Journal of Clinical and Experimental Neuropsychology 2004, Vol. 26, No. 7, pp. 857–873
Script Generation Following Frontal and Parietal Lesions
Journal of Clinical and Experimental Neuropsychology
Lucie Godbout, P. Cloutier, C. Bouchard, C.M.J. Braun, and S. Gagnon Departement de Psychologie, Universite du Quebec a Trois-Rivieres, Trois-Rivieres, Qc, Canada,
ABSTRACT The purpose of this investigation was to distinguish putative effects of parietal lobe lesions on script generation, in distinction from the better known and established effects of frontal lobe lesions. Nine patients, most with excised parietal lesions, were compared to nine age, gender and education matched normal participants. Eleven patients with excised tumors of the frontal lobe were compared to twelve age, gender and education matched normal subjects. Participants were requested to generate, out loud, scripts corresponding to everyday activities. Half the scripts were relatively more demanding with respect to temporal representation (understanding the time line of events) and the other half with respect to spatial representation (understanding the layout of the actions in space). These two conditions were further broken down into conditions of high and low demands on working memory (reciting the scripts backwards versus forward). The frontal lobe patients enunciated significantly fewer actions overall. They were also significantly more impaired than the normal participants on all tasks with high demands on working memory, and more often, high temporal demands (sequencing and perseverative errors). The parietal lobe patients had significant difficulty in sequencing in all conditions, and manifested no perseveration. Though script generation tasks have been primarily associated with frontal lobe function until now, consideration should be given to the type of activity being scripted as a function of relative demands on spatial or temporal representation, as well as working memory, and the contributions of other lobes ought to be taken into consideration.
INTRODUCTION Importance of the Frontal Lobes in Script Generation The importance of the frontal lobes in the planning of complex actions has long been known in behavioral neurology (Luria, 1965). Shallice (1982, 1988) has since proposed a more articulated neuropsychological model of planning of complex actions. Shallice found inspiration in language function which also involves complex action chains (Schank & Abelson, 1977),
thus leading him to term such action generally as the ability to generate “scripts.” The basis of Shallice’s proposal was that planning of daily activities depends on a mental representation of these activities which he termed “cognitive schemata”, of which he distinguished two hierarchically arranged levels: those having to do with novel situations on top and those having to do with routine ones below. The former, Shallice proposed, depends on a frontal lobe circuit which he termed the Supervisory Attentional System (SAS). The second, involving the basal ganglia,
Address correspondence to: Lucie Godbout, Ph.D. Professeure, Departement de Psychologie, Universite du Quebec a Trois-Rivieres, C.P. 500, Trois-Rivieres, Qc, Canada, G9A 5H7. Telephone : (819) 376-5011, poste 3556. Email:
[email protected] Accepted for publication: March 11, 2003.
1380-3395/04/2607-857$16.00 © Taylor & Francis Ltd.
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he termed the Contention Scheduler (CS). The SAS was considered to involve cognitive effort, while the latter was proposed to act more automatically, as a time saver, a mechanism designed to capitalize on overlearned sequences by managing them and blending them into the workings of the SAS, online. Zanini, Rumiati and Shallice (2002) recently attempted to operationalize the SAS/CS distinction using abstract (SAS) and concete (CS) scripts predicting a selective deficit of frontal lobe patients in the abstract and not the concrete conditions. The group x condition interaction failed to reach significance. Grafman (1989) and Grafman and colleagues (1991, 1993) have also developed models of frontal lobe articulation of mental scripts. Their model differs slightly from Shallice’s in one outstanding respect: they believe all complex action chains principally require frontal lobe activity regardless of whether they are routine or novel. In both models, Shallice’s and Grafman’s, the key property of a script is the constraint of a single valid chronological sequence with a definite beginning and end, somewhat similar to constraints imposed by the rules of grammar. For example, if one is to imagine a script concerning going to a restaurant, paying the bill before eating would violate the basic rule of a valid script, which is proper sequentialization of the elements (“nodes”) of the script. Grafman’s model insists, more than Shallice’s, on the temporalization constraints inherent to valid script generation, a cognitive ability which inspired him to link script generation to frontal lobe activity, with no mention of an important role for the basal ganglia. Sequencing errors (and to a lesser extent perseveration and intrusion errors) in script generation tasks ought to be a hallmark of frontal lobe patients according to Grafman’s model, regardless of the type of script. Sirigu, Zalla, Pillon and Grafman (1995) had indeed observed that a group of prefrontally lesioned patients committed significantly more sequence errors than a group of patients with posterior lesions. Several investigations have tested Shallice’s and Grafman’s models empirically with patients bearing frontal lobe lesions (Godbout & Doyon, 1995; Karnath, Wallesch and Zimmermann, 1991; Le Gall, Aubin, Allain, & Emile, 1993; Shallice &
Burgess, 1991; Sirigu and colleagues, 1995, 1996, 1998; Zalla, Placiart, Pillon, Grafman & Sirigu, 2001; Zanini, Rumiati & Shallice, 2002). Frontal lobe patients have never been found deficient in the representation of script nodes per se, that is, they are able to enunciate the actions considered important to reach the goal. However, they exhibit poor sequencing of events, and have difficulty avoiding irrelevant associations, as well as properly weighting essential and nonessential elements. Brain imaging studies have confirmed an important role of the frontal lobes for script generation in normal participants (Crozier et al., 1999; Partiot, Grafman, Sadato, Flitman & Wild, 1996). In the study by Partiot and colleagues (1996), in which emotional and nonemotional action plans had to be imagined, the temporal lobes were activated, as well as the frontal lobes. There can now be little doubt that the frontal lobes play a key role in script generation. More specifically, it appears that it is the dorsolateral prefrontal cortex which most specifically contributes to script generation, whereas Broca’s area is really limited to organizing words in syntactic order (Sirigu, Cohen, et al. 1998). Shallice’s notion to the effect that script generation ought to be impaired in a special way in patients with lesions of the basal ganglia has been recently indirectly supported (Zalla et al. 1998; Godbout & Doyon, 2001). While the contribution of the frontal lobes to temporal organization (time lining) of mental representations has a long history and is well established both in the language domain (Sirigu et al., 1998) and in the planning of non-verbal actions sequences (see Goldman-Rakic, 1987), there have been few studies (but see Villa, Gainotti, de Bonis & Marra, 1988) designed to demonstrate that temporal organization of mental representation is dependent upon frontal lobe function more than non-temporal, say, spatial, organization of mental representations. Karnath, Wallesch & Zimmermann (1991) implemented a computerized visuospatial learning task which they administered to frontal lobe patients, patients with retrorolandic lesions (temporal and parietal lobes) and controls. The task required that participants navigate in a maze, discovering its structure gradually, so as to eventually represent the shortest trajectory from entry to exit. The task structure
