Rates of forgetting in normal ageing: A comparison with dementia

0028-3932/89 $3.00+0.00 ,Ts 1989 Pergamon Press plc

N~“n,p,?choloy,u. Vol. 27. No 6, pp 849-860. 1989 Printed m Great Britain

RATES OF FORGETTING IN NORMAL AGEING: A COMPARISON WITH DEMENTIA FELICIA *Department

of Psychiatry,

and

A. HUPPERT*

Cambridge

University,

MICHAEL

Cambridge, U.K.

D.

KOPELMAN~

U.K.; and tInstitute

of Psychiatry,

London,

(Received 5 February 1986; accepted 28 November 1988)

Abstract-This paper examines the effect of normal ageing on the forgetting rate of visuo-spatial material in a sample of 74 subjects, aged between 16 and 83. It finds that normal ageing produces a mild acquisition deficit as well as a significant increase in the forgetting rate; and it demonstrates that the relatively rapid rate of forgetting in the elderly cannot be accounted for by differences in the initial level of acquisition. The present result is contrasted with that obtained in studies of dementia and the Korsakoff syndrome, which have demonstrated a profound acquisition deficit but a normal forgetting rate once initial learning has been accomplished. Possible explanations of these differing patterns of

results are briefly considered.

INTRODUCTION

EXPERIMENTAL INVESTIGATIONS of memory are usually concerned with comparing how different groups perform on a single occasion. There have been relatively few studies of normal ageing, examining memory changes occurring through time. Individuals or groups may perform equally well within a single test session but show markedly different forgetting rates when retested on subsequent occasions. The starting point for this study was HUPPERT and PIERCY’S [28] suggestion that patients who have hippocampal lesions might be distinguished from those with diencephalic lesions in terms of their rate of forgetting. Diencephalic and hippocampal lesions both produce a severe “acquisition” (or learning) deficit, but, in addition, hippocampal lesions (but not diencephalic) may produce accelerated forgetting once learning has been accomplished [cf. 43,48, but contrast 14, 311. Previously, BLESSED et al. [S] had suggested that the particular susceptibility of the hippocampus to histological changes in normal ageing (and dementia) might be detectable on formal testing. In normal ageing, the histological abnormalities, such as neurofibrillary tangles [52], and sometimes senile plaques [S], tend to be confined to the hippocampus and the immediately adjacent antero-medial temporal structures. In Alzheimer’s disease, these changes are much more intensive and are found throughout the neocortex [S, 541. This suggested that forgetting rates might be accelerated in normal ageing, and Alzheimer-type dementia. The present paper reports findings in a study of normal ageing and compares the results with those obtained in an earlier study of Alzheimer-type dementia

c311. The relationship

between

normal

ageing

and

dementia

has been

debated

since the

l-Now at the Department of Psychiatry, Charing Cross and Westminster Medical School, London, U.K. 849

850

FELICIA A. HUPPEKT and

MICHAEL D. KOP~.LMAN

beginning of the century [I 7, 191, and within the clinical, pathological, and neuropsychological literature. Whilst the clinical features of dementia might appear to suggest an abrupt discontinuity from normal ageing [cf. 29, 341, epidemiological studies have revealed many cases of “mild” dementia within the community [lo, 201. Noting the overlap in the histological features of ageing and dementia, some neuropathologists have argued that dementia represents “accelerated ageing” [53, 601, whilst others have emphasized points in which the pathological characteristics differ [7, 223. Likewise, within the neuropsychological literature, some researchers have identified abnormalities in dementia which are essentially a severe accentuation of those seen in normal ageing [41, 573, while others have tried to draw attention to qualitative differences [6, 301. Despite continued discussion, the issue remains essentially unresolved [3, 393. Memory impairment in the elderly has been demonstrated both in the laboratory and in a number of “applied” contexts: for example, in the recall of medical information Cl]. In laboratory studies, the finding that memory after a delay is poorer in the elderly than in young subjects has usually been attributed to an “acquisition” deficit, rather than to faster forgetting [ll, 15, 23, 40, 59 but see 241. These studies have all employed verbal material. However some investigations of brain-damaged patients suggest that there may be an age effect in the forgetting rate of visuo-spatial material [8, 3 1, 441. There was evidence within two of these studies that an age correlation might also occur amongst healthy subjects [3 1; POWELL, personal communication]. The present investigation employed a test of visuospatial forgetting, the picture recognition test of HUPPERT and PIERCY [27]. In a series of recent studies considerable information has been accumulated about the properties of this test and the performance of different clinical groups [14, 25-28, 31, 37, 481.

