Proper Names in Patients With Early Alzheimer's Disease

Neurocase 2003, Vol. 9, No. 1, pp. 63–69

1355-4794/03/0901–063$16.00 # Swets & Zeitlinger

Proper Names in Patients With Early Alzheimer’s Disease C. Semenza1, S. Mondini2, F. Borgo1, M. Pasini2 and M. T. Sgaramella3 1

Department of Psychology, University of Trieste, Italy, 2Department of General Psychology, University of Padova, Italy and 3Ospedale S. Bortolo, Vicenza, Italy

Abstract The objective of this study was to seek evidence of the particular sensitivity of proper name retrieval and to check the usefulness of proper names as diagnostic material in the early stages of Alzheimer’s disease (AD). Whether a generalized naming deficit is an early symptom of AD it is not yet clear. Previous studies suggest that proper names might be the category of names that is indeed more sensitive to AD. Seventy AD patients (subdivided into ‘‘very mild’’, ‘‘mild’’ and ‘‘moderate’’) and 47 control subjects participated in the study. The performances in two short distinct tests requiring proper name retrieval (Naming People on Definition and Naming Faces), one test of common name retrieval, short (MMSE, 3MS) and long (MODA) batteries for the detection of dementia were compared. Proper name retrieval tests were shown to be more sensitive to early AD than any other tests and batteries that failed to distinguish ‘‘very mild’’ AD from controls. These findings suggest that proper name retrieval tasks might be profitably included in diagnostic tools for the early diagnosis of AD.

Introduction Proper names seem especially difficult to retrieve and are, by most people, considered to make one experience temporary failures more often than other nouns (Cohen and Burke, 1993). This difficulty has received several explanations (Semenza, 1997), all however related to the rather weak and arbitrary link that proper names entertain with their reference. In the most recent theory (Semenza et al., 1998), the basis of this fragility has been identified in the peculiar organization of semantic information labeled by proper names. Unlike common names, that label categories, proper names designate individual (or groups of individual) entities. As a consequence, while, in the act of naming, common names are activated by attributes that have a high probability of being linked to each other, proper names are activated, via a different mechanism, by sets of attributes that happen to be linked together only incidentally. Hence the particular sensitivity of proper names to lack of cognitive resources, as well as the difference between the two retrieval mechanisms, increase the possibility for the two categories to selectively dissociate after focal brain damage (Semenza and Zettin, 1988, 1989; Semenza and Sgaramella, 1993). This theory makes, between common and proper name retrieval, a distinction that is clearly analogous to that between semantic and episodic memory mechanisms, but for an important difference: the name retrieval mechanisms are more periph-

eral and operate at the lexical level. Both types of memory mechanisms are expected to undergo physiological changes with age and, of course, to be sensitive to neurological deterioration. Several studies are reported in the literature documenting a word finding difficulty with increasing age (Nicholas et al., 1997). It is also widely accepted that proper names are particularly sensitive to the age factor (Cohen, 1994), although convincing experimental support for this view is surprisingly sparse. Experimental evidence, however, has been recently produced (Semenza et al., 1996), showing how an ubiquitous, across-ages, proper name disadvantage in noun retrieval becomes, in normal people, dramatically greater from the age of seventy. The technique used in this study, learning of supra-span lists of names, allowed avoiding traditional difficulties (Cohen, 1994) entailed in diary studies (forgetting a proper name may be, in fact, less easy to compensate and socially more relevant than forgetting a common name) and in studies comparing object naming with face naming (in this case perceptual difficulty is hard to balance). A series of factors like word frequency, length and phonological complexity were, in fact, controlled and could not be held responsible for such an effect. The same study showed that in Alzheimer’s dementia (AD) the proper name disadvantage appeared earlier and in an even more striking fashion.

