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