METHOD Seventy-four subjects were tested in the main study and a further seven elderly subjects in a subsidiary experiment. The groups in the main study were: (i) Schoolchildren. These were 16 sixth formers (5 male, I I female) from a South London Comprehensive school. Their mean age was 16.9 (range 1619). (ii) Youny adults. The 22 subjects in this group (14 male, 8 female) included Cambridge University undergraduates and postgraduates, clinical and laboratory staff and people seeking employment through a job centre. Their mean age was 22.6 (range 19-29). (iii) Middle aged. The 12 subjects in this group (7 male, 5 female) were primarily recruited from the MRC Applied Psychology Research Pane1 and non-academic staff of the Institute of Psychiatry. The mean age was 55.1 (range 38- 64). (iv) Elderly. This group of 24 (12 male, 12 female) comprised both retired professional people and working class people living independently in the community. Their mean age was 70.1 (range 65-83). These groups had originally been recruited for two separate studies (most of groups I and 3 by MDK; most of groups 2 and 4 by FAH). However the similarity of our results and the fact that we had used identical test materials encouraged us to combine them into this larger study. Groups 1 and 3 had been matched by IQ and groups 2 and 4 by professional qualifications. For the combined group of young subjects (Groups I and 2) l6,/38* had a professional qualification compared with 12136 of the combined older group (Groups 3 and 4). Procrdure Subjects were shown 120 coloured slides of pictures taken from magazines, including pictures of people, animals, landscapes, etc. The exposure time was 0.5 set/slide, and subjects were asked to try to remember the slides. Following a 10 min interval, during which the subjects’ attention was distracted by engaging them in conversation or getting them to perform some irrelevant task, the subjects were given a recognition test consisting of 40 of the

*This includes levels.

three schoolchildren

who intended

to go IO University

and already

had

sufficient

“0”

and

“A”

RATES OF FORGETTING

IN AGEING

851

original slides and 40 (randomly interspersed) “distracters”. Subjects were told that some of the slides had been seen before and some not, and they were asked to say “Yes” or “No” according to whether they had seen each slide before or not. Forgetting was assessed at 24 hr and 1 week. On each occasion, the subjects were given a further recognition test consisting of another 40 of the original slides and another 40 “distracters”. Each subject was tested individually on each occasion. One of the experimenters randomized the order in which blocks of test slides were shown to individual subjects, and the other experimenter always showed the same blocks of slides in the same order, but this appeared to make no difference to the overall pattern of results. In a subsidiary experiment, a further seven “elderly” subjects were tested using a procedure identical to the above, except that the exposure time at the initial presentation of the 120 slides was 1.O set/slide. These subjects had a mean age of 70.3 yr (range 62-93). Data analysis The conventional method of analysing data from recognition memory experiments is in terms of the percentage of correct responses. This involves adding together the number of true positives (TP) and the number of true negatives (TN) and expressing the sum as a percentage of the total number of items. The resulting statistic is informative, easy to interpret, and has the advantage of being a distribution-free measure of performance, i.e. it is valid whatever the underlying distribution of scores. The d’ transformation is often used for analysing recognition memory, but our data do not appear to be well suited to this transformation. The d’ transformation was originally developed in the context of signal detection, where the “noise” or error component was assumed to follow a normal distribution, and where the distributions of “signalfnoise” and “noise” were assumed to have equal variance 1491. Some early work 1181 suggested that the assumption of normality may in fact be quite reasonable even in recognition memory research, but that the assumption of equal variance was unlikely to be satisfied. In the present study, there are a large number of zero false positives responses, which correspond to the “noise” in the d’ theory. The normal deviate is not defined rigorously for zero responses so that an arbitrary adjustment is required to produce the transformed variable. This adjustment produces a relative under-estimation of performance. Further, many of the true positive responses are close to the maximum 100% value, again casting some doubt on the equivariance Gaussian assumption. In view of these difficulties, we feel that a statistic such as percent correct responses will provide a clearer picture, and an easier interpretation of the data. However, we recognize that a given value of percent correct can correspond to many different combinations of TP and TN. Therefore, in order to provide as much of the available information as possible, we also present the raw data separately for true positives and false positives (FP), the latter providing an index of the guessing rate.

