Visuoperceptual-spatial ability and visual memory in vascular dementia and dementia of the Alzheimer type

Nuarop~~~holu~~to.

Pergamon

Vol.

32. No.

IO, pp. 12X7-1296. lYY4 Elsevier ‘hence Ltd Prmted in Great Britam 0028-3932 94 S7.00+0.00

0028-3932(94)00064-6

VISUOPERCEPTUAL-SPATIAL ABILITY AND VISUAL MEMORY IN VASCULAR DEMENTIA AND DEMENTIA OF THE ALZHEIMER TYPE JOSEPH

H. RICKER,*

P. A. KEENAN?

and MARK

W. JACOBSON-I

*Department of Rehabilitation Psychology and Neuropsychology, Rehabilitation Institute of Michigan, Wayne State University School of Medicine; and tDivision of Psychology, Department of Psychiatry, Harper Hospital, Wayne State University School of Medicine, Detroit, Michigan, U.S.A. (Receiced 3 December 1993; accepted 2 1 April 1994) Abstract-This study investigated the relationship between visuoperceptual ability and visual memory in dementia. Twenty individuals with probable dementia of the Alzheimer type, 24 individuals with probable vascular dementia, and 20 healthy, elderly adults underwent neuropsychological evaluation. Hierarchical multiple regression analyses suggested that perceptual organization skills contributed to a significant amount of the variance in novel, but not famous, face recognition. This finding was most robust in the clinical groups. Causality cannot be attributed from this regression model. Results suggest, however, that visual processing deficits are more strongly related to the memory process at the time of encoding rather than during recognition of remote information. Key Words:

Alzheimer’s

disease; vascular

dementia;

spatial ability;

visual memory.

INTRODUCTION Visuospatial-perceptual abilities decline with advancing age [ 1,481, but visual processing disturbances can be of pronounced severity and specificity in individuals with extensive cognitive compromise such as that seen in Alzheimer’s disease [36] and cerebrovascular disease [24]. Combined, dementia of the Alzheimer type (DAT) and vascular dementia (VaD) account for up to 70% of all cases of elderly dementia [30]. In both syndromes, it is common to observe impairment in visuoconstruction, visuoperception, visuospatial reasoning, organization of the visual environment, and facial identification [ 11, 19, 33, 36, 39, 41, 471. In VaD, visuospatial deficits may exceed impairment in other domains (e.g. language) if areas of cerebrovascular compromise are present or predominant in the nondominant hemisphere [26]. Compromised performance on such tasks is also frequently observed, however, following dominant hemisphere lesions [21, 541. Because of the severity and extent of complex visual disturbances in dementia, it has been suggested that there is the increased potential for exacerbation of other cognitive symptoms secondary to visual deficits [37]. Furthermore, impaired memory for visual information is a consistent finding in DAT and VaD [23]. In spite of the pervasiveness of both visuospatial and visual memory impairment in DAT

*Address for correspondence: Joseph H. Ricker, Department logy. Rehabilitation Institute of Michigan, 261 Mack, Detroit, 1287

of Rehabilitation Ml 48201. U.S.A.