SCRIPT GENERATION FOLLOWING FRONTAL AND PARIETAL LESIONS
was such that the first trial could be considered “novel” while the last could be considered “routine.” A subgroup of mediofrontally lesioned patients obtained the worst score overall, while lateral-frontal and retrorolandic lesions did not result in performances worse than control. In short, Grafman’s assumption of a preponderant and selective role of the frontal lobes in the temporal organization, more than the spatial, of complex action sequences seems quite plausible but still requires investigation. Potential Importance of the Parietal Lobes in Script Generation One of the early studies of frontal lobe involvement in script generation, that of Godbout and Doyon (1995), presented a surprising finding. A small group of parietally lesioned patients committed a significant number of sequencing errors on the script generation task. These authors reasoned that script generation tasks used in the cognitive literature and in the neuropsychological literature comprise varyingly demanding visuospatial representation. For example, the commonly used script prompt “going to a restaurant” involves a spatial frame: leaving one’s residence, navigating toward the restaurant, parking the car, selecting a table, and so on. The parietal lobes have, of course, long been known to heavily contribute to visuospatial processing (McFie, Piercy & Zangwill 1950; McFie & Zangwill, 1960; Warrington & James, 1967). Villa and colleagues (1988) reported a double dissociation of deficits as a function of parietal versus frontal lobe lesion location in 129 patients. The frontal patients were impaired on the “Temporal Rule Induction” (TRI) test and the parietal patients on Raven’s “Coloured Progressive Matrices” (CPM). The authors interpreted these deficits as temporal versus visuospatial processing deficits, respectively. Research on the parietal lobes has shown that they contribute significantly to the realization of simple and moderately complex arbitrary gestures and even gesture sequences, particularly of the limbs (c.f., apraxia) (Kolb & Milner, 1981). Godbout & Doyon (1995) speculated that the visuospatial demands of the script generation tasks could have been principally responsible for sequencing errors of the parietal lobe patients, whereas, the temporal dimensions
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could have been more selectively responsible for the sequencing errors of the frontal lobe patients. On the other hand, they proposed that the parietal lobe lesions could have impaired sequential aspects of script generation in a manner similar to frontal lobe lesions. Interestingly, Crozier and colleagues found, by means of a metabolic imaging investigation that the left angular gyrus of the parietal lobes was activated, as well as frontal lobe areas, during script generation. Any script generation task is not only a planning task (executive function) but necessarily, a complex movement representation task. Another label for a deficit of representation of complex movements is ideational apraxia. Ideational apraxia has traditionally been associated with parietal lesions (Ochipa, Rothi & Heilman, 1989; but see Buxbaum, Schwartz & Montgomery, 1998), particularly of the left hemisphere (Concha, 1987; De Renzi, Pieczuro & Vignolo, 1968), and consists of deficient representation of complex movement sequences in the absence of deficits of individual movements, or of tool use or instrumental action representation, that is, ideomotor apraxia. In a historical review of the term apraxia, Heilman, Rothi and Leslie (1997) state the following: Hugo Liepmann, at the beginning of the 20th century, was the 1st to perform systematic studies of limb apraxia. He described 3 forms of apraxia: limb kinetic, ideomotor, and ideational. Patients with limb kinetic apraxia are unable to make precise, independent finger movements. Ideomotor apraxia causes spatial and temporal errors even when performing with the hand that is ipsilateral to the hemispheric lesion. The term ideational apraxia was used to describe both sequencing and conceptual errors. However, currently the term is used to denote the inability of patients to perform a series of acts leading to a goal and the term conceptual apraxia is used to denote the disorder characterized by content errors, a loss of tool-object associative knowledge, and other forms of mechanical knowledge. p. 16.
In short, ideational apraxia, possibly of parietal origin, could express itself in the form of a deficit in the verbal representation of action sequences leading to a goal, that is, of script generation. Rumiati, Zanini, Vorano and Shallice (2001) exhaustively investigated two ideomotor and ideational apraxics with aphasia who had sustained a parietal lesion
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and one frontal lobe patient with dysexecutive syndrome but no apraxia. One of their tasks consisted of putting in proper sequence 4-5 written words to form a script. The parietal apraxics made sequence errors within the normal range whereas the frontal patient made a significant number of sequencing errors. On the other hand, the apraxic patients were impaired in generating actions but not in sequencing abstract elements (nonactions) whereas the frontal patient was able to generate actions. This and performance on other tasks led the authors to conclude that the parietal patients had an impairment of the contention scheduler (CS) while the frontal patient had an impaired supervisory attentional system (SAS). Finally, it is possible that the frontal lobes are more specialized than the parietal for any type of highly effortful complex task engaging working memory (see Baddeley, 1986) and that the impairment of the very small cohort of parietal patients in the Godbout and Doyon study was just an artefact. Objectives of the Present Investigation and Experimental Hypotheses This article presents an investigation of temporally versus visuospatially charged judgments and similarly laden scripts which patients with frontal or parietal lobe lesions attempted to generate. Because Shallice proposed a distinction between a frontal lobe SAS and a basal ganglia CS, this investigation was designed to distinguish performance on novel script generation (controlled processing, i.e., high demands on working memory) and on a more routine form of generation of scripts (automatic processing, i.e., low demands on working memory). Novel scripts were defined as scripts where the normal sequence of actions is reversed. It must be said that though our controlled processing condition is certainly “novel” for the subjects (nobody mentally inverses >10 segment plans in their minds in daily life), it does not call upon novel scripts per se. It simply adds working memory demands on the mental operation in the same way backwards digit span adds working memory demands on the more routine or everyday digit span operation. It is not feasable to compare novel scripts to routine scripts per se: if a script were to be novel, then it would be unfamiliar to the subject and then the semantic network
underlying it would necessarily be patchy and its scoring (see methods sections) would become very tedious if not impossible. In short, specific support for Grafman’s model would accrue from a GROUP main effect, the frontally lesioned patients manifesting more errors than the other groups. Grafman’s model would also receive specific support from a GROUP x TEMPORAL/SPATIAL interaction, with the frontal patients making the most errors on the temporally laden scripts. Specific support for the Shallice (1983, 1988) account of script generation would follow from a GROUP x FORWARD/BACKWARD interaction, wherein the frontally lesioned subjects would make significantly more errors than the two other groups (see the Method section for details).
