Bmn(1991).114,727-741 DEFICITS IN STRATEGY APPLICATION FOLLOWING FRONTAL LOBE DAMAGE IN MAN by TIM SHALLICE and PAUL W.BURGESS (From the National Hospital.Oueen Square.London and the MRC Applied Psychology Unit.Cambridge SUMMARY A quantitative investigation of the ability to carry ou a variety of cognitive tasks was performed ded tasks min period.They iemfcnd2cromedcwcdonaaiey,of er test enerad inenonseealy prey could be excluded.It is INTRODUCTION It has been known for many years that frontal lobe lesions can produce a gross effect n the anc of ryday lif ties other than the m routin th gical tests est that the co gnitive cha s that hay ed a nor (e 1936:Ackerly d B 1047)Fo Esl and Damasic i985) tad th ountant who 6 r a for the noval of a bilateral hitof ha d an IQ of 120 nd perfo ide n ts,inclu obe dam exce by gues est his y mp He wa. ven tougn .Re p uld take hou ide go ou uire ed that on April 8.201 ma of each an d he busy eac was still ble 011 pat ents vith la can hay 90 Stuss ar 198 ng th who have c ng eve diff de but th given e pa in thev re proba e th appro tient's impa ikely to pa ent typi ly has explicit pro any one time,the trials tend to be very short (I min or so or even ess).tas ©Oxford Universiry Pres时I9l
Brain (1991), 114, 727-741 DEFICITS IN STRATEGY APPLICATION FOLLOWING FRONTAL LOBE DAMAGE IN MAN by TIM SHALLICE and PAUL W. BURGESS (From the National Hospital, Queen Square, London and the MRC Applied Psychology Unit, Cambridge) SUMMARY A quantitative investigation of the ability to carry out a variety of cognitive tasks was performed in 3 patients who had sustained traumatic injuries which involved prefrontal structures. All 3 had severe difficulties in 2 tests which required them to carry out a number of fairly simple but open-ended tasks over a 15 — 30 min period. They typically spent too long on individual tasks. All patients scored well on tests of perception, language and intelligence and 2 performed well on a variety of other tests of frontal lobe function. Explanations for their difficulty on the multiple subgoal tasks in terms of memory or motivational problems could be excluded. It is argued that the problem arose from an inability to reactivate after a delay previouslygenerated intentions when they are not directly signalled by the stimulus situation. INTRODUCTION It has been known for many years that frontal lobe lesions can produce a gross effect in the performance of everyday life activities other than the most routine, even though neuropsychological tests suggest that the cognitive changes that have occurred are at most minor (e.g., Brickner, 1936; Ackerly and Benton, 1947). For instance, Eslinger and Damasio (1985) reported the case of an accountant who 6 yrs after an operation for the removal of a large bilateral orbitofrontal meningioma had an IQ of over 130 and performed well on a wide variety of neuropsychological tests, including some held to be sensitive to frontal lobe damage. Despite this excellent performance on quantitative tests, however, his ability to organize his life was grossly impaired. He was dismissed from a series of jobs even though his basic skills, manner and temper were appropriate. He went bankrupt and was involved in two divorces in 2 yrs. Relatively simple matters would take hours; thus to go out to dinner required that he consider the seating plan, menu, atmosphere and management of each restaurant and he might even drive to see how busy each of them was, but was still unable to come to a decision. Of course, patients with relatively severe frontal lesions can have deficits on a range of quantitative neuropsychological tests {see Stuss and Benson, 1986, for review). It is possible that all patients who have debilitating everyday life difficulties would also show severe quantitative deficits on standard neuropsychological tests, but that the relevant tests were not given to the patient. However, a more probable explanation is that certain of the implicit approaches adopted in the design of neuropsychological tests makes the patient's impairment less likely to manifest themselves in the test situation. Thus in neuropsychological tests the patient typically has a single explicit problem to tackle at any one time, the trials tend to be very short (1 min or so or even less), task initiation Correspondence to: Professor Tim Shallice, Department of Psychology, University College, Gower Street, London WCIE 6BT. © Oxford University Press 1991 by guest on April 8, 2016 http://brain.oxfordjournals.org/ Downloaded from
728 t.SHALLICE AND P W BURGESS is strongly prompted by the examiner and what constitutes successful trial completion is clearly characterized.Rarely are patients required to organize or plan their behaviour over longer time periods,or to set priorities in the face of two or more competing tasks. Yet it is these sorts of'executive'abilities which are a large component of many everyday activities. For instance,consider a situation which gave problems for a patient who had had a right frontal glioma removed and who was Wilder Penfield's sister.In Penfield and Evans(1935)he writes:'She had planned to get a simple supper for one guest(Penfield) and four members of her family.She looked forward to it with pleasure and had the whole day for preparation.When the appointed hour arrived she was in the kitchen, the food was all there,one or two things were on the stove,but the salad was not ready. the meat had not been started and she was distressed and confused by her long continued effort alone.'If in addition to the actual preparation of the meal one also has to decide the menu,then an everyday task such as this will require certain capacities,none of which are clearly captured in the standard neuropsychological test.Planning will have to be carried out and preparatory purchases made.Different considerations- osts,tastes. available time,etc. may have to be weighed against each other.Many minor decisions mereoenmy ee over the time available. Before this second explanation can even be seriously considered,however,it is necessary to develop quantifiable analogues of the op en-ended multiple subgoal situations where this subset of frontal patients would theoretically have problems.Only then can this possibility be realistically considered.In this paper we describe 3 patients with severe problems in the organization of everyday life activities arising from head injuries primarily affecting the frontal lobes.Their performance on a large set of standard neuropsychological tests ranged from generally good with patchiness on some'frontal'tests in the worst of the 3 patients,through to almost consistently bright average to superior performance in the b-st of the 3.However,all 3 patients performed especially poorly on two tests designea w assess performance in more open-ended multiple subgoal situations.Various alternative explanations for their poor performance are then assessed. CASE HISTORIES n April 8,2016 Case I 0f23 ossa fracture.req ltipl His condition grac ally improved not able to ear later he asa a patient to Hospita for rehabilitation.He was wel and keen but uld not carry ou even the simplest activity be use of an inability to keep his mind or outside the thera mto fetch s letel was that tobe doing.Hewas unable to shop for himself because othe as methodsd ity to organ