Correspondence to: Sara Mondini, Dipartimento di Psicologia Generale, via Venezia 8, 35131, Padova, Italy. Tel: þ39 049 827 6616; Fax: þ39 049 827 6600; e-mail: [email protected]

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Whether or not a generalized naming problem must be considered an early symptom of Alzheimer’s dementia (AD) is still a matter of debate: while some authors include a visual confrontation naming problem in early symptoms, others do not consider it so typical in the early stages of the disease (Nicholas et al., 1997; Luzzatti, 1999). The above reported findings suggest, however, that, of all names, proper names might be, indeed, those showing a typical sensitivity at the onset of progressive, generalized cortical damage. Further reasons for this hypothesis may be found in the pathology of AD, more typically starting in the temporal and the hyppocampal regions. The temporal lobe seems more involved in the retrieval of proper names with respect to other grammatical classes including common nouns (Semenza et al., 1995; Damasio et al., 1996; Gorno Tempini et al., 1998) while the hippocampus is the key area in episodic learning (see the above reported argument). The present study was thus meant to seek further evidence of the particular sensitivity of proper name retrieval to cortical deterioration (on both confrontation and definition) and to check the usefulness of proper names as diagnostic material in the early stages of AD.

Method Two distinct tests (henceforth ‘‘Proper Name tests’’ when referring to both) requiring proper name retrieval were prepared: Naming Faces (15 items) and Naming People on Definition (15 items) of very famous people (including contemporary, e.g. Clinton, and a few historical personages, e.g. Napoleon); while some of these people were known worldwide (e.g. Queen Elizabeth), some others, like Italian TV characters or politicians, were only locally popular. A careful selection brought to the choice of this testing material (see also the corollary for principles inspiring the selection criteria). Only items where a preliminary investigation documented success in 92 to 98 out of 100 subjects (50 to 70 y.o.) were included in the final test. As a result of this selection only five famous people appeared in both Naming Faces and Naming People on Definition. Half of the experimental subjects was administered Naming Faces first, while the other half started with Naming People on Definition. In order to minimize practice effects on the five common items the two Proper Name tests were never administered one immediately after the other. A further naming on definition of Common Name test (16 items: 8 objects and 8 substances, see Appendix 1) was used, matched for difficulty to the Proper Name tests (92 to 98% success for each items in the same 100 control subjects). A confrontation (picture) naming condition was not included in the study because it turned out to be very difficult to select items according to criteria comparable to those used for Proper Name tests. Typically, in fact, naming of pictures of objects either elicited, in normal subjects, 100% correct in the easier items responses or a much worse performance (less than 80% correct) for the most difficult ones.

These tests were administered together with the MiniMental State Examination (Folstein et al., 1975; Toumbaugh and McIntyre, 1992; Mitrushina and Satz, 1994) and an Italian version of the Modified MMSE (3MS), (Teng and Chui, 1987). All AD patients (but not controls) also received the MODA (Milan Overall Dementia Assessment), an extensive and widely used battery for the detection and assessment of dementia (Brazzelli et al., 1994). The MODA battery encompasses two subsections: a first part concerning ‘Orientation ability’ (a series of questions about time, space and, family information) and a ‘Testistic’ part tapping cognitive abilities (attention, memory, learning, verbal fluency, visual perception, copy and digital agnosia).

Subjects Seventy patients referred as suspected AD (meeting NINCDS-ARDRA criteria, McKhann et al., 1984) and 47 control subjects participated in the study. Controls were recruited among non-neurological patients from the day care hospital and they were age- and education-matched with AD patients [age: t(115) ¼ 1.1, n.s.; education: t(115) ¼ 1.69; n.s.]. The AD subjects were subdivided on the basis of the MMSE scores in three groups: 15 ‘‘very mild’’ (range 30–26), 33 ‘‘mild’’ (25–21) and 22 ‘‘moderate’’ (20–16). MMSE scores for the controls were comparable to those of very mild AD [t(60) ¼ 0.313; n.s.]. The four groups did not differ from each other in age and educational level. Table 1 summarizes demographic information and MMSE scores of patients and controls. A safe diagnosis of ‘‘very mild’’ AD was made possible only by reassessing participants six months after the collection of the experimental data. Thus the ‘‘very mild’’ group was selected starting from a pool of 40 participants, who were evaluated on formal request from their family physician because of suspected AD. Their MMSE ranged between 26 and 30 and on formal neuropsychological assessment they did not meet NINCDS-ARDA criteria; these subjects would thus belong, in all likelihood, to the Mild Cognitive Impairment Table 1. Demographic information of AD patients and controls Age

Education (years)

