Pergamon

Neuropsychologla, Vol 33, No 3, pp 261-268, 1995 Copyright ~ 1995 Elsevier Science Lid

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0028-3932(94)00124-3

F L U I D I N T E L L I G E N C E A F T E R F R O N T A L L O B E L E S I O N S

JOHN DUNCAN,* PAUL BURGESS]" and HAZEL EMSLIE*

*MRC Applied Psychology Unit, 15 Chaucer Road, Cambridge CB2 2EF, U.K.; and iDepartment of Psychology, University College London, Gower Street, London WC1E 6BT, U.K.

(Recewed 16February 1994; accepted 24 October 1994j

Abstract--Generally positive correlations between different ability tests provide the evidence for a factor of"general intelligence" or Spearman's g. Though a possible neural substrate for g is suggested by executive impairments following frontal lobe lesions, preserved IQs in some frontal patients have been taken as strong evidence against this interpretation. We show that such results depend on how g is measured. Patients with superior IQs on the most clinically popular test-- the Wechsler Adult Intelligence Scale--show impairments of 2 ~ 6 0 points on conventionally measured fluid intelhgence or novel problem solving. On psychometric grounds, it is fluid intelligence that is most closely related to Spearman's g. The data suggest that g may in large part be a reflection of frontal functions.

Key Words: frontal lobe; fluid intelligence; executwe function.

INTRODUCTION

Central to the study of individual differences is the concept of "general intelligence" or Spearman's g [27]. Ifa battery of cognitive tests is administered to a broad sample of people, the result will be a matrix of positive correlations: For almost any pair of tests, better performance on one is associated, strongly or weakly, with better performance on the other. One interpretation, introduced by Spearman, is that some "general" or g factor makes a contribution to success in all manner of cognitive activities.

Within psychometrics the definition ofg is reasonably exact [6, 27]. For example, g factors extracted from quite different test batteries are strongly correlated, a principle termed by Spearman "indifference of the indicator". Using factor analysis it is easy to show which tests are most strongly correlated with g; this is the basis for design of standard tests of "intelligence" or IQ. An enduring question concerns the neural substrate of the g factor that psychometrics defines.

Recently, Duncan [11] has suggested that g may largely be a reflection of frontal lobe functions. This proposal rests on a number of considerations. Following frontal lesions there can be a widespread disorganization of behaviour, reflected in many different cognitive domains--planning, perceptual tasks, memory, regard for social conventions, and many more--and in diverse forms of error including perseverations, passivity, susceptibility to distraction, and behaviour that seems impulsive or ill-judged [21]. Deficits in such a diversity of behaviour are immediately reminiscent of the concept of g. Working memory, especially its ~executive" aspect, has been seen as central to both frontal lobe function [17] and g [20]. "'Executive" functions are considered most important in novel as opposed to well-learned behaviour; at least in simple tasks, practice may reduce both g correlations [1] and frontal

261

262 J DUNCAN, P. BURGESS and H. EMSLIE

lobe involvement [23, 24]. Neglect of a task requirement, even though it has been understood, has occasionally been described in frontal patients [e.g. 21]. The phenomenon may be termed goal neglect [11]. Recently we showed goal neglect even in some normal people under conditions of novel behaviour and weak error feedback [12]. Under these conditions neglect was closely related to g; in patients with severe frontal deficits it was the rule.

Despite its apparent appeal, Duncan's [11] hypothesis is contrary to much conventional wisdom in neuropsychology. At least since the work of Hebb and Penfield [18], it has been accepted that frontal executive functions have little to do with conventional psychometric intelligence. The reason is straightforward. If g is largely a reflection of frontal functions, then deficits in standard IQ tests should be specifically associated with frontal lesions. Using standard tests such as the Wechsler Adult Intelligence Scale or WAIS [31], this prediction has been repeatedly disconfirmed. Warrington et al. [30], for example, found rather similar WAIS scores in patients with lesions of each major lobe of the brain. Particularly damaging to the frontal lobe hypothesis has been the report of occasional patients with major cognitive impairments resulting from frontal lobe lesions, but preserved, superior WAIS IQs [e.g. 13, 26]. Results such as these have led to the view that standard intelligence tests are especially unsuitable for revealing frontal impairments [28]. The paradox has been accepted that frontal patients have impaired "planning", "problem-solving", etc., but preserved "intelli- gence".