728 T. SHALLICE AND P. W. BURGESS is strongly prompted by the examiner and what constitutes successful trial completion is clearly characterized. Rarely are patients required to organize or plan their behaviour over longer time periods, or to set priorities in the face of two or more competing tasks. Yet it is these sorts of 'executive' abilities which are a large component of many everyday activities. For instance, consider a situation which gave problems for a patient who had had a right frontal glioma removed and who was Wilder Penfield's sister. In Penfield and Evans (1935) he writes: 'She had planned to get a simple supper for one guest (Penfield) and four members of her family. She looked forward to it with pleasure and had the whole day for preparation. When the appointed hour arrived she was in the kitchen, the food was all there, one or two things were on the stove, but the salad was not ready, the meat had not been started and she was distressed and confused by her long continued effort alone.' If in addition to the actual preparation of the meal one also has to decide the menu, then an everyday task such as this will require certain capacities, none of which are clearly captured in the standard neuropsychological test. Planning will have to be carried out and preparatory purchases made. Different considerations—costs, tastes, available time, etc.—may have to be weighed against each other. Many minor decisions will need to be made and typically they are undertaken in parallel with other activities. There is no clearly correct solution and many different activities may have to be scheduled over the time available. Before this second explanation can even be seriously considered, however, it is necessary to develop quantifiable analogues of the open-ended multiple subgoal situations where this subset of frontal patients would theoretically have problems. Only then can this possibility be realistically considered. In this paper we describe 3 patients with severe problems in the organization of everyday life activities arising from head injuries primarily affecting the frontal lobes. Their performance on a large set of standard neuropsychological tests ranged from generally good with patchiness on some 'frontal' tests in the worst of the 3 patients, through to almost consistently bright average to superior performance in the b"*5t of the 3. However, all 3 patients performed especially poorly on two tests designed io assess performance in more open-ended multiple subgoal situations. Various alternative explanations for their poor performance are then assessed. CASE HISTORIES Case 1 A.P., a right-handed man was involved in a road traffic accident at the age of 23 yrs, approximately 4.5 yrs before the present investigation. He sustained a serious open head injury involving an anterior fossa fracture, requiring multiple operations. His condition gradually improved, but he was not able to return successfully to his job. A CT scan that year showed evidence of extensive bifrontal damage. A year later he was admitted as a day patient to St Andrew's Hospital for rehabilitation. He was well-motivated and keen but could not carry out even the simplest activity because of an inability to keep his mind on the task in hand. For example, on one occasion he was discovered on the local golf course having originally stepped outside the therapy room to fetch some coffee. At these times he maintained that he 'completely forgot' whatever it was that he was supposed to be doing. He was unable to shop for himself because he would buy one item at a time returning to his car after his every purchase. Rehabilitation as a day patient had limited success, and after 3 months A.P. was transferred to another rehabilitation centre as an inpatient. There he was treated with behavioural methods described by Wood and Burgess (1988) with a slow but progressive improvement in his ability to organize his activities of by guest on April 8, 2016 http://brain.oxfordjournals.org/ Downloaded from
FRONTAL LOBE DAMAGE 729 re the accident his clea inand laundry areon for him.rarely of said he h d for the coming weekend,was unable to give ologcalarp all and then 2 yrs later satisfactorily.At St Andrew's Hos pital he obt ed a Verbal IQ of 121 and a Performance IQ of 120 oy the r the Digi a repea 2 yrs la e scored in the Superior range on the otest.His performance on oth subtest nd on a uals proba metic and m ).out he The one mem ory est where his performance was bel w ave age was the Petrides anc nade errors by c for their c the p comparable s within I SD of the mean of a posterior lesion control group(see Table lesions he performed very satistactonly PERFORMANCE ON BASELINE TASK Cater Verbal 3 3 Picture Completion 14 13 212 11 cabulary Verbal IQ 128 126 135 129 112 114 Cases NARTSI 2 17 ed Namins Tet PCeia0fesniles (War and Jams. Dot Centre 50 50 6 Unconyentional views 西 25 0 9gionanNhne ton and Taylor 973 Conventional Views 0 50 50 ton and Taylor, 1973)
FRONTAL LOBE DAMAGE 729 daily living. He remained in rehabilitation for approximately 1 yr and then returned home to live with his parents. In response to a clinical interview, he said that before the accident his room was immaculate ('5/5 tidiness') but it is now untidy with 'hotchpotch piles of magazines' on the floor. He had had an efficient filing system but had abandoned it. Shopping, cleaning and laundry are done for him. His social life is very rarely organized in advance. When questioned he said he had nothing planned for the coming weekend, was unable to give any example of consciously organizing an activity beforehand. Clinical neuropsychological investigations. A.P. was tested at St Andrew's Hospital and then 2 yrs later, at the National Hospital on a large range of neuropsychological tests. On almost all he performed very satisfactorily. At St Andrew's Hospital he obtained a Verbal IQ of 121 and a Performance IQ of 120, which corresponds well with the estimate of 124 for his premorbid IQ as measured by the NART. There was one exception—the Digit Span subtest where he scored only in the Dull Normal range; however, on a repeat testing 2 yrs later he scored in the Superior range on the subtest. His performance on other subtests was slightly better, which is probably a practice effect (see Table 1). His spontaneous speech was not aphasic and on all perceptual, language, arithmetic and memory tests carried out he performed satisfactorily (see Tables 1,2). The one memory test where his performance was below average was the Petrides and