may be a valid ecological approach to estimate the severity of deficits indaily life activities.
Key words: script generation and execution, planning, dysexecutive syndrome,ecological approach, frontal lobe lesions, closed brain injury
Planning is the ability to organize behavior in relation to a goal that must beachieved through a series of intermediate steps (Luria, 1966; Owen, 1997). Thisability is currently assessed with laboratory tests, such as maze tracing (Porteus,1959; Karnath, Wallesch and Zimmerman, 1991) and problem resolution (Luria,1966; Lhermitte, Derouesn and Signoret, 1972; Klosowska, 1976), including theTower of London Task (Shallice, 1982, 1988). The performance of patients withfrontal lobe lesions on such tests is regularly impaired (Owen, Downes,Sahakian et al., 1990; Morris, Miotto, Feigenbaum et al., 1997), underlining therole of the dorsolateral prefrontal cortex in cognitive organization (Stuss, Eskesand Foster, 1994). This cognitive role has recently been confirmed by PETstudies of normal subjects resolving Tower Tasks (Baker, Rogers, Owen et al.,
Cortex, (2000) 36, 649-669
1996; Owen, Doyon, Petrides et al., 1996). Planning is also important forbehavioral adaptation in daily life. For example, following frontal lobe surgery awoman failed to prepare an entire family meal, although she was capable ofcooking the individual dishes (Penfield and Evans, 1935). Since this description,several neuropsychological studies showed that daily life activities might beimpaired despite normal cognitive performance in the laboratory (Eslinger andDamasio, 1985; Shallice and Burgess, 1991). As underlined by the latter, thedifference might be due to the need of maintaining the plan over longer periodsof time in the face of competing alternatives in daily life situations.
However, assessing planning in daily life is difficult. Due to a reduction ininsight associated with frontal lobe lesions (Stuss, 1991; Prigatano, 1991),patients generally underestimate their functional impairment in everydaysituations. Relatives or caregivers rating on behavioral scales (Lhermitte, Pillonand Serdaru, 1986) has been found to correlate with the metabolism of specificregions of the frontal cortex, namely orbitofrontal areas (Sarazin, Pillon,Giannakopoulos et al., 1998). Rating depends, however, on subjective feelingsand many caregivers also tend to underestimate the patients deficits. Therefore,more objective evaluations have been proposed, such as the Six Element or theMultiple Errands Tests (Shallice and Burgess, 1991), the Executive FunctionRoute Finding Test (Boyd and Sautter, 1993) or the Behavioural Assessment ofthe Dysexecutive Syndrome (Wilson, Evans, Emslie et al., 1998). Althoughecologically valid, these tests show a great variability of performance even innormal controls, some of them being as severely impaired as patients withfrontal-lobe lesions (Levine, Stuss, Milberg et al., 1998). The impairedperformance of normal subjects on these tasks underlines the importance ofusing more familiar plans of actions in order to limit the inter-individualvariability of normal control subjects and allow a better differentiation betweenpatients and controls. Naturalistic actions, even as simple as preparing a slice oftoast with butter and jam or packing a lunchbox, may be impaired in patientswith brain lesions, at least in cases of closed head injury (Schwartz,Montgomery, Buxbaum et al., 1998).
One recent cognitive model postulates that planning deficits are related toimpairments in a domain specific to managerial knowledge involved in therepresentation and manipulation of script-like structures (Grafman, 1989).Managerial Knowledge Units would be overlearned sequences of events with abeginning and a end and a hierarchical organization going from more abstract(eating to a restaurant) to more concrete levels (paying the bill). Frontal lobelesions would specifically affect this kind of representations. In agreement withthis hypothesis, script generation and sorting has been shown to be impaired inpatients with frontal-lobe lesions (Le Gall, Aubin, Alain et al., 1993; Godboutand Doyon, 1995). In previous studies, we found that these patients made errorsin ordering actions in the correct temporal sequence, failed to close scripts andremain within the stated boundaries, and made deviant estimates of actionimportance (Sirigu, Zalla, Pillon et al., 1995, 1996).