RESULTS Figure 1 plots the mean percent correct responses (true positives plus true negatives) of the four age groups in the main study at the 10 min, 24 hr and 1 week retention intervals. Analysis of variance of performance at each of the three retention intervals indicated that there was a highly significant effect of age (F=9.2, 18.7 and 23.4, P
852

FELICIAA. HUPPERTand MICHAELD. KOP~LMAN

10 mins

Schoolchildren

+

Young

O---o

adults

-+

1 week

24 hrs

FIG. I. Percent correct responses on recognition memory test for four age groups as a function of retention interval. (Data points are + I SE.) Schoolchildren N= 16, young adults N= 22, middle age N = 12,elderly N= 24.

percent score, the rate ofTP and FP responses are presented in Table I. It can be seen that the number of TPs decreases over time for all groups. Analysis of variance of difference scores showed a significant effect of age at each retention interval (P~0.01 ). Difference scores were used to compare the rate ofchange over time between groups. Analysis of variance showed a significant effect of age between 10 min and 24 hr (F=9.3, P
TABLE I. Mean numbers

of true positive and false positive responses and retention interval 10 min

True positive (max =40) Schoolchildren Young adults Middle aged Elderly False positives (max =40) Schoolchildren Young adults Middle aged Elderly

SE 1.7

24 hr

36.0 32.0 29.0 29.5

2.5 0.9

31.2 29.9 17.4 21.1

4.0 1.6 5.5 5.4

I .2 0.7 1.x 0.6

5.4 4.5 6.3 7.7

I .o

as a function

SE 2.1 1.3 3.2

of age

1 week SE 1.9

1.2

25.3 24.6 16.4 1x.4

3.0 I.1

1.6 I.0 2.4 0.‘)

7.5 5.X 9.0 10.2

I.9 1.2 2.9 1.0

I.7

RATES OF FORGETTING

IN

AGEING

853

This analysis indicates that, in our study, older subjects forgot more rapidly than young subjects. The significant difference in forgetting rates occurred within the first 24 hr. However, before concluding that the difference in forgetting rate represents a true age effect, we must examine the possibility that our finding is a consequence of the age differences in initial level of performance on this task. It is possible that subjects whose initial performance is high may forget more slowly than those whose initial performance is low. We have examined this possibility by undertaking a number of additional analyses of our data. An analysis of covariance was performed to reduce any effect of initial performance level on subsequent performance. When scores at 24 hr and 1 week were covaried with scores at 10 min, the age differences remained highly significant (F= 8.0,12.1, P < 0.001 for 24 hr and 1 week respectively). Moreover, within both young and old groups there was a relationship between initial level of performance and subsequent forgetting rate but it was in the opposite direction to that hypothesized above. Namely, we found that young and old subjects, whose initial performance was high, forgotfaster than their counterparts whose initial performance was low. Therefore age differences in forgetting rate on this task cannot be the consequence of young subjects starting at a higher level of performance. A further set of analyses was undertaken with the aim of comparing rates of forgetting in those subjects whose performance was matched at the initial 10 min retention interval (all of these subjects having received a 0.5 set exposure time). The lowest score in the two young groups was 80%; accordingly we included only subjects scoring at least 80% correct at the 10 min interval. We also excluded all subjects scoring more than 90% correct so as to avoid ceiling effects. The criterion of 80-90% correct was attained by 28 young subjects (11 school children, 17 young adults) and 18 older subjects (8 middle aged, 10 elderly). Because there were no significant differences between the two younger groups or between the two older groups on any of the subsequent analyses, we present the data for the combined younger group (mean age =20.4) and the combined older group (mean age 62.1). These data are presented in Fig. 2. As a result of our matching procedure, there was no significant difference between the younger and older groups at the 10 min retention interval. However there was a marked difference between the groups at each of the longer retention intervals (F= 14.3 and F= 36.5, P
F~LIUA A. HUPPEKT and MICHAEL D. KOP~LMAN

854

100

I

I

I

10 mins

I

24 hrs

16 - 29

yrs

*

36 - 63

yrs

o--O

4

1 week

FIG. 2. Percent correct responses on recognition memory test as a function ol’ rctcntion interval. Young and older subjects were matched on their initial performance at the IO min retention interval. each scoring between 80 and 90%) correct. There were 28 young subjects and 18 older subjects. (Data points are mean + 1 SE)

curve upwards, in relation to that of the elderly group given a 0.5 set exposure. The mean initial recognition score of the elderly group given a 1.0 set exposure per slide closely matched that of the young adult group given a 0.5 set exposure (85.9% vs 87.4%, 1 = 0.59, ns), whereas there is a significant difference between their performance at 24 hr (t-3.4. PcO.01) and 1 week (t=2.6, P
DISCUSSION The present findings suggest that older subjects tend to forget visuo-spatial material faster than younger subjects. Age appears to account for 3&48X of the variance in correct recognition scores, and 1430% of the variance in percent retention scores. However, three possible criticisms might be raised, which need to be considered before discussing further the implications of this finding:

855

RATESOF FORGETTINGIN AGEING

100 ,-

g

Young

adults

(0.5

set

exp.)

o--_-o

Elderly

(0.5

set

exp.)