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and Neuropsycho-

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and VaD. no research has been published comparing the relationship between such performance domains in these clinical groups. Little research has been published examining the relationship between these domains in other or non-clinical groups. The relationship between visuoperception and visual memory is important clinically. Such information may assist in determining if an individual’s poor recall of information is a function of poor storage. or if impaired “primary” visuospatial abilities are compromising the accurate encoding of visual information. The relationship between visual information processing and visual memory is also important to know from a heuristic perspective, as it can provide insight into how visual information may be differentially affected in the memory system. Although there is variation in the literature about specific processes. contemporary theories of visual perception and visual memory are concordant in that visual information must be successfully encoded before it can be accurately consolidated and stored [ 14. 38). However, some investigations have suggested no relationship between the ability of DAT patients to understand visual information and their subsequent ability to recall or recognize visual stimuli. Several previous investigations have studied the effects of associated visual operations on visual memory in DAT. One study [SS] has concluded from the lack of statistically significant relationships between matching-to-sample tasks and visual memory performance that t.istctr/pr~~~ptiotz was not systematically related to visual memory. Another group has suggested that simultaneous matching-to-sample was not significantly related to delayed matching-to-sample [43]. Although both of these latter studies clearly demonstrate that matching-to-sample does not covary with visual memory, one cannot generalize this finding to other domains of visual information processing. Matching-to-sample is a \‘ery primary process, requiring essentially that a subject have visual acuity and attention sufficient to detect a target stimulus from an array of similar stimuli [ 1I]. The functions of visual discrimination and visual perception can be partially dissociated from one another [35]. A more recent investigation [X] studied a sample of individuals with probable DAT, and suggested that domain-specific impairments in visual memory were not related to impairments in visuospatial ability. As with the aforementioned studies. one of the visuospatial measures was purely visually discriminative (a function rarely impaired until the late stages of DAT). and other tasks were visuoconstructive (thus introducing the potential confound of graphomotor apraxia). Thus, although this study presented further evidence that visual discrimination and visuoconstruction kvere not related to specific types of visual information retrieval, it did not provide cotnpelling evidence that no higher-order visual operation impacted upon memory for non-verbal information. Other investigators have presented data supporting a relationship between visuospatial abilities and visual memory. In a sample of young. neurologically unimpaired adults, evidence was presented suggesting that performance on spatial tasks was significantly associated with spatial memory [29]. This study showed that an individual’s ability to correctly recall visual information was at least partially a function of the ability to accurately perceive and process visuospatial stimuli in the first place. In another investigation [46], “perceptual clustering”. an encoding strategy based on perception of a visual stimulus. was significantly related to delayed recall on the Rey-~Osterreith Complex Figure in a sample of consecutively referred neurologic and psychiatric patients. The findings of these two investigations suggest that certain visual operations can systematically impact subsequent memory for visual information. These studies do not, however, address specific clinical populations who have been demonstrated to have impairment in visual processing and visual

PERCEPTION

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memory. In addition, non-neurologically impaired elderly individuals have not been specifically addressed in these studies. The present study investigated the relationship between complex visual task performance and recognition memory for faces in normal elderly subjects, as well as individuals with DAT and VaD. The specific domains of complex visual processing investigated were visuoperception (i.e. the application of meaning to a complex visual array), visuoconstruction (the ability to construct a visually presented target item), and visuospatial ability (the ability to efficiently process spatial relationship among visual stimuli) [l 11. These domains were chosen because they represent the most common visual impairments in individuals with Alzheimer’s disease [36, 391 and cerebrovascular compromise [33], and are consistent with a conceptual framework for complex visual processing [l 11. The modality of visual memory assessed was recognition memory for unfamiliar faces. Although recall paradigms are typically used in the assessment of memory in general, recognition paradigms were selected given previous research suggesting that recognition is a more sensitive index of total amount of information acquisition in demented populations [3, 25, 40, 441. A comparison with recognition offamous faces was also conducted to ensure that the findings were specific to the storage of novel faces [ 15,453.

