WORD-ASSOCIATION RESPONSES AND SEVERITY OF DEMENTIA IN ALZHEIMER DISEASE '"

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1 Psychological Reports, 1790, 66, O Psychological Reports 1970 WORD-ASSOCIATION RESPONSES AND SEVERITY OF DEMENTIA IN ALZHEIMER DISEASE '" FRANCIS EUSTACHE Univeniti de Caen CHRISTIANE COX, JASON BRANDT johns Hopkins UniuersiQ School of Medicine, Baltimore BERNARD LECHEVALIER AND LOUIS PONS Uniuersiti de Caen Summary.-To test the impairment of semantic memory in Alzheimer Disease, two groups of patients (one French and one American) were given a free-word-association task. Analysis showed a strong correlation between the scores of the Mini-Mental State Examination and an index of commonality of responses in both groups. As the severity of dementia increased, Alzheimer patients were less likely to give common responses. Our results are consistent with those of previous studies showing a relationship between dementia severity and impairment in semantic memory in Alzheimer Disease. Memory dysfunction is probably the most notable feature of all forms of dementia and is virtually obligatory for this diagnosis. The severity of memory loss may differ among types of dementia, but by itself is insufficient for differentiating dementias of different causes (Brown & Marsden, 1988). Recently, memory impairment has become a necessary criterion for the diagnosis of Alzheimer Disease in relation to other symptoms (McKhann, Drachman, Folstein, Katzman, Price, & Stadlan, 1984). Concerning verbal memory in Alzheimer Disease, deterioration of semantic memory (Martin & Fedio, 1983) as well as of episodic memory (Martin, Brouwers, Cox, & Fedio, 1985) have been reported. However, in the case of semantic memory, the data are controversial as to whether there is disorganization of, or impaired access to, semantic memory structures (Nebes, 1989). These conflicting results partially result from use of different experimental paradigms for assessing semantic memory. As pointed out by Brandt, Spencer, McSorley, and Folstein (1988), and in accordance with Shimamura, Salmon, Squire, and Butters (1987), the apparent semantic-processing defect (Weingartner, Kaye, Smallberg, Ebert, Gillin, & Sitaram, 1981; Weingartner, Grafman, Boutelle, Kaye, & Martin, 'Louis Pons died on May 13, In this article the coauthors wish to give a proof of their kiendship. Send correspondence to Francis Eustache, Service de Neurologie Dejerine, CHU Cdte de Nacre, Caen Cedex, France.

2 1316 F. EUSTACHE, ETAL. 1983) may be specific to tests of explicit memory and may be overcome by employing cognitive tasks that require memory only implicitly (Moscovitch, 1982; Nebes, Martin, & Horn, 1984). Furthermore, when these tasks are conducted without "effortful processing" at the time of stimulus presentation, normal semantic memory may be observed. While some aspects of the mental representation of lexical items may be weakened or degraded in Alzheimer Disease, the semantic network is not totally disorganized as assessed by semantic priming tasks. The discrepancies among studies could also be due to methodological problems. One is a recruitment bias in a disease that might consist of different subtypes (Martin, Brouwers, Lalonde, Cox, Teleska, & Fedio, 1986). Another methodological issue is that Alzheimer Disease is a developmental disorder since it involves both qualitative and quantitative changes in cognitive functions over time (Jorm, 1986). The aim of ths study was to measure the relationship between semantic memory and the severity of dementia. To this end, we employed a free-word-association task for assessing semantic memory in two groups of patients with Alzheimer Disease (one French and one American). The commonality of the responses given (frequency of responses, according to word-association norms) were correlated with the score on a widely used cognitive screening test. METHOD Patients All patients had received the diagnosis of probable Alzheimer Disease based on the clinical criteria of the NINCDSIADRDA (McKhann, et al., 1984). None of the patients had an history or signs of other major psychiatric or neurological diseases. Two groups of Alzheimer Disease patients, one French, one American, were assembled for this study. In the French group were 20 patients. They were 5 men and 15 women (age M = 66.9; SD = 8.9). AU belonged to the same out-patient neurological clinic and showed varied degrees of Illness. The US group consisted of 19 patients, 7 men and 12 women (age M = 72.6; SD = 7.9). They also belonged to a single neuropsychiatry clinic and showed varied degrees of illness. Procedure Each patient (French and American) was given the Mini-Mental State Examination (Folstein, Folstein, & McHugh, 1975) and a word-association test. For French patients, one list of 20 words was randomly selected from those of Palermo and Jenkins (1964). For American patients, the 13 words were as described by Pack and Pons (1985); see Table 1. The test instructions were: "I am going to read you a word. Upon hear-