M

Elderly

(1.0

set

exp.)

o---O

go-

:

0 0

t

00-

5 L

‘0 0 ?Oti

60 I

1

10 mins

24 hrs

I

1 week

FIG. 3. Percent correct responses over time on recognition memory test as a function of initial duration of stimulus exposure. (Data points are mean + 1 SE). Young adult N=22, elderly (1 set) N = 7, elderly (0.5 set) N = 24.

TABLE 2. Correlations performance

(a) Correct 10 min 24 hr 1 week

recognition

(b) Percent 24 hr 1 week

retention

*P
and shared variance between age and on the Huppert-Piercy test

scores: -0.55* -0.69* -0.66*

30 48 44

-0.55* -0.38*

30 14

scores:

(one-tailed).

(1) Initial acquisition level? Although there was a difference between age groups in the initial (10 min) recognition scores, it seems unlikely that acquisition level or a “ceiling” effect would account for the difference in forgetting rates because: (i) the groups also differed significantly after co-varying for the initial level of performance; (ii) “titration” of the initial exposure time in a small group of elderly subjects equated their initial recognition score to that of the young adult group, but they still forgot faster; (iii) when the analysis was restricted to those in the main sample whose initial recognition scores (ScrSO%) were similar, the older subjects still forgot faster. (2) Change in response bias? In order to examine the possibility that changes in response bias through time might underlie the apparently faster forgetting of the older groups, we have presented the data for true positive and false positive responses within each group. These failed to reveal any consistent change in response bias in the two older groups which would account for their faster forgetting. As discussed above, the application of signal detection analysis involves

856

F~LICIAA. HUPPEKT and

MICHAEL D. KOPELMA~

questionable assumptions when a number of subjects either obtain maximum true positive scores or make no false positive errors. For this reason, HUPPERT and PIERCY [25] previously rejected the use of the d’ statistic; and SAHGAL [47] has similarly criticized its employment in recognition memory tasks. (3) Dehy

inter&

matched?

The present study employed a procedure identical to that of earlier studies, involving a 10 min delay between the end of the presentation of the slides and the initial recognition test. This technique has previously produced evidence of faster forgetting in some studies [28,48] but not in others [14, 27, 311. However, MAYES [38] has criticized the procedure on the grounds that subjects who are given prolonged exposure times have a longer delay from the mid-point of viewing the slides until initial testing. We think it unlikely that modifying the procedure to take account of Mayes’s argument would have produced any important change in the results of these various studies, because: (i) in the present study, consistent results were obtained, whether presentation and delay conditions were identical for young and old groups (Fig. 1) or a “titration” procedure was employed (Fig. 3). (ii) Mayes’s criticism applies only to findings obtained between the initial and the second test intervals, and it is very unlikely to be relevant to findings beyond the second test interval. (iii) Interference effects between the end of slide presentation and initial recognition testing may be of critical importance in determining forgetting rates, and our technique controls for this. (iv) Interpolation of the results of earlier studies 127, 311 suggests that delaying the initial recognition test in healthy subjects to fulfil Mayes’s requirements would have had negligible effect on overall forgetting rates. Another factor to be considered in drawing conclusions about forgetting rates is the type of material employed (verbal or non-verbal). Various studies using verbal material have failed to find a relationship between age and forgetting [ 15, 23,40, 59 but see 241. POWELL [44] reported that visuo-spatial retention declines with age, whereas verbal retention is unaffected. His subjects were a mixed group of brain-damaged patients and healthy controls, but his conclusions still held when the data from his 64 controls were analysed separately (Powell, personal communication). BENTON et ul. [2] have reported deterioration with age on a test of short term visual retention; and KOPELMAN [31] reported age correlations in Korsakoff patients on the Huppert-Piercy test which closely matched those found in the present healthy subjects. The fact that the age correlations in Korsakoff patients and healthy subjects are so similar (despite the narrower age range in the Korsakoff study) suggests that the effect previously reported in Korsakoff patients [31] may simply be a consequence of normal ageing. In addition, there is ample evidence that, compared with young subjects, normal old people also have difficulty in ucquiring new information [e.g. 111. This is borne out by the present study, since (a) when given the same stimulus exposure (0.5 secislide) the older subjects performed significantly more poorly than the younger subjects at the 10 min retention interval and (b) increasing the stimulus exposure (to 1.O set) for a group of elderly subjects, resulted in comparable performance between old and young subjects. Relationship

between normal ugeing and Alzkeimer’s

disease

There is substantial evidence that patients with Alzheimer-type dementia (AD), even in the early stages, are impaired in the acquisition of new information [e.g. 30, 39, 411. The magnitude of this acquisition defect in Alzheimer patients appears to be very much greater