In this paper we deal specifically with the question of superior WAIS IQ despite manifest cognitive impairment in some frontal patients. We suggest that the paradox of preserved "intelligence" may be resolved by considering more carefully the psychometric concept of g and how it should be measured. As defined in psychometrics, g reflects a person's overall tendency to perform tasks well or less well. It may be measured in two broad ways. In the WAIS and similar tests used in the vast majority of clinical investigations, g is estimated by averaging together performance on a diverse range of sub-tests. Two considerations may be important. First, many sub-tests (e.g. vocabulary, general information) emphasize knowledge. Such tests of"crystallized intelligence" may reflect g at the time of learning rather than g at the time of test [6]; once learned, knowledge may be rather insensitive to a subsequent g change (cf. the conventional distinction between "hold" and "don't hold" sub- tests of the WAIS, and the difficulties it has encountered; see [33]). Second, some individual sub-tests in themselves have rather low g correlations [22]; the g factor emerges only through averaging sub-tests together [27]. As we have said, providing there are a reasonable number of diverse tests, average performance on almost any test set will give much the same g estimate [27].

The contrasting approach is taken in tests of "fluid intelligence" [6]. Most importantly, such tests have strong g correlations even without averaging over diverse sub-tests; in large- scale factor analyses, these are the tests most closely related to g [5]. Furthermore, an attempt is made to minimize dependence on prior knowledge; typically the tests involve novel problem-solving with spatial or other materials. Whatever characteristic is reflected in g, this characteristic seems most important in fluid intelligence tests. On these psychometric grounds, these are probably the most suitable tests for a theoretically-based investigation of changes in g after brain lesions.

In this study we examined two patients of exactly the kind classically taken to show that frontal functions are not central to g. These were patients with obvious cognitive impairments following frontal lesions, but preserved superior WAIS IQs. Their preserved

FRONTAL LESIONS AND INTELLIGENCE 263

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1 2 3

Fig. 1. Typical fluid intelligence test item.

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IQs despite manifest cognitive impairments have been previously documented [16, 26]. We predicted that, examined again with the more appropriate test of fluid intelligence, these same patients would reveal substantial impairments.

There are several suitable tests of fluid intelligence, sharing the properties of low knowledge dependence and high g correlation. Well-known examples are Progressive Matrices [25] and Cattell's Culture Fair [19]; the latter was used here. The test has four types of spatial problems (series completions, odd-man-out, matrices, topology), and a published 9 correlation of 0.81. A problem resembling its matrix items is shown in Fig. 1. The task is to decide which of the five alternatives on the right correctly completes the matrix on the left. To choose correctly, the subject must recognize variations in shape, size and angle of diameter, and compute a solution respecting all of these [4].

In addition to the two patients previously reported, we found one more, whose lesion extended beyond the frontal lobe, but whose cognitive profile was broadly similar. For each of these three patients, we selected one normal control matched carefully in age, sex, socioeconomic group and WAIS IQ. Though these patients were our major concern, we wished also to check the possibility that any brain lesion might lead to impairment of Culture Fair as compared to WAIS IQ. For example, the more knowledge-based tests of the WAIS might simply be less sensitive to brain damage in general. Accordingly we tested an additional, mixed group of patients with focal posterior lesions.

METHOD Procedure

For patients, WAIS IQs were measured using standard seven-test short forms [30] of the WAIS or more recent WAIS- -R . Short forms provide excellent estimates of the full-length IQ [10]. The more difficult WAIS- -R has been standardized to reflect population gains in test score since the original standardization of the WAIS; in the current population, IQs are roughly 8 points lower measured by the WAIS- -R than by the WAIS [9]. Controls were selected from a large sample of normal people to whom the WAIS or WAIS- -R had previously been administered. Control IQs were obtained from the full-length tests.

Scale 2, Form A of the Culture Fair Test was administered individually to both patients and controls. The test has four series of problems, each with a time limit. The norms [19] provide IQs with a mean of 100 and standard deviation (S.D.) of 16; for comparability with the WAIS (S.D. 15), deviations from 100 were multiplied by 15/16

Frontal patients

A.P. [26] was a male teacher trainee with a university degree, who suffered severe blfrontal damage from an open head injury at age 23. Administered 3 years later, the WAIS showed a full-scale IQ of 128. The Culture Fair was administered at age 29. A.P.'s control was a male accountant , whose full-scale WAIS IQ was 128 at age 29. He was given the Culture Fair at age 33.

C.J.E. [16] was a male chartered engineer, who underwent left frontal lobectomy for removal of tumour at age 49 Administered 2.5 years later, the W A I S - - R showed a full-scale IQ of 126 (estimated for this patient on the basis of six rather than seven sub-tests). The Culture Fair was administered 5 months after the WAIS- -R . C.J.E?s control was a

264 J. DUNCAN, P. BURGESS and H. EMSLIE

Table 1. Posterior patients: background information

Patient Age Lesion Aetiology

S.A. 31 L occipital AVM J.B. 57 L temporo-parietal Meningioma T.T. 23 R medial temporal Histocytoma R.B. 54 L occipital Glioma J.D. 36 L temporal Glioma

male university lecturer in geography, whose full-scale WAIS--R IQ was 127 at age 47. He was given the Culture Fair at age 51.