METHOD Subjects It is extremely difficult to recruit patients with focal lesions limited to a frontal lobe, and even more so to a parietal lobe. Cerebrovascular accident (CVA) territory rarely limits itself to such areas. Most researchers having compared groups of parietal to frontal patients have thus used wartime cases of penetrating injury (Warrington, James & Maciejewski, 1986) or tumor patients (Arseni, Voinesco & Goldenberg, 1958). If the objective includes comparing groups of lesioned patients, it is imperative that the etiology be comparable because etiologies carry very dramatic associations with them. Malignant tumor cases are progressive and CVAs are eventually static; however, benign tumors can grow slowly enough for cognitive function to reorganize in intact tissue, even in adults; infarcts carry fewer complications than hemorrhages, and so on. The sample of the present study consisted of 11 patients with a magnetic resonance image determined frontal lesion (excluding the basal ganglia and Broca’s area) and 12 normal comparison participants on the one hand, and 9 patients with a similarly confirmed and circumscribed parietal lesion (excluding the basal ganglia) and 9 normal comparison participants. The most accessible etiology for the targeted lesion sites was tumor. However, en route, it became obvious that a few nontumor cases with parietal lesions had to be recruited to form a reasonably sized group. Participation was voluntary and unpaid and was preceded by the signing of a consent form. The patients were selected from archives of the Centre Hospitalier Régional (Pavillon Ste-Marie) in Trois-Rivières, the Centre Hospitalier Affilié Universitaire
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(Pavillon Enfant-Jésus), and the Institut de Réadaptation en Déficience Physique, both located in Québec city. Patients with any clinical evidence of apraxia or aphasia in their files were excluded. The normal participants were recruited in Quebec city and were matched with the patients for age, gender and education. Participants with a prior psychiatric history or substance abuse were excluded. No subject was aphasic. All participants were right handed except one frontal subject. For further clinical description of these patients see Table 1. All the normal participants were right handed, and none had a neurological history. Frequencies of each
gender were identical in each group. Demographic details of both groups are presented in Table 2.
Procedure Socio-Demographic and Medical Questionnaires Participants completed questionnaires (Godbout, 1994) designed to identify the participants for matching purposes, determine handedness and apply inclusion and exclusion criteria.
Table 1. Clinical Characteristics of the Patients Age (years)
Education (years)
Gender
33 25 47 31 29 41 36 18 59 47 68
18 16 17 14 11 11 14 12 19 18 13
F F F F F M F M M F M
30 57 59 35 55 30 32 58
10 11 8 17 12 11 19 5
M F M M F F M F
32
10
F
Hemisphere lesioned
Etiology
Interval between onset and testing (months)
Patients with frontal lobe lesions Left Glioblastoma Left Glioblastoma Left Parasagittal meningioma Left Oligodendroglioma Left Glioma Left Glioma Left Astrocytoma Right Glioma Right Glioblastoma Right Astrocytoma Right Mengioma
16 6 25 3 16 12 26 17 11 22 73
Patients with parietal lesions Left Head injury Left Emboly Left CVA Left Astrocytoma Left Meningioma Left Astrocytoma Left Glioma Right Meningioma with a local bleed Right Astrocytoma
23 24 24 30 24 16 14 19 40
Table 2. Demographic and Biographic Characteristics of the Participants. Gender
Age (years)
Education (years)
Information Scale score (WAIS-R)
Group
M
F
Mean
SD
Mean
SD
Mean
SD
Frontal Control
4 4
7 8
39.45 41.00
14.89 12.67
14.82 13.00
2.93 3.36
9.23 9.85
3.44 2.01
Parietal Control
4 4
5 5
43.11 43.11
13.53 12.75
11.44 11.67
4.28 3.00
8.22 9.33
2.91 2.24
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As script generation tasks draw upon semantic memory (Rathus, 1995) as well as executive function, and since it was the latter that this project aimed at, two procedures were used to assess various types of knowledge.
Assessment of General Knowledge General knowledge was assessed using the Information Subtest of the Wechsler Adult Intelligence Scale – Revised. The metric analyzed and presented in this report is the scale score (normal population mean = 10).
Assessment of Knowledge of Scripts A questionnaire taken from Godbout (1994) assessed knowledge of 16 scripts: going to the cinema, going to a wedding, going to a doctor’s office, going to a restaurant, shopping for groceries, going to the hairdresser, going to a swimming pool, going to the beach, taking a train, writing a letter, taking an aircraft flight, washing one’s hair, washing the family car, taking a photograph, getting a sun tan and attending an evening course (see Galambos, 1983). Each script was rated on the following 3-point scale: 1 = very familiar with the activity; 2 = moderately familiar; 3 = not familiar. These particular scripts were chosen because reliability ratings and norms for a francophone population are available (see Corson, 1990). Activities equally familiar to all groups were retained for the subsequent experimental phase of the study. The difference between groups was not significant.
