Normative data for two neuropsychological tests sensitive to frontal dysfunction

Original Articles Ital I Neurnl Sci 17:201-209, 1996

Normative data for two neuropsychological tests sensitive to frontal dysfunction Pomati S., Farina E., Magni E., Laiacona M. ~. Mariani C.

Unitgz di Neurologia Riabilitativa, I.R.C.C.S. Centro "S: Maria Nascente" - Fondazione Don Carlo Gnocchi, Universit?~ di Milano; 1 Fondazione Sah,atore Maugeri Clinica del Lavoro e della Riabilitazhme, Servizio di Neuropsicologia (Divisione di Neurologia), LR.C.C.S., Veruno (No). Italy

Interest in frontal functions has progressively hwreased over recent yealw: however, despite this. there are only a few '~frontal" rusks for which lmlian normative data are available. The objective of this study was to obtain reference values for two frontal tests from a random sanq~le ~f normal adults: the .fir~'t (the Test ~]" Classification and Recall of Pictures) has been shown to reveal selective impairnwnt in patients with unilateral frontal excision; the second (the Odd-Man-Out Test) derives from tasks which have been used to evaluate .fi'ontul functions hz animals and detect.frontal impairment in Parkinson patients. We tested 100 nomzal subjects, aged 22 to 79 years, stratified bv education according to the Italian school system. The correction grids for both tests are also presented. The usefulness of these tests is represented not only by their sensitivity to frontal impairment, but also hy the possibili~ of dissociating the various cognitive aspects of frontal lobe dysfunction,

Key Words: Normative study - - Frontal functions - - Neuropsychotogical tests.

Introduction

Interest in frontal functions has progressively increased since the first classical descriptions of behavioral disturbances and intellectual deficits in patients with frontal lesions [1 I, 15], and we now know that the ability to pertbrm many different cognitive functions may be dis- rupted by damage to the frontal lobes or their intercon- nections [1, 25, 26]. The neuropsychological and behavioral disturbances associated with frontal lobe damage can be roughly classified into problems of starting, dif- ficulties in making mental or behavioral shifts (with a tendency to perseveration), problems ill stopping or modulating ongoing behavior with "loss of control", deficient self-awareness, and the loss of planning with the impairment of abstract aptitude [6, 15- t 7, 27]. Significant frontal-like deficits have also been recently reported in some diseases that were not originally considered to be associated with cognitive deficits, such as Parkinson's disease and multiple sclerosis [2, 7, 14, 21 ], and a new type of degenerative dementia with prominent frontal symptoms has been described [12, 18]. Despite this interest, there are only a few tasks which have the specific purpose of testing frontal functions for which Italian normative data are available [20. 24J. In this paper, we present normative data relating to two "frontal" tests. In the Test of Classification and Recall of Pictures, described by lncisa della Rocchetta in t986 [13], the subject is first asked to classify items, then to recall them (immediately and ~'ter a delay), and finally to explain the criteria used in the categorization. The task

has been shown to reveal selective impairment in categorization in patients with unilateral frontal excision, and impaired recall in patients who have undergone left temporal tobectomy: ill a previous study, we also used this task to identify frontal dysfunction ill patients with Par- kinson's disease [8]. The Odd-Man-Out Test [9] derives t¥om tasks which have been used to evaluate frontal functions in animals [22], and has been used to detect frontal impairnlent in Parkinson patients. The subject is required to indicate which of a set of letters or shapes is different from the others on two series of cards, alter- nately using two rules of classification for successive trials. The usefulness of these tests is represented not only by their sensitivity to frontal impairment, but also by the possibility of dissociating the various cognitive aspects of frontal lobe dysfunction. The Test of Classification and Recall of Pictures can be considered a sorting task which primarily explores concept formation and secondarily shitting aptitude, or "'the ability to reorganise behavior according to the requirement of the task" [25l; but it is also a task which amplifies the need for self-directed planning in generating task-specific strategies (it is well known that patients with frontal excision have great difficulty in self-directed behavior and oRen appear to look for an external cue to guide their performance) [17]. On the other hand, the Odd-Man-Out Test emphasises not only shifting abilities, but also the ability to maintain a mental set tbr as long as necessary (a mental set can be defined as a state of brain activity which predisposes a subject to respond in one way when various alternatives are available) [9]. Moreover, a practical advantage of the

Received 7 August 1995 - Accepted in revised form 11 November 1995 201

The Italian Journal of Neurological Sciences

first test is that verbal memory can be assessed alongside frontal functions; the second test allows mental process- es to be followed step by step, and is easy enough to be usefully administered even to patients who cannot per- form more demanding tasks, such as the Wisconsin Card Sorting Test.