Milner (1982) self-ordered pointing task which is most appropriately considered a frontal test. On the picture version he made 7 errors by comparison with a mean of 3 errors for their control subjects who were of comparable age. (However, he was within 1 SD of the mean of a posterior lesion control group (see Table 3).) On all of a sizeable group of other tests thought sensitive to frontal lesions he performed very satisfactorily (see Table 3). TABLE I. PERFORMANCE ON BASELINE TASKS Wechsler Adult Intelligence Scale (WAIS) Subtest Age-Scaled Scores Cases Verbal Arithmetic Similarities Digit Span Vocabulary Verbal IQ WAIS Full Scale IQ NART FSIQ equivalent Language (Scaled Score) Graded Naming Test Perception (percentiles) Cube Analysis Dot Centre Unconventional Views Conventional Views 13 15 15 16 128 2 14 14 14 15 126 15 15 15 17 135 130 124 A. P. 14 A. P. 50 50 50 50 Picture Completion Block Design Picture Arrangement Performance IQ Cases 2 121 119 D.N. 14 D.N. 50 50 25 50 127 127 F.S. 14 F.S. 50 50 10 50 14 15 13 129 Cases 2 12 12 11 112 3 13 13 11 114 (Wechsler, 1955) (Nelson and O'Connell, 1978) (McKenna and Warrington, 1983) (Warrington and James, 1988) (Warrington and James, 1988) (Warrington and Taylor, 1973) (Warrington and Taylor, 1973) by guest on April 8, 2016 http://brain.oxfordjournals.org/ Downloaded from
730 T.SHALLICE AND P.W.BURGESS Case 2 s head injury in a road traffic acciden em frontal depres dskull fracture and an intracerebral haematom nsive low at oeddnorhtre atrophy of the right medial i corex.Both later after stay of6 months he hanges but w unahle to carr it out.He failed a higher d but obtained a eacher's.For the next5yrs he held a succession of jobsfrom his wife's testimony were in ement over his domestic behaviour.He is untidy.He only bathes if going somewhere important.Shaving. ving his ed out when his v NesheprepaaionofamcalihsI0y,ods8.1Wa task she ome er.,his wife 50c1 th rela uld Clinical neuropsychological tests.D.N.was tested in the Nationa of neuropsychological ss On the WAIS,he obt ned a V bal IQ of 126 and a Pe and in the e 1).On memoryt PCasiiwetoftonitallotbclesionshispet ormance was ger satisfactory.but it was rather poo on of the Sel ory tes t(see Tab 3). while his performance on verbal mem memory tasks Case 3 ith slight let paralysis ness but as a result has had a p of her ss of smell DA CT scan carried out yrs after the oral ventricle For the past room.He very untidy ever ou and virtually never travels way from h hom tow Others always make a when any activity s to be carric for h weeken d could give no example anything.Her sister that these comptheprm Newdu Rdin Ver
730 T. SHALLICE AND P. W. BURGESS Case 2 D.N. a right-handed professional man, had sustained a serious head injury in a road traffic accident at the age of 26 yrs, involving a right frontal depressed skull fracture and an intracerebral haematoma treated surgically. He still has severe left hemiparesis. He says that consciousness was reduced or altered for 3 months. A CT scan carried out at age 48 yrs showed an extensive low attenuation area in the right frontal lobe and marked local atrophy of the right medial insular cortex. Both lateral ventricles were enlarged, the right more than the left. There were additional mild changes in the left frontal lobe. On leaving hospital after a stay of 6 months he returned to his previous employment but was unable to carry it out. He failed a higher degree but obtained a teacher's certificate. For the next 5 yrs he held a succession of jobs from most of which he was dismissed. His responses in a clinical interview and his wife's testimony were in agreement over his domestic behaviour. He is untidy. He only bathes if going somewhere important. Shaving, changing his clothes or undergarments, washing his hair and having his hair cut are only carried out when his wife tells him. He hardly ever spontaneously tackles any domestic chores such a laundry, cleaning, cooking, making repairs or paying bills. If his wife is out he normally leaves the preparation of a meal to his 10-yr-old son. When he shops he never makes out a list himself and also usually comes home without all the items on the list his wife prepares. When she gives him a task she has to specify exactly what is required and even so he might carry out some parts only and then starts reading a newspaper. In addition, his wife organizes all trips, outings and social contacts with relatives. His wife said that he was occasionally irresponsible over money; for instance, even though they were in financial difficulties as he was out of work, he would buy gadgets they did not really need, including a sophisticated music system, costing £500. Clinical neuropsychological tests. D.N. was tested in the National Hospital on a wide range of neuropsychological tests. On the WAIS, he obtained a Verbal IQ of 126 and a Performance IQ of 112, which may well be a little below his premorbid level but in fact corresponds well with the results of the National Adult Reading Test (Nelson, 1983) of 119. For all Verbal subtests he was in the superior range and in the Performance subtests in the average or bright average ranges (see Table 1). On memory tests he performed well with verbal material but poorly with visual material (see Table 2). On tests held to be sensitive to frontal lobe lesions his performance was generally satisfactory, but it was rather poor on the picture version of the Self-Ordered Memory test (see Table 3). In summary, D.N. performed well on a wide range of perceptual language and frontal lobe tests. However, while his performance on verbal memory tests was well within the normal range, it was impaired on visual memory tasks. Case 3 F.S., a 55-yr-old right-handed woman, employed in an undemanding post, as a 'media resources officer', had earlier sustained two separate head injuries. Thirty years before she had been thrown from a horse, had fractured her skull and had been left with a posttraumatic amnesia of unknown length. She was also aphasic at the time. The accident had left her with slight left-sided facial paralysis. Two years before being tested she had been knocked off her bicycle by a car and hit her head on the road; she did not lose consciousness but as a result has had a permanent loss of her sense of smell. A CT scan carried out 2 yrs after the second accident showed an extensive lesion to the left frontal lobe with atrophy causing enlargement of the frontal hom of the lateral ventricle. There was also some atrophy in the left temporal lobe. For the past 25 yrs she has worked in the same position. She lives by herself in a single room. Her responses in a clinical interview show that she undertakes virtually no inessential or novel activities. She is very untidy, never putting things away. She seldom goes out in the evening, and virtually never travels away from her home town. Others always make arrangements when any joint activity is to be carried out. She is said by her sister never to organize anything. She shops every day buying only a few things on any occasion and never visits supermarkets. She had no activity planned for the following weekend and could give no example where anyone had relied on her to do anything. Her sister confirmed that these behaviours were characteristic. Clinical neuropsychological tests. F.S. was tested at the National Hospital on a large range of neuropsychological tests. On the WAIS she obtained a Verbal IQ of 135 and a Performance IQ of 114 comparable with the estimate of the premorbid IQ of 127 derived from the New Adult Reading Test. Verbal by guest on April 8, 2016 http://brain.oxfordjournals.org/ Downloaded from
