virtual planning in patients with frontal lobe lesions

VIRTUAL PLANNING IN PATIENTS WITH FRONTAL LOBE LESIONS

Eliane C. Miotto1 and Robin G. Morris2

(1Department of Psychology, Institute of Psychiatry, London, U.K.; 2NeuropsychologyUnit, Institute of Psychiatry, London, U.K.)

ABSTRACT

The VIrtual Planning Test (VIP) was developed to investigate the planning andorganisational abilities of 25 patients with frontal lobe neurosurgical lesions, comparingtheir performance with 25 matched control subjects. The task, presented in the form of aboard game, simulates planning and execution of a set of target activities that have to takeplace over a four day period, involving those that are either preparatory for a fictional “trip”abroad, or those that relate to the subject’s current environment (context). The frontal lobepatients were impaired overall, tending to select inappropriate activities associated withtheir current context and showing greater impairment on subtasks requiring only one, ratherthan two, preparatory acts. The findings are discussed in terms of the validity of the VIPtest in identifying executive functioning impairment and the degree to which the pattern ofdeficits are consistent with neuropsychological models of executive function.

Key words: planning, frontal lobe, executive functions

INTRODUCTION

The association between damage to the prefrontal cortex and difficulties inplanning has been known about for a long time (Luria, 1966). Despite theapparently normal intellectual functioning, patients with significant frontal lobedamage are impaired in their ability to regulate everyday functioning in anordered fashion. For example, Goldstein, Bernard, Fenwick et al. (1993)described a 51 year old patient who had undergone a left frontal lobectomy forthe removal of a tumour. Despite being an ex-senior manager, he showed thetypical features of frontal lobe syndrome including “... difficulty makingdecisions, culminating in his taking two weeks to decide which slides to use fora work presentation; the decision was never finally reached.” (cited in Goldsteinet al., 1993, p. 274).

There is substantial evidence that the cognitive components of everydayplanning and organisational ability are impaired in such patients. Firstly, planningability has been explored using the Tower of Hanoi task (TOH) and the variantTower of London (TOL). With this procedure, the subject has to move around anumber of “discs” that are threaded into rods to achieve a goal state. Accurateperformance can be achieved by planning the sequence of moves carefully priorto responding. Patients with focal frontal lobe lesions have been shown to beimpaired on both TOH (Goel and Grafman, 1995; Morris, Miotto, Feigenbaum etal., 1997a, 1997b) and TOL versions of the task (Shallice, 1988; Owen, Downes,

Cortex, (1998) 34, 639-657

Sahakian et al., 1990). Secondly, there is evidence that the temporal organisationof activities is impaired in frontal lobe lesion patients, as demonstrated by tasksinvolving working or long-term memory (Miotto, Bullock, Polkey et al., 1996;Petrides and Milner, 1982; Shimamura, Janowsky and Squire, 1990; Milner,1971, 1974). Thirdly, the utilisation and organisation of the knowledge base thatguides behaviour appear to be impaired, for example with difficulties incategorising and sequencing script information and in solving everyday problemsrelating to social interaction (Sirigu, Zalla, Pillon et al., 1995, 1996; Godbout andDoyon, 1995; Dimitrov, Grafman and Hollnagel, 1996).

To what extent are these neuropsychological deficits reflected in everydaybehavioural impairment? The move to develop tests with “ecological” validity inthis context led to a number of investigations exploring planning andorganisation in a setting more akin to “real life”. One of the first of these studieswas by Shallice and Burgess (1991), who developed the Multiple Errands task,administered initially to three high IQ patients with frontal lobe lesions. Thepatients were required to undertake a series of “errands” in a pedestrian precinct.For example, the had to buy certain items such as a brown loaf and a packet ofthroat pastilles. Some tasks were made more complex, such as obtaining thenecessary information to send a postcard, and particular rules were built into thewhole task, such as having to spend as little money as possible or only enteringa shop when buying something. The patients had substantial difficulties with thisprocedure, showing grossly inefficient strategies and frequently breaking therules of the task. Recently, the “Zoo Test”, from the “Behavioural Assessment ofDysexecutive Syndrome Battery” (Wilson, Alderman, Burgess et al., 1996), wasdeveloped using a similar conceptual structure. This test, presented as a boardgame, involved the subject visiting locations in a “zoo”, printed in a map form,with certain constraints built in, such as only using certain paths once. A mixedsample of brain damaged patients, including those with frontal lobe lesions, weresignificantly impaired on this task.