MMSE

Controls Mean DS

69.53 10.47

8.47 5.43

27.85 2.17

Very mild AD Mean DS

68.00 5.90

7.40 4.32

27.67 1.23

Mild AD Mean DS

71.55 6.23

7.58 5.15

22.73 1.31

Moderate AD Mean DS

73.14 6.48

5.57 2.62

16.77 2.20

Proper names and Alzheimer’s disease

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using either Mann-Whitney U Test for independent groups or Wilcoxon test for dependent groups given the limited number of subjects for each severity level. These analyses aimed to compare the four groups of subjects in performing MMSE, 3MS, Common names, Proper names and MODA. Table 2 summarizes results of all groups in each test. The MMSE was unable to discriminate between the control group and ‘‘very mild’’ AD patients [U(47,15) ¼ 307.5, p ¼ .107], while it effectively distinguished the other groups [‘‘very mild’’ vs ‘‘mild’’: U(15,33) ¼ 0, p < .0001; ‘‘mild’’ vs ‘‘moderate’’: U(33,22) ¼ 0, p < .0001]. The 3MS was more sensitive but it could not yet discriminate between controls and ‘‘very mild’’ AD [U(47,15) ¼ 245.5, p ¼ .078] but it only distinguished ‘‘very mild’’ and ‘‘mild’’ [U(15,33) ¼ 41, p ¼ .0001] and ‘‘mild’’ and ‘‘moderate’’ [U(33,22) ¼ 134.5, p < .0001]. The Common Names test could not discriminate controls from ‘‘very mild’’ [U(30,10) ¼ 92, p ¼ .072]; ‘‘very mild’’ vs. ‘‘mild’’ [U(10,22) ¼ 77.5, p ¼ .190], ‘‘mild’’ vs. ‘‘moderate’’ [U(22,14) ¼ 108, p ¼ .141], while distinguishing the other groups.

(Petersen et al., 1999, 2001) category, although all the diagnostic criteria for inclusion in this category were not fully considered. All these patients were nonetheless administered the experimental proper name tests and were given a second assessment six months later. At this time 15 out of the initial 40 patients met unequivocally the NINCDSARDRA criteria and their MMSE scores had dropped to a clearly pathological level (25 patients received, instead, a diagnosis of pseudodementia, vascular disease and were dropped from the study). These 15 patients constituted the ‘‘very mild’’ AD group and their score in the Proper Name test at the time of the first assessment entered the statistical computations of this study. None of these patients have been taking psychoactive medications at any time during this investigation.

Results The first group of analyses investigated the sensitivity of each test in discriminating controls and ‘‘very mild’’ Alzheimer patients. A series of non-parametric analyses were conducted

Table 2. Results of control subjects and AD patients (very mild, mild and moderate) in MMSE, 3MS, Naming People on definition, Naming Faces, Common names and MODA Controls

MMSE 3MS Naming People on definition Naming Faces Common names MODA

Very mild

Mild

Moderate

Mean

C.I.

SD

Mean

C.I.

SD

Mean

C.I.

SD

Mean

C.I.

SD

27.85 97.74 13.32 14.17 30.87

0.64 2.19 0.64 0.34 0.5

2.17 7.44 2.19 1.17 1.70

27.67 91.87 8.60 8.80 29.40 90.08

0.68 4.1 2.26 2.5 1.66 4.08

1.23 7.41 4.08 4.52 2.32 7.07

22.73 74.79 6.00 7.85 26.00 80.14

0.46 3.32 1.26 1.25 3.01 2.65

1.31 9.36 3.55 3.53 6.78 7.49

16.77 61.59 3.86 4.62 23.50 67.38

0.98 6.86 1.39 1.72 3.81 5.10

2.20 15.47 3.14 3.77 6.61 11.50

Fig. 1. Comparison between controls and very mild Alzheimer patients in the different tests.

