Neurocase (2001) Vol. 7, pp. 383–389

© Oxford University Press 2001

Executive Amnesia in a Patient with Pre-frontal Damage due to a Gunshot Wound Ricardo de Oliveira-Souza, Jorge Moll, Fernanda Tovar Moll and Dayse L. Gusma˜o de Oliveira Neuroimaging and Behavioral Neurology Group (GNNC), LABS-Rede D’Or, Rua Pinheiro Guimara˜es, 22/4° andar, Botafogo, Rio de Janeiro 22281-080, Brazil

Abstract This paper reports the case of a young patient with extensive pre-frontal damage in whom we tested the hypothesis that intensive training improves executive performance as assessed by the Wisconsin Card Sorting Test (WCST). As long as her declarative memory, complex perceptual abilities and global cognitive status were spared, we surmised that any deficit in executive learning would have occurred in relative isolation. We showed that her abnormal performance on the WCST, both on the standard as well as on the post-instruction condition, was due to an impairment of shifting attention across perceptual dimensions (extra-dimensional). In contrast, her ability to shift attention within perceptual categories (intra-dimensional) was spared, as were her declarative memory, object and visuospatial perception, oral language comprehension and praxis (ideomotor, tool use and constructional). This case supports the hypothesis that executive amnesia is a type of amnesic disorder distinct from the classic amnesic syndrome due to mamillotemporomedial damage. As such, it is probably closely related to procedural learning and may depend on the same fronto-subcortical loops that mediate the actual execution of behaviour.

Introduction Previous work on neuropsychiatric patients arrived at conflicting results as to the possibility of remediation of deficits on the Wisconsin Card Sorting Test (WCST) (Oliveira et al., 1999). This issue, which has obvious implications for the rehabilitation of brain-damaged patients, has been complicated by modifications of the original task in several ways and by the fact that most studies have concentrated on patients with schizophrenia (Goldberg and Weinberger, 1994). More recently, the ability to shift attention across and within perceptual dimensions has been implicated as a major mechanism underlying normal performance on the WCST (Roberts et al., 1988; Rogers et al., 2000). According to this view, an impairment of the ability to shift attention across categories (extra-dimensional) gives rise to perseverative responses, whereas an impairment of the attentional mechanisms that promote the perceptual adherence to the categories of colour, form or number (intra-dimensional), leads to failures to maintain set (Pantelis et al., 1999). We had a unique opportunity to probe the effects of intensive instruction and the role of the frontal lobes on executive learning in a young patient with a long-standing pre-frontal injury, whom we have followed during the past 10 years with structured behavioural observations and serial neuropsychological testing. Qualitative analyses also offered

new insights into the mechanisms of failure on the WCST and how they may relate to an abnormality of those mechanisms that regulate attentional shifting within and across perceptual categories.

Clinical presentation An 18-year-old right-handed girl (SR) was brought in by her parents for neuropsychiatric evaluation and rehabilitation in 1991. Five years previously, following an argument with her boyfriend, she shot herself in the head with a 32-calibre handgun. At the clinical interview, she recalled aiming the revolver at her right temple and pulling the trigger. She immediately lost consciousness and remained unresponsive for a few weeks. As she recovered, she began to experience episodes of absence and automatisms which have been successfully controlled with carbamazepine (400 mg/day) ever since. SR comes from an affluent family, is the third of five daughters and was described as a gifted student. There was evidence from history of severe depression and suicide attempts in other family members. After the accident, SR would never initiate conversation and tended to stay still or walk around aimlessly. She needed moment-to-moment prompting and cueing in daily chores,

Correspondence to: R. de Oliveira-Souza, Grupo de Neuroimagem e Neurologia do Comportamento, LABS-Rede D’Or, Rua Pinheiro Guimara˜es, 22/4° andar, Botafogo, Rio de Janeiro 22281-080, Brazil. Tel: ⫹55 21 284 1789; Fax: ⫹55 21 571 4435; e-mail: [email protected]