The Script Generation Tasks Participants were required to generate 16 scripts using a method similar to Bower, Black and Turner (1979), Godbout (1994) and Light and Anderson (1983). The instruction was: List 10 to 20 actions generally carried out in a particular activity and do so in chronological order. In order to test Shallice’s notion to the effect of a frontal SAS (representation of novel action chains) and a nonfrontal CS (representation of routine action chains), a procedure was introduced wherein routine scripts were made nonroutine by requiring that they be generated backward - thus purportedly solliciting the SAS, while others were left routine by requiring that they be recited in forward order - thus purportedly solliciting the CS. A quarter of the scripts (N = 4) had to be generated in forward order and were spatially laden, a quarter (N = 4) had to be generated in backward order and were spatially laden, a quarter (N = 4) were to be generated in forward order and were temporally laden (i.e, low in spatial demands) and a quarter (N = 4) were to be generated in backward order and were temporally laden. During the experimentation, participants were to answer verbally, but were informed that they could request repetition of the instructions at will. There was no time limit. All the participants’ verbalizations were
noted in writing as well as magnetically recorded for future verifications. Scripts judged to contain relatively high « spatial » and low « temporal » demands included, in the forward condition: going to the doctor, going to the restaurant, going to a marriage, going to the cinema, and in the backward condition, buying the groceries, writing a letter, going to the swimming pool, and going to the hairdresser for a haircut. Scripts judged to contain relatively high « temporal » and low « spatial » demands included, in the forward condition : taking a photograph, getting a sun tan, grilling a steak on the BBQ, washing the clothes, and in the backward condition : cashing a check, washing the dishes, eating at the restaurant and washing one’s hair. The selection of these scripts, as spatial or temporal, was based on a pilot study involving judgements by 32 normal participants with a criterion of .8 inter-judge agreement minimum. See Table 3 for examples of a spatially laden and of a temporally laden script. The classification of scripts into a forced choice category of spatial versus temporal was significant for each of the scripts selected (p < .05). Performance on the script tasks was measured by means of three types of errors : sequence errors, irrelevant intrusions and perseverations as in Bower et al, (1979), Godbout (1994; Godbout & Doyon, 1995) and Roman, Brownell, Potter, Seibolk and Gardner (1987). A sequence error consists of improper sequencing of actions. An irrelevant intrusion is an activity which does not fit in the script (as judged from previous research and normative data (Bower et al., 1979, Godbout, 1994, and Roman et al., 1987). A perseverative error is an action repeated more than once within a script. A validity check on 30% of these scores was subjected to a test of inter-judge reliability. The spatial and temporal organization tasks and script tasks were presented in a freshly randomized order to each subject. There was no time constraint on any of these tasks. Because women are known to outperform men on verbal fluency tasks (Loonstra, Tarlow & Sellers, 2001), and since this at least remotely resembles script generation, GENDER was included in all parametric inference tests, unless otherwise specified.
RESULTS Total Number of Actions A 2 x 2 x 3 x 2 repeated measures analysis of covariance was carried out comparing forward and backward script conditions (the FORWARD/ BACKWARD factor), the spatial and temporal script conditions (the SPATIAL/TEMPORAL factor)
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Table 3. Scripts Presented as Examples to the Participants in Each of Four Conditions. Spatial Forward condition
Spatial Backward condition
Temporal Forward condition
Temporal Backward condition
Getting up in the morning
Getting up in the morning
Paying one’s way at the cinema
Paying one’s way at the cinema
-Leaving -Locking the door -Putting on one’s coat -Preparing one’s things -Clearing the table -Brushing one’s teeth -Dressing -Having breakfast -Grooming -Going to the bathroom -Getting up -Turning the alarm off -Hearing the alarm
-Waiting in line -Taking one’s wallet -Opening one’s wallet -Taking out money -Giving the money to the attendant -Waiting for the attendant to hand back the change -Putting the change in a pocket -Putting away the wallet -Getting the ticket -Thanking the attendant -Giving the ticket to the doorman -Entering the cinema
-Giving the ticket to the doorman -Thanking the attendant -Getting the ticket -Putting away the wallet -Putting the change in a pocket -Waiting for the attendant to hand back the change -Giving the money to the attendant -Taking out money -Opening one’s wallet -Taking one’s wallet -Waiting in line
-Hearing the alarm -Turning the alarm off -Getting up -Going to the bathroom -Grooming -Having breakfast -Dressing -Brushing one’s teeth -Clearing the table -Preparing one’s things -Putting on one’s coat -Locking the door -Leaving
and comparing the normal participants to the parietal patients and to the frontal patients (the GROUP factor) as well as gender (GENDER factor). Age, education and the Information subtest of the WAIS were covariables, the influence of which was removed from the design. The total number of actions was the dependent variable. The GROUP main effect was the only significant effect (F(2, 34) = 4.84, p < .015) - the frontal patients always producing the fewest actions, followed by the normal participants, followed by the parietal patients, regardless of the type of action (adjusted means : 41.44, 49.96, 53.96 respectively, see
Table 4 for unadjusted data). More specifically, adjusted post hoc tests (LSMEANS procedure) revealed that in the FORWARD/SPATIAL condition the frontal patients generated significantly fewer actions than the parietal patients (p < .03). In the BACKWARD/SPATIAL condition the same contrast reached significance (p < .043) and the frontal patients generated significantly fewer actions than the normal comparison group as well (p < .034). In the FORWARD/TEMPORAL condition, the frontal patients generated significantly fewer actions than the parietal patients (p < .034) and than the normal comparison group (p < .012).