Methods

We tested 100 normal subjects, aged 22 to 79 years, stratified by education according to the Italian school system (mean age 51.6 years; mean education 10.16 years); 42 were males and 58 females. Although none of our subjects underwent any particular diagnostic examination, we excluded those with a history of any disease potentially conditioning a CNS dysfunction, such as cerebrovascular disease, Parkinson's disease, seizures, a history of drug or alcohol abuse, en- docrine disorders (particularly of the thyroid gland), or any systemic failure of clinical relevance. MMSE [10] was performed in order to exclude subjects with cognitive deterioration (those with a score of less than 25).

Test of Classification and Recall of Pictures The test and the procedures adopted were the same as those used by Farina et al. [8]: i.e., a slight modification of the original version by Incisa della Rocchetta [13]. The stimulus material consisted of 36 coloured pictures (7 × 8 cm). The items were selected with the aim of con- structing a symmetrical set consisting of three major categories: food, household items and animals. For each of these categories, four sub-categories were formed (making a total of twelve). Three items were then assigned to each sub-category. The twelve sub-categories were: fruit (banana, apple, orange), vegetables (onion, tomato, green peas), meat (steak, roast beef, roast chicken) and sweets (cake, pudding, caramels) for the food category; kitchen items (teapot, pitcher, cup), workshop tools (hammer, paintbrush, saw), parts of a house (window, door, roof) and writing tools (pen, pencil, ink) for the household items category; birds (parrot, swallow, duck), insects (bee, spider, butterfly), cats (cat, lion, leopard) and hors- es (horse, donkey, zebra) for the animal category. It must be underlined that this set was not intended as a model for scoring the subjects' classifications, any self- consistent arrangement being permissible. The pictures were arranged on a large desk in a pseudo-random fa- shion, and the subjects were told that they were about to be given a memory test in which they had first to arrange the pictures of common objects into groups, in any way that they thought would make it easier for them to remember the names of the objects. There was ample free space on the table to allow the cards to be easily mani- pulated. The subjects were allowed to work without any time constraints, but those who took less than three minutes to arrange the cards were invited to continue look- ing at the arrangement up to the three-minute limit. Upon completion of categorization (the subjects were

asked if they had finished), the examiner covered the pictures and asked the subjects to recall every picture they could remember (if the name could not be remembered, a full description of the picture was considered acceptable). Once again, there was no time limit, but the recall procedure was stopped when the subject was unable to remember any new item after a one-minute interval. After about 45 minutes, the subjects were again asked to recall as many of the items as they could. The pictures were then uncovered and the subjects were asked to name the categories they had formed; every name had to identify clearly the procedure used for the categorization. A name had also to be given to all of the pictures. During the interval between the immediate and delayed recall, the MMSE and the Odd-Man-Out Test were performed. The measures of recall and categorization considered in the evaluation of the test were the same as those described in the original paper by Incisa della Rocchetta [13]. The measures of recall were the number of items remembered during the immediate and delayed recall sessions (a picture was considered correctly recalled if the subject could provide the right name, an acceptable syn- onym or a full description of it); and the number of categories recalled (a category was considered correctly recalled if at least one of the pictures belonging to it was recalled); instrusions were the items reported by the subject but not present in the experimental set (any mis- identification was considered correct). The measures of categorization were the number of categories sorted (that is, the number of groups the subjects had specified when confronted with their own card arrangements), the overlap errors (the subject had not clearly separated the categories, so that some items in one category could also have been correctly placed in anoth- er) and the number of items in remainder categories (a remainder category (RC) was defined as a subset of items that subjects treated as residual members of a major category, without any further classification; for example, if they arranged the meat on one side and all the other food items on the other, interpreting them only as "other things to eat"); misplaced items were the items not properly belonging to the category in which they had been placed (e.g. "chicken" in the category of "fruits"). Finally, uncategorized items (NC) were the pictures that the subjects had left unsorted after categorization. Although all of these measures were calculated, only those which had been previously demonstrated to be sensitive to memory impairment or frontal damage were analysed: that is, the immediate and delayed recall scores, the number of categories sorted, the number of items in remainder categories and the uncategorized items.