In the current study, a further task was developed with the aim ofinvestigating planning and organisation of everyday life activities in the samevein as Shallice and Burgess (1991), but in the form of a board game. The task,named the “VIrtual Planning” Test (VIP) (Miotto, Mockler and Morris, in press),involves planning four days worth of activities, some of which relate topreparing for a fictional trip abroad and others to tasks that are unrelated. Eachday is organised by selecting from an array of “action cards” the ones whichrepresent the activities that the subject has to undertake. When a particular dayhas been completed, the activities selected are then placed onto an “executionboard”, the latter symbolising their execution. To simulate the constraints of“real” planning, once the daily activities have been “executed” the subjectcannot change their mind and have to move on to the next day. The task wasdesigned so that it could be used to explore certain features of problem solvingrelevant to frontal lobe disorder:

(1) The task differentiates between actions that are of more immediateconsequence, in other words related to the person’s current context (e.g. “Payyour electricity bill by Friday”) and those related to a removed scenario, such asplanning a trip overseas (e.g. “Buy a suitcase you will need for the trip”). This

640 Eliane C. Miotto and Robin G. Morris

addresses the question as to whether frontal lobe patients are more prone tofailure if the purposes of the activities are made more remote? Within thisdistinction, the task also used distraction actions, which were either related tothe “trip” or the “week”. Here, the prediction is that the frontal lobe patientsmay be more prone to being “captured” by a task related to the more immediatecontext;

(2) The task explores the “prospective memory” element of organisation, inwhich a task has to be done at a particular time (Cockburn, 1995). In this case,some of the activities have to be carried out on a specific day in either themorning or afternoon. Frontal lobe patients who have difficulty with prospectivememory may be more prone to making errors when such constraints are applied;

(3) In addition, it explores the complexity of the individual tasksadministered, using activity units that involve more than one action to complete.One possibility is that more complex tasks will be less easy to sequenceaccurately, leading to more errors. On the other hand, larger sequences ofactivities may be less sensitive to impairment in patients with frontal lobedamage because the overall structure acts as a more powerful retrieval cue forthe individual tasks. In the VIP task, two complexity levels were established formulti-componential tasks by varying the number of preparatory acts needed tocomplete the overall sequence of actions.

MATERIALS AND METHODS

Subjects

Patients

Twenty five patients were included in the study, all of whom had undergone unilateralor bilateral prefrontal lobe neurosurgery and are currently patients of the King’sNeuroscience Centre, London, UK. Ten had right-sided prefrontal lobe lesions (RF),including four cases where a meningioma had been removed, three cases of frontallobectomy for the relief of pharmacologically intractable epilepsy, two cases where ananeurysm of the anterior communicating artery had been clipped causing unilateral damage,and one case where a glioma had been removed (see Figure 1). Nine patients had left-sidedprefrontal lobe lesions (LF), with six cases of frontal lobectomy for the relief ofpharmacologically intractable epilepsy, one case where an astrocytoma had been removed,one case of infarction caused by elevation of a skull fracture and one where a discretelesion was caused by insertion of a shunt (see Figure 2). A further six cases were included,with bilateral prefrontal lesions (BF), with three cases in which a meningioma had beenremoved, one case of removal of a glioma, one case of infarction and one case where anastrocytoma had been removed (Figure 3).

Controls

These patients were compared to 25 healthy normal controls recruited from a pool ofcontrol subjects registered at the Department of Psychology, Institute of Psychiatry. Table Ipresents the main background characteristics of the different type of patients and controlsshowing approximate matching for age, education, sex, handedness, estimated generalintelligence using the National Adult Reading Test Revised (NART-R) (Nelson andWillison, 1991) and pro-rated Verbal IQ using the subtests Vocabulary, Comprehensionand Digit Span from the WAIS-R (Wechsler, 1981). One way ANOVAS confirmed that onall of these measures the two groups did not differ significantly.

Virtual Planning and frontal lobes 641

Memory Assessment

A neuropsychological assessment of memory functioning was conducted on both maingroups using the Logical Memory and Visual Reproduction subtests from the WechslerMemory Scale – Revised (Wechsler, 1987) (in both cases immediate and delayed versions)(see Table II). The patients were found to be unimpaired on all of these procedures.


Fig. 1 – Diagrams showing in black and white the extent of the cortical excisions for the patientswith right prefrontal lobe neurosurgery.

J.C. P.L. G.S. B.K.

O.E. P.D. L.M. T.C.

F.H. M.D.

Fig. 2 – Diagrams showing in black and white the extent of cortical excision for the patients withleft prefrontal lobe neurosurgery.

G.W. S.R. G.J. T.M.

T.S. L.S. C.E. O.O.

J.T.

TABLE I

The main clinical characteristics of the prefrontal lobe patients (N = 25) and control subjects (N = 25). Mean values given with standard deviations in brackets

Prefrontal lobe patients Controls

Mean S.D. Mean S.D.