frontal LoBe DAMaGE 立 TABLE 2.PERFORMANCE ON TESTS OF MEMORY (SCALED SCORES) Tes 9 NT ayed aired A on (Sum)s 0 H04 IZM TABLE 3.PERFORMANCE ON FRONTAL LOBE'TASKS 3 Comment =17 Personal Orientation Test(errors) 8 14 =2.4s00_23 onal Cases 2 and 3 >1 SD than a lesion contro s(errors) group (me 20.1 7.321.0C 233 pnil 8.201 ls:m 15.725.649.0*Controis: n二29.6 34 33 Controls mean 34.8,SD 14.3 (n =30)2 6 6 6 Controls mean =5,SD 1.6 3 t Cont 0ys45,sD14 9.2,SD8.5(0=46:mean age M and Cole (1966).2 Nonlesio F0=14.9 and Le 1082,SD9 (1978) 40 10gtpostieriorlesionpatic ts(mean S10108 mean a 98 Scor a7.2 958.2M 8(dull average)). 1974 thy (se
FRONTAL LOBE DAMAGE 731 TABLE 2. PERFORMANCE ON TESTS OF MEMORY (SCALED SCORES) Cases Test Auditory Verbal Learning1 Complex Figure Recall1 Immediate Delayed Digit Span4 Paired Associates (Sum)5 Recognition Memory6 Words Faces Story Recall1 Immediate Delayed Visual Reproduction5 / 122 NT* 173 15 11 10 14 135 145 13 2 8 NT 3 3 15 NT 10 4 11 10 14 3 9 6 6 15 7 15 11 11 12 NT • NT = not tested. ' Coughlan and Hollows (1985). 2 Score on Worst Trial of Rey Auditory Verbal Learning Test (Rey, 1964). 3 Osterrieth (1944-1945). 4 Wechsler (1955). 5 Wechsler (1945). 6 Warrington (1984). TABLE 3. PERFORMANCE ON 'FRONTAL LOBE' TASKS Cases Comment Mean of controls = 3.0, SD 2.62 Mean of left frontal group = 11.9; normals = 1.7 Mean of right posteriors = 4.1, SD = 3.5 Mean of left posteriors = 2.4, SD = 2.7* Cases 2 and 3 > 1 SD worse than a lesion control group8 (mean = 5.9, SD 2.8) Control: mean = 23.3, SD = II 2 Controls: mean = 24.9, SD = 4.52 Controls: mean = 29.6 s, SD = 4.52 Controls mean = 34.8, SD = 14.3 (n = 30)12 Controls mean = 5, SD 1.6 Controls mean = 9.2, SD 8.5 (n = 46; mean age (yrs) 45, SD 14) * More than 2 SD worse than controls. ' Chorover and Cole (1966). 2 Nonlesion patient controls (n = 24, mean FSIQ = 114.9, SD 12.7): Shallice, Warrington, Watson and Lewis (unpublished study). 3 Shallice and Evans (1978). 4 Butters et at. (1972). 5 Semmes el al. (1963). 6 10 right posterior lesion patients (mean FSIQ 108.2, SD 9.8, mean age 45.7 yrs, SD 14.0) and 10 left posterior lesion patients (mean FSIQ 108.1, SD 12.2, mean age 41.8 yrs, SD 14.0). 7 Petrides and Milner (1982). 8 8 right posterior patients (mean FSIQ = 107.1, SD 8.9, mean age 45.5 yrs, SD 14.8. Mean Scaled Score FC Faces = 7.25, SD 4.8 (dull average)). 9 Perret (1974). 10 Shallice and McCarthy (see Shallice, 1982). " Reitan (1958). l2 Miller (1984). Note, however, that if Miller's formula for predicting fluency from WAIS verbal subtests is used, Cases 2 and 3 both fall below the expected range. l3 Nelson (1976). Alternation task1 (trial of last error) Bilateral hand movements Cognitive Estimates3 (error score) Money's Road-Map Test4 (errors) Personal Orientation Test5 (errors) Proverb Interpretation Self-Ordered Memory7 Representational Pictures (errors) Stroop9 (time) Tower of London (score)10 Trail Making: Letters and Numbers" (completion time in s) Verbal Fluency: Letters FAS, each 60 s (total retrieved) Modified Wisconsin'3 (categories achieved) Total errors / 90%ile Good 2 0 0 Good 7 20.1 33 15.7 70 6 3 2 75%ile Good 4 3 4 Good 10 17.3 23 25.6 34 6 3 3 5%Ue Good 5 5 14* Good 9 21.0 24 49.0* 33 6 1 by guest on April 8, 2016 http://brain.oxfordjournals.org/ Downloaded from
732 T.SHALLICE AND P.W.BURGESS Summary of patients Overall the I close to thei id level o la al me on some fronta tasks.All show severe organizationa difficulties in everyday life. NEUROPSYCHOLOGICAL TESTS Multiple subgoal scheduling tests which apply across all tasks The Six Element Test (SE).The purpose of this test,which is undertaken in a standard hospital office is to as s in enio e (5 min) tic problems and writ rithmetic problems c n0.8isg×4,n0.18is201+187-86 and no.28is29×8+(6×4). endix 1).The examiner the subject(S xplain nwhich stacks o E品a wed to do th tasks,and may influ the the way in which yo n sheet is then turned over and thes his recall of the rules.Am Two subsidi en removed,had nstructed to stop as cl .This time the stop watch time the E made no indication that they were to stop,and they were allowed to continue. yrs)
732 T. SHALLICE AND P. W. BURGESS subtests were all carried out at the Superior level. Visual subtests were carried out at the Bright Normal level except for Picture Arrangement which was at the average level. She had no aphasic difficulties and performed in the normal range on language and perceptual tests (see Table 1). Her performance on memory tests was mixed (see Table 2). However her pattern of spared/impaired performance, with difficulty on learning span +1 , which she was unable to do in 12 trials for both digits and spatial positions (Corsi span (see Milner, 1971)); also on the Rey Figure, in the context of spared Recognition Memory, Logical Memory and free recall suggests that she has a memory problem secondary to frontal difficulties (Signoret and Lhermitte, 1976). On tests thought sensitive to frontal lobe damage her performance was variable (see Table 3). On a number it was satisfactory, but on 4 tests it was impaired. Thus both memory and cognitive tasks showed evidence of frontal impairment. Summary of patients Overall the 3 patients perform well and close to their premorbid level on a wide range of perceptual, language and general cognitive tests. Case 1 has no problem with memory tasks but Case 2 has a primary visual memory impairment and Case 3 has difficulties on certain tasks of a 'frontal memory' type. Two of the patients perform very well on a wide range of tasks thought sensitive to frontal lobe lesions but 1 shows impairments on some frontal tasks. All show severe organizational difficulties in everyday life. NEUR0PSYCH0LOGICAL TESTS Multiple subgoal scheduling tests Two tests were developed to measure the ability of a subject to schedule the performance of a number of simple tasks when the demands made are rather open-ended and there are a number of simple rules which apply across all tasks. The Six Element Test (SE). The purpose of this test, which is undertaken in a standard hospital office, is to assess the ability of the patients to carry out 6 open-ended tasks in a fixed period of time (15 min) in a