Odd-Man-Out Test The test consists of two parts, which will be described separately.

Part One Two packs of 16 cards (9 × 12 cm) were used, with eight of the cards showing three geometrical shapes ("shape"

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cards) and eight showing three letters ("letter" cards): on each card, the three items were chosen in such a way that two of them could be sorted according to their shape and two according to their size (e.g.: on a "shape" card, two of the shapes were the same and the third different, and two were small and the third large - see Fig. 1). The subjects were asked to point out which was the odd-man- out (i.e. which item was different from the other two on the card). The items were randomly distributed on each card so that it was not possible to choose the position of the item as a sorting criterion. The examiner sat in front of the subjects, showed them the cards of a pack one at a time, and asked them to indicate the odd-man-out (warning them that they should always choose in according to the same rule): if a subject decided that the odd-man-out for the first card should be based on size, the "size" criterion had to be used for all of the pack. The examiner told the subjects each time they had chosen an incorrect item (i.e. when they had used the other criterion or had indicated a "common item"), and drove them to try again until they had found the correct item. When the first pack had been gone through, it was placed on the table in front of the subjects and they were then shown the second pack in the same way as the first; however, this time they were told they had to indicate the odd-man-out according to a different criterion (i.e. the one they had not used for the first pack). When the second pack had been gone through, the examiner picked up the first pack again and asked the subjects to repeat the task according to the rule they had already used for that pack. Five other trials followed, with the two packs being alternated in the same way. After the eighth trial, the subjects were asked to reveal which criterion they had used for each pack and then, after their answers had been recorded, two more trials were performed. The evaluation criteria were the total number o f incorrect choices, separating those made without feedback from the examiner ("first-type errors": sorting index) from those made with feedback ("second-type errors": perseveration index). The sorting index was considered a measure of the ability of the subject to use a reasonable sorting criterion: a large number of errors was suggestive of random performance and an unstable mental set; the perseveration index, indicated the inability to use a new rule, (ignoring the previous one), despite the feedback received (the examiner told the subjects whenever their choice was incorrect). The original evaluation criterion [9] was the number of correct choices made in each trial but, since our aim was to obtain a practically usable and easily recorded score, we decided to consider the total number of incorrect choices (with the sub-division described above).

Part Two This involved the use of four packs of 12 cards ( 9 x 12 cm), two of which (the "shape set") had cards showing geometrical shapes and the other two (the "letter set") had

D Fig. 1. Odd-Man-Out test: an example o f a "shape '~ card. Subjects have to indicate which of the three items on the card they think is different from the other two using one of two possible rules: they can choose according to shape (diamond) or according to size (small rectangle).

cards showing letters. Every card included four items chosen in such a way that three of them could be sorted according to size, three according to shape and three on the basis of their open or filled form. The items were randomly distributed on each card so that it was not possible to choose its position as a sorting criterion. The "shape set" was presented to the subject just after the first part of the Odd-Man-Out Test (Part Two/A); the "letter" set about 20 minutes later, after the "delayed recall" of the Test o f Classification and Recall o f Pictures (Part Two/B). The examiner acted in the same way as during the first part of the test, but the possible criteria that the subjects could choose to indicate the Odd-Man- Out were not two but three. The evaluation criteria were the same as for the first part, the perseveration index being the sum of the errors made after the first and (if it occurred) the second feedback. The following measures of the two parts of the test were analysed: - P a r t One: first-type (range 0-160) and second-type errors (range 0-160). - P a r t Two/A and Part Two/B: first-type (range 0-120) and second-type errors (range 0-240).