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Naming People on Definition was, instead, found to discriminate between controls and ‘‘very mild’’ AD [U(47,15) ¼ 115.5, p < .0001], ‘‘very mild’’ vs ‘‘mild’’ [U(15,33) ¼ 152.5, p < .05] and ‘‘mild’’ vs ‘‘moderate’’ [U(33,22) ¼ 224.5, p < .05]. Naming Faces also discriminated between controls and ‘‘very mild’’ AD [U(47,15) ¼ 96, p < .0001], ‘‘mild’’ vs. ‘‘moderate’’ AD [U(33,22) ¼ 183, p < .01], but not between ‘‘very mild’’ and ‘‘mild’’ AD [U(15,33) ¼ 212.5, p < .435]. A practice effect on the five items that were common to the two Proper Name Tests was not found. The patients’ performance was then examined on a single case basis to look for subjects who, reversing the general pattern, would be significantly better at Definition than at Faces. No such patient was found. Fig. 1 shows the performance of controls and ‘‘very mild’’ AD patients in the four tests (Naming Faces, Naming People on Definition, MMSE, 3MS and Common Names). The raw scores of all tests were subject to linear transformation to the range (0–1). In order to further investigate the predictive value of each test, a logistic regression was performed on the scores of normals and very mild AD in MMSE, 3MS, Common name tests, Naming People on Definition and Naming Faces. The resulting function correctly classified 87% of cases: the only significant predictor being the Proper Name tests (p ¼ .003), see Table 3. The second part of the analysis investigated the sensitivity of MODA. AD patients’ performances in the MODA and in Proper Name Tests were compared. All AD patients, regardless of the severity level, showed

Table 3. Logistic regression of analysis of Alzheimer diagnosis as a function of each test

MMSE 3MS NP NC Constant

B

S.e.

Wald

df

p

Odds ratio

.723 .022 .656 .347 14.053

.649 .176 .223 .466 13.041

1.242 .016 8.645 .555 1.161

1 1 1 1 1

.265 .899 .003 .456 .281

2.061 .978 .519 1.415 .000

more difficulties in naming proper names than in performing the MODA [Wilcoxon test: Naming People on Definition, Z ¼ 7.016; p < .001; Naming Faces, Z ¼ 6.569; p < .001]. Proper Name tests were also much more sensitive than both the Orientation [Wilcoxon test: Naming People on Definition, Z ¼ 7.08; p < .001; Naming Faces, Z ¼ 6.98; p < .001] and the Testistic [Wilcoxon test: Naming People on Definition, Z ¼ 5.67; p < .001; Naming Faces, Z ¼ 4.13; p < .001] sections of the MODA. Finally, an analysis was performed reclassifying the patients according to MODA: 14 patients were still within the normal limits (AD N), nine were classified as ‘‘uncertain’’ (AD U) and 47 were diagnosed as demented (AD D). The Proper Name Tests, however, effectively discriminated not only between AD patients of different level of severity, but even AD N from control subjects [Naming People on definition: U(47,15) ¼ 107, p ¼ .001; Naming Faces: U(47,15) ¼ 60.5, p < .001], as shown in Fig. 2.

Fig. 2. Performance on Proper Name Tests (including Naming People on Definition and Naming Faces) of normal subjects and AD patients whose severity of disease is classified according with MODA (AD N ¼ Alzheimer patients whose MODA score identified a normal performance; AD U ¼ Alzheimer patients whose MODA score identified an uncertain diagnosis of dementia; AD D ¼ Alzheimer patients whose MODA score identified a clear diagnosis of dementia.