3 WORD-ASSOCIATION: SEVERITY OF DEMENTIA 1317 ing the word, please tell me the first word that comes to your mind. Do not worry whether your response is appropriate. I will read you 20 [or 131 words in all and after each one, again, please answer me with the first word you think of." No other instructions were given. If the subject had any questions the instructions were repeated with emphasis on the subject's providing the first word that came to mind. During the test session the list was presented once [Time 11 and then repeated after a 1.5-min. interval [Time 21 with the same instructions for each presentation. During the 15-min. interval between Time 1 and Time 2, patients engaged in an unrelated conversation with the examiner. The rate of presentation of the word stimuh was determined by the rapidity of response by the subject, with the next new word stimulus following immediately upon the subject's response. TABLE 1 S T ~ UWORDS S AND SOURCEST A B C Altitude Bitter Mer Solitude Digestion Feuille Eclairage Nuit Soled Manger Loi Dieu Travail Amer Terre* Ennui* Soldat Chou-fleur Dur Aigle Estomac* Tige* Lampe* Reve* Jaune* Pain* Justice* Gaqon Lumikre SantC Bible* Earth Cabbage Hard Eagle Stem Lamp Dream Yellow Bread Justice Light Bible ta: List of 10 words in the free-recall test. These words are the third most common associations for the word stimuli on the same line of list B. B: List of 20 word stimuli selected from those of Palermo and Jenkins (1964) given to the French patients. Words marked with an * are the "biased words". C: List of 13 words for the American patients (Pack & Pons, 1985). For the French group only, 10 of the stimulus words were selected so that their third most common associations, according to the French norms, were items from a free-recall test administered immediately prior to Time 1. We call these 10 words "biased" because, in ths situation, the commonality of responses could be due to the priming effect from the free-recall test. In

4 1318 F. EUSTACHE, ETAL. addition, the Wechsler Memory Scale (Wechsler, 1969) was also administered to the French patients. Commonality and repetition indices.-the common&ty index was the number of the "Most Common Responses" given by each subject at Time 1 (MCR index). Most Common Responses are those words occurring with a frequency 7% or more in Palermo and Jenkins' Word Association Norms for the American sample and in a reference sample for the French. The 7% threshold for frequency was selected because responses occurring with a frequency of 7% or more represent half of the total number of responses in the reference samples. The number of responses repeated for a given stimulus at Times 1 and 2 was termed the Repetition Index (RR index). RESULTS US Group The mean values of the three measured variables (Mini-Mental State Examination, Most Common Responses, Repetition Index) are given in Table 2 and their Pearson correlations in Table 3. The Repetition Index is TABLE 2 MEAN VALUES ON THREE MEASURES FOR US GROL~P Measure M SD Mini-Mental State Examination 19.6 Most Common Responses 5.6 Re~etition Index 5.5 significantly correlated with the Most Common Responses. Moreover, the Most Common Responses and Repetition Index are both significantly correlated with scores on Mini-Mental State Examination. Thls indicates that as severity of dementia increases (decreasing Mini-Mental State Examination scores), Alzheimer Disease patients are less likely to give common responses and are less likely to give the same responses at both Time 1 and Time 2. TABLE 3 PEARSON CORRELA~ONS AMONG THREE MEASURES FOR US GROUP Measure Most Common Responses 2. Mini-Mental State Examination.56* 3. Re~etition Index.60*.55" French Groups Controls.-For comparison with the Alzheimer Disease group, a sample of normal volunteers was studied (N = 28; M age = 68.5 yr.; SD = 5.3). This

5 WRD-ASSOCIATION: SEVERITY OF DEMENTIA TABLE 4 MEAN VALUES OF MOST COMMON RESPONSES AND ~PETTTIoN INDEX FOR FRENCH CONTROL GROUP Measure M SD Most Common Responses Repetition Index sample consisted of 14 men and 14 women. Results are given in Table 4. Pearson correlations between Most Common Responses and Repetition Index was moderate (T=.57, p<.01). TABLE 5 MEAN VALUES FOR ALL VAIUABLES MEASURFD FOR FRENCH PATIENTS Measure M SD Mini-Mental State Examination Wechsler Memory Scale Global Most Common Responses Global Repetition Index Unbiased Most Common Responses Unbiased Repetition Index Biased Most Common Responses Biased Repetition Index Activated Responses Patients.-As described earlier, 10 of the stimuli were biased and 10 were not. The 20 stimd were first considered all together and then the 10 unbiased and 10 biased ones were considered separately. We did consider also the number of responses activated by the biased words. In addition, the TABLE 6 PEARSON CORRELATIONS FOR FRENCH GROUP Measure Wechsler Memory Scale 2. Mini-Mental State Examination, Global Most Common Responses.SO*, Global Repetition Index ll 5. Unbiased Most Common Responses.49'.57t.83t Unbiased Repetition Index , Biased Most Common Responses.36.86t.65t.74t Biased Repetition Index t *p <.05. tp <.01. Mini-Mental State Examination and Wechsler Memory Scale were also administered. The means are reported in Table 5. The Pearson correlations among these variables are given in Table 6. In addition, activated responses