way that maximizes their overall score. The 6 tasks divide into 2 sets of 3—dictating a route, carrying out arithmetic problems and writing down the names of approximately 100 pictures of objects. Each set of arithmetic problems contains 35 problems generally of increasing difficulty. Thus in set A, no. 8 is 2^x4 , no. 18 is 201 + 187-86 and no. 28 is ^x 8 + (6x4). The 2 sets are equivalent in difficulty. The subject is presented with the instructions written on a card (see Appendix 1). The examiner (E) first reads through the complete test instructions with the subject (S), explaining which stacks of cards are piles A and B and which arithmetic set is I and II and so forth. Having read through the task descriptions the E says 'But before you go on, there are a number of important rules you must follow which govern the way you are allowed to do these tasks, and may influence the way in which you decide to organize the way you do the test'. The 5 rules are read through with the S and explained as fully as necessary. The instruction sheet is then turned over and the S is 'tested' on his recall of the rules. Any errors are corrected. If she/he has forgotten any, the entire rules are read through and then the S is tested again. This procedure is repeated until all the rules are recited correctly. It is explained to the S that the instructions will be left in front of them at all times to consult at will. Two subsidiary tests were also undertaken. First, the subjects, whose watches had been removed, had to carry out the Digit Symbol subtest of the WAIS, stopping themselves after 1 min 15 s. A stop watch was visible throughout. Secondly, Rey's (1964) Tangled Lines test had to be carried out with the subjects instructed to stop as close as possible to 2 min 30 s after starting. This time the stop watch was covered by a small cardboard box. The box could be moved whenever the subjects wanted to know the time but had to be immediately replaced. With both these tests, were the Ss not to stop themselves at the appropriate time the E made no indication that they were to stop, and they were allowed to continue. Controls. 10 control subjects were tested. They were matched to the patients on age (mean 41, range 25-6 2 yrs), educational background, and NART IQ (mean 120.2, range 113-127 yrs). by guest on April 8, 2016 http://brain.oxfordjournals.org/ Downloaded from
FRONTAL LOBE DAMAGE 733 TABLE 4.PERFORMANCE ON THE SIX ELEMENT TASK Case 44 3(+2 incorrect) Controls 5.7(±0.5) 5.35(±0,53) ad cotrolandal pe more time on their ubtas they nmpedforongest6ee Table 4). o ontask.but in fac only atter oted 2 subasks On his only 4 of the subtask ent much longer than an over min Oparate periods of the subta sks (maths 1)without e trying its complem entary only 14 s and 20 s on hem-instead of w them down:no norm al subject carned out a subtask 0n6 f subtask er another part I;th she correctly applie Case 3,on her first atte .0 nly tackle 3 subta switch tasks well on both (1.5 m stop at I min 15 s.On the econd task his perform was very poo d.ch on med well on the 25 min ta min 15 s). on the more difficu min task she did not st stop until 3 min 2 0s had passe .201 Comment s of perfor ance on the eof this ation ere min which has subc cur. eem ably de for son the Q level and cultural background of e patients.While still inside the ital the patient is giver nth n after starti of information have to be obtained and writte oa postcard,namely:(1)the nam o the shop in the stre the (d)th the price
FRONTAL LOBE DAMAGE 733 TABLE 4. PERFORMANCE ON THE SIX ELEMENT TASK Max. time on any sublask Case No. of subtasks tackled (min, s) 1 (I) 2 7,30 1 (II) 4 6,19 2(1) 5 10,11 2 (II) 3(+2 incorrect) 6,22 3 (I) 3 7,18 3 (II) 2 9,30 Controls 5.7 (±0.5) 5,35 (±0,53) Results. Two measures of task performance are shown in Table 4. Two different attempts were made by each patient, at least 3 wks apart. On the first attempt Cases 1 and 3 tackled less subtasks than any control and all 3 spent more time on their subtask they attempted for longest (see Table 4). Qualitatively the behaviour of the patients was also atypical. On his first attempt A.P. made notes for over 4 min to help with the dictation task, but in fact never dictated at all. He only attempted 2 subtasks, the second of these occupying the last 7.5 min. On his second attempt he tackled only 4 of the subtasks claiming that he did not dictate his journey back as he had not decided where he would go when he would leave the hospital! Case 2 succeeded in tackling 5 subtasks but spent much longer than any normal subject— over 10 min in 3 separate periods—on 1 of the subtasks (maths I) without ever trying its complementary task (maths II). On his second attempt he behaved bizarrely, changing task 63 times (mean task changes of controls 5.7, SD 2.19) and dictating the two sets of picture names—spending only 14 s and 20 s on them—instead of writing them down; no normal subject carried out a subtask incorrectly. Also on 6 occasions he carried out a subtask immediately after the complementary one, so breaking one of the rules. (One control also made this error. She said she had mistaken the rule as not doing a part I of a pair of subtasks after another part I; this she correctly applied.) Case 3, on her first attempt, only tackled 3 subtasks. On the second she wrote her journey instead of dictating it, attempted only 2 other subtasks and spent the last 9 min on just 1 of them. During this time she looked at the stopwatch on 7 occasions but did not switch tasks. On the 2 timing tasks Case 1 performed well on both (1.5 min, stopped 1 min 17 s; 2.5 min, stopped 2 min 28 s). Case 2, however, failed the first, stopping at 1 min 38 s although being fully aware he had to stop at 1 min 15 s. On the second task his performance was very poor on both testing occasions. On the first attempt he stopped after 1 min 37 s, saying that he thought 2 min 45 s had elapsed and on his second he failed to stop until 3 min 26 s had elapsed. Case 3 performed well on the 1.25 min task (stopping at 1 min 15 s). However, on the more difficult 2.5 min task she did not stop until 3 min 20 s had passed, despite having looked at the watch at 2 min 38 s. No control was more than 1 s out on the first task or more than 5 s out on the second. (Mean time out for task 1, 0.1 s, SD 0.3; task 2, mean 2.9 s, SD 2.0). Comment All 3 patients performed at below the normal range on quantitative measures of performance on the Six Element task. In addition their performance was also qualitatively atypical. Multiple Errands Test (ME). The purpose of this test, which is undertaken in a pedestrian precinct near the hospital previously unknown to the patients, is for them to carry out a number of tasks in situations where minor unforeseen events can occur. The subtasks the patients had to carry out are basically very simple except for one, which has subcomponents designed to be reasonably demanding for someone of the IQ level and cultural background of the patients. While still inside the hospital the patient is given a card with 8 tasks written on it, 6 of which are simple (e.g., buy a brown loaf, buy a packet of throat pastilles). A seventh requires the subject to be at a certain place 15 min after starting. An eighth is more demanding, 4 sets of information have to be obtained and written on a postcard, namely: (1) the name of the shop in the street likely to have the most expensive item; (2) the price of a pound of tomatoes; (3) the name of the coldest place in Britain yesterday; and (4) the rate of the exchange of the French franc yesterday. by guest on April 8, 2016 http://brain.oxfordjournals.org/ Downloaded from