Script generation, which is mainly based on the ability to access script-related content, only involves the first stage of planning, i.e. thepredetermination of a course of action aimed at achieving some goal. The
650 Mathilde Chevignard and Others
second stage entails self-monitoring and guiding the execution of the plan to asuccessful conclusion (Hayes-Roth and Hayes-Roth, 1979). Two qualitativelydistinct processes could determine which particular schema of action would beactivated at a given moment of the script execution: an automatic process, theContention Scheduling, which would operate in familiar situations, and acontrolled process, the Supervisory Attentional System, which is thought tomodulate operations when situations are unfamiliar (Shallice, 1988). The twoprocesses could allow integration between plan execution and environmentalcontingencies by operations such as marker creation, marker triggering andevaluation of the consequences of action. Only the Supervisory AttentionalSystem would depend on the prefrontal cortex (Damasio, Tranel and Damasio,1991; Shallice and Burgess, 1991; Verin, Partiot, Pillon et al., 1993; Dubois,Levy, Verin et al., 1995).
If the frontal lobes are indeed involved in both managerial knowledge andmonitoring of action, script execution would be more sensitive than scriptgeneration to planning dysfunction. The first aim of the study was to test thishypothesis by comparing execution and generation of relatively familiar scripts,such as shopping for groceries, cooking and answering a letter and findingthe way to post the reply. The second aim of the study was to evaluate thevalidity of such script execution as an ecological approach to deficits of dailylife activities and to test the hypothesis that it provides a more reliable indicationof dysexecutive deficits in real life than performance in cognitive tests.
MATERIALS AND METHODS
Given the aims of the study, criteria for inclusion were: (1) the evidence of executivedeficits in daily life activities shown by a score > 25 on the dysexecutive questionnaire ofWilson et al. (1998), according to the rating of either the caregiver or the occupationaltherapist; and (2) the existence of structural damage within the frontal lobes on CT scannerand/or MRI (see Figure 1 and Table I). Exclusion criteria were: (1) pre-existing psychiatricor neurological disorders; (2) intellectual deterioration (performance < centile 50 on the PM38 Ravens Progressive Matrices); (3) motor or linguistic deficits, sufficiently severe tointerfere with the tasks. Eleven patients (9 men, 2 women) were selected: two had focalbrain damage restricted to the frontal lobes (left dorsolateral prefrontal cortex haemorrhagein one patient, orbitofrontal lesion resulting from the surgical removal of a meningioma inthe other); nine suffered from severe post-traumatic brain injury. Age ranged from 23 to 60years [mean (SD) = 35.4 (12.3)], and educational level from 8 to 19 years of scolarity [13.8(3.4)]. Duration of disease ranged from 3 to 80 months [27.3 (12.3)]. The performance ofpatients in laboratory tests aimed at assessing executive functions are shown in Table II.For the 9 patients with post-traumatic brain injury, the initial Glasgow score was 6.6 (1.4;range: 3-8), coma duration was 16.6 (12.8) days, and post-traumatic amnesia duration was76.3 (60.9) days.
All patients showed severe difficulties in daily life. Two of them had returned toemployment (OM worked part time in a sheltered employment and JFC worked full timewith his former employer), but both lost their job a few months later. One other subjecthad attempted to return to work, though without medical team approval, but was soon fired.Several caregivers reported accidents in everyday life, some of them being obviously
Script execution 651
652 Mathilde Chevignard and Others
Fig. 1 Lesion location and extent.