384 R. de Oliveira-Souza et al.

otherwise she became unconcerned and sloppy. She developed voracious eating and gained 15 kg since the first consultation, despite vigorous attempts to restrict her food intake. Her behavioural repertoire became restricted to those actions that suffice to accomplish her immediate needs. Because of this, her actions are often left unfinished. Thus, she usually leaves damp towels on the floor after she has dried herself off and, unless closely supervised, she does not flush the toilet or turn off the tap after she has washed her hands. Urinary incontinence is common. During the past 5 years her drug schedule has been stable, including carbamazepine, sertraline (100 mg/day) and bromocriptine (25 mg/day). Despite the fact that she followed a regular occupational programme in well-structured environments 5 days a week, social and cognitive progress during this period was never obvious to the medical staff. However, her relatives’ impression that she has steadily improved was supported on several different occasions by a drastic worsening of the abulic state when we attempted to withdraw gradually either sertraline or bromocriptine. Her clinical examination has changed little since we first met her. She is awake and oriented, but seldom initiates conversation or goal-directed activities. Her replies are coherent, but made up of only one to three words. She does not scan the environment with her eyes. Her face is expressionless and her voice is devoid of both emotional and grammatical prosody, even if the conversation turns to the suicide attempt. However, her ability to experience emotions, such as sadness or joy, ‘did not change at all’. Remains of emotion consist of a vocal-motor display commonly seen among surfers to indicate content and excitement (she was an avid surfer before the accident). Such stereotypes are context-congruent (for example, when her mother concedes to take her to the movies when the consultation is over). Intermittent interruption of behaviour and speech is frequent and most evident on tasks that demand attentional effort. Her demeanour is childish and she has little concern for social appropriateness. Some of her actions convey sexual intentions. For example, on one occasion she wrote ‘I want to f_ _ _’ on the writing item of the Mini-Mental State Examination (MMSE). SR can pantomime the use of common tools and utensils and execute complex actions following verbal or gestural commands. However, she needs much prompting to comply with the examiner and her actions soon fade away. She does not have hemispatial neglect or sensory extinction. She recognizes and names objects by sight or active touch. She has a left spastic hemiparesis that does not prevent her from walking or using the hands in writing and dressing. Sensation is intact. Tendon jerks are globally hyperactive with bilateral foot clonus. An extensor plantar response is easily elicited on the left side. Magnetic resonance imaging revealed a bilateral and grossly symmetric injury occupying the frontal lobes (Fig. 1). It included Brodmann’s area (BA) 6, 8, 9, 10, 11, 24, 25, 32, 44, 45, 46 and 47 (Damasio and Damasio, 1989). On

T2-weighted images the area of signal abnormality extended posteriorly through the white matter up to the central sulcus (BA 4). There was partial bilateral sparing of regions caudal to the axial plane of the genu of the corpus callosum, including areas 24, 32 and 12, as well as the temporal stem and pole, amygdala, hippocampus and parahippocampal gyrus. There was a small area suggestive of gliosis in the right temporal pole (BA 38) and in the left superior parietal lobule. Small areas of abnormal signal were present in the subcortical white matter of the occipital and temporal lobes. The corpus callosum was markedly thinned throughout its extent. The third and lateral ventricles were notably enlarged, especially at the frontal horns. The thalamus and striatum were bilaterally intact up to the level of the nucleus accumbens. On MR angiography, the intracranial course and flow of the major branches of the carotid and vertebro-basilar systems were normal.

Materials and methods Neuropsychological assessment During the follow-up period, SR underwent repeated neuropsychological evaluations. Here we report her performance on a subset of the tests employed in these evaluations.