Statistics

An analysis of co-variance was made for each of the test in order to obtain the best linear model that could explain the variability in the scores. An evaluation was made as to whether there was a significant effect due to age, education and sex, the effect of the concomitant variables being first assessed individually and then stu- died inside a simultaneous regression model to partial out their overlap; the effects were included in the final model only if they were still significant after this adjustment. A model of expected scores was computed for each test, and then corrected in such a way as to make all of the subjects comparable in terms of age and education, and to control the possible effect of sex as a variable. The internal and external limits of tolerance of the adjusted scores were calculated, the former indicating the

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TABLE 1. Test of Classification and Recall ~ Pictures: mean values by age group (standard deviations).

Age 20-29 30-39 40-49 50-59 60-69 t>70 Total

Immediate recall 25.42 28.07 24.43 21.12 18.64 20.00 22.38 (6,71) (5.14) (4.09) (6.46) (5.22) (4.00) (6.25)

Delayed recall 24,17 28.43 24.29 20.04 18.36 19.69 21.89 (6.51) (4.67) (5.03) (6.77) (6.21) (4.27) (6.64)

Number of categories 10.08 10.57 9.14 8.72 9.64 9.92 9.56 (1.44) (3.08) (3.18) (3.31) (2.38) (2.78) (2.83)

Items in remainder categories 0,91 2.92 3.07 2.48 4.09 1.69 2.69 (2.15) (3.98) (5.74) (4.63) (2.67) (3.47) (4.01)

Uncategodzed items 0.00 0,00 0.14 1.36 1.32 1.54 0.85 (0.00) (0.00) (0.36) (3.25) (2.70) (2.70) (2.33)

limit for discriminating {with a confidence level of 95%) the worst 5% of the population, and the latter for deter- mining (with the same confidence level) the best 95% of the population. Therefore, the subjects whose score was above the internal limit were considered normal and those whose score was below the external limit "'abnormal" with a controlled risk. Between the two limits of tolerance there is a region where no controlled judgement or unequivocal assignment is possibIe: any subjects with a score falling between the inner and the outer tolerance limits hits to be classitied as a "'borderline" case. The width of the region of uncertainty is inversely pro- portional to the size of the sample: lbr a sample of 100 subjects, and using non-parametric unidirectional limits of tolerance [5], the region of uncertainty is defined by values corresponding to the 2nd and 10th worst observations included. In addition, equivalent scores (E.S.) were detined lbr each test and interrelated with the adjusted scores. The E.S. [5] range from 0 to 4 : 0 indicates an adjusted score that is lower than that of the worst 5% of the normad population, with a confidence level of 95%; 4 refers to an adjusted score that is equal to or better than the central value of the control population: 1, 2 and 3 are interme- diate between 0 and 4 on a quasi-interval scale. For a sample of 100 subjects, the four vah|es of the adjusted scores which identify the five E.S. are the 2nd, 10th, 25th and 50th observation. The use of E.S. makes it possible to compare the scores obtained by the sante subject at different tests. Whereas the lower limit of the "borderline" region of the adjusted scores always coin- cides with the cut-off point between the E.S. of zero and one, its upper limit generally falls within the range of E.S. = 2 and sometimes E,S. = 1 {also see Tables 1II and VI). For each of the tests, the tables show: a) the mean values for each age group; b) the values identifying the three diagnostic regions of

the adjusted scores and the subdivision of the adjusted scores into areas of E.S.;

c) the correction values to be added to or subtracted fl'om the raw score for each patient on the basis of his/her age, education and sex; no correction should be ap- plied to the lowest and highest scores (the maximum and the minimum).