METHOD Strbjrcts The subjects in the present investigation were enrolled as part of an ongoing research investigation concerning memory in dementia. The subjects were grouped into three diagnostic classes: Dementia of the Alzheimer Type, Vascular Dementia, and Non-demented Elderly Control Subjects. The subjects in the dementia of the Alzheimer type (DAT) sample were 17 women and three men diagnosed with probable Alzheimer’s disease. Mean age was 82.6 years (S.D.=8.2 years); average number of years of formal education was 12 (S.D. = 2.1 years). All DAT subjects were below the suggested statistical cut-off for dementia (DRS total score = I23 [31]), with a group mean on the Mattis Dementia Rating Scale of 85.90, S.D. = 10.13). Four of the subjects were AfricanAmerican and 16 were Caucasian. The subjects were recruited from a senior health-care facility that 1s part of a larger suburban retirement community; a geriatric evaluation clinic affilitated with a large urban medical center; and community support groups. All patients were diagnosed as having probable Alzheimer’s Disease by a senior neurologist, psychiatrist. or geriatrician according to the criteria developed by the NINCDSADRDA Work Group [34]. Patients with a history of chronic alcohol or drug abuse, head trauma with loss of consciousness, hypertention, stroke, significant psychiatric history, present use of neuroleptic medication. positive neuroimaging studies (other than atrophy), or other neurological disease were excluded. The vascular dementia (VaD) group was composed of 24 subjects: mean age = 79.4 years (S.D. = 5.2 years): education = 10.9 years (S.D. = 1.9years). All VaD subjects were below the suggested statistical cut-off for dementia. with a mean Mattis Dementia Rating Scale total score of 96.04 (S.D.= 12.14). Fourteen subjects were AfricanAmerican. and 10 were Caucasian. Seventeen subjects were women. This sample was gathered through Inpatient neuropsychological assessment referrals at a large, Midwestern, university-based rehabilitation hospital. All subjects were right-handed and diagnosed based on recent infarction observed on CT head scanning. One-third of the subjects had received MRI in addition to CT. All subjects met the criteria for probable ischemic vascular dementia set forth by the 1992 Alzheimer’s Disease Diagnostic and Treatment Centers (ADDTC) [1X], In addition. all subjects had evidence ofat least one region of probable infarction in the non-language dominant (in this sample, right) hemisphere. The control group consisted of 20 healthy, elderly individuals who resided in a retirement community (Mean age = 83.6 years; S.D. = 6.48 years). The average number of years of forma1 education was 15.2 years (S.D. = 2.19 years; range = 12 -20 years). The mean Mattis Dementia Rating Scale total score was 137.2 (S.D. = 6.41), which is well above the suggested cut-off for dementia on this measure. All control subjects were Caucasian; two control subjects were male. As with the clinical sample. individuals with a history of stroke, head injury, substance abuse, or psychiatric disturbance were excluded.

The following standardized neuropsychological measures were selected for analysis in the present investigation: Geriatric Depression Scale (CDS) 1133, Mattis Dementia Rating Scale (DRS) [31], estimated premorbid intellectual functioning [S], Hooper Visual Organization Test (HVOT) [27], Judgment of Line Orientation

1290

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P. A. KEENAN

and

M

W. JACOBSON

(JOLO) [IO]. WAIS-R Block Design L53]. Recognition Memory for Faces (RMF) [jl]. The Famous Faces Test [Z] was also administered with necessary modifications to reduce the potential effects of Impaired nammg ability in the clinical sample. The first modification of this measure was the addition of photographs of notable faces from the 1980s 1281. The second modification was the use of a recognition paradigm. The subjects were shown each photograph and provided verbally with three choices (e.g. “Is this Bob Hope, Bing Crosby, or Eddie Cantor?“). The alternate choices for each photograph were individuals within the same category (e.g. motion picture celebrity. sports figure), gender. race. age, and decade. The complete response form is available from the first author.

The control and DAT subjects were provided with a brief description of the study and informed consent was obtained. An alternate consent form was provided for family members of individuals in the DAT sample. The VaD patients were all seen as inpatients, and the present measures were part of the standard neuropsychological assessment battery. The Mattis Dementia Rating Scale and Geriatric Depression Scale (CDS) were administered as screening measures of general cognitive functioning and depression, respectively. Individuals &ho obtained a score of 15 or higher on the GDS. the cut-o8score for mild depresslon. were to be excluded given the potential negative effects of depression on neuropsychological test performance [49, 521. No subjects had to be excluded. however. based on GDS score. Although order effects were not expected to be a significant factor. the administration of test\ was randomized to preclude such a possibility.

Descriptive statistics and statistics for between group differences for the normal elderly. DAT. and VaD samples are presented in Table 1. Years of formal education was statistically different among groups [F(2,61)=20.61, P
In each of the three groups, significant univariate correlations were obtained between the total number correct on Recognition Memory for Faces (RMF) and age. DRS total score. and HVOT total score. In no group did JOLO or Block Design achieve statistical significance when correlated with the RMF score. The Famous Faces Test total number correct was not found to correlate significantly with any of the aforementioned variables in any of the groups. A stepwise multiple regression, with age, DRS, and HVOT was performed to determine the total variance in visual memory accounted for by these significant demographic and cognitive factors. The multiple regression indicated that in the DAT sample, only scores from the HVOT made significant contributions to the variance in Recognition Memory for Faces (RMF) performance [R=0.69, R'=O.47:F(?. lb)=16.08. P
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Table 1. Between-group differences on demographic and screening variables in normal elderly (NE), dementia of the Alzheimer type (DAT), and vascular dementia (VaD) subjects (d.f.=2, 61) VaD

F

82.60 8.31

79.42 5.20

2.76

15.20 2.19

12.25

10.92 1.89

20.61

<0.0001

110.95 3.22

103.20 4.05

100.17 6.00

21.09

<0.0001

GDS Mean S.D.

