fluency deficits in patients with alzheimer's disease and frontal lobe lesions

European Journal of Neurology (1996), 3, 102-108

Fluency deficits in patients with Alzheimer’s disease and frontal lobe lesions L.H. Phillips’, S. Della Sala’ and C. Trivelli2

’Psychology Department, University of Aberdeen, Old Aberdeen AB9 2UB, Scotland, UK, and 2Servizio di Neuropsicologia, Centro Medico di Veruno, Fondazione Clinica del Lavoro, IRCCS

Correspondence to S. Della Sala at the above address

Fluency tests are widely used in clinical settings to assess cognitive function. Fluency deficits In patients with Alzheimer’s disease (AD) are generally attributed to deteriorated language storage. In contrast, patients with lesions to the frontal lobes (FL) of the brain are thought to have poor fluency due to executive deficits of retrieval. This study examined the relationships between fluency performance and cognitive measures of language and executive function in both AD and FL patients. In both groups, fluency performance related to measures of language comprehension and executive control of attention. However, in AD patients, fluency deficits were most closely associated with language and verbal memory deterioration, while In FL patients fluency deficits were more strongly associated with executive measures of strategic planning and attention. Qua- litatively different patterns of functional deficits may influence fluency performance in different neuropsychological groups. Caution Is therefore urged in the interpretation of poor fluency scores as Indicative of either language or executive dysfunction, without additional information about the reasons for poor performance.

Keywords: Fluency - Alzheimer’s disease - Frontal lobe lesions - Executive function - Language - Neuropsychological tests

INTRODUCTION

Verbal fluency tests require the rapid generation of words to fit specified semantic or phonemic rules (e.g. types of fruit, words beginning with “F”). Measures of fluency are widely used for clinical assessment of cognitive dysfunction, for example in the Mattis Dementia Rating Scale (Mattis, 1976), and in batteries of so-called “frontal lobe” tests (e.g. Whelihan and Lesher, 1985; Bhutani et al., 1992). Fluency deficits have been found in patients with a wide variety of neuropsychological disorders (e.g. schizophrenia, Allen el al., 1993; frontal lobe lesions, Milner, 1964; Alzheimer’s disease, Monsch er al., 1994; Parkinson’s disease, Raskin et al., 1992). Good performance on fluency tasks requires both intact storage of words and the ability to construct effective strategies to retrieve those words (Randolph er al., 1993). Therefore, either a loss of structured linguistic information in memory or an inability to generate effective retrieval strategies could cause poor fluency performance.

Within different areas of the neuropsychological litera- ture different assumptions are made as to which of these two deficits underlies poor fluency performance. Fluency deficits in degenerative conditions such as Alzheimer’s Disease (AD) are usually attributed to linguistic storage deficits (e.g. Monsch er al.. 1994), while fluency deficits in disorders linked to frontal lobe dysfunction are usually explained in terms of poor executive control of the gen-

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eration of retrieval strategies (e.g. Baddeley and Wilson, 1988). Of course, it is quite plausible that different patient groups perform poorly on fluency tests for distinct reasons, but unfortunately little empirical evidence is avail- able to differentiate between groups as to why they do badly on the tests. This leads to the confbsing situation that some neuropsychological studies assume fluency deficits to indicate deterioration of linguistic storage, while others assume that fluency deficits are indicative of executive deficits of retrieval strategy generation. In- deed, sometimes these opposing assumptions have been made about fluency performance within the same patient group (Bhutani et al., 1992, use fluency as a measure of executive fUnction in AD patients, while Binetti er al., 1993, use fluency as a measure of language b c t i o n in AD patients). In order for fluency tests to be clinically useful indicators of cognitive dysfunction, more evidence is needed as to why particular patient groups perform poorly.

There is considerable evidence to show that AD patients perform poorly on tests of fluency: they produce few words, and are liable to perseverate (repeat a word which has already been produced). Fluency deficits in AD patients are usually attributed to a deterioration in semantic networks within memory, i.e. to a linguistic storage problem (Martin and Fedio, 1983; Binetti er 41..

