Downloaded from http://jnnp.bmj.com/ on July 31, 2017 - Published by group.bmj.com Journal of Neurology, Neurosurgery, and Psychiatry 1989;52:334-337 Defective concept formation in Parkinsonians is independent from mental deterioration CARLO CALTAGIRONE, AUGUSTO CARLESIMO, UGO NOCENTINI, STEFANO VICARI From the Clinica Neurologica, II Universita di Roma, Rome, Italy SUMMARY An extensive neuropsychological battery (the Mental Deterioration Battery) was utilized to distinguish, within a sample of 24 idiopathic Parkinsonians, those showing signs of diffuse mental deterioration (n = 9) from those without deterioration (n = 15). Performances ofcontrol subjects on a wide range of tests exploring mnesic, visuo-constructive, linguistic and general intellectual functions (n = 21) did not differ from analogous performances ofParkinsonians without signs of diffuse mental deterioration. The Wisconsin Card Sorting Test was then used to verify the hypothesis that a selective impairment of cognitive functions subsumed by the integrity of frontal lobes could be demonstrated in Parkinsonian patients. Our results provide evidence that in this task, defective performances are obtained by Parkinsonians and even by patients without signs of diffuse cognitive impairment. These findings seem to confirm that a deficit in concept formation, maintenance and shifting is largely independent of the dementia frequently noticed in Parkinson's disease. It is no longer disputed that there is a prevalence of dementia in patients affected by Parkinson's disease which is higher than in the normal population.' Moreover, even when diffuse mental deterioration has been absent in Parkinsonian patients, selective deficits of cognition may be found.2 Some authors claim that an asymmetrical pattern of cognitive performances can be found in Parkinsonians with worst scores on visuo-spatial tasks.34 However, this selective impairmenf of visuo-spatial functions has not been confirmed when the motor-speed component of these tasks is taken into account.25 Impairment of mnesic functions seems to be better documented. Long term recall of visual and verbal material seems to be affected even in the presence of normal scores on tasks of short term memory and long term storage.67 After the description by Bowen et ar of a selective disorder in concept formation in Parkinsonians, many authors have described these patients as particularly compromised in tests sensitive to lesions of frontal Parkinsonians, the weight of a more general mental deterioration should be checked. In most ofthe studies pointing to an impairment of frontal functions in patients affected by Parkinson's disease this factor has not convincingly been ruled out. The presence of a more global cognitive impairment has generally been excluded on the basis of the IQ' derived from the WAIS, while a detailed survey of mnesic, visuoconstructive and general intellectual functioning is often missing.8 10 To verify the hypothesis that there is a selective deficit offunctions normally subsumed by the integrity of frontal lobes in Parkinsonians, we planned a study in which a careful evaluation of mental functioning was performed together with a specific assessment of concept formation, maintenance and shifting. Material and methods Neuropsychological assessment To assess the presence of a general impairment of mental functions we used the Mental Deterioration Battery (MDB). lobes.>" This consists of eight tasks capable of yielding distinctive In any case, before positing that a selective impair- information about mnesic, linguistic, visuo-constructive and ment of cognitive functions is actually present in general intellectual functions. The battery has been extenin described a 1 sively Address for reprint requests: Prof C Caltagirone, Institute of MDB tests and the previous study.'2 In table the single corresponding cognitive functions invesNeurology, II Universita di Roma, Osp S Eugenio, P le dell'Umanetigated are summarised. As demonstrated in a previous simo 10, 00144 Roma, Italy. paper,'2 the MDB is able to classify correctly normal and deteriorated subjects on the basis of the number of pathoReceived 19 January 1988 and in final revised form 8 August 1988. Accepted 26 August 1988 logical performances. A patient is classified as demented 334 Downloaded from http://jnnp.bmj.com/ on July 31, 2017 - Published by group.bmj.com Defective conceptformation in Parkinsonians is independentfrom mental deterioration 335 Table I Tasks used to build up the MDB: the corresponding Table 3 Mean scores (and standard deviations) normalised cognitivefunctions investigated by the single tests are indicated in z points obtained on various MDB tasks by control subjects Word Fluency (WF) Phrase Construction (PC) Rey's Verbal/sor memory test\long Verbal attainments Vra tanet trrealRS) termn recall (RLT) Immediate Visual Memory (IVM) Visuospatial Memory General Intelligence on visuospatial data Copying designsjfree copy (CD) \copy with landmarks Visuoconstructive (CDL) functions when he obtains four or more pathological performances on the eight tasks of the MDB. The cutting scores differentiating normal from pathological performances are derived from previously published normative data.'2 The