2.05 1.39

5.30 2.29

5.17 2.26

12.03


DRS Mean S.D.

137.20 6.41

85.90 10.13

96.04 12.14

112.14

<0.0001

HVOT Mean S.D.

24.75 1.41

11.30 4.11

11.46 3.97

108.40

<0.0001

JOLO Mean S.D.

23.90 9.69

9.70 2.82

Il.92 2.99

175.82


Block design Mean S.D.

19.85 4.88

2.00 I .67

2.63 1.74

221.27


43.60

32.50 3.29

33.62 3.06

135.16


9.80 2.48

30.04 5.1 1

172.85

<0.0001

NE

DAT

Mean S.D.

R3.60 6.48

Educarim Mean S.D.

-

P

Age

Estimated Mean S.D.

RMF Mean S.D. FF Mean S.D.

1.97

Il.S.

IQ

1.47 47.30 3.45

Note: GDS -Geriatric Depression Scale; DRS = Dementia Rating Scale: HVOT= Hooper Visual Organization Test; JOLO = Judgment of Line Orientation; RMF = Recognition Memory for Faces; FF = Famous Faces.

F (3,20)= 5.83, P
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J H KICKER.

Table 2. Regression

DRS HVOT

Ic’orl\t‘r,lr1

1

.Vorc,: DRS = Dementia

memory

for faces performance

Type Sample

B

St- B

Brru

7

Sk/ T

-0.14 ~0.05 0.52 39.48

0.08 0.06 0.12 5.65

-0.37 -0.16 0.65

~~1.21 ~ 0.x0 4.29 6.Y9

0.246 0.440 0.005 0.00 I

Vascular Dcmcntia Sample liw/ciR/c\ ,!I tl1c Equtrri0il u Age -- 0.08 DRS - 0.04 HVOT 0.48 (C‘mutrur

and M W. JACOBSON

models on recognition

Dementia of the Alzheimer r’Lll.l~lhleSifI r/w Eqlctrliorl kc

P A. KEENAN

41.o.!

Rating

SE B

Bercr

T

Si
0.10 0.04 0.13 IO.49

-0.14 -0.17 0.62

-0.x0 -0.97 3.69 3.91

0.432 0.340 0.00 I

SE B 0.06

Brto 0.17

T

Sig 7

0.05 0.1 I IO.06

-0.06 0.57 _

0.53 -0.23 1.30 3.40

0.601 0.812 0.03 I 0.003

Scale: HVOT = Hooper

Visual Organiration

0.001

Test

Had the relationship between the selected covariate and the dependent measures been equivxlent across groups, a multivariate analysis of covariance (MANCOVA) would have been performed with all three groups. Given that the assumption of covariate homogeneity was violated, however, such an analysis could not be performed. A MANCOVA was performed, however. on the data from the DAT and VaD groups given that the homogeneity of covariance assumption was not violated by using only these two groups. The population from which the subject was sampled served as the grouping variable, (DAT vs VaD), with scores from Recognition Memory for Faces (RMF) and Famous Faces Test (FFT) as dependent variables. The score from the HVOT was used as a covariate because of its significant statistical contributions in the regression equations. The initial MANOVA (without taking covariance of HVOT scores into account) was statistically significant [Wilks Lambda=0.69, F (2,40)=8.61, P=O.OOl]. Post-h univariate P-tests suggested significant between group differences for both R M F [F ( 1, 41) = 14.86, P
DISCUSSION The present study supports the well-established finding of differences in storage of information between normal elderly subjects and individuals with dementia [6. 7. 261.