Age 42.9 (16.1) 39.0 (11.5)Sex (male/female) 12/13 — 12/13 —Handedness (right/left) 20/5 — 21/4 —Education (years) 13.4 (3.0) 12.3 (2.5)NART VIQ 108.2 (11.2) 109.0 (6.7)WAIS-R VIQ 108.1 (16.0) 110.8 (14.2)

Executive Function Assessment

In addition, the prefrontal lobe lesion patients were tested on a battery of executivetests known to be sensitive to the effects of frontal lobe damage. These were the Controlled


Fig. 3 – Diagrams showing in black and white the extent of excision for the patients withbilateral prefrontal lobe neurosurgery.

TABLE II

Background neuropsychological variables, including the assessment of memory and executivefunctioning for the prefrontal lobe neurosurgical patients (N = 25) and normal control group

(N = 25)

Prefrontal lobe patients Controls

Mean S.D. Mean S.D.

MemoryDigit span age-scale score 10.0 2.4 — —Logical memory (immediate) 21.6 7.9 24.5 6.4Logical memory (delayed) 19.1 7.3 20.9 6.9Visual reproduction (immediate) 35.9 3.2 38.0 2.7Visual reproduction (delayed) 32.5 5.3 33.8 6.1

Executive functioningFAS (mean of three trials) 27.4 12.8 43.7 8.8Trail making test A (seconds) 47.6 16.9 34.00* —Trail making test B (seconds) 105.0 39.7 78.00* —Trail making executive (B-A) (seconds) 47.3 29.3 — —

Wisconsin Card Sorting TestCategories 3.9 1.9 5.4** 1.3**% perseverative errors 21.5 9.8 11.8** 7.1**

* Davies (1968); ** Heaton (1981).

A.W. M.O. S.O.

C.M. R.S. J.G.

Oral Word Association Test (FAS version) (Spreen and Benton, 1977), the Wisconsin CardSorting Test (WCST) (Heaton, 1981) and the Trail Making Test (Reitan and Wolfson,1985). For the FAS test, the performance of the frontal lobe patients was compared to thenormal control group of this study. The results of the WCST and Trail Making Test werecompared to control normative data. Table II indicates the impairment of the patients on allthree tests of executive function.

The VIrtual Planning Test

Design

The test is presented as a “board game” in which the main object is to plan and executea sequence of target activities specified beforehand. It consists of: (1) a “workboard”surrounded by a choice of 28 activities printed on individual cards to be selected bytransferring the relevant cards into a central “day frame” (see Figure 4); (2) a “summarycard”, which specifies all the activities that have to be done during the week (see TableIII); and (3) an “execution” board used to place the cards representing activities that thesubjects had selected for each day (Monday to Thursday). Four actions are selected for eachday and these are then “executed” by transferring them from the workboard to the executionboard, placed next to the subject (see Figure 4). When they have been executed, the subjectmoves on to planning the next day, and so on until all four days have been completed. Amain feature of the task is that the subject is not allowed to return to a previous day, onceit has been executed, thus reinforcing the planning aspect of the task. The target activitiesare either single “activities” or require a series of component activities for completion.


Fig. 4 – The VIrtual Planning Test (VIP) showing a sequence in which a subject (left) is beingtested by the psychologist (right). The workboard is to the front of the subject, the execution board tothe right. The summary card (upright) is also shown. In the sequence: (1) the subject is planning theactivities; (2) the subject chooses the activities for “Monday”; (3) to “execute” the days’ activitiesthe psychologist transfers the cards to the execution board; (4) the task is finished when all the daysare completed.


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Prefrontals Controls

Fig. 5 – The mean % correct scores for the Total comparing the 25 prefrontal lobe patients and25 normal controls.

TABLE III

Activities as in Order Listed on the “Summary Card”

1. Book and collect your flight tickets.2. Buy a suitcase and pack your smart clothes that are currently at the dry cleaners.3. Get a guide book.4. Get some travellers cheques.5. Do some shopping and prepare dinner for your friend. Give your friend instructions to get to your

place.6. Book and collect some theatre tickets.7. Write a letter to your old friend and take it to the Post Office to stamp and send.8. Pay your electricity and telephone bills.

Another feature is the inclusion of “distracter” items in the choice of activities, those thatthe subjects has not been instructed to complete at the beginning of the task.