WCST procedures To verify the hypothesis that SR could learn how to do the WCST, we investigated her performance several times after she received explicit instructions. To this aim, the 128-card version of the WCST was first administered as a simple verbal–visual matching task (the open key, or ‘OK’, condition), for which the examiner asked her to match the stimulus cards for colour, form and number in that order. Following 10 consecutive correct sorts, the examiner informed her that the matching criterion had changed and of the new criterion at play from then on. If she made an error, the examiner reminded her of the correct principle, otherwise he just said ‘right’ or ‘wrong’ in response to each sort. The basic procedure was repeated once, so that the three categories of colour, form and number were completed twice. Because the correct matching principle was not pronounced by the examiner on a card-by-card basis, the OK administration was ideally suited to probe intra-dimensional attentional shifts, because the perceptual dimension ruling each sort was supposed to bias the sorting choice at the expense of all other perceptual dimensions. As soon as the OK procedure was over, SR was administered the standard test (the postopen key, or ‘pOK’, condition). The OK/pOK procedure was repeated 16 times. The standard test was administered 20 times, in seven of which it preceded the OK condition without delay. The three conditions (standard, OK and pOK) were scored according to standard guidelines (Heaton et al., 1995). Three indexes were obtained for each condition (Rogers et al., 2000): categories completed (a measure of overall

Executive amnesia following a gunshot wound 385

Fig. 1. Magnetic resonance imaging scans showing a bilateral and grossly symmetric injury occupying the frontal lobes.

success), perseverative errors, and set failures (a measure of the ability to maintain a pattern of response to a salient stimulus attribute, such as colour, at the expense of others). We hypothesized that if learning did take place, performance on the pOK condition would be superior to that of the standard performance. Global cognitive status was assessed with the MMSE (Folstein et al., 1975). The Enhanced Cued Recall Test (ECRT) was administered as a measure of genuine memory (Grober et al., 1988). By semantically tagging the stimuli, the ECRT controls for the encoding of new information and gives separate scores for memory encoding and recall. It is sensitive to the effects of medial temporal damage and is typically abnormal in conditions in which the amnesic syndrome is a major feature (Golomb et al., 1994). Language comprehension, complex visual perception and praxis were evaluated with the Token Test (De Renzi and Faglioni, 1978), and the Facial Recognition Test, Judgement of Line Orientation and the Three-dimensional Block Construction Test (Benton et al., 1994).

Statistical analysis Data were analysed following the N ⫽ 1 single case design (Motulsky, 1995). WCST standard, OK and pOK scores were

compared with repeated measures analyses of variance. The significance of mean differences was assessed post hoc with Scheffe´ ’s test. The patient’s individual test scores were compared with those of a sample of 27 normal controls gathered from our normative neuropsychological database. The age and level of education of the normal controls ranged from 18 to 39 years (mean ⫽ 23 ⫾ 6 years) and from 9 to 14 years (mean ⫽ 11 ⫾ 1.3 years), respectively. Statistical comparisons were performed with a modified t-test for independent samples (Crawford and Howell, 1998). This procedure is particularly suited for testing the hypothesis that a single observation differs significantly from the mean of a control sample, especially when this sample’s size is small, that is, when it includes fewer than 30 subjects. A 0.05 level of significance, two-tailed, was set for all tests (Welkowitz et al., 1991).

Results The WCST results are shown in Table 1. Instructions did not essentially change the profile of performance on the WCST (Table 2). Yet, the patient was always able to point correctly to the matching principles at the end of each testing session; that is, she exhibited the classical pattern of verbal–behavioural

386 R. de Oliveira-Souza et al. Table 1. Results of Wisconsin Card Sorting Test (WCST) administration in the standard (std), open key (OK) and post-open key (pOK) conditions (abnormal scores are marked with an asterisk) Date 1992 1994 1995