Table 4. Mean Number of Actions Generated (and SD) per Script as a Function of the Type of Script and Group. Conditions Spatial forward
Spatial backward
Temporal forward
Temporal backward
M
SD
M
SD
M
SD
M
SD
Group Frontal Control
14.3 14.1
4.3 2.6
11.0 12.4
2.5 3.3
10.5 12.2
2.2 2.8
9.8 11.7
1.8 2.2
Parietal Control
14.5 13.6
3.6 2.6
12.1 12.4
3.2 3.8
11.8 11.8
2.9 3.2
11.7 11.3
2.8 2.5
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Finally, in the BACKWARD/TEMPORAL condition, the frontal patients generated significantly fewer actions than the parietal patients (p < .012) and than the normals (p < .024). No other contrasts were significant. Removal of GENDER from the design had no effect on the list of significant versus nonsignificant effects. See Table 4. Any comparison of the groups could conceivably have been influenced by two variables which apply only to patients, namely the hemisphere lesioned (HEMISPHERE factor), the interval of time between the brain disease or injury and testing (INTERVAL factor) and the etiology of the lesion (tumor versus other etiology: ETIOLOGY factor). See Table 1. We compared the two patient groups with the same statistical model as above, but with the HEMISPHERE, INTERVAL and ETIOLOGY factors included as additional covariates. The significant GROUP factor (F(1, 11) = 9.3, p < .012) indicated that the frontal patients generated fewer actions than the parietal patients despite statistical control for age, education, Information (WAIS-R), hemisphere damaged, interval since lesion onset, gender and etiology. Adjusted post hoc tests (LSMEANS procedure) indicated that it was in the FORWARD/SPATIAL (p < .021), the FORWARD/TEMPORAL (p < .037) and the BACKWARD/TEMPORAL (p < .034) conditions that this group difference reached significance. No other main effects or interactions involving the GROUP factor reached significance. The previous analysis was carried out again, but without any of the covariables, and the same pattern of results emerged, indicating that regardless of the manner of approach, in this investigation, the frontal patients generated significantly fewer actions than the other groups. Nonparametric Analysis of Errors For these analyses, a subgroup of the normal subjects, best matched for the frontally lesioned group was selected (N = 12), as well as another subgroup (N = 9), composed of entirely different subjects, likewise selected to create an optimal comparison group for the parietally lesioned patients. Differences between the frontal group and its normal comparison group did not reach significance for age [t (21) = 0.79, n.s.], education [t (21) = 0.18, n.s.] or the Information sub-test of
the WAIS-R [t (21) = 0.69, n.s.]. Likewise, there were no statistically significant differences between the parietal group and its normal comparison group with regard to age [t (18) = 0.00, n.s.], education [t (18) = 0.13, n.s.] or the Information sub-test of the WAIS-R [t (18) = 0.91, n.s.]. Inter-judge agreement was perfect for two error types (sequence errors, and perseverative errors). The agreement was 98% for irrelevant intrusions. There were many normal participants who presented no errors at all as well as some patients (see Table 5). Some patients presented several errors in a specific category. Each clinical group was therefore compared to its own normal comparison group with a nonparametric statistic, Fisher’s Exact Test, as in Godbout & Doyon (1995). Analyses were always of the frequencies of participants in each group manifesting or not a given type of error. Forward Recital of Spatially Laden Scripts The difference between the frontal group and its normal comparison group did not reach significance for sequence errors or irrelevant intrusions and there were no perseverative errors at all. However, a greater proportion of parietal patients (8/9) than their normal comparison group (0/9) produced sequence errors, p = .0004. These latter two groups were comparable with regard to irrelevant intrusions. There were no perseverative errors on this task for either group (see Table 5). Backward Recital of Spatially Laden Scripts In this condition, the frontal patients committed significantly more sequence errors (8/11) than their normal comparison group (2/12) (p = 0.01). There were no group effects for perseverative errors or irrelevant intrusions. With regard to the parietal patients, a higher proportion of patients produced sequence errors (9/9) than of their normal comparison group (1/9), p = .0004. This was not the case for irrelevant intrusions or perseverations (see Table 5). Forward Recital of Temporally Laden Scripts The frontal patients presented significantly more perseverative errors (4/11) than their normal comparison group (0/12) (p = .04). These groups
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Table 5. Numbers of Cases Commiting at Least One Sequence, Perseveration or Intrusion Error. Spatial forward
Spatial backward
Temporal forward
Temporal backward
Sequence Perseveration Intrusion
3/11 0/11 3/11
Group with frontal lesions 8/11* 3/11 1/11
3/11 4/11* 0/11
7/11* 4/11* 1/11
Sequence Perseveration Intrusion
Normal comparison group for frontal patients 1/12 2/12 1/12 0/12 0/12 0/12 0/12 0/12 0/12
1/12 0/12 0/12
Sequence Perseveration Intrusion
8/9* 0/9 1/9
Group with parietal lesions 9/9* 3/9 3/9
9/9* 2/9 3/9
Sequence Perseveration Intrusion
Normal comparison group for parietal patients 0/9 1/9 1/9 0/9 0/9 0/9 1/9 0/9 0/9
8/9* 1/9 0/9
1/9 0/9 0/9
Note. * < .05, inference tests compare each patient group with its respective normal comparison group.