Target Activities

These are all listed in Table IV. They are activities judged to be well known within thecultural and social background of the subjects. The test was piloted on a small group ofindividuals to screen out any item that would seem unfamiliar or strange. It is presented inform of a “game” in which all the target activities have to be completed before the subjectgoes on a trip abroad (on Friday). Some of these relate to things that have to be donespecifically for the trip, whilst other are not related, other than having to be done in thedays before the trip (e.g. pay your telephone bill by Friday). For target activities with morethan one action the overall activity is described by a single phrase (e.g. booking andcollecting flight tickets), and comprises the single activities to be selected by the subject (inthis case, “Call the travel agency to book the air flight tickets for your Friday trip overseas”,and “on Thursday morning go to the travel agency to collect your flight tickets”). For thesetarget activities, there is always one final act and either one or two preparatory actions.These activities are defined in terms of complextity by the number of preparatory actsneeded in order to complete the final one (respectively: Complexity 1 – one preparatoryact; and Complexity 2 – two preparatory acts) (see Table IV for examples).

The types of target activities are constructed with overlapping categories, namely (1)Context: Whether they are activities related to the trip (ART; 7 items) or to the week (ARW;


TABLE IV

Actions to be completed categorised according to number of components (in addition, the context and time specificity categorisation is also given for each activity; see text). The alphanumeric labels

are used to aid administration of the test

Single Activities(A1) Pay your electricity bill. This has to be done by Friday or you will be cut off (TNSA; ARW)(A2) Pay your telephone bill by Friday (TNSA; ARW)(A3) On Monday afternoon go to your friend’s house to borrow a guide book you will need for your

trip (TSA; ART)(A3) Go to the bank to get some travellers cheques for your trip. This has to be done on Thursday

morning (TSA; ART)Complexity 1I. Get the flight tickets for the Friday trip overseas:(B1) Call the travel agency to book the air flight tickets for your Friday trip overseas (TNSA; ART)(B2) On Thursday morning go to the travel agency to collect your flight tickets (TSA; ART)II. Post a letter to a friend:(C1) Buy the envelope you will need to send your letter (TNSA; ARW)(C2) Go to the Post Office to send your letter on Wednesday morning (TSA; ARW)III. Get some tickets to go to the theatre(D1) Telephone the theatre box office to book your tickets for the Wednesday night play (TNSA;

ARW)(D2) Collect your theatre tickets from the box office on Wednesday morning (TSA; ARW)Complexity 2I. Get clothes packed for the trip.(E1) Pick up your smart clothes from the dry cleaners that you have to take on your trip (TNSA;

ART)(E2) Buy a suitcase you will need for the trip (TNSA; ART)(E3) Pack your clothes on Thursday afternoon (TSA; ART)II. Organise dinner for a friend(F1) The dinner with your friend is on Tuesday night. Call your friend to give him/her directions to

get to your place (TNSA; ARW)(F2) Buy what you need to cook for the Tuesday night dinner with your friend (TNSA; ARW)(F3) Cook the meal for the dinner with your friend. Your should do this on Tuesday afternoon in time

for the evening (TSA; ARW)

9 items); (2) Time Specificity: When they have to be done by a particular time, namelythose which only have to be done by the end of the week, but not on a specified time (TimeNon-Specific Acts – TNSA; 9 items) and those that have to be done at a specified time(Time Specific Acts – TSA; 7 items); (3) Number of components: How many componentsactivities are reqired, one (Single Activities; 4 items), two (Complexity 1; 6 items) or three(Complexity 2; 7 items).

Distracter Activities

The subject is presented with 12 distracter items (see Table V). These are split intothose that could be related to the trip (e.g. “buy a film for your camera”) and those that arenot (e.g. “stay in doors and take it easy for a while”). Within these two categories, halfhave to be done at a particular time and half can be done at any time.

Materials and Procedure

The main workspace consists of the workboard (60 × 50 cm) with a central region forplanning each day (the day frame), surrounded by spaces for the 28 action cards (8 × 4 cm)(see Figure 4). The day frame is headed by a “day card” which specifies the day of theweek to be worked on; below this are spaces for the four action cards, a space for twocards in the “morning” and two in the “afternoon”. On the right side of the work board isthe “execution board” where the cards are transferred after each day has been decided upon.This contains four separate areas corresponding to the days of the week used. Next to theworkboard is the “summary card” that specifies all the target activities (see Figure 4). Inthe case of the single activities, these are written in the summary card. For the complexactivities, a phrase summarising the overall activity is listed on the summary card. Thissummary card is kept within sight of the subject throughout the test.