Results

A) Analysis of the Test of Classification and Recall of Pictures Table I shows the mean scores for each measure of the different age groups. Age, education and sex were all found to affect significantly (p<0.000t) the scores for both immediate iF 1.96= t5.9, 34.5 and 13.9 respectively) and delayed recall (F 1,96= 16.6, 16.8 and 16.6 respectively) even after the effect they had in common with the other variables had been partialled out. An education effect was also evident on the uncategorized items measure IF 1,96 = 5.4, p = 0.022). Nothing else of statistical significance was fi)und. The statistical model ~vhich proved to be most effective in reducing the residual variance in immediate recall was: y = 22.38 + 5.85 [log ( 100-age)-3.821 + 4.51 [(,/education)-3.12l - 1.79 (if male) or + 1.79 (if female); for delayed recall, it was: v=21.89-0.15 (age-51.60)+0.57 {education-10.2) - 2.23 (if male) or +2.25 (if female); and for uncategorized items, it was: y = 0.85 - 1.08 [{4education)-3.121. Table 11 shows the adjustments to be added to or sub- stracted from the raw scores in various age/education combinations. For the combinations not reported, either an interpolation between the reported adjustments has to be made, or the adjustment has to be directly calculated using the linear models above and reversing the sign of the parameters. Table III shows the diagnostic regions of the adjusted scores, as well as the values delimiting the E.S. for each measure, With regard to the correlations between the different test measures, it is worth noting that the lowest observed correlation was between NC and RC errors (r=0.035), whereas immediate and delayed recall were closely re- lated {r = 0.896).

B) Analysis of the Odd-Man-Out Test Table IV shows the mean scores for each part of the different age groups. For Part One, age, education and sex were all found to affect significantly the number of first-type errors (F 1,96= 11.4, 16.1 and 4.8 with p=0 . 001 , 0.0001 and 0.030 respectively); the number of second-type errors was

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TABLE I1. Test of Classification and Recall of Pictures: correction grids.

Immediate Recall Age 25

Educ. M

5 2.89 8 0.22

13 - 3.29 17 - 5.62

35 45 F M F M F

-0.70 3.73 0,14 4.70 1.11 -3.37 1.05 -2.54 2.03 -1.56 -6.88 -2.45 -6.04 -1.47 -5.06 -9.21 -4.78 -8,37 -3.81 -7.40

55 65 75 M F M F M F

5.88 2.29 7.35 3.76 9.29 5.71 3.21 -0.38 4.68 1.09 6.62 3,04

-0.30 -3.89 1.17 -2.42 3,12 -0.46 -2.63 -6.22 -1.16 -4.75 0.78 -2.80

Delayed Recall Age 25

Educ. M F

5 1.29 - 3.20 8 -0.42 - 4.92

13 -3.29 - 7.79 17 -5,58 -10.08

35 45 M F M F

2.77 -1.73 4.24 -0.26 1.05 -3.45 2.52 -1.98

-1 .82 -6.32 -0.35 -4.85 -4.11 -8.37 -2.64 -7.14

55 65 75 M F M F M F

5.71 1.21 7.18 2.68 8.72 4.22 3.99 -0.51 5.46 0.96 7,01 2,51 1.12 -3.38 2.59 -1.91 4,16 -0.34

- 1,17 -5.67 0.30 -4.20 1.88 -2.62

Uncategorized items Educ.

8 t -0.32 13 1 0.53 17 t 1.09

affected by age and education (F 1,96 = 7.9 and 6.0 with p=0 .006 and =0.015 respectively). The statistical models which proved to be most effective in reducing residual variance in Part One first and second-type errors were respectively: y = 2 3 . 1 6 + 0 . 3 8 (age-51.60) - 1.73 (education- 10.16) - 3.63 if male or + 3.63 if female, and y = 6.15 + 0.17 (age-51.60) - 0.60 (education - 10.16). Part Two/A first-type errors were affected by age and education (F 1,97= 22.5 and 5.2 with p<0.0001 and =0 .024 respectively), whereas only age affected the number of second-type errors (F 1,97 = 5.5, p = 0.021). The statistical models which proved to be most effective in reducing the residual variance in Part Two/A first and second-type errors were respectively: y = 8.27 + 0.29 (age-51.60) - 0.55 (education-10.16), and y = 1.71 + 0.095 (age-51.60). Finally, only age was found to have a significant effect on both Part Two/B first and second-type errors (F 1,97 and 1,98 = 12.9 and 14.6, with p = 0.0005 and 0.0002 respectively). The statistical models for these two variables were respectively: y = 8 .52+0.36 (age-51.60) and y = 2.46 + 0.18 (age-51.60). Table V shows the adjustments to be added to or subtracted from the raw scores in various age/education

combinations. As previously mentioned, the adjustments for other combinations of age/education have to be either interpolated or directly calculated. Table VI shows the diagnostic regions of the adjusted scores, as well as the values delimiting the E.S., for each measure.