did not differ with regard to sequence errors or irrelevant intrusions. A greater proportion of parietal patients (8/9) produced sequencing errors, compared to their normal comparison group (1/9), p = .003. There were no irrelevant intrusions and the two groups were comparable on perseverative errors (see Table 5). Backward Recital of Temporally Laden Scripts The frontal patients made more sequence errors (7/11) than their normal comparison group (1/11) (p = 0.01) and more perseverative errors (4/11 vesus 0/12) (p = 0.04). Irrelevant intrusions did not significantly differentiate these groups. As for the parietal patients, significantly more participants in the parietal group made sequence errors (9/9) compared to their normal comparison group (1/9), p = .0004. However, these two groups were comparable with regard to irrelevant intrusions and perseverative errors (see Table 5). Parametric Analyses of Errors It was decided to seek the benefits of parametric analyses of errors despite failure to meet all the postulates of analysis of variance, but with a statistical model as conservative and stringent as possible. To this end several covariates were
included, and error types were pooled into larger categories to minimize the obvious ceilng effect present in the normal participants (see Tables 5 and 6). Advantages of this approach were 1) statistical control of shortcomings of matching, particularly on the Information subtest of the WAIS-R, 2) the possibility of comparing the frontal and parietal patients directly, with post hoc tests, 3) the possibility of testing effects of proportions of errors over actions (precluding the eventuality of group differences in errors being an artefact of the rate of production of actions), and 4) the possibility of taking into account potential effects of gender. The best distribution of error scores in terms of normality, equality of variances, ceiling effects, and so on was the total error proportion. A 3 x 2 analysis of covariance was therefore carried out on total errors/total actions comparing the normals, parietal patients and frontal patients (GROUP factor) and the genders (GENDER factor) with age, education and the information subtest of the WAIS-R as covariates. The corresponding data (prior to adjustment by covariates) are presented as percentages in Table 6. The GROUP factor was the only significant effect (F(2, 34) = 9.7, p < .003) with the parietal patients presenting the greatest proportion of errors,
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followed by the frontal patients and then the normal participants. Adjusted post hoc tests (LSMEANS procedure) revealed that the parietal patients made significantly more errors than did the normal participants (p < .002), and that the frontal patients made significantly more errors than did the normal participants (p < .03). The difference between the frontal and parietal patients was not significant. Removal of GENDER from the design had no effect on the list of significant versus nonsignificant effects. Intrigued by this unexpected finding, and therefore suspicious of it, we proceeded to determine whether this effect could be broken down into an effect of working memory (the forward versus backward conditions) and/or of spatial versus temporal demands of the scripts. Analysis of variance is robust with regard to violation of the postulate of normality (Peres-Neto & Olden, 2001). The reader is nevertheless cautioned that several postulates of analysis of variance are not respected by the distributions under consideration here. A 2 x 2 x 3 x 2 repeated measures analysis of covariance was carried out comparing forward and backward script conditions (the FORWARD/ BACKWARD factor), the spatial and temporal script conditions (the SPATIAL/TEMPORAL factor) and comparing the normal participants to the parietal patients and to the frontal patients (the GROUP factor) as well as the genders (GENDER factor). Age, education and the Information subtest of the WAIS were covariables, the influence of which was removed from the design. The dependent measure was thus the sum of perseverative, sequence and intrusion errors/actions in each of the four within factor levels/total actions. The GROUP effect presented the same pattern as above, with the post hoc tests revealing significantly more errors in the parietal (LSMEASN test : p < .002) and frontal (LSMEANS test : p < .03) than the normal comparison group, but no difference between the two patient groups (adjusted means : 16.09, 10.35 and 0.38, respectively). The FORWARD/BACKWARD main effect reached significance (F(1, 37) = 8.9, p < .006), more errors occurring in the backward condition. More interestingly, the FORWARD/BACKWARD factor interacted significantly with the GROUP factor (F(2, 37) = 4.1, p < .025). Adjusted post hoc
tests (LSMEANS) revealed the following : The parietal patients made significantly more errors than the normal participants in the FORWARDSPATIAL condition (p < .0002) but the frontal patients did not. The frontal patients made significantly more errors than the normal participants in the FORWARD-TEMPORAL condition (p < .037) but the parietal patients did not. The parietal patients made significantly more errors in the BACKWARD-SPATIAL condition (p < .003), but the frontal patients did not. The parietal patients made significantly more errors in the BACKWARD-TEMPORAL condition than the normal participants (p < .002), but the frontal patients did not. Finally, the parietal patients made significantly more errors than the frontal patients (p < .008) in the FORWARD-SPATIAL condition and this was the only condition where the parietal patients differed significantly from the frontal patients. Removal of GENDER from the design had no effect on the list of significant versus nonsignificant effects. The two previous analyses were carried out again, but without the covariables, and on error sums instead of proportions, and the same pattern of results emerged, indicating that regardless of the manner of approach, in this investigation, though both patient groups had significant error rates the parietal patients made more errors than the frontal patients overall, with or without GENDER in the design. Here, as in the first part of the results section, any comparison of the groups could conceivably have been influenced by three variables which apply only to patients, namely the hemisphere lesioned (HEMISPHERE factor), the interval of time between the brain disease or injury and testing (INTERVAL factor) and the etiology (tumor versus other etiology: ETIOLOGY factor). For the same reasons as previously, we compared the two patient groups (only) with the same model as above, but with the HEMISPHERE, INTERVAL and ETIOLOGY factors included as additional covariates. This represents a very costly design in degrees of freedom for such small samples, but we found the results enlightening. The GROUP effect was short of significance as were all interactions involving the GROUP factor. Detailed manipulation of the design led us to realize that
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Table 6. Percentages of Errors (All Types Summed*) Over Actions (Errors/Actions x 100) and SDs as a Function of Experimental Condition and Group. Average per script
Spatial forward
Spatial backward
Temporal forward
Temporal backward
Error %
Group with frontal lesions (n = 11) 1.2 (1.7) 4.2 (6.6) 12.9 (25.1)
13.2 (24.3)
Error %
Group with parietal lesions (n = 9) 3.1 (2.5) 3.4 (4.4) 37 (64.8)
31 (42.1)
Error %
Normal comparison group (n = 21) .25 (0.8) .25 (2,4)
.19 (0.6)
.22 (0.7)
Note. The values are not corrected for covariables. * = sequence, perseverative and intrusion errors
this was due to the fact that the three parietal patients with a nontumorous etiology presented a higher proportion of errors (18.59%) than the other parietal patients (15.63%) after correction for all the covariables mentioned above (F(1, 8) = 1.8, p < .4). Though not significant in itself, this effect, combined with all the others, was sufficient to adjust the parietal patients’ error proportion (adjusted estimate: 17.36%) to a level similar to that of the frontal patients (16.85%). The other covariables (AGE, EDUCATION, INFORMATIONWAISR, HEMISPHERE, INTERVAL) together did not wipe out the GROUP effect, that is, the parietal patients presented a higher proportion of errors than did the frontal patients. Removing GENDER from the design also did not change the result pattern. Envisaged in another manner, all effects involving the GROUP factor were wiped out even when the sole covariable was ETIOLOGY. No other covariable had this effect. This will come as no surprise to neuropsychologists: it is commonly known that because of the gradual development of their condition tumor patients tend to present milder deficits than CVA or head trauma patients.