The subjects are seated in front of the workboard and then instructed concerning themain features of the task. They are to play a board game in which at the end of a “week”(on Friday) they are going away on a “trip” overseas. The main goal is to organise andcarry out a series of activities by the end of the “Thursday”. They are asked to read thesummary card which specifies the activities that should be done. The examiner thendemonstrates how to select an action card from the workboard and place it on the day frame


TABLE V

Distracter items categorised according to the context and time specificity (alphanumeric label used in administration of test)

Trip related distractionTime non-specific(TRA1) Buy some films for your camera(TRA2) Buy some suntan lotion from the pharmacy(TRA3) Buy a book you would like to readTime specific(TRD1) Buy a new pair of shoes on Wednesday morning(TRD2) Buy a new hat on Thursday morning(TRD3) Buy a new pair of sunglasses on Tuesday afternoon

Week related distractionTime non-specific(WRA1) Go to a picnic with your friends(WRA2) Go to the park for a walk(WRA3) Stay indoors and take it easy for a whileTime specific(WRD1) Watch a very important football match on Monday afternoon(WRD2) Some friends of yours are meeting on Thursday morning. You can join them(WRD3) Watch a very good film on television on Wednesday morning

using “dummy action cards” (selected so as not to interfere with the subsequent planning).These are then removed prior to the subject starting the task. The subject is told that thereare two important rules relating to the task. Firstly, not all the activities on the workboardcan be completed, so they should concentrate on doing the ones that have to be doneaccording to the summary card. They are also told that some of the activities can be doneonly at a particular time, as indicated on the action cards.

They are instructed not to start before they are sure of the first selection. They thenselect the four action cards corresponding to the first day (Monday) and when they signalthey are ready, these are transferred to the execution board. The day heading is changed sothat the subject starts again with the next day (Tuesday). This continues until all the dayshave been completed (Monday to Thursday). The subjects are allowed to inspect theexecution board whenever they wish to check their previous choices.

RESULTS

Test Performance

For the main analysis, the performance of the total patient group wascompared with the matched control subjects. Since the data for each group didnot conform to a normal distribution, a non-parametric approach was taken forthe analyses. To compare across accuracy measures, the performance scoreswere expressed in terms of the percentage of correct responses.

Total Score

A total score was constructed by adding the number of time a subjectperformed an activity either at or by the appropriate time (see Figure 5). AMann-Whitney U-test showed a highly significant impairment in the frontalgroup (U = 123, W = 448, p < 0.001).

Time Specificity

All the activities were split according to whether they had to be done at aspecific time (TSA) or had no time constrains other than completion by the end ofthe week (TNSA). The proportion of correct responses for both patient andcontrol groups are presented on Table VI. For TSA, the patients were significantlyimpaired (U = 109.15, W = 434.5, p < 0.001). The types of errors for this measure


TABLE VI

The mean % correct scores and standard errors for the Time Specific Actions (TSA), Time Non-Specific Actions (TNSA), Activities Related to the Trip (ART) and Activities Related to the Week

(ARW), comparing the 25 prefrontal lobe patients and 25 normal controls

TSA TNSA ART ARW

PatientsMean 78.3 78.2 91.4 71.6S.E. 3.8 3.7 2.6 4.5

ControlsMean 96.0 92.0 98.3 90.2S.E. 1.3 1.8 0.9 2.1

were analysed, splitting them into whether the subject failed to perform anactivity (Absent Errors, patients: 22 errors; controls: 5 errors) or whether theycompleted the activity but at an an inappropriate time (Wrong Order, patients: 16errors; controls: 2 errors). The proportion of Absent Errors were computed for thetwo groups in the cases of subjects who made errors on the TSA measures (21patients, mean: 0.68, S.E.: 0.10; and 7 controls, mean: 0.71, S.E.: 0.18). For thesesubjects, there was no significant difference between the two groups in thisproportion (note that the proportion of wrong order errors are one minus theabsent error proportions). TNSA errors were also compared between groupsshowing a significant impairment in the frontal lobe patients (U = 164, W = 489,p < 0.001). This measure was divided into Absent (patients: 36 errors; controls: 8errors) and Wrong Order errors (patients: 13 errors; controls: 4 errors). Hereagain, the proportion of Absent Errors were computed for the two groups in thecases of subjects who made errors on the TNSA measure (22 patients, mean: 0.72,S.E.: 0.08; and 9 controls, mean: 0.72, S.E.: 0.15). The proportion of AbsentErrors was again not different between the two groups.

Context

The data were split according to whether they included activities related tothe “trip” (ART) or to the “week” (ARW) (see Table VI). This showed that onboth measures the patients were significantly impaired (ART: U = 220.5, W =545.5, p < 0.05; ARW: U = 146.5, W = 471.5, p < 0.001). The proportion of thetwo types of errors was also computed in the two groups, but there was nosignificant difference.

Number of Components

The data were analysed in order to investigate whether the complexity of themulticomponential tasks was related to the impairment seen by the patients (seeFigure 6). For this analysis, complexity level (1 and 2) had the same totalnumber of activities (6 in each). Single activity tasks were not included in thisanalysis because of their qualitatively different nature (no preparatorycomponent). A Mann-Whitney U-test revealed that for Complexity 1 there was asignificant impairment in the frontal lobe patients (U = 151.5, W = 476.5, p < 0.001), but not for Complexity 2. A Wilcoxon Matched pairs test showedalso that the frontal lobe group differed significantly on Complexity 1 and 2 (Z = – 2.49, p < 0.05), but not the control group.