0 1996 Rapid Science Publishers

FLUENCY DEFICITS IN PATIENTS

1993; Chan et al., 1993; Monsch et al., 1994; Para~ura- man and Vaxby, 1993). However, sometimes fluency deficits in AD are interpreted as an indication of dyshction in more active, executive processes (Hart et af., 1988; Bhutani et al., 1992; Della Sala et al., 1993). This therefore raises questions as to whether language storage or executive retrieval deficits underlie poor fluency in AD. The fluency production of AD patients shows less evidence of categorical organization than that of age-mat- ched healthy controls (Martin and Fedio, 1983; Ober et al., 1986; Chan et al., 1993) and this has generally been interpreted to reflect a deterioration of the storage of semantic infomtion in these patients. However, it is also possible that the stored networks are in fact relatively intact, but the patients m o t generate systematic strategies to organize retrieval (Bandera et al., 1991).

There is also ample evidence that patients with frontal lobe (FL) lesions perform poorly on fluency tasks (Mil- ner, 1964; Perret, 1974; Baddeley and Wilson, 1988; Crowe, 1992; Randolph ef al., 1993). Fluency performance in these patients is qualitatively similar to that of AD patients, with low production and high perseveration. However, in FL patients poor fluency performance is routinely atbibute to dysexecutive failure of retrieval strategy generation (Baddeley and Wilson, 1988; Crowe, 1992; Parker and Crawford, 1992; Randolph et al., 1993; Lezak, 1995). A contrary position has also been put for- ward: that frontal lobe deficits in fluency are in fact due to aphasic language disorders disrupting the structure of semantic information (Reitan and Wolfson, 1994). Flu- ency deficits have sometimes been found to be particu- larly pronounced in those with left frontal lesions (Milner, 1964; Perret, 1974). Because left hemisphere brain damage is known to affect language functioning, it is possible that the fluency deficits in FL patients might be due to left-hemisphere linguistic problems rather than defects in executive control.

The different anatomical lesions in the two groups of patients may also play a role. FL patients by definition have lesions limited to the frontal lobes. On the other hand, the degenerative thinning out of neurons in the early stages of AD, although rather heterogeneous (Boiler et al., 1992), is typically located in the temporo-parietal and limbic systems, and the pathology is more Pro- nounced in the left hemisphere (Capitani ef d., 1990), encroaching upon the frontal lobes in the later stages of the disease. Therefore, it is foreseen that the performan- ces o f m patients on the whole will be poorer than those of FL patients.

There is surprisingly IittIe evidence to enable evalua- tion of the contrasting cognitive explanations for fluency deficits in AD patients (language storage disorders) and FL patients (executive retrieval disorders). Randolph et a]. (1993) compared semantic fluency performance in

AD and FL patients in two conditions. They found that AD patients’ performance did not improve when given retrieval cues, whereas a FL patient was aided by using these retrieval cues. AD fluency deficits were therefore interpreted to reflect aphasic deterioration of language storage, while FL fluency deficits reflect executive control of retrieval processes. However, only one FL patient was studied, and frontal lesions are notoriously unreliable in terms of the pattern of cognitive deficits they produce (Parker and Crawford, 1992).

The current study looks at fluency performance in FL and AD patients in relation to performance on cognitive tests of both language and executive functions. If the predominant dysexecutive interpretation of fluency deficits in FL patients is correct, then fluency performance in these patients should correlate most highly with executive measures. Also, if the predominant linguistic storage explanation of AD fluency disorders is correct then fluency scores among these patients should relate most highly to measures of language and verbal storage.

METHOD

Patients Frontal lobe (FL) patients. Forty three patients (26 men, 17 women) with CT-proved lesions limited to the frontal lobes were included in the study. Of these patients, 20 had lesions in the left frontal lobe only, 13 had lesions in the right frontal lobe only, and 10 had bilateral lesions. Their mean age was 47.6 years (SD 17.3), mean time spent in education was 8.84 years (SD 4.37), and mean length of illness was 12.6 months (SD 21.5).

Alzheimer’s disease (AD) patients. Fifly seven patients (32 men, 25 women) entered the study. Their mean age was 63.5 years (SD 7.58) and mean length of time in education was 7.68 years (SD 4.72). The average length of illness was 29.1 months (SD 18.2). They were selected from a sample of 179 patients with “probable” AD, di- agnosed according to formal criteria (Spinnler and Della Sala, 1988), which broadly correspond to those proposed by NINCDS-ARDA (h4cKhann et al., 1984) and the MRC AD Workshop Steering Committee (Wilcock et al., 1989). In 94 patients the global cognitive impairment W ~ S mild to moderate according to DSM-IV (APA, 1994). Two patients were excluded because they refused neu- psychological testing. Another 35 patients were excluded because one or other test in this retrospective study was missing in their neuropsychological examination. Therefore, the AD patients included in the study are 61% of the mild-moderate subgroup.