Discussion Simple and short tests of proper name retrieval were found to compare favorably with widely used clinical instruments in discriminating between unselected subjects and age- and education-matched patients suffering from AD. Not only short batteries like MMSE, or the more powerful 3MS, but also longer and time-consuming batteries like MODA could not distinguish AD patients from normal controls as effectively as proper name naming could do. A test requiring retrieval of common names was not found to be as sensitive, thus confirming the uncertainty about whether a generalized naming deficit can be considered an early symptom in AD. Indeed, while many authors consider that naming deficit appears in early stages of AD (Flicker et al., 1987; Hodges and Patterson, 1995), other authors consider it less typical (Benson, 1979; Bayles, 1982; Obler, 1983). When found in early stages, the naming deficit was often considered the result of a visuo-perceptual disturbance rather than of a primary lexical semantic deficit (Rochford, 1971; Kirshner et al., 1984; Gavazzi et al., 1986; Shuttleworth and Huber, 1988; Cormier et al., 1991). A similar argument could hold for retrieving proper names vis-a-vis faces rather than definitions. Quite to the contrary, however, naming on verbal definition was even more sensitive to damage brought by AD than naming from visual input stimuli as complex as faces. The multiple single case analysis did not single out any dissociation reversing the general trend, i.e. one featuring a deficitary face naming with spared naming on definition. This sort of dissociation could indeed follow two disturbances: (a) prosopagnosia (where recognition of faces is the problem) which, from the present study, does not appear to specifically affect early AD or (b) prosopanomia (if the problem selectively concerns naming faces that are nonetheless recognized when information about the person is spared). Prosopanomia, however, while in principle compatible with current theoretical models of proper name and face processing (Valentine et al., 1996; Semenza et al., 1998) has never been convincingly demonstrated so far (indeed, no patient has ever been reported who could not name people faces while able to recognize them and to name their bearers on definition). The present findings, therefore, lead to the conclusion that the deficit in very early AD is based on problems in lexical semantic abilities rather than on perceptual difficulties. The ability of the patients to provide biographical information about the items they could not retrieve was not systematically tested. This study cannot establish, therefore, whether AD patients’ early deficit on Proper Names lies at the semantic level or at the lexical level (or in mapping from the former to the latter). Our findings, however, agree with Greene and Hodges’s (1996) conclusion according to which poor naming performance is over and above the deficit in face identification score, and may be due to additional impairment at a postsemantic level of processing. In conclusion, quite irrespective of the nature of the input stimulus, proper name retrieval has proved to be a very

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sensitive task for the early diagnosis of AD. This finding suggests that proper name retrieval should be assessed in the earliest suspicion of the disease, even in screening conditions, where a time-saving rather than a time-consuming diagnostic tool should be used. While it would be obviously unwise to rely on proper name retrieval tasks only for an early diagnosis, the inclusion of such tasks in both screening and long, complete batteries for detection of AD should be strongly recommended. Corollary: A word of caution should be given before proper name retrieval systematically enters AD detection batteries. Knowledge of proper names (Semenza et al., 1998) varies across subjects in a much wider way than common names. In order to build a useful battery it appears necessary to choose only items representing extremely famous characters, i.e. those known, at a certain period of time and within a certain culture, by virtually 100% of the healthy adult population, conceding only for momentary lapses of memory. Longer and graded difficulty tests could be used only with a population extremely homogenous from the cultural point of view. This does not, however, eliminate interindividual variability due to lack of personal interest in specific areas of knowledge (e.g., sports, politics, movies, etc.). Except for a few historical figures, most of the items must be changed over the years (and over different locations where the investigations are taking place), because fame is subject to oblivion, physical features also change and so do biographical facts. Updating the material every few years is thus compulsory, and matched controls must be always specifically tested.

Acknowledgements This research is supported by a Major Collaborative Research Initiative grant from the Social Sciences and Humanities Research Council of Canada (Grant #412-95-0006) awarded to G. Jarema (Director), E. Kehayia and G. Libben. Further support was provided to Carlo Semenza from Regione Veneto and MURST.

References Bayles KA. Language function in senile dementia. Brain and Language 1982; 16: 265–80. Benson DF. Aphasia, alexia and agraphia. New York: Churchill Livingstone, 1979. Brazzelli M, Capitani E, Della Sala S, Spinnler H, Zuffi M. A neuropsychological instrument adding to the description of patients with suspected cortical dementia: The Milan overall dementia assessment. Journal of Neurology, Neurosurgery and Psychiatry 1994; 57: 1510–7. Cohen G. Age related problems in the use of proper names in communication. In: Hurmmart ML, Wieman JM, Nussbaum F, editors. Interpretation communication and older adulthood: An Interdisciplinary research. Los Angeles: Jage, 1994. Cohen G, Burke DM. Memory for proper names: A review. Memory 1993; I: 249–63. Cormier P, Margison JA, Fisk JD. Contribution of perceptual and lexicalsemantic errors to the naming impairment in Alzheimer disease. Perceptual and Motor Skills 1991; 73: 175–83. Damasio H, Graboski TJ, Tranel D, Hichwa RD, Damasio R. A neural basis for lexical retrieval. Nature 1996; 380: 499–505.