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Simply replicating this finding, however, was not the primary purpose of this investigation. More importantly, the data suggest that deficient visual information processing, as assessed in this investigation by the Hooper Visual Organization Test, is related to, and may indeed partially cause, the primary visual information storage deficit seen in patients with DAT or VaD. The amount of variance in recognition memory accounted for by impaired HVOT performance was by no means total, however, thus suggesting that compromised visuoperceptual ability does not fully explain the pronounced visual memory impairment in either group. In other words, impaired visuoperception may further attenuate an already impaired capacity to encode and store novel visual information. A comparable pattern was observed in both ofthe clinical groups, which is not surprising in light of previous research on level of visuospatial task performance in these populations [24]. This pattern differs from that ofpurely amnestic patients who exhibit intact initial encoding of visual information, but with dramatically decreased delayed recognition. A generally suppressed pattern of performance on the Famous Faces Test was observed only in the DAT group, which is consistent with previous investigations [SS]. The VaD group, while impaired, did not exhibit a comparable pervasive deficit. Thus, both clinical groups performed comparably on the visual episodic recognition task. but they were markedly discrepant on the “visual semantic” task of recognizing famous faces. These findings provide support for the hypothesis that individuals with DAT have not only deficient storage for recent information, but also exhibit a general breakdown in semantic knowledge, in this case recognition of public figures. Given that the primary analysis used in this study was regression-based, direct “cause and effect” statements cannot be made. However, the strong relationship between visual perception and recognition memory for novel, but not remote, faces could suggest a partial dissociation, i.e. that complex visual organization is more strongly related to memory processing at the time of storage rather than during retrieval of previously stored “visual memories”. Thus, it appears that older, previously stored visual memories are likely to be activated through systems different from those involved in the acquisition of new information [ 16,221. As for the lack of significant relationships between recognition memory performance and performance on tasks of visuoconstruction (Block Design) and visuospatial judgment (Line Orientation), it is proposed that HVOT performance required object organization and identification (i.e. parts needed to be integrated into a meaningful whole and recognized), which is also essentially a prerequisite for successful facial recognition memory performance. Line orientation, block design, and similar tasks are more specifically tests of spatial discrimination, and there is clear evidence in the literature for neuroanatomical distinction between simple visuospatial discrimination and visual perception [38]. This finding is also consistent with previous studies that also have not found a relationship between visual memory and discriminative or constructional abilities [8]. Theories of human cognition have conceptualized information processing as occurring in a “sequential” manner, i.e. information must pass through various stages of processing [ 14, 501. Although many such theories have points of disagreement, e.g. serial vs parallel processing [4], most agree that information must pass through several initial stages such as sensation, attention, and perception. Visual information must be encoded accurately in order to be stored appropriately into long-term memory [14, 381, and impairment in a “primary” process can prevent the efficient performance of related or subsequent visual operations [42]. Thus, in the same manner that acquired impairments in executive control abilities [9] and language [20] can adversely impact subsequent verbal memory

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performance, or that executive control deficits can impact upon visuospatial task performance [12], impaired visuoperceptual-spatial abilities may impair subsequent performance on visual recognition paradigms. This may be a possible explanation for the present results, as well as recent findings in non-clinical [29] and mixed clinical [46] groups that have demonstrated a relationship between visuoperceptual-spatial abilities and visual memory performance. Of additional interest is the finding that the clinical samples demonstrated a more robust relationship between visuoperceptual-spatial ability and recognition memory when compared to the non-demented elderly sample. One hypothesis is that the compromised brain attempts to process information in the way it always has, but the introduction of cerebrovascular insult or a degenerative process may result in cognitive processes becoming more dependent upon serial or sequential aspects of processing. The system becomes more “concrete” and is not capable of compensating for impairments in processing. In other words, the introduction of a lesion into a neurobehavioral system results in an over-reliance on serial rather than parallel processes. The damaged system thus operates in a manner similar to the intact system, minus one or more components [32]. Another, and perhaps more parsimonious explanation for the present results, is that there is greater variability in visuospatial encoding and recognition memory performance among demented patients as compared to normal elderly individuals. The greater amount of variability among demented patients may allow for the detection and measurement of certain relationships that can become obscured in groups with a more restricted range of performance. As with any regression-based findings, cross-validation will be necessary before any clinical attempts at correction formulae are made. At present, the current results can serve as a heuristic in the clinical interpretation of performance on tasks of visual memory, and in neurobehavioral formulations of the relationship between visual perception and visual memory. .-I
REFERENCES I 2.