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Procedure Tests. Fluency: subjects were asked to generate as many words as possible from each of four semantic categories (colours, animals, fruits, cities), with 2 min allowed for each category.

Verbal tests. Verbal span (vspan): span tasks are the most common method of assessing short-term memory capacity. Subjects were required to repeat lists of auditorily presented, bisyllabic words, in the order of presentation. Three sequences of words were presented at each list length, beginning with two words, and incrementing the list length by one until the subject was no longer able to successfilly recall all of the words. Scores were defined as the maximum list length for which the subject recalled correctly two sequences out of three (Spinnler and Tog- noni, 1987). With a few exceptions (e.g. Shimamura et af., 1991), verbal span is not generally considered a test tax- ing frontal functions (e.g. Luria, 1973; Risse et al., 1984; Stuss and Benson, 1986; Owen et al., 1990 all found no impairment of span in frontal patients).

Token test (token): the shortened version of this test of oral language comprehension was used (De Renzi and Faglioni, 1978), which is known to be very sensitive to disrupted linguistic processes ( L e d , 1995; for an exten- sive review see Boller and Dennis, 1979). Subjects were shown tokens of different colour, shape and size (five big and five small circles, five big and five small squares; of every five, one each was red, white, green, yellow and black). They were asked to execute simple and complex instructions given by the examiner (e.g. simple instruction: “touch a square”; complex instruction: “instead of the white square, take the yellow circle”). Possible scores on this test ranged from 0 to 36. The critical anatomical areas associated with poor performance on the Token Test are the middle posterior thirds of the temporal circonvo- lution and the underlying insular structures of the domi- nant hemisphere (Vignolo, 1979). The only demonstrated executive involvement in the Token Test is the generation of “back-tracking” to facilitate the comprehension of the more verbose and complex items (Della Sala and Logie, 1993).

Executive rests. Digit cancellation (digcan): in this time- constrained visual searching test, which primarily taxes selective attention (Della Sala et al., 1992), subjects were asked to cross out target digits from three different ma- trices (1,2 and 3 targets), the first of which was used as a practice trial. Possible scores ranged from 0 to 50. This task is known to be sensitive to frontal lobe damage (Teuber er of., 1951; Teuber, 1972; Della Sala ef af., 1992).

Elithom Perceptual Maze Task (elimaze) (Elithorn, 1955): this spatial planning task consisted of printed net-

104 European Journal of Neurology . VO~ 3 . 1996

works of paths, superimposed with black dots. Subjects were required to find a bottom to top pathway which passed through a specified number of dots (3, 4, 5 or 6). Subjects were instructed not to cut across from one path to another, or to move backwards. Possible scores ranged from 0 to 16 (Spinnler and Tognoni, 1987). Maze tests are thought to tap the ability to formulate and carry out strategic plans of action (Parker and Crawford, 1992), and are known to be sensitive to frontal damage (Benton el af., 1963).

Scoring procedures. Normative data on all the tests used in this study were obtained from healthy people in previous investigations (Spinnler and Tognoni, 1987; Della Sala et af., 1992). The influence of age, education and sex on the scores achieved by healthy people was studied by means of a linear multiple regres- sion model (Capitani and Laiacona, 1988). The effects of age and education were significant in every test considered. In the current study, for each subject an adjusted score was calculated by adding or subtracting the con- tribution made by age and education. Pearson product- moment correlations were calculated between adjusted fluency performance and adjusted scores on the four tests outlined above in each of the two patient groups. A variable measuring “language function” was created by adding together standardized (2) scores of vspan and token performance; and a variable measuring “executive function” was created by adding together standardized scores of digcan and elimaze performance. Correlations between fluency and “language” and “executive” functioning in AD and FL patients were then calculated.