test used to assess the ability of concept formation, maintenance and shifting was the Wisconsin Card Sorting Test (WCST), which was administered in full measure (128 cards) according to the procedure employed by Milner."3 In the evaluation of the results we considered the categories obtained together with the number of perseverative and total errors produced. As originally described by Milner,'3 and subsequently confirmed by other authors"'5 patients with frontal lobe damage do particularly badly in this test. In these studies the performance of patients with frontal lobe damage was indicative of a defective acquirement of categories, and exhibited a perseverative behaviour in comparison with both normal subjects and patients with lesions restricted to posterior regions of the brain. Subjects Twenty four consecutive outpatients of the Neurological Clinic of our University showing clinical evidence of idiopathic Parkinson's disease were included in our study. None of them had clinical signs of cerebrovascular disease, alcoholism or depression nor had they undergone thalamotomy or other surgical procedures for the relief of Parkinsonian symptoms. The mean length of the illness was 4-1 years (SD 1-4). All the patients demonstrated a level of disability between stages II and III of the Hoehn and Yahr scale." Eighteen Parkinsonian patients were in a pharmacological wash-out period; the others were receiving therapy with levodopa alone or associated with anticholinergics. Twenty one subjects, most of them relatives of the Parkinsonian subjects, without clinical evidence of Table 2 Age and literacy levels of control and Parkinsonian subjects Age (years) Years of schooling Controls (n = 21) Parkinsonians 596 (7-8) 7-0 (41) 24) t p 615 (7-6) 0.81 6-5 (33) 045 NS NS = Controls Verbal memory Coloured Raven's Progressive Matrices (PM'47) (n and Parkinsonian patients; statistical comparisons on Student's t test are also reported (n WF CF RST RLT IVM PM'47 CD CDL = 21) 016 (10) 0-15 (1-0) 0 31 (1-0) 0-17(0.97) 015(086) 0-25 (0 79) 0-23 (0-58) 0-23 (0 84) Parkinsonians (n = 24) t p -0-14 (0-95) -0 13 (0-97) -0-27 (0 89) 10 0 99 2-05 108 1-04 0-96 1-62 1-49 NS NS -014(10) -0-19 (1-0) -0-13(1-1) -0.21 (1-1) -0-20 (1-2) <0-05 NS NS NS NS NS neurologic or psychiatric disorders were used as the control group. Results Although the age and literacy levels demonstrated by Parkinsonians and control subjects were comparable (table 2), performance scores for the two groups on the various tasks of the MDB were adjusted for age and years of schooling on the basis of the standard procedures reported in a previous paper.'2 Moreover, so that results obtained in tests having different ranges could be compared, the adjusted scores were transformed into normalised Z scores. The results obtained on various MDB tests by both Parkinsonian and control groups are summarised in table 3. Parkinsonian patients obtained lower scores than control subjects on most of the tasks. A two-way analysis of variance, in which the results obtained in the eight MDB tests were taken into consideration, reveals that the difference between the two groups approaches the level of significance (F = 3-6; p = 006). These results are in agreement with the data of several other authors."7'8 Brown and Marsden2 suggested that in non-selected Table 4 Mean scores (and standard deviations) normalised in z points obtained on various MDB tasks by control subjects and non-demented Parkinsonian patients; statistical comparisons on Student's t test are also reported Controls (n= 21) WF CF RST RLT IVM PM'47 CD CDL 0-16 (1-0) 0-15(1.0) 0.31 (1-0) 0-17 (0-97) 0-23 (0 84) 0.15 (0-86) 0 25 (0-79) 0-23 (0-58) Non-demented Parkinsonians (n= 15) t p 0-10 (0-91) 0.36(0-74) 0-18 (0-75) 0-29 (0.83) 0 33 (0-69) 0 40 (0-95) 0-27 (0-80) 0-35 (0-82) 0-20 0-64 0-41 NS NS NS NS NS NS NS NS 0-39 0 40 0-80 0-05 0-61 Downloaded from http://jnnp.bmj.com/ on July 31, 2017 - Published by group.bmj.com Caltagirone, Carlesimo, Nocentini, Vicari number of pathological performances below four and then were classified as non deteriorated. A comparison of performances on the various MDB 0tasks obtained by control subjects and non-Controls o-----0-2deteriorated Parkinsonians is reported in table 4. A Parkinsonians * *o ND two-way analysis of variance does not reveal any -0.4D Parkinsonians significant difference for any factor (F always < 1). -0-6No significant difference can be detected even in the -0.8comparisons of single tests. Profiles exhibited on the various tasks of MDB by -1. control subjects and Parkinsonian patients are shown WF PC RST RLT IVM PM CD CDL in the figure. Profiles of performances obtained by controls and non deteriorated Parkinsonians are Fig Neuropsychological profiles exhibited on the MDB by almost superimposable while the profile shown by our samples ofcontrol subjects and Parkinsonian patients affected (D) or not (ND) by mental deterioration. deteriorated Parkinsonians is quite different from these. The WCST results for the three groups, control populations mean performance values may be affected subjects, non-demented and demented Parkinsonians, significantly by the inclusion of subjects suffering from are summarised in table 5. mental deterioration. Since