1996 1997 1998 1999

2000

2001

8 December 29 December 25 November 5 May 5 May 5 May 30 June 13 November 5 January 28 April 14 July 12 August 12 August 5 January 21 June 21 June 21 June 27 August 27 September 29 November 22 December 22 December 11 January 11 January 11 January 30 March 30 March 31 March 31 March 3 April 3 April 5 April 5 April 6 April 6 April 10 April 10 April 12 April 12 April 3 May 24 November 24 November 24 November 11 December 11 December 11 December 2 January 2 January 2 January 2 May 2 May 2 May

Condition

Categories

Perseverative errors

Failures to maintain set

std std std std OK pOK std std std std std OK pOK std std OK pOK std std std OK pOK std OK pOK OK pOK OK pOK OK pOK OK pOK OK pOK OK pOK OK pOK std std OK pOK std OK pOK std OK pOK std OK pOK

1* 2* 2* 3* 6 3* 4* 4* 3* 1* 4* 6 1* 2* 0* 6 2* 3* 4* 4* 6 3* 1* 6 3* 6 2* 6 2* 6 5* 6 4* 6 5* 6 3* 6 3* 4* 0* 6 1* 0* 6 3* 1* 6 1* 4* 6 4*

86* 66* 71* 57* 0 61* 50* 44* 44* 32* 36* 0 31* 66* 96* 1 15* 18* 44* 27* 0 31* 21* 0 18* 0 39* 0 35* 1 23* 1 52* 1 21* 0 34* 0 42* 10 74* 0 76* 92* 0 65* 64* 0 88* 21* 0 26*

1 1 0 0 0 0 1 0 1 4* 1 0 4* 0 0 0 4* 3 0 1 1 2 3 0 5* 1 3 0 2 1 2 0 0 1 2 0 3 0 1 7* 0 0 1 0 0 0 1 0 0 1 0 1

dissociation. Poor performance on the WCST standard and pOK conditions stood in sharp contrast with performance on the other tasks, including the WCST OK condition. Memory encoding and cued recall were intact, as were complex visual perception, language comprehension and constructional praxis (Table 3). However, free recall, immediate and delayed, was also impaired. Table 3 also shows that neuropsychological performance across time was rather stable. Comparisons of SR’s test scores with those of the normative sample showed that the large majority of her standard and

pOK WCST categories and perseverative error scores were abnormal. In contrast, the number of set failures on most trials was within the normal range. Finally, our patient’s age and education were not significantly different from those of the controls (P ⬎ 0.14).

Discussion The main finding of this study was that instructions did not improve executive performance on the WCST. This improve-

Executive amnesia following a gunshot wound 387 Table 2. Results of performance (means ⫾ standard deviations) on the three Wisconsin Card Sorting Test (WCST) conditions

Categoriesa (艋 5) Perseverative errorsb (艌 16) Set failuresc (艋 3)

Standard (std)

Open key (OK)

Post-open key (pOK)

Statistical comparisonsd

2.3 ⫾ 1.5 52 ⫾ 25 1.3 ⫾ 1.8

6.0 ⫾ 0 0.2 ⫾ 0.4 0.3 ⫾ 0.5

2.7 ⫾ 1.3 42 ⫾ 22 1.9 ⫾ 1.6

std µ pOK ⫽ OK ⫽ std std µ pOK ⫽ OK ⫽ std std µ pOK ⫽ OK µ std

aF (2,46) ⫽ 43.80; P ⫽ 0.0001. bF (2,46) ⫽ 31.04; P ⫽ 0.0001. cF (2,46) ⫽ 4.88; P ⫽ 0.012. dSignificantly different means (P

⬍ 0.05) are indicated by the symbol ⫽; non-significant differences are indicated by the symbol µ. Scheffe´ ’s test was employed in all post hoc comparisons. Cut-off scores, derived from our normative sample (n ⫽ 27) according to Crawford and Howell’s (1998) technique, are indicated in parentheses for each domain assessed. Table 3. Neuropsychological test results (abnormal scores are indicated by an asterisk) Results Test