Script execution 653
654 Mathilde Chevignard and Others
TABLE ILocalisation of Cerebral Lesions
Patients Duration Initial Coma PTA Localisation of cerebral lesionsof disease Glasgow duration duration on CT scanner or MRI(months) score (days) (days)
OM 31 5 7 120 Left prefrontal cortical and subcortical;bilateral frontal subcortical
EG 5,5 8 7 7 Bilateral anterior prefrontal cortexDG 24,5 5 21 111 Bilateral prefrontal cortical and subcortical,
left temporal, left internal capsuleJFC 1,5 8 6 15 Left prefrontal and temporal cortexAG 81 8 45 180 Right prefrontal cortical and subcorticalLD 18,5 5 21 135 Bilateral (left > right) prefrontal cortical and
subcorticalSL 41 7 20 60 Bilateral prefrontal cortical and subcortical;
right internal capsulePR 8,5 5 14 90 Bilateral prefrontal cortical; left temporalMT 2 6 8 20 Left prefrontal cortical and subcortical;
left internal capsuleMFG 39 Left dorsolateral prefrontal cortexMC 36 Bilateral (right > left) orbitofrontal
TABLE IINeuropsychological Characteristcs of Patients
Mean Standard pdeviation
Wisconsin CSTNumber of criteria 5.7 0.9Number of errors 3.5 3.4Number of perseverations 1.2 1.7
Tower of London Task3N-Number of moves 3.5 1.13N-Time (sec.) 16.2 19.45N-Number of moves 7.7 2.75N-Time (sec.) 26.8 11.65I(+)-Number of moves 7.5 2.35I(+)-Time (sec.) 32.6 21.25I(-)-Number of moves 10 5.55I(-)-Time (sec.) 42 37.6
Six Elements TestGlobal score 880 176.9Number of errors 6.3 3.3 *
Trail Making TestForm A 54.5 24.2 *Form B 118.2 67.6 *B A 63.6 47.6
Verbal fluencyCategory (animals) 20.7 5.1Literal (P, F, L) 28.5 8.1
Grober and Buschke Verbal Learning TestTotal free recall 30.1 7.1 *Total recall 47.2 0.9Sensitivity to cues 95%Delayed free recall 10.7 3.7 *Delayed total recall 15.5 0.7
* p < 0.05 compared to norms.
abnormal. One patient (DG), previously an engineering student, suffered burns while tryingto make holes in plastic bottles with a screwdriver previously heated on the stove; he thentook a shower for 21 minutes and went to bed without calling a doctor, despite havingthird degree burns on all the upper part of his body. Although the caregivers were able tosignal behavioral disorders, they currently underestimated their importance and potentialconsequences: the score of the patients on the dysexecutive questionnaire (Wilson et al.,1998) was 26.9 (12.9) when rated by the caregivers versus 35.3 (13.0) when rated byoccupational therapists.
The control group comprised ten subjects with no history of neurological or psychiatricdisease. They were matched for sex (8 males, 2 females), age [31.6 (9.4) years] andeducation level [15.0 (2.1) years] with the frontal patients.
All subjects gave informed consent.
We chose scripts among current activities of daily life. They had to be complex enoughto be sensitive to impaired dysexecutive functions and to be feasible in a rehabilitationcenter, over a relatively short time period. Three scripts were studied: (1) shopping forgroceries; (2) preparing two recipes of different levels of difficulty (scrambled eggs for twoand a chocolate cake); a written recipe was only proposed for the cake, as cookingscrambled eggs is easy, even without a wide experience of cooking; and (3) answering aletter and finding ones way to a given post-box to post the reply. The familiarity of eachsubject with the scripts was previously controlled using a 3-point scale (0-2): never (0),sometimes (1), often put into practice (2). There was no significant difference in scriptfamiliarity between patients and controls. For each script, execution and verbal generationof actions were compared and the order of presentation was randomized.
The shopping for groceries and cooking scripts were performed on the same day.On a shelf, several items were displayed always in the same location: (1) salt, pepper andoil (usually found in a standard kitchen); (2) all the utensils necessary for the cookingactivity; and (3) some items unnecessary for this particular activity, but normally present ina kitchen, that were used as distracters. On the same shelf, there was a closed cookbook:the cake recipe was on page five. One of the examiners (MC) defined each activity with astatement describing its goal and the scripts starting point and ending point. The examinermade sure the subject had correctly understood the instructions and told him he couldwhenever necessary consult them on a cue card, which remained available throughout thetask. For shopping for groceries, the instructions were: You must go shopping and buyeverything you need to cook scrambled eggs for two persons and bake a chocolate cake.The recipe for the cake is in this book. None of the ingredients are available here (exceptsalt...