the purpose of our study scores obtained did not fit a that Given performance in was to detect a possible selective deficit in cognition was performed statistical distribution, normal Parkinsonian patients without clinical and neuro- by means of a non parametric analysis test (Mann-Whitney U psychological signs of dementia, we subdivided the test). total sample of Parkinsonians into two groups. On the Non-deteriorated Parkinsonians produced sigbasis of MDB performance, the patients of the total nificantly more perseverative errors and obtained sample were identified as being affected or not by fewer categories (this difference only approaches statof was composed The first group deterioration. mental significance: p = 0-07) than control subjects. In istical 15 patients classified as not deteriorated while the the comparison between performance scores demonremaining nine patients, classified as deteriorated, strated by the two subgroups the made up the second group. The prevalence of de- difference regarding the numberofofParkinsonians categories and of mentia in our group of Parkinsonians is comparable perseverative errors approaches significance with that reported in larger samples.'920 (categories: p = 005; perseverative errors: p = 0.06), The two subgroups of Parkinsonians did not differ while the difference in the number of total errors as regards mean age (non deteriorated: 60-0, SD 8 1; reaches the level of statistical significance. No sigdeteriorated: 63 5, SD 6-9; t = 1 -1, p = NS) and years nificant difference was detected in the number of total of schooling (non deteriorated: 6-9, SD 2-2; between normal subjects and non-deteriorated deteriorated: 5-7, SD 2-0; t = 1-4, p = NS). Non errors deteriorated Parkinsonians had a mean duration of Parkinsonians. disease (3-6 years; SD 1.2) significantly shorter than deteriorated ones (4-8 years; SD 1 3) (t = 2 3; p = Discussion 0-03). Thirteen of the non deteriorated Parkinsonians were in a pharmacological wash-out period while the Several authors have described impaired performremaining two patients were receiving levodopa. ances on "frontal tasks" in patients affected by In the deteriorated group, five patients were in a Parkinson's disease which did not show clinical and pharmacological wash-out period. The remaining four neuropsychological signs of general intellectual patients were receiving levodopa alone (two patients) deterioration. Bowen et a15 found that Parkinsonian or in association with anticholinergics (two patients). patients formed significantly fewer concepts, as All the control subjects demonstrated on the MDB a measured by WCST, than controls matched for age, 336 0.40.2- -- -1 *0 Table 5 Medians (and ranges) ofscores obtained on WCST by control subjects, non-deteriorated and deteriorated Parkinsonians; statistical comparisons on Mann- Whitney U test are also indicated Control subjects (n = 21) Categories Total errors Perseverative errors 5-8 (3-6) 360 (1-72) 10-0(0-52) z p Non-demented Parkinsonians (n = 15) 1-8 1-4 2-0 NS NS =004 50 (1-6) 420 (14-82) 250 (3-71) z p Demented Parkinsonians (n = 9) 1.9 2-0 1-8 NS = 004 NS 20(0-5) 580 (38-74) 340 (22-40) Downloaded from http://jnnp.bmj.com/ on July 31, 2017 - Published by group.bmj.com Defective conceptformation in Parkinsonians is independentfrom mental deterioration 337 literacy and verbal WAIS IQ. For Parkinsonian patients. " Furthermore, a reduction of dopamine patients with normal IQ Lees and Smith9 reported content and of its metabolites in frontal cortical areas difficulty in shifting conceptual sets and a per- has been found in the brain ofParkinsonian subjects.2' severative behaviour on both the modified WCST and This finding is probably related to the degeneration of Benton's Word Fluency test. A similar shifting a mesocortical dopaminergic pathway projecting from aptitude disorder was observed in tests of block and the mesencephalon to cingulate, entorhinal and frontal cortex.22 animal sorting and finger pushing sequences.'" In these studies a general intellectual impairment was excluded on the basis of a normal WAIS IQ. Nevertheless, the WAIS, a battery of tests widely used References for determining the intellectual level of normal I Brown RG, Marsden CD. How common is dementia in Parkinson's disease? 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Neurology 1980;30:1326-30. ergic activity in the caudate nucleus of Parkinsonian Downloaded from http://jnnp.bmj.com/ on July 31, 2017 - Published by group.bmj.com Defective concept formation in parkinsonians is independent from mental deterioration. C Caltagirone, A Carlesimo, U Nocentini and S Vicari J Neurol Neurosurg Psychiatry 1989 52: 334-337 doi: 10.1136/jnnp.52.3.334 Updated information and services can be found at: http://jnnp.bmj.com/content/52/3/334 These include: Email alerting service Receive free email alerts when new articles cite this article. Sign up in the box at the top right corner of the online article. Notes To request permissions go to: http://group.bmj.com/group/rights-licensing/permissions To order reprints go to: http://journals.bmj.com/cgi/reprintform To subscribe to BMJ go to: http://group.bmj.com/subscribe/
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