734 t.SHALLICE AND P W.BURGESS The card also conains the following instructions:You are to spend as lit money as possible (within nd take as lit time as possi y o shop sho are not to anything not bought on the street (other than a watch)to assist you.You may do the tasks d nart of the ins ken th rt distance to a s hopping prec er he or she s as al rge street ending in the pedestr onend and lights e oth e be Nine c Resuls.Table s gives the numberruced by each of the patients.Each produced at SDs more t han the controls in the a e boundaries or leaving a shop with a newspaper without paying tthe info cand rather than the postcard:( either not carried out or not completed satisfactorily. TABLE 5.ERRORS ON MULTIPLE ERRANDS Cases 8 Task failu n failures 12 2 More than 2 SD worse than the control subjects. 一 and on the numbe The in the rate of error qed was place the back he instructron shee which by hen she br hop wit em t h utbuying anything)because when in the hop (a 11 she foundt the task was ting.Cases I and 2 both became ing he ne the previous day's aper.They had,so he walked out with it,incidentally breaking the buy ing rule He was pursue into the street by the shopkeepe e paid for it.A.H d just assumed th ors shop simply k about the location of that ype of shop (b He
734 T. SHALLICE AND P. W. BURGESS The card also contains the following instructions: 'You are to spend as little money as possible (within reason) and take as little time as possible (without rushing excessively). No shop should be entered other than to buy something. Please tell one or other of us when you leave a shop what you have bought. You are not to use anything not bought on the street (other than a watch) to assist you. You may do the tasks in any order.' This second part of the instructions—the 'rules'—is then read aloud to the patient who is asked to repeat them. If the rules cannot all be repeated satisfactorily the procedure is repeated until they can be. The subject is then taken the short distance to a shopping precinct where he or she is asked to repeat the rules again. If there is any failure to reproduce the gist of any instruction the subject is reminded of it. It is then indicated to the patient where the limits of the test area are; they are very clearly demarcated by a large street ending in the pedestrian precinct at one end and a set of traffic lights at the other. The behaviour of the subjects while carrying out the activity is monitored by 2 observers and they are also debriefed after the task had been completed. Controls. Nine control subjects were tested. They were matched with the patients for age (mean 40, range 24-63 yrs) and NART IQ (mean 122, range 113-127). Results. Table 5 gives the number of errors produced by each of the 3 patients. Each produced at least 2 SDs more than the controls. Table 5 also shows the errors broken down into subcategories: (1) inefficiencies—where a more effective strategy could have been applied, e.g., entering the same shop more than once; (2) rule breaks—where a specific rule (either social or explicitly mentioned in the task) is broken, e.g., going outside the boundaries or leaving a shop with a newspaper without paying; (3) interpretation failure—where the requirements of a particular task are misunderstood, e.g., assuming that the information must be written on the birthday card rather than the postcard; (4) task failure—a task either not carried out or not completed satisfactorily. TABLE 5. Inefficiencies Rule breaks Interpretation failures Task failures Total errors ERRORS ON / 6* 5* 1 0 12* MULTIPLE Cases 2 9* 8* 1 5* 23* ERRANDS 3 5* 8* 1 4* 17* Control 1.4(1.1) 1.6(1.3) 0.4 (0.7) 1.1 (1.4) 4.6(2.1) * More than 2 SD worse than the control subjects. All 3 patients performed at the 5% level or worse, as estimated from the control data, on both the number of inefficiencies and on the number of rule breaks. There was no difference overall in the rate of errors of the other two types, although Case 3 produced more task failures. Thus 2 normal controls as well as the patients failed to provide the required information on the postcard, probably because the information required was placed on the back of the instruction sheet. Qualitatively the performance of the patients was even worse. They made types of error which were not produced by any control. Case 3 used a clearly irrelevant criterion inappropriately when she broke a rule (entering a shop without buying anything) because when in the shop (a chemist) she found it did not have a soap she especially liked; other cheap soap—which would have been at least as adequate for the task— was available. She also failed to note the time when starting. Cases 1 and 2 both became involved in social complications. Case 1 made the interpretative error of deciding he needed yesterday's newspaper (to find the coldest place in Britain on the previous day). He entered a newsagents and asked if they had the previous day's paper. They had, so he walked out with it, incidentally breaking the buying rule. He was pursued into the street by the shopkeeper who wanted to be paid for it. A.P. had just assumed that because a previous day's newspapers are generally worthless he could have one without paying. Case 2 produced a complex set of errors. Thus one series of actions began with his being the only subject to enter a shop simply to ask about the location of another type of shop (breaking buying rule). He was referred to a shop outside the allowed area, went to that shop (breaking the limit rule) and became involved in by guest on April 8, 2016 http://brain.oxfordjournals.org/ Downloaded from