3. 4. 5. 6. 7. X. 9. IO.

Albert. M. S. Cognitive function. In Gcviorric, ,~~ltrop.\!,ch~,loy?. M. S. Albert and M. B. Moss (Editors). pp. 33 53. Guilford Press. New York. 1989. Albert. M. S.. Butters. N. and Levin. J. Temporal gradients In the retrograde amnesia ofpatients with alcoholic Korsahoff’s disease. Arc,h. ,VL~~(I/. 36, 2 I I ~216. I Y7Y. Backman, L. and Herhtz, A. The relationship between prior knowledge and face recognition memory in normal aging and Alzheimer’s disease. d. Gr,o~rro/o~/~. 45, 94 -100. 1990. Baddeley. A. D. 7% P.v~~&oloq~ o/‘h/r~nor~. Basic Books, New York, 1976. Barona. A.. Reynolds, C. R. and Chastain, R. A demographically based index of premorbid intelligence for the WAIS--R. J. co,~.\u/r. c,/irr. P,+tr,/. 25, 885 887. 1984. Becker. J. T., Boiler. F.. Saxton. J. and McGonigle-Gibson. K. L. Normal rates of forgetting of verbal and nonverbal material in Alzheimer’s disease. C’orrr.~ 23, 59 72. 19X7. Becker, J. T., Hulf. F. J.. Nebes. R. II., Holland. A. and Belier. F. Neuropsqchologicnl function in Alrhelmer’a disease: Pattern of impairment rates of progression. .1~<,11.?v’r~&. 45, 263 268. 1988. Becker, J T.. Lopez, 0. L and Wess. J. Material specific memory loss in probable Alzheimer’a disease. J. Nr~rr~l. .Yruro.\rrrq. P.s.ldliirr. 55, I I77 I I8 1, 1992. Bccson, P. M., Bayles, K. A., Rubens, A. B. and Kaszniak. A. W. Memory impairment and ezccut1ve control in individuals with stroke-induced aphasia. Brrri,~ Lrr~lq. 45, 353 175. Benton, A. L.. Hamsher. K. deS. Varney. N. R. and Spreen. 0. Judgment oflmc orientatmn. In Co~~rr/h~~ir~r~~ IO

PERCEPTION

11.

12. 13. 14. 15.

16. 17. 18.

19. 20.

21. 22. 23. 24.

25.

26.

AND MEMORY

1295

Neuropsychological Assessment, A. L. Benton, K. deS. Hamsher, N. R. Varney and 0. Spreen (Editors), pp. 44-54. Oxford University Press, New York, 1983. Benton, A. L. and Tranel, D. Visuoperceptual, visuospatial, and visuoconstructive disorders. In Clinicul Neuropsycholoyy, K. M. Heilman and E. Valenstein (Editors), 3rd edn, pp. 165-213. Oxford University Press, New York. Bondi, M. W., Kaszniak, A. W., Bayles, K. A. and Vance, K. T. Contributions offrontal system dysfunction to memory and perceptual abilities in Parkinson’s disease. Neuropsychology 7, 89-102, 1993. Brink, T. L., Yesavage, J. A., Lum, O., Heersema, P. H., Adey, M. and Rose, T. S. Geriatric Depression Scale. Clin. Geronto/. 1, 37-13, 1982. Bruce, V. and Young, A. Understanding face recognition. Br. J. Psycho/. 77, 305-327, 1986. Butters, N., Miliotis, P., Albert, M. and Sax, D. Memory assessment: Evidence of the heterogeneity ofamnesic symptoms. In Advances in Clinical Neuropsychology, G. Goldstein (Editor), Vol. 1. Plenum Press, New York, 1984. Cermak, L. S. The episodic-semantic distinction in amnesia. In Neuropsychology qfMemory, L. R. Squire and N. Butters (Editors). Guilford Press, New York, 1984. Chandra, V., Philipose, V., Bell, P. A. and Lazaroff, A. Case-control study of late onset “probable” Alzheimer’s disease. Neurology 37, 129551300, 1987. Chui, H. C., Victoroff, J. I., Margolin, D., Jagust, W., Shankle, R. and Katzman, R. Criteria for the diagnosis of ischemic vascular dementia proposed by the State of California Alzheimer’s Disease Diagnostic and Treatment Centers. Neurology 42, 473480, 1992. Cogan, D. G. Visuospatial dysgnosia. Am. J. Ophthalm. 8, 361-368, 1979. Crosson, B., Cooper, P. V., Lincoln, R. K., Bauer, R. M. and Velozo, C. A. Relationships between verbal memory and language performance after blunt head injury. C/in. Neurapsychol. 7, 25tX-267, 1993. Damasio, A. R., Damasio, H. and Chui, H. C. Neglect following damage to frontal lobe or basal ganglia. Neuropsychologia 18, 123-132, 1980. Damasio, H. and Damasio, A. R. Lesion Analysis in Neuropsychology. Oxford University Press, New York, 1989. Flicker, C., Ferris, S. H., Crook, T. and Barthus, R. T. Age differences in the vulnerability of facial recognition memory in proactive interference. Exp. Aging Res. 15, 189-194, 1990. Freedman, L. and Dexter, L. Visuospatial ability in cortical dementia. J. c/in. e.up. Neuropsychol. 13,677-690, 1991. Hanger, P. A., Montague, J. R. and Smith, M. A recognition memory test for the Visual Reproduction subtest of the Wechsler Memory Scale-Revised. Paper presented at the annual conference of the International Neuropsychological Society, San Antonio, Texas, 1991. Horn, J. and Reitan, R. M. Generalized cognitive function after stroke. J. c/in. e.xp. Neuraps~chol. 12,644654,