Discussion

The aim of this study was to obtain reference values for two frontal tests from a random sample of normal adults of both sexes with different ages and educational levels. It is well known that reference criteria are needed in both clinical practice and research in order to assess the possible presence of a cognitive dysfunction, and this is particularly true when evaluating patients with suspected dementia, especially those in the early stages of the disease. Impaired frontal function is frequently observed in cortical dementia. In patients with Alzheimer's disease (the model of this type of dementia), frontal dysfunction often follows the first clinical manifestations, which are due

TABLE IlL Test of Classification and Recall of Pictures: mean raw scores (S.D.) and equivalent scores (E.S.), with definition of the diagnostic regions for the adjusted score.

Measures E.S.: 0 E.S.: 1 E.S.: 2 E.S.: 3 E.S.: 4

Diagnostic region Pathological Borderline Normal

Immediate recall ~< 10,50 11.00-15.00 15.5 16.00-19.00 19.50-22.00 ~>22.50 Delayed recall ~<9.50 10.00-14.50 15.00-17,50 18.00-21.50 >~22.00 No. of categories ~<2 3-5 6-7 8-10 I>11 Items in remainder Cat. />16 8-15 7 5-6 1-4 0 Uncategorized items />10.50 3.00-10.00 2.5 0.50-2.00 0 0

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TABLE IV. Odd-Man-Out Test: Mean values by age group (standard deviations).

Age 20-29 30-39 40-49 5 0 5 9 60-69 />70 Tota l

Part One First-type errors 11.58 13.14 16.93 19.96 28.32 48.77 23.16

(6.92) (6.88) (10.08) (15.28) (22.64) (25.38) (19.97) Second-type errors 2.08 1.93 1.57 5.80 7.95 17.00 6.15

(3.68) (3.56) (2.24) (8.39) (8.38) (16.69) (9.66) Part Two /A First-type errors 2.58 2.36 5.43 4.56 12.59 22.77 8.27


(0.00) (0.00) (0.75) (0,76) (9.61) (10,29) (6.10) Part Two/B First-type errors 2.83 5.14 4.43 4.92 8.64 28.54 8.52


(1.00) (0.53) (0.58) (0.47) (6.47) (16.65) (7.80)

TABLE V. Odd-Man-Out Test: correction grids. Part One: first-type errors

Age 25 35 45 55 65 75 Educ. M F M F M F M F M F M F

5 4.69 - 2.58 0.93 - 6.34 - 2.83 -10 .10 - 6.59 -13 .86 -10 .35 -17 .62 -14.11 - 21 .38 8 9.89 2.62 6.13 - 1.14 2.37 - 4.90 - 1.39 - 8.66 - 5.15 -12 .42 - 8.91 - 16 .18

13 18.56 11.29 14.80 7.53 11.04 3 . 7 7 7.28 0.01 3.52 - 3.75 - 0.24 - 7.51 17 25.49 18.23 21.73 14.47 17.97 10.71 14.21 6.95 10.45 3.19 6.69 - 0.57

Part One:second-type errors

Age Educ.

5 8

13 17

25 35 45 55 65 75

1.53 -0 .21 - 1 . 9 5 - 3 . 6 9 - 5 . 4 3 - 7 . 1 7 3.33 1.59 - 0 . 1 5 - 1 . 8 9 - 3 . 6 3 - 5 . 3 7 6.33 4.60 2.86 1.12 - 0 . 6 2 - 2 . 3 6 8.74 7.00 5.26 3.52 1.78 0.04

Part Two/A: first-type errors

Age Educ.