FRONTAL LOBE DAMAGE 735 DISCUSSION We have described 3 patients,each of whom had sustained head injuries in which the area of focal damage lay in frontal regions.The 3 patients performed well on those cognitive tests which were not designed to load specifically on 'frontal functions'.On 'frontal'tests their performance varied.Case 3 performed poorly on a number of such tests.A second(Case 2)performed generally satisfactorily except for a borderline impairment on the Petrides and Milner Self-Ordered Memory.The third (Case 1) performed very satisfactorily on all standard 'frontal'tests.In daily life,however,all 3 appeared unable to act effectively on their own initiative as they organized virtually no nonroutine activities.In addition 2(Cases 1,2)were reported to have problems in carrying out multiple subgoal tasks such as shopping and the third (Case 3)avoided such activities These difficulties were mirrored in the 2 tests where they had to perform multiple activities,the Six Element Test and Multiple Errands.The 2 tasks required the subject to carry out a number of fairly simple activities in an efficient manner.One,the Six Element,basically involved the devising of a simple plan,scheduling the subtests efficiently and keeping a check on time.The second involved dovetailing the activities in a more real-life setting where minor unforeseen events could occur.All 3 patients performed both quantitatively and qualitatively worse than the normal controls. If one considers what is involved in carrying out these multiple subgoal tasks,then at a very general level,four basic types of process are relevant.Motivational and memory processes are clearly required and so are a variety of special-purpose cognitive processes of the sort that standard neuropsychological tests assess.In addition there are certain bridge processes which enable the special-purpose cognitive processes to be used to satisfy motivational requirements.A deficit in basic special-purpose cognitive processes pnl 8. seems an implausible explanation of their difficulties on the experimental tasks,given the performance of the patients on the baseline tests.Indeed the most difficult Multiple Errands subtest gave problems for some of the controls as well as the patients;it was the least sensitive part of the procedure.However,frontal patients often manifest inappropriate affect and have frequently been described as apathetic or impulsive(Blumer and Benson,1975),and also they can have memory problems (e.g.,Hecaen,1964) The possibility of motivational or memory difficulties therefore needs to be considered, especially as the patients,when asked to account for some action,often said that they had completely forgotten their prior intention. A possible motivational explanation of the impaired performance of the 3 patients is that they require continuous social reinforcement to carry out psychological tasks, and without it their spontaneous motivation would tend to dwindle rapidly;without it they do not persevere.This account is unsatisfactory.Case I was given the entire AH6 followed by the Watson-Glaser Critical Thinking Appraisal (Watson and Glaser,1980)
FRONTAL LOBE DAMAGE 735 a heated argument with a shop assistant as he asked her to give him a birthday card free (which would have also broken the buying rule)! Comment As with the Six Element task, all 3 patients had quantitatively impaired performance, in particular as far as rule breaks and inefficiencies were concerned. Their performance was also qualitatively unusual. DISCUSSION We have described 3 patients, each of whom had sustained head injuries in which the area of focal damage lay in frontal regions. The 3 patients performed well on those cognitive tests which were not designed to load specifically on 'frontal functions'. On 'frontal' tests their performance varied. Case 3 performed poorly on a number of such tests. A second (Case 2) performed generally satisfactorily except for a borderline impairment on the Petrides and Milner Self-Ordered Memory. The third (Case 1) performed very satisfactorily on all standard 'frontal' tests. In daily life, however, all 3 appeared unable to act effectively on their own initiative as they organized virtually no nonroutine activities. In addition 2 (Cases 1, 2) were reported to have problems in carrying out multiple subgoal tasks such as shopping and the third (Case 3) avoided such activities. These difficulties were mirrored in the 2 tests where they had to perform multiple activities, the Six Element Test and Multiple Errands. The 2 tasks required the subject to carry out a number of fairly simple activities in an efficient manner. One, the Six Element, basically involved the devising of a simple plan, scheduling the subtests efficiently and keeping a check on time. The second involved dovetailing the activities in a more real-life setting where minor unforeseen events could occur. All 3 patients performed both quantitatively and qualitatively worse than the normal controls. If one considers what is involved in carrying out these multiple subgoal tasks, then at a very general level, four basic types of process are relevant. Motivational and memory processes are clearly required and so are a variety of special-purpose cognitive processes of the sort that standard neuropsychological tests assess. In addition there are certain bridge processes which enable the special-purpose cognitive processes to be used to satisfy motivational requirements. A deficit in basic special-purpose cognitive processes seems an implausible explanation of their difficulties on the experimental tasks, given the performance of the patients on the baseline tests. Indeed the most difficult Multiple Errands subtest gave problems for some of the controls as well as the patients; it was the least sensitive part of the procedure. However, frontal patients often manifest inappropriate affect and have frequently been described as apathetic or impulsive (Blumer and Benson, 1975), and also they can have memory problems (e.g., Hecaen, 1964). The possibility of motivational or memory difficulties therefore needs to be considered, especially as the patients, when asked to account for some action, often said that they had completely forgotten their prior intention. A possible motivational explanation of the impaired performance of the 3 patients is that they require continuous social reinforcement to carry out psychological tasks, and without it their spontaneous motivation would tend to dwindle rapidly; without it they do not persevere. This account is unsatisfactory. Case 1 was given the entire AH6 followed by the Watson-Glaser Critical Thinking Appraisal (Watson and Glaser, 1980) by guest on April 8, 2016 http://brain.oxfordjournals.org/ Downloaded from