RATES OF FORGETTING

IN AGEING

857

than that found in normal ageing. In order to match the recognition scores of Alzheimer patients and their (age-matched) controls at 10 min as closely as possible, KOPELMAN [31] had to give the Alzheimer group approx. 14 times as long as long to view each slide. What is particularly significant is that, in contrast to the findings of the present study, the Alzheimer patients subsequently showed a normal rate of forgetting on this test-a result consistent with that in a similar study by FREED et al. [14], as well as a study of Huntington’s disease patients [37], and earlier studies of Korsakoff patients [27,48]. This indicates that AD has a selective effect on memory. Acquisition, which may already be compromised in the elderly, is reduced very much further in AD, although the rate of forgetting remains unaffected, once learning has been accomplished. There have been many attempts to show that dementia produces effects which are qualitatively different from normal ageing, but most previous studies of memory have found only quantitative differences. For example, there have been attempts to show that Alzheimer patients show a specific impairment in making use of semantic encoding or categorization in verbal recall [56], but such studies are confounded by the problem of “floor” effects. Using a different technique, which achieves relatively high levels of performance even in impaired populations, we have found a qualitative difference in the effect on memory of normal ageing and dementia. Normal ageing produces a mild acquisition deficit and a slight increase in the forgetting rate (Fig. l), whereas dementia superimposes a severe acquisition defect but no further effect on forgetting rate, using this same test. It should be noted that the largest decrement in performance occurred between the young adult subjects (mean age 23.3 yr) and the middle-aged group (mean age 58.8 yr). Some previous studies [4, 161 have also reported that performance at some cognitive and memory tests deteriorates at a faster rate before the age of 60 than after that age. On the other hand, the classical histological changes of ageing (senile plaques, neurofibrillary tangles and granulovacuolar degeneration) occur most commonly after the age of 60 [54,55]. It seems likely that the change in the forgetting rate detected in the present study may reflect some factor other than these age-related histological lesions. One possibility would be a mild metabolic decrement, in view of the fact that the gross metabolic disruption which follows electro-convulsive therapy [ 131 appears to be associated with markedly accelerated forgetting [48]. In this connection, some studies have reported a decline in the number of glial cells (thought to have metabolic function [35]) in normal ageing [7,21 but contrast 511, although this does not appear to worsen in dementia [42, SO]. The severe acquisition deficit in Alzheimer patients may be related to the widespread proliferation of histological abnormalities throughout neocortical and subcortical structures, including cholinergic nuclei (nucleus basalis, septal nucleus, diagonal band of Broca). Cholinergic neurons appear to be relatively well preserved in normal ageing [7,9,45], but to be substantially depleted in Alzheimer’s disease [7,36,45, 581, and present evidence suggests that cholinergic depletion would be expected to produce a severe acquisition deficit rather than accelerated forgetting [32, 331. Any such hypotheses must remain somewhat speculative until there are further advances in our understanding of the relationship between ageing and dementia at a neuropathological level.

CONCLUSION In conclusion, the present results indicate a distinction between ageing and of dementia. Normal ageing produces a mild acquisition

the effects of normal deficit and somewhat

858

FELI~IA A. HUPPEKT and MICHAEL D. KOPIXMAN

faster forgetting of visuo-spatial material, whereas dementia gives rise to a severe acquisition deficit while producing no further effect on the forgetting rate. These differing effects are consistent with those neuropathological findings which suggest a distinction between the effects of ageing and of dementia [7,22], but further evidence will be required before the neuropathological basis of these memory deficits can be specified more precisely. Nevertheless, the present findings provide support for DORKEN’S [ 123 conclusion that “senile dementia is qualitatively, as well as quantitatively, different from normal senescent decline, is independent of it, and probably superimposed on it”. Acknowledgements-We would like to thank Professor W. A. Lishman for reading and commenting upon an earlier draft of this paper and Dr D. E. Walters for advice and assistance with statistical analysis. We are grateful to the various agencies who helped provide us with subjects. These include the teaching staffof Walworth Comprehensive School, the MRC Applied Psychology Unit Research Panel, and the wardens of various sheltered accommodation units in Cambridge and London. FAH was supported by a project grant from the Medical Research Council; MDK was supported by a Wellcome Trust Lectureship.

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