DISCUSSION Productivity and Error Patterns of the Frontal Lobe Patients on the Script Tasks The findings of the present investigation support previous research to the effect that frontal lobe patients are capable of generating a sufficient number of actions to form a script (Godbout &
Doyon, 1995; Sirigu, Zalla, Pillon, Grafman, Agid & Dubois 1995). However, the findings show, with a larger subject sample than the above cited precursor studies, that frontal patients can be significantly frugal in their generation of actions -- not only in comparison to the normal comparison group, but even to the group of parietal patients. This cannot be brashly assimilated to an impoverishment of mental content, of creativity, or of planning on the script tasks, though this would be a tempting speculation. Recall that the participants were not required to generate more than 10 actions per script (max: 20) -- a task requirement which was basically met by the frontal patients (the normal participants and parietal patients simply generated more actions than required). Judgment must therefore be suspended on this issue until it is demonstrated that frontal patients are unable to generate as many actions as other patients or controls, and do not simply just prefer to generate fewer. On the other hand, the frontal patients of this investigation, as in the studies just cited, organized the elements of their scripts differently from the normal comparison participants. More of the former made sequence errors than their normal comparison group in backward recital of scripts, regardless of their spatial or temporal nature. More frontal patients made perseverative errors on the temporally demanding scripts than on the spatially demanding scripts, relative to their normal comparison group. This difference was clear but not overwhelming. It would be an overstatement and even an obvious mistake to claim, on the
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basis of these results, that the frontal lobe contribution to script generation is limited to the temporal domain. Perseverations were discriminative in this investigation, and should therefore not be overlooked in future investigations of script generation in brain damaged patients. We do not attach any specific meaning to perseverative errors other than the implication from their presence that working memory is overtaxed. However, when working memory is overtaxed, perseverations are just one among many types of errors which are known to occur. Furthermore, as has clearly been shown in aphasiology, any group of brain damaged patients will perseverate when it reaches its range of impairment on any cognitive task (Buckingham, Whitaker & Whitaker, 1981). In short, though important, perseverative errors on script generation tasks have not yet been demonstrated to be in any way pathognomonic of frontal lobe lesions. On the other hand, there may be a weak link between perseverations and frontal lobe contribution to script generation in this study: indeed, perseverations were observed to appear significantly in the frontal patients only on script conditions making relatively heavier demands on temporal processing rather than spatial.
Grafman’s Model of Script Generation The parietal patients made more sequence errors than did the frontal patients (ns) -- a trend in the direction opposite to Grafman’s model, and the frontal patients were not relatively more affected than the other groups on the temporally laden scripts, contrary to what Grafman’s model might have predicted. We propose that Grafman may have placed too much emphasis on the timing and sequentialization contribution of the frontal lobes to script generation, to the detriment of ecological validity: real organized action sequences in everyday life occur in a space-time continuum, both axes of which draw heavily upon working memory and thereby on the frontal lobes. At most, it can be said that there may exist a “preponderance” of frontal contribution to time domain processing in script generation, although this remains to be demonstrated. So rather than supporting Grafman’s (1989) model of frontal lobe contribution to script generation, these findings suggest that any neuropsychological model of script generation should consider the existence of a “space-processing component” in the frontal lobes on the one hand and a parietal lobe contribution to both temporal and spatial processing demands of script generation on the other.
Productivity and Error Patterns of the Parietal Lobe Patients on the Script Tasks The most interesting finding of the present study concerning the parietal patients was that they made at least as many errors as the frontal patients, before and after correction for matching variables, and before and after correction for number of actions enunciated, and they presented significantly more errors than the normal comparison group. They were significantly impaired on the script generation tasks with regard to sequence errors, regardless of whether the scripts were spatially or temporally laden. On the other hand, these patients were comparable to their normal comparison group with regard to irrelevant intrusions or perseverative errors. Recall that their self rated knowledge of the scripts themselves was comparable to the normal comparison group and that they generated scripts comprising plenty of actions.
The Supervisory Attentional System (SAS) and the Contention Scheduler (CS) What might the results obtained here tell us about brain systems underlying Shallice’s (1982, 1988) constructs of SAS and CS? The supervisory attentional system (SAS), according to Shallice, is supposed to deal primarily with non-routine script generation (operationalized in the present investigation as the backward recitation condition) and is proposed by him to lodge in the frontal cortex. The contention scheduler (CS) on the other hand, according to Shallice, is supposed to handle routine script generation (the highly overlearned scripts of the forward conditions of the present investigation) and has been proposed by him to lodge in the basal ganglia. Recall that more than twice as many frontally lesioned patients made sequence errors in the backward (8/11, 7/11) than forward conditions (3/11, 3/11) suggesting that these patients had a rather specific impairment of the SAS, far worse than their impairment, if any,
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of the CS. Note that a similar profile was not observed in the parietally lesioned cohort. The parametric analyses of the present investigation failed however to yield all the critical interactions in support of this interpretation. Indeed only one GROUP x FORWARD/BACKWARD interaction emerged out of several designs, and post hoc tests did not show frontal patients to be any more deficient in the BACKWARD condition as would have been expected form Shallice’s model (see Zanini et al., 2002, for a similar failure to distinguish the SAS and CS). Of course, in either case this could just as well be due to failure to design a specific enough operationalization of the SAS versus the CS (genesis of a novel script would necessarily be an act of creation -- thus introducing a confound). At any rate, the suggestion by Rumiati et al. (2001) to the effect that the parietal lobes contribute to the CS and not the SAS finds no support in the present investigation, leading us to suspect that though ideomotor/ideational apraxics may have a specific CS impairment (as in Rumiati et al.’s two cases), nonaphasic and nonapraxic parietal patients are probably affected as much at the level of the SAS as the CS. Methodological Issues Our failure to support Grafman’s theoretical model of script generation, and the weak support we were able to muster for Shallice’s model could be a result as much of weaknesses of our method as of the theories under consideration. The samples were small. Patient groups were not perfectly matched for etiology, though they were well matched on several other criteria such as gender, age, education and post lesion onset. The sizes of the lesions were not quantified, as is usually the case in studies recruiting patients from hospital records. A neuropsychological work-up of the patients would have helped de-mystify some of the marked variability of performance on the script tasks. A battery of tests of apraxia and aphasia would have helped resolve issues of the sources of errors in the patients. There were four blocks of four scripts each in this investigation: FORWARD/SPATIAL, FORWARD/TEMPORAL, BACKWARD/SPATIAL and BACKWARD/ TEMPORAL. The scripts should have been presented in counter-balanced order within and across