Distraction

Distraction errors were split into those involving selecting items related tothe trip (Trip Related Distraction, “TRD”) and those relating to the week (WeekRelated Distraction, “WRD”). Here the measure was the total number of actioncards selected in each category. The frontal lobe patients showed the samenumber of TRD errors as the controls, but significantly more WRD errors (U = 155, Z = – 3.68, p < 0.001) (see Figure 7). To explore this finding further,


the proportion of Week Related distraction errors were calculated for each groupwhich was shown to be significantly greater in the frontal lobe group (U = 64.5,Z = – 2.57, p < 0.05).

Latencies

The subjects had been told not to start until sure of their first response.Accordingly, the time between the start of the test and the first “action card”selected was recorded using a stop watch and termed the Planning Time(PT).The subsequent time to complete the task was labelled the Execution Time(ET)


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Fig. 6 – The mean % correct scores for the Complexity Level 1 (CP1) and Complexity Level 2(CP2) measures, comparing the 25 prefrontal lobe patients and 25 normal controls.

TABLE VII

Mean and Standard Errors for the VIP Planning and Execution Times (seconds)

Planning time Execution time

PatientsMean 46.7 542.6S.E. 13.3 67.0

ControlsMean 32.6 436.3S.E. 7.5 54.0

(see Table VII). To establish homogeneity of variance in this case, the data weretransformed logarithmically and the two groups compared. There were nosignificant differences between the two groups on either measure.

Association with Background Measures

The association between the background measures and VIP accuracyperformance was explored through correlative analysis. To reduce the number oftests, a restricted number of measures were used on the following basis: (1) TheTotal Score was used as an aggregate performance score; (2) The TimeSpecificity and Context performance measures were not included because thesedid not show differential effects between the groups; (3) Both the TaskComplexity (CP1 and CP2) and the Related Distractor (TRD and WRD)distinctions were included because they showed differential impairments betweenthe patients and controls.

Age and Intelligence

The above measures were correlated against Age and Verbal Intelligence(NART-R and WAIS-R). In the patients, significant correlations were found


0

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1

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Fig. 7 – The mean number of week related (WRD) and trip related (TRD) distractor itemsselected, comparing the 25 prefrontal lobe patients and 25 normal controls.

between the Total Score and WAIS-R Verbal IQ (R = 0.43, p < 0.05).Additionally, the CP2 measure correlated with NART-R Verbal IQ (0.62, p < 0.05) and WAIS-R Verbal IQ (R = 0.45, p < 0.05). For the controls, theTotal Scores also correlated with WAIS-R Verbal IQ (R = 0.42, p < 0.05).

Memory

The five memory measures were used in this analysis (Digit Span, LogicalMemory Immediate and Delayed, and Visual Reproduction Immediate andDelayed). The only significant correlations were for the patient group betweenthe CP2 measure and Logical Memory/Delayed (R = 0.50, p < 0.05) and VisualReproduction/Delayed (R = 0.46, p < 0.05).

Executive Functioning

Here, the measures for the executive tasks administered to the patients wereselected, including the total FAS score, the Trails B-A score (Executive Trails)and the number of Categories and Percent Perseverative Errors on the WCST(see Table VIII). For the total score and CP1 measure, there was a significantnegative correlation with time taken on the Trails B-A (R = – 0.47, p < 0.05,and R = – 0.46, p < 0.05, respectively). For the Trip Related Distractors therewas a positive correlation with Percent Perseverative Errors (R = 0.44, p < 0.05).

DEX Questionnaire (BADS)

In order to investigate the association between the subjects performance onthe VIP task and their real-life behaviour, correlational analyses were performedusing the DEX Questionnaire (Wilson et al., 1996). This is a 20-itemquestionnaire which investigates four areas of likely changes associated withDysexecutive Syndrome, such as behavioural, cognitive, personality andmotivational changes. For the present analysis only the ratings made by thepatients were considered. The individual items’ scores were added up to producea total DEX score for each patient. The highest the score the greater the


TABLE VIII

Correlations between selected VIP measures (see text) and psychometric tests of executive functioningfor the prefrontal lobe neurosurgical patients (N = 25) (executive measures used: FAS mean score,The Trail Making Test (B-A) (seconds) and the Wisconsin Card Sorting Test, categories achieved

and % Perseverative Errors)

VIP FAS Trail executive WCST

(B-A) Categories % Pers.