1992

1999

Neuropsychological domain

MMSEa FRTb Token Testc JLOd 3DBCe ECRT immediate recall (trials 1–3)* freef cued totalc delayed 45-min recall (trial 4) freeg cued totalc

30/30 47/54 36/36 21/30 27/29

29/30 45/54 36/36 20/30 26/29

Global cognitive status Perception of complex objects (human faces) Comprehension of spoken speech Perception of complex visuospatial relations Constructional praxis Genuine memory

24/48* 24/48* 48/48

16/48* 32/49* 48/48

6/16* 10/16* 16/16

7/16* 9/16* 16/16

⫽ 0.54, d.f. ⫽ 26, P ⬎ 0.54. ⫽ 1.36, d.f. ⫽ 26, P ⬎ 0.18. achieved highest possible score. dt ⫽ 1.41, d.f. ⫽ 26, P ⬎ 0.17. et ⫽ 1.64, d.f. ⫽ 26, P ⬎ 0.12. ft ⫽ 4.71, d.f. ⫽ 26, P ⬍ 0.0001. gt ⫽ 3.79, d.f. ⫽ 26, P ⬍ 0.001. MMSE, Mini-Mental State Examination; FRT, Facial Recognition Test; JLO, Judgement of Line Orientation; 3DBC, Three-dimensional Block Construction Test; ECRT, Enhanced Cued Recall Test. at bt

cPatient

ment failure may reflect a kind of learning disorder which is distinct from the classic amnesic syndrome of mamillotemporomedial damage (Kopelman, 1995). This assertion was supported by our patient’s results on perceptual and memory tasks. In particular, SR’s normal ability to remember new information immediately after learning and following a 45min delay (as shown by her ECRT total scores) indicated that the basal forebrain–medial temporal lobe memory systems had been functionally preserved (Salazar et al., 1986). Recall, however, was abnormally dependent on cueing, as is usually the case in patients with damage to the frontal lobes or to its subcortical connections (Shimamura et al., 1991). In such individuals, information is easily encoded and retrieved by automatic processes, but fails during free recall, which is an effortful process (Cummings, 1986). Repeated administration probably changed the WCST into a procedural learning task. Procedural learning is ‘a form of knowledge (...) in which memory is expressed in changes in performance as a result of prior experience’, regardless of

whether a conscious memory of such experience is formed or not (Pascual-Leone et al., 1995). Our observations indicate that the WCST could be employed as a measure of executive, in contrast to procedural motor, learning. They also challenge the view that ‘‘a task will be a ‘frontal test’ so long as it is novel’’ and that ‘with practice, most tasks will cease to be frontal’ (Frith, 1991). Although this may hold true for normal individuals and for memory tasks that are typically declarative, executive learning may be grossly defective in patients with pre-frontal damage, even when they are able to verbalize solutions and principles correctly (Cohen et al., 1985). Thus, in contrast to the aforementioned views, knowing the key to a puzzle does not assure that it will be successfully solved in the future (Jacoby, 1978). The fact that SR scored almost perfectly on the OK condition and that the number of set failures did not significantly differ between the standard and OK conditions indicates that her intra-dimensional attentional shifting mechanisms were relatively preserved. These findings are in agreement