D.S. was the male managing director of a software company, who suffered a white matter infarction of the left frontal lobe, accompanied by other areas of infarction in the white matter of the left hemisphere, at age 52. Administered 6 months later, the WAIS showed a full-scale IQ of 126. The Culture Fair was administered 5 months after the WAIS. D.S.'s control was a male university lecturer in history, whose full-scale WAIS IQ was 130 at age 51. He was given the Culture Fair at age 56.

In daily life these patients revealed characteristic frontal impairments, including disorganization, impulsivity, and bizarre behaviour [16, 26]. All three had failed to return to their previous employment. Their performance in standard tests of "executive function" was varied, but all were clearly impaired in the Multiple Errands test of Shallice and Burgess [26]. In this test, a number of requirements must be satisfied in the setting of a real street with a variety of shops. Requirements include buying certain items, discovering certain information, deciding which shop is likely to sell the most expensive item, etc.; rules include not entering a shop without making a purchase, not leaving the street, etc. Impairments of A.P. and C.J.E. have been reported elsewhere [ 16, 26]; the performance of D.S. was approximately 2 S.D.s below that of matched controls.

Posterior patients

The five posterior patients are described in Table 1. J.B., R.B. and J.D. had all undergone surgery several years prior to testing; S.A. and T.T. had no surgery. The miscellaneous cognitive impairments of these patients were not formally assessed, but in 4/5 cases were known from background testing. S.A.'s problems included recall and visual memory; J.B. has a well-documented short-term memory deficit [29]; R.B.'s impairments included reading, arithmetic and word retrieval; J.D. complained of memory problems and had been unable to return to work. Short forms of the WAIS (J.B., R.B., J.D.) or WAIS--R (S.A., T.T.) were administered along with the Culture Fair.

RESULTS

Frontal patients WAIS and Culture Fair IQs of frontal patients and their controls are shown in Table 2.

Two comparisons may be made. First, for each patient there was a substantial discrepancy between WAIS and Culture Fair IQs, the Culture Fair score being 22-38 points lower. Based on the published reliabilities of the tests [19, 31, 32], this difference was significant (see [2], p. 137) for each of the three patients (A.P., z = 2.7, P < 0.01; C.J.E., z = 3.6, P<0.001; D.S., z=4.8, P<0.001).

Such a comparison between tests is complicated by various factors, however. The patients were selected for high WAIS IQs, suggesting that Culture Fair IQs might be lower through regression to the mean. WAIS IQs are corrected for age, while Culture Fair IQs are not; with reference to the 25-34 year age group, WAIS IQs would have been 9 and 7 points lower respectively for C.J.E. and D.S. The age of the norms themselves will also be important given gradual population gains in test scores over time [15]. Fortunately, such problems are bypassed in comparing the Culture Fair IQs of patients and controls, and here the results were even stronger. Culture Fair IQs were reduced by 23-60 points in the patients, each difference between patient and control being significant (A.P., z=2.2, P<0.05; C.J.E., z=4.9, P<0.001; D.S., z=5.8, P<0.001).

Scores for patients and controls on the various sub-tests of the WAIS are shown in Table 3.

FRONTAL LESIONS AND INTELLIGENCE 265

Table 2. WAIS and Culture Fair IQs of frontal patients and controls

WAIS IQ Culture Fair IQ

A.P. 130 108 Control 128 131

C.J.E. 126" 97 Control 127" 148

D.S. 126 88 Control 130 148

*WAIS--R.

Table 3. Scaled scores (not age corrected) on each WAIS sub-test for frontal patients and controls

A.P. Control C.J.E.* Control* D.S. Control

Arithmetic 13 13 14 9 14 15 Similarities 15 15 14 14 15 13 Digit span 15 10 13 13 14 14 Vocabulary 16 15 15 13 19 18

Picture completion 14 14 10 11 11 19 Block design 15 14 -- 10 13 Picture arrangement 14 13 11 12 9 11

Digit symbol 11 14 7 9 8 10

Mean 14.1 13.5 12.0 11.6 12.5 13.0

*WAIS--R.

These are scaled scores (mean 10, S.D. 3 in the reference population), not corrected for age, on the tests that both patients and controls completed. In the seven-test short form used for patients, Verbal IQ is based on the top four tests, Performance IQ on the next three. Though not included in IQs, Digit Symbol scores are also given for information. Several points may be noted. First, there was a small tendency for patients to do better than controls on verbal sub-tests, but worse on performance sub-tests. This is consistent with preservation of performance on the most heavily knowledge-based tasks. Second, there was no obvious association between deficits and speed requirements of a sub-test. Like the Culture Fair, for example, Arithmetic, Picture Completion, Block Design and Picture Arrangement all require that problems be solved accurately at speed. Finally, the data do suggest a frontal deficit in the simplest test of processing speed, Digit Symbol. In terms of scaled score, however, the mean difference between patients and controls was only 2.3 (0.8 S.D. in the reference population), certainly not comparable to the difference in Culture Fair scores (3.0 S.D.s). These data do not suggest that the frontal deficit is best captured by a simple processing speed measure. The biggest deficit, rather, is in the fluid intelligence test itself.