Total – 0.50 – 0.47* 0.30 – 0.20Complexity 1 0,10 – 0.46* 0.35 – 0.15Complexity 2 0,22 – 0.02 0.06 0.15Week Related Distraction – 0.01 0.33 – 0.22 0.37Trip Related Distraction 0.05 0.35 – 0.33 0.44*

Spearman coefficient: * p < 0.05.

impairment. For this measure, significant negative correlations were found withTNSA (R = – .421, p < 0.05) and ET (R = – .428, p < 0.05) and a positivecorrelation with WRD (R = .424, p < 0.05).

Lesion Effects

Side of Lesion

The patient group was divided according to the side of the lesion, generatingRight Frontals (RF, N = 10), Left Frontals (LF, N = 9) and Bifrontals (BF, N = 6). The performance of the three frontal groups was compared on the mainexperimental measures (Total, CP1, CP2, TRD and WRD) using Kruskal-Wallisfor the analysis. There were no significant differences between the groups onthese measures.

Site and Size

The patients were subsequently divided according to the lesion site (Orbital,N = 11, including Brodmann’s areas 11, 13 and 47; Dorsolateral, N = 5, areas9, 10, 44, 45 and 46; and Orbito-Dorsal, N = 9, combined orbito anddorsolateral areas) and size of the excision (less than 4.5 cm2, N = 10; and morethan 4.5 cm2, N = 15). Kruskall-Wallis and Mann-Whitney U-test, usedrespectively for the analysis, did not show any significant effect of thesevariables on the performance of the experimental measures mentioned above.

DISCUSSION

In summary, the test overall shows a clear impairment in the frontal lobepatients despite the patient and control groups being matched in terms ofbackground variables such as age, educational background and verbalintelligence. In terms of the variables investigated, the deficit was independentof whether the actions were related to the future event (the “trip”) or to theimmediate context (the “week”). It was the same in the two groups whether ornot the action had to be completed at a particular time. However, the mostcomplex activity unit requiring three actions produced less errors than a lesscomplex activity, requiring two actions. In terms of type of distractor itemschosen, the controls showed a tendency to select “trip related” distractor items inpreference to “week related”, whilst the patients were prone to select both typesto the same extent. Finally, the patients were found not to be slower on any ofthe latency measures.

The deficits in the frontal lobe patients do not appear to be related tointellectual or memory impairment, at least in a straightforward fashion, sincethe patients were matched to the controls with respect to these factors. Verbaland visual delayed recall was, however, correlated with VIP performance (CP2measure only) in the patients, suggesting that long-term memory function mayhave an influence on planning ability in this group, or alternatively, a deficit in


organisational ability could predict difficulties in the efficient encoding andretrieval of information. The patients showed average range Digit Span, and thismeasure was not correlated with VIP performance. This would suggest that theVIP impairment was not caused by a simple short-term or “working memory”impairment. To some extent, this mirrors the finding of Morris et al. (1997) whofound that immediate memory impairment did not account for the planningdeficit of frontal lobe lesion patients on the Tower of Hanoi task. Correlationswere also found with some of the measures of the tests to assess frontal lobefunctions such as the Trail Making Test and the WSCT, as will be discussed inmore detail below. The fact that site, size and side of the frontal lobe lesion inthe patients had no effect on performance suggests that planning andorganisational abilities encompass a complex set of cognitive processes. Forinstance, they can involve the retrieval of mental images or representations ofreal life behaviour, strategy formation, verbal regulation and social skills. Ifthese processes are associated with distinct regions within the frontal lobes,damage to any area of the frontal lobes could affect planning and organisationalperformance.

As well as developing a test that simulates “everyday planning” the task wasdesigned to investigate certain key components relating to this activity. The firstwas the effect of the “proximity” of the actions in relation to the context or“scenario” used, the main distinction between those relating to the week (such aspaying a bill) or the trip (getting the air tickets for the flight). An analysis ofresponses by the subjects on these two types of activities showed no differencebetween the two groups in the proportion of errors (the absolute differenceappears to be greater in the week related activities, but this may be becausethese activities were slightly harder to perform efficiently overall).

The effect of contextual “proximity” is, nevertheless, reflected in the types ofdistracter items selected. For both frontal lobe lesion patients and controls, therewas an equal tendency to select trip related distractor items. This is possiblebecause these items were relevant to the trip and could more easily have beenconfused as being “necessary” items (e.g., “buy some film for the camera”). Incontrast, the two groups differed significantly in the number of week relateddistractor items selected, although this difference was relatively small. Oneinterpretation of this finding is that for the patients, “proximal” types ofdistractor actions in relation to the week target activities are more easily“triggered”. For example, it may be consistent with the contention schedulingmodel by Norman and Shallice (1986), in which associated schemas have alower threshold for activation than more “distant” events. Such a finding is alsoreminiscent of Sirigu et al. (1996)’s report that semantically related distractoritems tend to be falsely incorporated into a script when frontal lobe patients arerequired to organise a series of actions into their relevant script sequence.Semantic relatedness or “contextual proximity” may have the same effect in thisregard. The further question is why this appears to be the case. One possibilityis that distractor “error” relating to activity is strongly determined by the contextof the overall actions, which in turn establishes a mental set of the subject. Thecontext lowers the threshold of activation for related “in context” actions,making their triggering more likely.