736 T.SHALLICE AND P.W.BURGESS and left to work through them on his own.He scored at the 50th and 80th percentiles respectively,the total of the task times being 2 h.Both Cases 2 and 3 carried out the long form of Raven's Matrices working through the test on their own.This took them 31 and 42 min,respectively-less than the 45 min that Raven et al.(1977)give as the upper limit of the normal range and yet longer than the 2 multiple-subgoal scheduling tests would normally take.They scored at above the 95th and 80th percentiles, respectively,for their ages on the Matrices. For the Six Element task a motivational explanation has in any case little immediate face validity.It requires little effort to switch from one simple task to another.More critically,Cases 2 and 3,the subjects for whom a motivational explanation is most plausible on clinical grounds,made errors analogous to the ones made on the Six Element task on an even simpler timing task.When they had to stop carrying out a perceptuomotor task after 2.5 min with no external timing signal but a stopwatch available,they continued after the time limit.Lack of perseverance-the motivational explanation being considered-should presumably not lead to overshoot!Thus motivational factors do not seem likely to be central to their deficit. Standard retrospective memory processes are also relevant,at least for carrying out the Multiple Errands test where retaining both the layout of the street and the instructions without using the card,would be helpful.The patients differed in this respect.Case I had no difficulties.Case 2 was entirely normal on verbal memory tasks but had visual memory problems which might have affected his performance of the Multiple Errands test;however,they would seem most unlikely to contribute to his difficulty with the Six Element task where there is no spatial memory load and where the instructions are continuously clearly visible on the desk.Case 3 had problems on some memory tasks but these were all in tasks where active organization of the input is required for adequate memory performance and her difficulties appear secondary to her frontal lobe problems (see Signoret and Lhermitte,1976).She was able to carry out memory tasks where the organization was provided for her and in particular she retained text normally,as indicated by her satisfactory performance on Logical Memory where the amount she retained showed no decline over an hour's delay.Like the other patients,she was able to recite correctly the instructions for the tasks in her own words after they had been presented to her.This makes it most unlikely that retrospective memory difficulties on April 8 lie at the root of her problems,at least on the Six Element test given that the problems these 3 patients exhibit on these multiple subgoal tests do not fit well with an ass mption of basic motivational impairments on the one hand or of special purpose cognitive or retrospective memory processes on the other,do they fit with impairments to the bridge processes that lie between the two?To assess this it is necessary to consider the bridge proce sses in more detail These process es lie in the domain of the creation and maintenance of goals and intentions of their realization at a oriate times(prospective memory(Meacham and Leiman.1982:Kvavilashvili.1987))and of plan ing.This is an area where well developed theories are lacking.How er a nosition develor ed hy one of us in collaboration with D.A.Norman is that where a task cannot be adequately carried out through the application of well-learned action or thought routines alone,it requires the use of a Supe rvisory System,which is anteriorly located in the cortex (Nor rman and Shallice,1980,1986: also Shallice,1988).We will provisionally follow this approach
736 T. SHALLICE AND P. W. BURGESS and left to work through them on his own. He scored at the 50th and 80th percentiles, respectively, the total of the task times being 2 h. Both Cases 2 and 3 carried out the long form of Raven's Matrices working through the test on their own. This took them 31 and 42 min, respectively—less than the 45 min that Raven et al. (1977) give as the upper limit of the normal range and yet longer than the 2 multiple-subgoal scheduling tests would normally take. They scored at above the 95th and 80th percentiles, respectively, for their ages on the Matrices. For the Six Element task a motivational explanation has in any case little immediate face validity. It requires little effort to switch from one simple task to another. More critically, Cases 2 and 3, the subjects for whom a motivational explanation is most plausible on clinical grounds, made errors analogous to the ones made on the Six Element task on an even simpler timing task. When they had to stop carrying out a perceptuomotor task after 2.5 min with no external timing signal but a stopwatch available, they continued after the time limit. Lack of perseverance—the motivational explanation being considered—should presumably not lead to overshoot! Thus motivational factors do not seem likely to be central to their deficit. Standard retrospective memory processes are also relevant, at least for carrying out the Multiple Errands test where retaining both the layout of the street and the instructions, without using the card, would be helpful. The patients differed in this respect. Case 1 had no difficulties. Case 2 was entirely normal on verbal memory tasks but had visual memory problems which might have affected his performance of the Multiple Errands test; however, they would seem most unlikely to contribute to his difficulty with the Six Element task where there is no spatial memory load and where the instructions are continuously clearly visible on the desk. Case 3 had problems on some memory tasks but these were all in tasks where active organization of the input is required for adequate memory performance and her difficulties appear secondary to her frontal lobe problems {see Signoret and Lhermitte, 1976). She was able to carry out memory tasks where the organization was provided for her and in particular she retained text normally, as indicated by her satisfactory performance on Logical Memory where the amount she retained showed no decline over an hour's delay. Like the other patients, she was able to recite correctly the instructions for the tasks in her own words after they had been presented to her. This makes it most unlikely that retrospective memory difficulties lie at the root of her problems, at least on the Six Element test. Given that the problems these 3 patients exhibit on these multiple subgoal tests do not fit well with an assumption of basic motivational impairments on the one hand or of special purpose cognitive or retrospective memory processes on the other, do they fit with impairments to the bridge processes that lie between the two? To assess this it is necessary to consider the bridge processes in more detail. These processes lie in the domain of the creation and maintenance of goals and intentions, of their realization at appropriate times (prospective memory (Meacham and Leiman, 1982; Kvavilashvili, 1987)) and of planning. This is an area where well developed theories are lacking. However, a position developed by one of us in collaboration with D. A. Norman is that where a task cannot be adequately carried out through the application of well-learned action or thought routines alone, it requires the use of a Supervisory System, which is anteriorly located in the cortex (Norman and Shallice, 1980, 1986; see also Shallice, 1988). We will provisionally follow this approach by guest on April 8, 2016 http://brain.oxfordjournals.org/ Downloaded from