5 8

13 17

25 35 45 5.5 65 75

4.92 2.01 - 0 . 9 0 -3 .81 - 6 . 7 2 - 9 . 6 3 6.56 3.65 0.74 - 2 . 1 7 - 5.08 - 7.99 9.29 6.38 3.47 0.56 - 2.35 - 5.26

11.48 8.57 5.66 2.75 - 0.16 - 3.07

Part Two/B : first-type errors

Age 25 35 45 55 65 75

9.47 5.91 2.35 - 1.21 - 4.77 - 8.33

Part Two/A: second-type errors

Age 25 35 45 55 65

2.53 1.58 0.63 - 0.32 - 1.27 - 2 . 2 2

75

Part Two/B: second-type errors

Age 25 35 45

4.68 2.92 1.16

55 65 75

- 0 . 6 0 - 2 . 3 6 - 4 . 1 2

to a breakdown in memory processing and "instrumen- tal" cognitive functions [23]. Some research groups have recently focused their attention on a type of cortical dementia in which the clinical course is characterised by early and prominent frontal symptoms [12, 18], and frontal-like deficits have also been described in "subcortical dementia" [4]. All of these observations em-

phasize the possible usefulness of the normative data reported here.

A) Test of Classification and Recall of Pictures Among the numerous variables derived from the test, only two were found to be sensitive to frontal dysfunction in the original paper by Incisa della Rocchetta [13]:

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TABLE VI. Odd-Man-Out test: equivalent scores (E.S.), with definition of the diagnostic regions for the adjusted score.

Measures E.S.: 0 E.S.: 1 E.S.: 2 E.S.: 3 E.S.: 4

Diagnostic region Pathological Borderline Normal

Part One First-type errors >57.25 48.00-57.25 46.25-47.75 32.00-46.00 21.50-31.75 ~<21.25 Second-type errors >28.00 19.00-28.00 18.00-18.75 9.00-17.75 2.25-8.75 ~<2.00 Part Two/A First-type errors >39.50 19.75-39.50 18.75-19.50 11.50-18.50 7.00-11.25 ~<6.75 Second-type errors >33.00 2.25-33.00 2.00 0.25-1.75 0 0 Part Two/B First-type errors >58.00 26.75-58.00 20.00-26.50 11.50-19.75 5.50-11.25 <~5.25 Second-type errors >37.75 7.25-37.75 6.25-7.00 0.25-6.00 0 0

the number of items in remainder categories and the number of uncategorized items. The performance of patients who had undergone frontal lobectomy was char- acterized by a higher number of errors than those made by normal controls and patients with temporal lobectomy. Both of these types of error reflect the inability of a subject to get through a complete classification and the tendency to fail to consider the whole set of pictures before forming the categories themselves (planning failure, defective concept formation) and during sorting (attention failure, defective shifting aptitude). When making NC errors, subjects do not classify pictures because they are not able to assign them to any of the categories they have already formed; RC errors demonstrate that subjects cannot discriminate sub-categories of major categories. Incisa della Rocchetta observed a complete partition between patients who made NC errors and those who made RC errors; in our analysis, the correlation value between these two measures was the lowest observed and thus also suggests a clear-cut distinction between these two types of errors in normal subjects. In a study of frontal dysfunction in early Parkinson patients [8], our group used the test of Classification and Recall of Pictures and found that one measure which was sensitive to frontal dysfunction in these patients was the number of categories sorted: Parkinson patients formed significantly fewer categories than controls. Paucity in the number of sorted categories can again be interpreted as the result of a difficulty in concept formation and planning or as an inability to switch between competing alternatives during sorting. Incisa della Rocchetta demonstrated an impaired recall performance in patients with either frontal or left temporal lobectomy, who recalled significantly fewer items than both normal controls and right temporal patients. He attributed this negative result to the extent of the lan- guage component of the task (in left temporal patients), and the lack of memory strategies (in frontal patients). In our previous study of parkinsonian patients with a slight motor disability, recall unlike categorization did not appear to be significantly impaired and we speculated that this reverse dissociation may be due to the ability of these patients to take advantage of the visual component of the