RESULTS

Descriptive statistics of the test scores obtained in the study can be seen in Table I. Of the two patient groups, AD performed more poorly on most of the cognitive tests, including fluency. The FL patients were split into three subgroups according to lesion site (IefVrighVbilateral). A comparison in terms of fluency scores revealed no significant effect of lesion site, F(2,40) ~0.503. This result is in agreement with previous findings (Bruyer and Tuyumbu, 1980; Owen et al., 1990). FL patients were therefore considered as a single group for all subsequent analyses.

Correlations between fluency performance and scores on the other cognitive tests can be seen in Table 11. In AD patients, there were significant correlations between performance on the two tests of language function and fluency scores. Both short-term verbal memory and language comprehension predicted fluency deficits in AD patients. There was also a substantial correlation between


TABLE I. Means and standard deviation of patients’ performance on tests ~

AD patients (n=57) FL patients (n=43) Variable Mean SD Mean SD

Vspan 3.19 0.83 3.73 0.71 Token 25.6 5.90 30.2 5.39 Digcan 20.3 10.8 29.6 10.7 Elimaze 4.81 4.88 9.67 5.69 Fluency 7.46 3.83 9.49 4.89

fluency scores and digcan performance, pointing to a role for selective attention in AD fluency deficits. In contrast, there was not a significant relationship between elimaze scores and fluency performance in the AD group, suggesting that executive factors of strategy generation were unlikely to be involved in fluency deficits in this group of patients. Relationships of fluency with both language and executive composite scores were significant, with the language relationship being higher.

In the FL group, the vspan measure of short-term memory capacity did not predict fluency scores, while the token test measure of language disturbance did. Dig- can and elimaze scores both predicted fluency performance, supporting the usual dysexecutive explanation of FL fluency deficits. The composite language and executive variables both predicted FL fluency performance, with a stronger prediction from executive than linguistic test. Overall, these correlational results for the two patient groups suggest a role for both linguistic and executive dysfunction in fluency deficits in both FL and AD groups. However verbal memory problems seem more pertinent in AD patients, while executive deficits seem more influential in FL patients. Scattergrams of the correlations reported in Table I1 were examined for evidence of outliers which might have influenced the obtained relationships, but there was no evidence that this was the case for either patient group.

DISCUSSION

Fluency tests are commonly used to assess “language function” in patients with dementing conditions. In the current study there was a significant correlation between fluency impairments in AD and poor performance on a test,of language comprehension, the token test. There was also a significant relationship between a measure of verbal short term memory (vspan) and fluency scores in AD. Inefficient short term memory in these patients might result in a tendency to forget which words had already been produced in the fluency test (Pasquier et al., 1995), resulting in poor performmce.

The results also suggested some executive involvement in poor fluency performance in AD patients. Fluency scores were correlated with digcan performance which

TABLE II. Correlations between fluency and cognitive test scores in AD and FL patients

Test AD patients FL patients

Vspan 0.41 8’ 0.131 Token 0.529‘ 0.478’ Digcan 0.505’ 0.537’ Elimaze 0.202 0.463’ ”Language” composite 0.547’ 0.395’ ”Executive” composite 0.421 ’ 0.567’

Significant at p<O.Ol, which accounts for the number of non- independent multiple comparisons.

demands selective attention. Deficits of attention are amongst the first, and most prevalent, signs of early AD (reviews in Spinnler, 1991 and in Parasuraman and Vax- by, 1993), with even mildly demented patients having problems in concentrating attention upon tasks which require effortful processing. Serious lapses of attention while attempting the fluency task might result in patients forgetting which category they were supposed to be gen- erating from, while more! minor lapses in attention might result in repetition of previously produced words. This supports the notion that cortical areas not primarily com- mitted to language may play a role in the verbal communication breakdown of AD patients (Bayles and Kaszniak, 1987; Alberoni et al., 1929; Della Sala et al., 1993) and suggests that the language deficits of AD are more multicomponential than those shown by “focal” aphasics (Bandera et al., 1991; Della Sala et al., 1993). However, the current study did not find a link between AD fluency performance and deficits of strategic planning (as measured by the elimaze test). This suggests that an impairment in the executive processes of strategy control is unlikely to be the cause of AD deficits in fluency.