388 R. de Oliveira-Souza et al.

with the concept that intra-dimensional attentional shifting is not critically impaired in patients with damage to the frontal lobes (Owen et al., 1993). They also lend support to the notion that the WCST is a sensitive probe of pre-frontal function (Stuss et al., 2000). However, still more important than its alleged sensitivity to pre-frontal damage is the possibility that failure to improve on the WCST despite intensive training may be more specific to pre-frontal damage than first-exposure failures. The injury in SR fell on regions most strongly activated by the WCST in normal individuals, namely, inferior dorsolateral pre-frontal cortex, inferior parietal lobule and middle temporal gyrus of both hemispheres (Berman et al., 1995). Focal symmetrical activations in the inferior frontal sulcus (Konishi et al., 1998) and inferior parietal lobule (Nagahama et al., 1996) are closely associated with set shifting (Moll et al., 2000). The observation that this pattern remains largely unchanged after training (Berman et al., 1995) suggests that ‘executive memory’ is stored in, or close to, the cortical areas that mediate executive behaviour, in a manner resembling what is known to occur in the sensory cortex, where agnosias often result from damage to areas that process perception (Feinberg et al., 1986). Thus, fronto-striatalcerebellar circuits might play a role in executive memory akin to the one played by the medial temporal system in the encoding and recall of declarative memory (Squire and ZolaMorgan, 1991). The pivotal role of the pre-frontal cortex in these mechanisms is indicated by the severe impairment of executive learning despite the relative sparing of the deep forebrain nuclei and cerebellum. SR completed four categories seven times in the standard condition and five categories twice in the pOK condition, showing that her performance was not random at all. These observations suggest that the basic cognitive processes required for success on the WCST do not depend strictly on the frontal cortices for, as shown by our patient, the three basic categories of the WCST can be completed without most of the pre-frontal cortex. This partial success, however, was achieved at the expense of an abnormally high rate of perseverative errors, which were extremely resistant to training. Execution of the WCST in the absence of the pre-frontal cortex is probably accomplished by vicarious cerebral circuits, a phenomenon known to be true in the process of cognitive recovery in other domains (Rosen et al., 2000). Regardless of the precise compensatory mechanisms which operate in cases such as the one reported here, our observations indicate potentially new uses for the WCST in neuropsychological assessment. In particular, they suggest that there may be individuals who fail on their first exposure to the WCST, but who achieve normal levels of performance after they undergo an OK session. These cases should probably be differentiated from others, like the present one, who never improve, no matter how hard they train. Whether these patterns conceal different meanings for predicting success in rehabilitation programmes, or even for predicting fitness in the real world (Siris, 1991), is an open field for future studies.

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Received on 8 February, 2001; resubmitted on 9 June, 2001; accepted on 11 June, 2001

Executive amnesia in a patient with prefrontal damage due to a gunshot wound R. de Oliveira-Souza, J. Moll, F. Tovar Moll and D. L. Gusma˜o de Oliveira Abstract This paper reports the case of a young patient with extensive pre-frontal damage in whom we tested the hypothesis that intensive training improves executive performance as assessed by the Wisconsin Card Sorting Test (WCST). As long as her declarative memory, complex perceptual abilities and global cognitive status were spared, we surmised that any deficit in executive learning would have occurred in relative isolation. We showed that her abnormal performance on the WCST, both on the standard as well as on the post-instruction condition, was due to an impairment of shifting attention across perceptual dimensions (extra-dimensional). In contrast, her ability to shift attention within perceptual categories (intra-dimensional) was spared, as were her declarative memory, object and visuospatial perception, oral language comprehension and praxis (ideomotor, tool use and constructional). This case supports the hypothesis that executive amnesia is a type of amnesic disorder distinct from the classic amnesic syndrome due to mamillo-temporomedial damage. As such, it is probably closely related to procedural learning and may depend on the same fronto-subcortical loops that mediate the actual execution of behaviour.

Journal Neurocase 2001; 7: 383–9

Neurocase Reference Number: O229

Primary diagnosis of interest Traumatic frontal lobe injury

Author’s designation of case SR

Key theoretical issue d Executive amnesia as a distinct form of amnesic disorder

Key words: amnesia; dysexecutive syndrome; frontal lobe syndrome; Wisconsin Card Sorting Test; executive behaviour

Scan, EEG and related measures Magnetic resonance imaging scan

Standardized assessment Neuropsychological assessment

Lesion location d Frontal lobes (cortico-subcortical), with bilateral sparing of basal ganglia, thalamus and cerebellum

Lesion type Traumatic, due to gunshot

Language English