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Flicker C, Ferris SH, Crook T, Bartus RT. Implication of memory and language dysfunction in the naming deficit of senile dementia. Brain and Language 1987; 31: 187–200. Folstein MF, Folstein SE, McHugh PR. ‘‘Mini-mental State’’: A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research 1975; 12: 189–98. Gavazzi P, Luzzatti C, Spinnler H. La patologia del linguaggio nella demenza di Alzheimer. Ricerche di Psicologia 1986; 4: 91–165. Gorno Tempini ML, Price CJ, Josephs O, Vanderghe R, Cappa SF, Kapur N, Frackowiak RSJ. The neural systems sustaining face and proper-name processing. Brain 1998; 121: 2103–18. Green JDW, Hodges JR. Identification of famous faces and famous names in early Alzheimer’s disease. Relationship to anterograde episodic and general semantic memory. Brain 1996; 119: 111–28. Hodges JR, Patterson K. Is semantic memory consistently impaired early in the course of Alzheimer disease? Neuroanatomical and diagnostic implication. Neuropsychologia 1995; 33: 441–59. Kirshner HS, Webb WG, Kelly MP. The naming disorder of dementia. Neuropsychologia 1984; 22: 23–30. Luzzatti C. Language disorders in Dementia. In: Denes GF, Pizzamiglio L, editors. Handbook of clinical and experimental neuropsychology. Hove, UK: Psychology Press, 1999: 809–46. McKhann G, Drachman D, Folstein M, Katzman R, Price D, Stadlin EM. Clinical diagnosis of Alzheimer’s disease. Neurology 1984; 34: 939–44. Mitrushina M, Satz P. Utility of the mini-mental state examination in assessing cognition in the elderly. Aging Clinical and Experimental Research 1994; 6: 427–32. Nicholas M, Barth C, Obler LK, Au R, Albert ML. Naming in normal aging and dementia of the Alzheimer type. In: Goodglass H, Wingfield A, editors. Anomia: Neuroanatomical and cognitive correlates. San Diego: Academic Press, 1997: 166–88. Obler LK. Language and brain dysfunction in dementia. In: Segalowits SJ, editor. Language function and brain organization. New York: Academic Press, 1983: 267–82.

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Received on 11 April, 2001; resubmitted on 10 April, 2002; accepted on 13 August, 2002


Appendix 1. List of items of the Common Name Test (8 objects and 8 substances) Name of substances: High frequency: 1. Sale (salt) 2. Sabbia (sand) 3. Legno (wood) 4. Fuoco (fire) Low frequency 5. Smalto (polish) 6. Farina (flour) 7. Tabacco (tobacco) 8. Paglia (straw) Name of objects (countable entities): High frequency: 9. Cane (dog) 10. Tenda (tent) 11. Albero (tree) 12. Letto (bed) Low frequency 13. Slitta (sledge) 14. Campana (bell) 15. Colomba (pigeon) 16. Leone (lion)

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Proper names in patients with Alzheimer’s disease C. Semenza, S. Mondini, F. Borgo, M. Pasini and M. T. Sgaramella Abstract The objective of this study was to seek evidence of the particular sensitivity of proper name retrieval and to check the usefulness of proper names as diagnostic material in the early stages of Alzheimer’s disease (AD). Whether a generalized naming deficit is an early symptom of AD it is not yet clear. Previous studies suggest that proper names might be the category of names that is indeed more sensitive to AD. Seventy AD patients (subdivided into ‘‘very mild’’, ‘‘mild’’ and ‘‘moderate’’) and 47 control subjects participated in the study. The performances in two short distinct tests requiring proper name retrieval (Naming Faces and Naming on definition), one test of common name retrieval, short (MMSE, 3MS) and long (MODA) batteries for the detection of dementia were compared. Proper name retrieval tests were shown to be more sensitive to early AD than any other tests and batteries, that failed to distinguish mild AD from controls. These findings suggest that Proper name retrieval tasks might be profitably included in diagnostic tools for the early diagnosis of AD.

Journal Neurocase 2003; 9: 63–69

Neurocase Reference Number: 451/01

Primary diagnosis of interest Early Alzheimer deterioration

Key theoretical issue * Proper names, Alzheimer disease

Key words: proper names; Alzheimer patients; early diagnosis

Scan, EEG and related measures T.C.

Standardized assessment MMSE, MODA, 3MS

Other assessment NICDS, ARDRA, Common name test, Naming People on definition, Naming Faces

Lesion location * Diffuse

Lesion type Degenerative

Language English