In neuropsychological disorders other than the demen- tias, poor fluency performance is usually taken to indicate failures of executive function. Fluency deficits in those with FL lesions are routinely attributed to dysfunction in the executive control of retrieval strategies. The relationship between fluency and elimaze performance supports the predominant executive/strategic explanation for poor fluency performance in FL patients. There was also a significant relationship between impairment on the digcan test and fluency, suggesting that inability to focus attention selectively may have a role in FL patient deficits in fluency. However, there was also evidence to support the involvement of language deterioration in FL fluency impairment (Reitan and Wolfson, 1994); token test performance correlates well with fluency scores. Language impairment might be a serious confounding factor in interpretation of fluency deficits in FL patients. However, there was no significant prediction from the vspan short- term memory measure to FL fluency scores, and very few FL patients had impaired span. Short-term memory track-

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L. H. PHILLIPS ErAL.

ing problems were therefore not implicated in FL deficits in fluency.

It should be noted that the semantic fluency test used here is proposed to be less dependent on executive function than letter fluency tasks which require the generation of words beginning with a specified letter (Martin et al., 1994). Letter fluency tasks require suppression of the usual tendency to search for words by meaning (Pea t , 1974), and therefore are more dependent on executive processes of strategy formation. In AD patients, a major source of evidence to support the proposal that fluency deficits reflect language rather than executive dyshnction has been the finding of greater deterioration of semantic than letter fluency (e.g. Monsch et al., 1994; Rosser and Hodges, 1994; Pasquier et al., 1995; although for contrary findings see Rosen, 1980; Ober et al., 1986; Hart et al., 1988). The opposite pattern has been often reported in FL patients who show impairments in list generation with letter cues, but not with semantic categories (Ben- ton, 1968; Newcombe, 1969; Hecaen and Ruel, 1981; Stuss and Benson, 1986). It would be of interest in future studies to look at the relationship between letter fluency and measures of executive and language dyshction in FLJAD patients to see whether the results differed from the current pattern of correlations with semantic fluency.

It has been argued (Hart er al., 1988; Miller, 1984; Cronin-Golomb et al., 1992) that fluency measures reflect general intellectual dysfunction, indeed fluency tests were originally conceptualized to assess intelligence (Thurstone and Thurstone, 1949). Although fluency tests are quite highly sensitive to the presence of brain damage, they sometimes do not appear specific to any particular hctional deficit or brain lesion site (Reitan and Wolf- son, 1994; Pasquier et al., 1995). The evidence here does provide some support for the idea that fluency impairment might reflect a fairly general intellectual deficit, because in both AD and FL patients fluency impairments related to executive and language composite scores. However, there was also some degree of dissociation between the two patient groups as to the cognitive correlates of fluency. In AD patients vspan related to fluency, while elimaze did not. In FL patients elimaze performance related to fluency, while vspan did not.

These differences between the two patient groups in the pattern of correlations with fluency was not just a function of the more severe fluency deficit in AD patients. In an analysis where degree of fluency deficit was accounted for, the pattern of correlations with fluency in the AD and FL patient groups was not altered. This suggests that fluency tests do not just assess the severity of brain damage, but also may have a qualitatively different cognitive profile in different neuropsychological disorders. However, because the current analyses are correlational, no definitive conclusions about the causal

106 European Journal of Neurology . vO1 3 . 1996

pathways involved can be drawn. Also, caution must be urged in interpreting any of the cognitive tests used here as representative of any particular single cognitive h c - tion.

The current results have implications for neuropsychological use of fluency tests, alone or in test batteries. Such tests are often used to assess either “language” or “executive’’ processes; depending on the theoretical back- ground of the study, rather than any empirical justification for a particular interpretation. The current results suggest that in both AD and FL patients, language and executive factors may be important in determining fluency impairments, with the AD deficit weighted more towards language, and the FL deficit more toward executive dysfunction. Qualitative information about the h c - tional processes involved in fluency tests in both normal and patient populations is needed before scores can be interpreted as representing any particular cognitive deficit with confidence. Such a conclusion can also be ex- tended more generally to the incautious interpretation of other neuropsychological test scores in clinical studies. There is always more than one potential reason to fail a cognitive test, and the assumption that poor performance on any individual test indicates a specific cognitive dysfunction is often premature.

Acknowledgements We thank Hans Spinnler, MD, for his usefd comments on a previous version of the manuscript.

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