Posterior patients

The five posterior patients were tested to check whether a WAIS-Culture Fair discrepancy is the norm following focal brain lesions. The data (Table 4) rule out this possibility. Among these patients, mean WAIS/WAIS- -R and Culture Fair IQs were 105 and 108, respectively.

266 J. DUNCAN, P. BURGESS and H EMSLIE

Table 4. WAIS and Culture Fair IQs of posterior patients

WAIS IQ Culture Fair IQ

S.A. 106" 112 J.B. 97 85 T.T 101" 131 R.B. 105 96 J.D. 118 117

*WAIS--R.

Though WAIS IQs were lower in these patients than in our (pre-selected) frontals, there was no apparent relationship between absolute WAIS IQ and WAIS-Culture Fair discrepancy. The patient with the highest WAIS IQ (118) had an almost identical Culture Fair IQ (117).

DISCUSSION

Our prediction was strongly supported by the data from frontal patients. Though WAIS IQ was preserved, re-testing with the Culture Fair revealed very substantial deficits. On psychometric grounds, as we have said, it is tests of fluid intelligence that are most appropriate for investigating the neuropsychological underpinnings ofg. Substantial deficits after frontal lesions suggest that g as defined psychometrically may be largely a reflection of frontal functions.

It is impossible to say why, at least in some patients, the WAIS IQ should be relatively insensitive to frontal lesions. Dependence on knowledge may be a part of the answer, but in our patients, even less knowledge-intensive sub-tests such as Block Design were largely preserved. Perhaps this is partially an artifact of having specifically selected patients with high WAIS IQs, producing a bias to good scores on all component sub-tests. The main point, in any case, is that patients with preserved WAIS IQ despite manifest frontal impairments cannot be taken as strong evidence against the hypothesis that Spearman's g is largely a reflection of frontal functions. Even in these patients, the most appropriate tests of g--fluid intelligence tests with high g correlations and low knowledge dependence--reveal a substantial impairment.

Especially in the monkey, there is good evidence for anatomical and functional differentiation within the frontal lobes [17]. With respect to the current data, at least two possibilities arise. One is that 9--reflected in a person's tendency to do relatively well or poorly no matter what the task--reflects some kind of joint or combined efficiency of several distinct frontal sub-processes. For example, different frontal sub-processes may generally work together to produce such general functions as goal activation or selection [12]. A second possibility is that g is related specifically to the function of particular frontal regions. Studies of cerebral blood flow, for example, show activation of both dorsolateral prefrontal cortex and the anterior cingulate in a wide variety of demanding cognitive tasks [e.g. 7, 14]. Little can be said based on the present data: for two patients frontal lesions were extremely large, while for the third, the lesion extended even beyond the frontal lobe. Further patients will be needed to address the role of distinct frontal regions.

One thirig that is special about the present three patients is that they combined conspicuous frontal deficits with (one may presume) high premorbid IQs. In a study of 10 further frontal patients [12], premorbid IQs were substantially lower and Culture Fair

FRONTAL LESIONS AND INTELLIGENCE 267

decrements, though highly significant, were accordingly less severe. It seems likely that fluid intelligence deficits will be especially substantial whenever a conspicuous frontal deficit is accompanied by high premorbid IQ.

In posterior patients we found no average discrepancy between WAIS and Culture Fair IQs. Though posterior patients were not selected to have high WAIS IQs, in these patients there was no evidence for a link between absolute WAIS IQ and WAIS-Culture Fair discrepancy. A further study [12] has also given little evidence of a general Culture Fair impairment among posterior patients. It would be wrong to conclude that posterior lesions never produce deficits in tests like the Culture Fair [3], though in some cases, such deficits may be related to factors such as unilateral neglect [8], which probably do not contribute to normal performance. Bearing this caution in mind, however, the data do suggest that deficits in fluid intelligence are especially marked after frontal lesions.

These data support the hypothesis of a close link between g as defined psychometrically and the functions of the frontal lobe. In the cases examined here, and despite preserved WAIS IQ, major frontal deficits were accompanied by substantial losses of fluid intelligence.

Acknowledgements--Financial support was provided by grant AFOSR-90-0343 from the Air Force Office of Scientific Research, Air Force Systems Command, USAF. The U.S. Government is authorized to reproduce and distribute reprints for Governmental purposes notwithstanding any copyright notation thereon. We thank Alan Baddeley for his support in this project, and John Crawford and Steven Greenhill for testing of controls.

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