1990. 27. Hooper,

H. E. The Hooper Visual Organization Test. Western Psychological Services, Los Angeles, 1983. 28. Jordan, C. M., Whitman, R. D. and Harbut, M. A comparative study of memory deficits in workers suffering from hard metal disease. J. c/in. exp. Neurapsychol. 14, 58, 1992. 29. Juhel, J. Spatial abilities and individual differences in visual information processing. huelligence 15, 117-137. 1991. 30. Lanska, D. J. and Schoenberg, B. S. The epidemiology of dementia: Methodologic issues and approaches. In Demenria, P. J. Whitehouse (Editor), pp. 3333. F. A. Davis, Philadelphia, 1993. 31. Mattis, S. Demenria Raring Scale. Psychological Assessment Resources, Inc., Odessa, FL, 1988. 32. McCarthy, R. A. and Warrington, E. K. Cognitire Neuropsychology: A Clinical Introduction. Academic Press, San Diego, 1990. 33. McFie, I. and Zangwill, 0. Visuo-constructive disabilities associated with lesions of the right cerebral hemisphere. Brain 82, 2433259, 1960. 34. McKhann, G.. Drachman, D., Folstein, M., Katzman, R., Price, D. and Stedlan, E. M. Clinical diagnosis of Alzheimer’s disease: Report of the NINCDS-ADRDA Work Group under the auspices of the Department of Health and Human Services Task Force on Alzheimer’s Disease. Neurology 34, 9399944, 1984. 35. Mendez, M. F. Visuoperceptual function in visual agnosia. Neurology 38, 17541758, 1988. 36. Mendez, M. F., Mendez, M. A., Martin, R., Smyth, K. A. and Whitehouse, P. J. Complex visual disturbances in Alzheimer’s disease. Neurology 40, 439443, 1990. 37. Mendez, M. F., Tomsak, R. L. and Remler, R. B. Disorders of the visual system in Alzheimer’s disease. J. c/in. Neuro-Ophthalm. 10, 62-69, 1990. 38. Mishkin, M., Ungerleider, L. G. and Macko, K. K. Object vision and spatial vision: Two cortical pathways. Trends Neurosci. 6, 414417, 1983. 39. Moore, V. and Wyke, M. A. Drawing disability in patients with senile dementia. Psychal. Med. 4,97 -105, 1984. 40. MOSS, M. B., Albert, M. S., Butters, N. and Payne, M. Differential patterns ofmemory loss among patients with Alzheimer’s disease, Huntington’s disease, and alcoholic Korsakoff’s syndrome. Arch. Nemo/. 43, 239-246, 1986.