test [8]. The fact that the test includes recall means that investigators can also use it as a memory task; as expected, there was a close correlation between the immediate and delayed recall scores. It is interesting to note that the measures of recall were both influenced by age, education and sex, a pattern frequently observed in many other memory tests. Further- more, it is worth noting that, as has been previously described [19, 24], the memory performance of women is better than that of their male counterparts. On the contrary, demographic variables do not seem to have any effect on the more "frontal" measures, although the effect of education on NC (but only on NC) was slightly significant in our analysis. This observation is in contrast with the findings in other "frontal" task studies [20, 24], and also with our own results relating to the Odd-Man- Out test (see below), in which all of the measures are greatly influenced by age, education or both. These re- suits also conflict with the hypothesis that the ability to elaborate and change strategy is impaired in elderly su- bects due to the involvement of the frontal system [3, 24]. It can be speculated that, whereas the ability to maintain or shift a mental set may decline with age, concept formation (probably the most important factor in the test) is a more enduring ability.

B) Odd-Man-Out Test The results obtained from our sample of normal subjects indicate that there is a clear relationship between age and performance: consequently, there is a real need for normative data that can abolish the effect of age. A very interesting result is that education is primarily re- levant in the case of first-type errors (sorting errors) but has less or no effect on errors of the second type (per- severations). Sorting errors may be explained in terms of an inability to sort, or the failure to maintain a mental set; they may also be due to distractibility. In other words, subjects may not be able to identify the rules at all, or the difficulty may consist of occasional intrusions from the alternative set; according to Flowers & Robertson's findings [9], the second case is the most frequent and, in the second part of the test, subjects may get diverted to a third rule. On the contrary, perseveration errors are a clear index of an

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inability to take the feedback received into consideration and to adapt to new circumstances, leaving behind what is no longer appropriate (a defective shifting aptitude). Since the two trials (A and B) o f the second part of the test demand the same kind of performance, we originally thought that a facilitation effect may have emerged; however, as the number and kind of errors overlap, this was clearly not the case. What we did observe was a worsening in the performance of the elderly in Part Two/ B, probably attributable to the greater fatigue tett by these subjects (Part Two/B was administered after about one hour o f testing). As both parts (One and Two) of this test investigate the

same functions, and there is a good correlation between the two scores, we suggest that only the second part be used in clinical practice because Part One proved to be more difficult than Part Two even in our normal population (many subjects chose the wrong item about ten ti- mes more frequently in Part One than in Part Two). An- other good reason for this choice is that our subjects completed Part Two in about half the time it took them to complete Part One and, especially for a test designed to evaluate frontal dysfunction (which often involves a considerable loss attention), the usefulness of being able to administer a test quickly is something not to be ig- nored in clinical practice.

Sommario

L'interesse nei coqfi'onti delle .fitnzioni /'rontali ~ progressivamente aumentato negli tdthni annL Nonostante cib, solo per pochi test "]'rontali" sono diwonibili ~htti normativi italiani. Lo scopo di questo studio era ottenere valori normativi per due test "fron- tali'" utilizzando un camlffone di soggetti normali selezionati in maniera casuale. H prhno test, ossia il Test di Classificazione e Rievocazione di Figure. risulta selettiwtmente compromesso ht paz.ienti sottoposti a esci~'sione ¢?ontale unilaterale; il secondo test, ossia U Test della Pecora Nera, ~&riva tht compiti utilizzati pet" rilevare la compromissione frontale negli animali ed ~ stato usato per individuare tnta di~funzione di tipo fi'ontale nei parkbtsoniani. Sono stati testuti 100 soggetti normali, di etb conwresa fra i 22 e i 79 anni, strat([icati per ¥c~htrit~) s'econdo il modello scolastico italiano. Vengono presentate le griglie di ¢~)rrezione per entrambi i test. La loro utilitgt consiste non solo nelht loro sensibilit& al &mno frontale, ma anche netla possibilitd di disso- ciare aspetti cognitivi diJ]~,renti della di.~fimzione dei lobi ]'rontatL

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Address reprint requests to: Prof. Claudio Mariani, Unith di Neurologia Riabilitativa, I.R.C.C.S. Centro "S. Maria Nascente" - Fondazione Don Carlo Gnocchi, Universit'~ di Mitano, via Capecelatro 66, 20148 Milano, Italy.

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Normative data for two neuropsychological tests sensitive to frontal dysfunction

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