In normal subjects, this effect, which could take part at the contentionscheduling level, may serve a more general purpose of producing actionsappropriate to a particular context. The tendency, however, has to be activelyoverridden where planning for “remote” activity is concerned, but if thesuperordinate co-ordination mechanism such as the SAS in the Norman andShallice (1986)’s model is impaired, this no longer happens. Alternatively, thethreshold of activation may be determined by the frequency rating of the item,in terms of the subject’s familiarity with the action, a factor suggested byGrafman (1989, 1995). Under this hypothesis, it is not the context thatdetermines whether the distractor item will be falsely selected, but theassociative strength between the action and environmental cue. To test thesealternatives directly, the context of each activity could be manipulated acrossdifferent types of material and frequency of exposure.

Of note, the number of action failures in frontal lesion patients wereequivalent whether or not they had to be performed at a specific time, in thiscase the time specificity relating closely to the concept of “prospectivememory”. This result might not have been predicted given that deficits inprospective memory are associated with frontal lobe lesions (Cockburn, 1995).An essential difference may be related to the provision of cues in the currenttask. In prospective memory tasks which have revealed deficits in frontal lobelesion patients, the requirement to act at a particular time is given in advance,but no specific cues are then provided. In the VIP task, the time specificity ofthe action is always provided by the action card (e.g. “collect your theatretickets from the box office on Wednesday morning”) which is maintained inview of the subject. This is closer to the “event based” prospective memoryprocedure, where the subject is provided with a specific cue at the appropriatetime and has the effect of ameliorating the prospective memory deficit. In thistask, the time non-specific activities, although not conforming to the timeconstraint to conventional prospective memory tasks (a task has to be done at aparticular moment), did not have the benefit of time related cues and so wereequally susceptible to deficit.

A third variable explored in the study was the complexity of the activities.This was investigated by varying the number of component activities required toachieve major subgoals (one versus two preparatory acts). Here, the morecomplex action sequences (CP2) did not show an overall impairment. Thisfinding would need to be replicated using different types of material andcounterbalancing material types in order to confirm that it is a “complexity”effect. If so, then it suggests that larger units of activity are less likely to causeimpairment in frontal lobe patients.

The association between the VIP and well established tests of executivefunctioning was explored using the main performance measures. As withprevious studies relating the inter-correlation of executive task measures inpatients with frontal lobe lesions the correlations tended to be low and notconsistent across all tests (see Shallice and Burgess, 1996). Firstly, nocorrelations were found with verbal fluency. The B-A Trail Making Test, ameasure of rapid set shifting correlated with the VIP Total score and with theless complex activity items (CP1), such that worse performance in the VIP


predicted slower rates B-A performance. This association might suggest that therapid switching between mental sets in Trails is related to the need to switchbetween different target activities or, indeed, between the “week” and “trip”context. This ad hoc explanation might point the way for future research inwhich the components of every day planning are dissected through modifiedversions of the VIP test. Finally, the Total score from the patients’ ratings on theDEX Questionnaire was significantly correlated with the Week RelatedDistraction, Execution Time and Time Non-Specific Acts measures of the VIP.A greater impairment on the DEX was associated with an increased number ofweek related distractor items selected, a tendency to spend less time in executingthe task and an impairment in the organisation and execution of TNSA. Of note,the remaining executive functioning measures (WCST, Trail Making Test andFAS) were uncorrelated with the Total score of the DEX Questionnaire. Theseresults suggest that tasks which involve everyday life components may be moreclosely related to real life behaviour.

In summary this paper present a task that goes some way to bridge the gapbetween laboratory based tests of planning and organisation, and “real life”behavioural investigation. It shows significant impairments in the frontal lobepatients in comparison to normal controls, but in specific aspects oforganisational abilitiy. How these relate to the precise nature of the cognitivedeficits that contribute to what is essentially a multicomponential task warrantinvestigation based around this type of measure. Laboratory control of the“virtual” environment, such as in the VIP test, can facilitate such investigation.

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Dr. Eliane C. Miotto, Department of Psychology, Institute of Psychiatry, De Crespigny Park, London SE5 8AF, U.K.

(Received 23 October 1997; accepted 28 May 1998)


virtual planning in patients with frontal lobe lesions

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