1296

J H. RI(‘KLR. P A KEENAN and M. W. JACOBSON

41. Near-y. D. and Snouden, J. S. Perceptuospatial disorder in Alzheimer’s disease. Srm. Ophrhalm.2, 151 158, 1987. 42. Reuter-Lorenr. P. A. and Ciazzaniga, M. S. Localization of function: A perspective from cognitive neuropsychology. In ~Yuwohrhurirm~ Cons~qur~ce.~ of C‘y~f,h~o~.n.s~u/rrr Disraw. R. A. Bornstein and G. G. Brown (Editors). Oxford University Press. Neu York. 1991. 43. Sahakian, 8. J.. Morrts. R. G. and ELerden. J. L. A comparative study of visuospatial memory and learning in Alrhcimrr-type dementia and Parkmson’h disease. Brtrr,~ 11 I, 695 718, 198X. 44. Salmon. D. P.. Granholm, E.. McCullough. D.. Butters, N. and Grant I. Recognition span m mildly and moderately demented patients with Alrheimer’s disease. /. clrn. r\-p. Vruwp,\~~+w/. 11, 429 443. 1989. 45. Shlmamura, A. P. and Squire. L. R. Korsakoff’s syndrome: A study of the relationship between amnesia and remote memory impairment. 5ehf1r. .l;ruroxi. 100, 165 -170. 1986. 46. Show, J. S.. Delis, D. C. and Massman, P. J. Memory for the Rey- Osterreith Figure: Perceptual clustering, encoding. nnd storage. .V~,wop.~.i’~ hr>ioy/\, 6, 43 50. 1992. 47. Speedie. L. and Heilman. K. Antcrograde memory deficits for visuospatial material after tnfarction of the right thalnmu. .~wh. .l’rwwl. 40, 183 186. 1983. 48. Strother. C. R.. Schaie. K W. and Horst. P. The relationship between ad\,anced age and mental abilities. J. .-ihn. .Y,w PI \.c,hr//. 57, I66 176. I Y57. 49. Sheet, J. J.. Newman. P. and Bell. B. Significance ofdcprewon in clinical neuropsycholngical assessment. (‘/III. P.\\~c~/Ir,/.Rc1. 12, 21 4s. 1992. 50. Tul\ing. E.. Schacter. D. L.. McLachlan. D. and Moscovitch, M. Priming of semantic autohiogr:+phical hnonledgc: A cast stud! of retrograde amnesia. BI.LI~~I (‘~~c~~~it. 8, 3 20. 1988. 5 I. Warrmgton. E. K. Rrc mqtririm .2lrmor~~ Teu. NFER-Nelson. Windbor. Berkshire. 1984. ._. 5’ Watts. E-. N.. Morris. L. and MxLeod. A. K Recognltwn memory in depression. .I. .4/w. PII~~~/I~~~. 96, 273 275. 19x7. 53. Wcchsler. D H’.,l/.S R Zf~~~u~rl.Pa!chological Corporation. Nea York. 1981. 54. Wcintrauh. S. and Mewlam. M.-M. Visual hemispatial inattention: Stimulus parameters and explorator! ~11.atcgiea. ./. \‘cwrr~/. lif,wwi.(/. P.\,I c/fit/l 51, IJHI 1488. 1988. 55. Wilwn. R. S.. Kasrniak. A. W.. Bacon. L. D.. F:ou. J. H. and Kell). hf. P. Fnc~al recogmrion memory in tlcmentla. (‘,11.1<‘\.18. 32’) 336. 1082. 50. Wilson. R S.. Kasrniak. A W. und Fox. J. Remote memory in semle dementia (‘~I.IL’\ 17. 4 4X. 19XI. 57. Zhang. hl.. Katzman. R.. Salmon. D.. Jin. H.. c‘ai. G.. Wang. 2.. Qu. G.. Grant. I. Yu. E.. Lcvj. P.. Klauhcr. hl. R. and Liu. T. The prc\alence of dementia and Alrheimcr’s disease !n Shanghai, ChIna: Impact of age. gender. and cducat~on. ?~‘~~w~~ir~~/j 27, 428 437. 19%).