6 1320 F. EUSTACHE. ETAL are significantly correlated with scores on the Mini-Mental State Examination (r =.45, p<.05). DISCUSSION The results of this study indicate an association between scores on the screening test sensitive to severity of dementia (Mini-Mental State Examination) and the index of commonality of responses (Most Common Responses) in both French and American patients with Alzheimer Disease. Furthermore, in the American group, scores on the Mini-Mental State Examination are correlated with Repetition Index but are not in the French group, regardless of which parameter used (biased or unbiased words or global score). These discrepancies can be related to those noted by Pack and Pons (1985) for normal subjects comparing two groups of French and American subjects in a free-word-association paradigm. In the present study, these differences may be due also to the fact that, in the French group, some of the words were biased. Whatever the situation (biased or unbiased), the Pearson correlation was moderately strong between scores on the Mini- Mental State Examination and Most Common Responses but was most important in the priming situation. Correlations were noted between Wechsler Memory Scale and global Most Common Responses, Most Common Responses for unbiased words but not with Most Common Responses for biased words. This last result can be due to the fact that Wechsler Memory Scale is not only a memory task but also requires attention, as pointed out by Kear-Colwell (1973). If the relation between a task measuring mostly episodic memory (Wechsler Memory Scale) and the commonality of word-association responses is unclear, the relation between severity of dementia assessed by the Mini- Mental State Examination and this index of commonality is very strong in both groups of patients. In our view, these results constitute an argument for a disturbance of semantic memory in Alzheimer Disease. Semantic deficits are a common component of the cognitive decrement produced by Alzheimer Disease but the nature of the cognitive dysfunction responsible for demented patients' problems on different semantic tasks is still not clear (Nebes & Brady, 1988; Nebes, 1989). Coupled with the diagnostic uncertainty, patients with clinical Alzheimer Disease often present markedly variable patterns of preserved and impaired cognitive abilities. Inconsistent results concerning semantic and implicit memory in this disorder can be explained by bias of recruitment, especially when small samples are studied. Free-word-association tests may be useful in assessing semantic memory in demented patients. Santo Pietro and Goldfarb (1985) reported a characteristic pattern of responses in patients with senile dementia which included marked reduction of "paradigmatic responses" (i.e., words within the same

7 WORD-ASSOCIATION: SEVERITY OF DEMENTIA 1321 grammatical class, such as "short" for the stimulus word "tall"), and a marked increase in unclassifiable and multiword responses not previously reported in the literature. The effects appeared linear and were correlated with severity of dementia. However, as pointed by these authors, the major lirnitation of their study lies in the methods of identifying senile dementia, and particularly that they did not identify demented patients by etiology. The same remarks apply to the study of Gewirth, Shndler, and Hier (1984), using word-association tests. These authors showed that, in dementia, the mechanism that generates paradigmatic responses becomes progressively less efficient. Consequently, more idiosyncratic responses emerge. In our study we did not measure the category of responses (paradigmatic, syntagmatic, etc.) but, consistent with the previous studies, showed that severity of dementia had an important influence on typicality of word-association responses. In a recent study, Brandt, et al. (1988) showed that moderately demented Alzheimer Disease patients display impairment of both explicit and implicit memory using a free recall of a word list and a subsequent word-association test. Another test for assessing semantic memory is word fluency, and most of the studies have showed a deficit in Alzheimer Disease (Rosen, 1980). However, Fischer, Gatterer, Marterer, and Danielczyk (1988) pointed out that this perturbation is not specific to Alzheimer Disease but was noted also in multi-infarct dementia. Responses to free-word-association tasks may be more specific to Alzheimer Disease, since Pons, Bielecki, Lechevalier, Schupp, and Morin (1986) found relatively normal semantic processes in Parkinson disease. Further studies using such tasks and comparing groups of mildly demented patients who differ by etiology are necessary to test the hypothesis of a specific decrement of commonality of responses in Alzheimer Disease. REFERENCES BRANDT, J., SPENCER, M., MCSORLEY, P, & FOLSTEIN, M. F. Semantic activation and implicit memory in Alzheimer Disease. Alzheirner Disease and Assoczated Disorden, 1988, 2, BROWN, R. G., & MARSDEN, C. D. Subcortical dementia: the neuropsychological evidence. Neuroscience, 1988, 25, FISCHER, P., G A ~ E G., R, MARTERER, A,, & DANIELCZYK, W. Nonspecificity of semantic impairment in dementia of Alzheimer's type. Archives of Neurology, 1988, 45, FOLSTEIN, M. F., FOLSTE~, S. E., & MCHUGH, P R. "Ahni-Mental State": a practical method of grading the cognitive state of patients for the clinician. Journal of Psychiatric Research, 1975, 12, GE~TH, L. R., SHINDLER, A. G., & HER, D. B. Altered patterns of word association in dementia and aphasia. Brain and Language, 1984, 21, JORM, A. F. Controued and automatic information processing in senile dementia: a review. Psychological Medicine, 1986, 16, KEAR-COLWELL, J. J. The structure of the Wechsler Memory Scale and its relationship to "brain damage." British Journal of Social and Clinical Psychology, 1973, 12,

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