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these categories, an oversight on our part. Errors were not normally distributed and there were important ceiling effects. Covariance analysis controlled for some of these problems, but at great cost in degrees of freedom, and these statistical corrections may have distorted several of the variance patterns (adjusted means fluctuated wildly). However, we remain assured of one basic finding: that parietal patients presented as great a deficiency in script generation as did the frontal patients, confirming the same early and tentative observation made by Godbout and Doyon in 1995. Ideational Apraxia Could our parietal patient’s impairment profile be suggestive of clincically undetected ideational apraxia? As stated in the introduction, ideational apraxia has been linked, though this has been disputed, to lesions of the left parietal lobe. Obviously, the parietal patients of the present investigation did not resemble the two ideomotorideational apraxics described by Rumiati et al. (2001). Their parietal apraxics made sequence errors within the normal range whereas the frontal patient made a significant number of sequencing errors. On the other hand, the apraxic patients were impaired in generating actions but not in sequencing abstract elements (nonactions) whereas the frontal patient was able to generate actions. Our result pattern is exactly the contrary. We feared, at first glance of the results, that the slightly higher proportion of left hemisphere cases in the parietal cohort of the present investigation than in the frontal cohort, may have contributed to the high rates of sequence errors observed in the former cohort. This would be compatible with the findings of Crozier and colleagues (1999) who found left parietal activation during script generation in normals. Because ideational apraxia has been linked to the left parietal lobe, particularly for sequencing of real actions (Rushworth, Nixon, Wade, Renowden & Passingham, 1998), it will be useful to test more unilaterally lesioned parietal patients so as to determine whether there is a hemisphere effect in the impairment on mental script generation tasks. Our prediction would be that contrary to the frontal lobe contribution, which we think is bilateral, the parietal lobe
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contribution ought to be clearly more left hemisphere based. At the same time, an exhaustive investigation of the various praxias, ideomotor and ideational, should be carried out with sophisticated tests (see Lucchelli, Lopez, Faglioni & Boller, 1993, for an example of an appropriate such battery of tests) in the next investigations of script generation. More case studies of script generation in patients affected by ideomotor apraxia or ideational apraxia would be enlightening, especially with patients devoid of aphasia, making a script generation task plausible. Ideational apraxics should be impaired on at least some aspects of script generation tasks and not ideomotor apraxics. Finally, it would surely be possible to devise script generation tasks which recruit, more selectively, spatial representation versus temporal representation : we opted for a strategy of using well known scripts from an existing data base, but new script tasks should be devised for this purpose. Tests of the GROUP x HEMISPHERE effect never reached significance in the present study, and the nonsignificant trend was, to our surprise, that the parietal patients with right hemisphere lesions made significantly more errors than did the parietal patients with left hemisphere lesions. Furthermore, the right hemisphere damaged patients (regardless of lobe damaged) committed significantly more errors on the script tasks than did the left hemisphere damaged patients, -- a finding which we hesitate to attempt to explain otherwise than as a small sample bias (the effect could be related to lesion size which was unfortunately not known in this investigation). Considerations for Future Research Future research on spatial aspects of script generation should perhaps distinguish egocentric space or time frames from allocentric space or time frames. We have in mind close-to-the body contexts as egocentric spatial contexts, and far-from-the-body as allocentric spatial contexts, and close-to-thepresent contexts as egocentric time contexts, and far-from-the-present contexts as allocentric time contexts. Similar distinctions have been found to dissociate in the neuropsychology of praxias, with egocentric representation being relatively more frontal lobe dependent and allocentric representation being more parietal lobe dependent (Semmes,
Weinstein, Ghent & Teuber, 1963). Imitation of meaningless action sequences has been found to dissociate in the following manner: buccofacial praxias (perhaps relatively more related to egocentric space) have been found to be more frontal lobe dependent and limb praxias (perhaps relatively more related to allocentric space) have been found to be more parietal lobe dependent (Kolb & Milner, 1981). We would predict that on script generation tasks, patients with parietal lobe lesions ought to manifest relatively more deficits in allocentric contexts than frontally lesioned patients who should manifest relatively more deficits in egocentric contexts. The various teams of researchers, whether associated with Sirigu, or with Shallice, or Godbout, are currently heavily involved in exploring the neuropsychology of scripts in activities of daily living (ADL). Zalla and colleagues (2002) found that providing a more concrete context (a videogame type of environment) seemed to markedly reduce rates of sequencing errors of frontal lobe patients on a script generation task. However, Fortin, Godbout & Braun (2003) found that an even more concrete context (quickly preparing a meal in a kitchen) drew relatively more significant numbers of sequencing errors in frontal lobe patients -- probably because this was a heavily multi-task situation under time pressure. A study comparing parietal and frontal patients in various ADL implementations of script tasks now needs to be carried out. Conclusion Despite the methodological limitations of the present investigation, we propose that there exists a complementary interaction between the frontal and parietal lobes in script generation, and that pending further research, script generation should not be considered to be a selectively “frontal lobe” construct.
ACKNOWLEDGMENTS This research was partially made possible by grants to the first and fourth authors from the Fonds de Recherche en Santé du Québec (Quebec government) and internal funding from the Université du Québec à Trois Rivières
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and the Université du Québec à Montréal to the first and fourth authors, respectively
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