A dissociation in the relation between memory tasks and frontal lobe tests in the normal elderly

~~~i~opa!ckuiuyro. Vol 32.

Pergamon

No. 12. pp. 1523-1532. 1994 Flsevier Science Ltd Pnnted in Great Br~kxn 002X-3932.94 S7.00+0 00

0028-3932(94)00096-4

A DISSOCIATION IN THE RELATION BETWEEN MEMORY TASKS AND FRONTAL LOBE TESTS IN THE NORMAL ELDERLY ALAN J. PARKIN* Laboratory

of Experimental (Receiced

and ANDREW

Psychology, 20 January

University

LAWRENCE?

of Sussex, Brighton

BNl 9QG, U.K

1994; accepted 23 July 1994)

Abstract-In this study a group of elderly subjects were examined on three tests of frontal lobe function. Two of these tests, FAS word fluency and the Alternate Uses Test, were considered tests of spontaneous flexibility, as defined by Eslinger and Grattan [Neuropsycholoyia 31,17-28,1993]. The third, the modified Wisconsin Card Sorting Test (WCST), is considered a test of reactive flexibility. Performance on two tests of memory, release from proactive interference (PI) and a matched recall and recognition test was also measured. The elderly were shown to be impaired on all tests when compared with young controls. Analysis revealed that release from proactive interference was significantly correlated with performance on alternative uses but not WCST while the size of subjects’ discrepancy between recall and recognition correlated strongly with WCST but not with Alternate Uses. In addition there was a strong correlation between the two measures of spontaneous flexibility but these measures did not correlate with WCST. Performance on the two measures of memory was also uncorrelated. The data indicate that the pattern of frontal deterioration in the elderly does not comprise a single deficit and, furthermore, that the relationship between frontal dysfunction and normal age-related memory loss is not unidimensional. Key Words:

memory;

aging; frontal

lobes.

In a recent series of studies we have been investigating whether normal age-related memory loss (NARML) is associated with the decline in frontal lobe function that is also known to be a feature of normal aging [20-221. Accelerated neural decline with age is evident in a number of brain regions including the basal ganglia, thalamus, and temporal lobes but, within the prefrontal cortex, the loss has been described as dramatic [29] and it is this which has prompted us to consider whether frontal dysfunction plays a dominant role in determining the nature of NARML. The role of the prefrontal cortex in memory has been slowly emerging via the study of patients with discrete lesions in this area. From these studies a number of memory functions that seem dependent on frontal function have been identified including memory for source and memory for temporal order [28], release from proactive interference [29], and normal free recall relative to recognition [ 14, 241. Within the domain of normal aging, studies have sought a link between frontal function and memory loss via correlational studies in which performance on memory tests thought to *To whom all correspondence should be addressed. tAndrew Lawrence is now at the Department of Experimental Street, Cambridge CB2 3EB, U.K. 1523

Psychology,

University

of Cambridge,

Downing

1524

A. .I. PARKIN

and A. LAWRENCE

have a frontal component are related to neurobehavioural measures of cognitive abilities thought to be mediated by the prefrontal cortex. Studies using this approach have already shown that recall, as measured by the BrownPeterson task, correlates significantly with performance on both the Wisconsin Card Sorting Test (WCST) and word fluency [20]. Memory for source in older subjects has also been associated with more intact frontal functioning [6] and, in a recent study, Parkin and Walter showed that the extent of recollective experience in a recognition memory test was directly related to subjects’ correct performance on the Wisconsin Card Sorting Test 1211. Before reporting the current study it is important to clarify a theoretical point. The measurement of frontal lobe function is a complex matter and there is considerable debate as to what constitutes a test of frontal function. A good case in point is the WCST. Many authors have considered it unequivocally as a test of frontal function [see 26 for a recent review] but others [e.g. 51 have challenged this view and claimed, for example, that it makes considerable demands on the hippocampal formation. Another point is that the term “frontal” can often be extended to include structures associated with the frontal cortex (e.g. the basal ganglia). From our perspective the exact neuroanatomical substrate of a given behavioural measure is not of primary importance. What matters is the psychological process underlying performance on that task and how this might relate to other mental abilities such as memory. At present there is a consensus view that the non-memory tasks used in our study are “frontal”inasmuch as deficits are observed on these tasks in patients with focal frontal lesions or lesions of adjacent structures such as the basal ganglia [l 11. However, it is not essential to the logic of our investigation that this localisation assumption is correct. Our concern is how the age related decline in the functions measured by tests such as WCST relate to NARML. For convenience we will refer to tasks such as WCST as frontal merely to maintain consistency with the current literature. The aim of the present study was to attempt a more refined analysis of the relationship between frontal lobe dysfunction and NARML. Human memory and frontal lobe functions are both complex entities and it seems unlikely, on intuitive grounds at least, that the relation between them should be unidimensional. More likely both memory and frontal function are multicomponential so that any given memory function might be associated with a particular subset of frontal functions. This idea has not, as yet, received any investigation because there has been little development of frameworks within which an idea of this kind might be expressed. However, in a recent study Eslinger and Grattan [ 1 l] have proposed that frontal tasks might be divided into two fundamental types, reuctive and spontaneous. Reactive flexibility refers to the readiness to shift cognition and behaviour freely according to the changing demands of a situation. Spontaneous flexibility describes the ready flow of ideas and answers in response to a question. Eslinger and Grattan examined reactive flexibility, as measured by WCST, and spontaneous flexibility, as measured by the Alternate Uses Test [ 131, in a group of patients with varying degrees of damage to the frontal lobes and basal ganglia. Reactive flexibility was found to be adversely affected in patients with either frontal or basal ganglia lesions whereas spontaneous flexibility was greatly impaired by frontal lesions but far less so by basal ganglia damage. Eslinger and Grattan’s data suggest strongly that there may be a functional dissociation between tests of reactive and spontaneous flexibility. This being so it raises the question as to whether this distinction has any implication for our understanding of the relation between

AGING

AND

MEMORY

1525

frontal lobe function and memory performance-especially as related to NARML. The present study thus examined how performance on the tests of reactive and spontaneous flexibility related to performance on two tests of memory thought to be sensitive to the frontal dimension of NARML. The first of the two tasks chosen was release from proactive interference. This is a variant of the Brown-Peterson Task in which subjects first study three successive trials involving shortterm retention of stimulus triads drawn from the same taxonomic category. On the fourth trial subjects may be presented with a further triad from the same taxonomic category (nonshift) or three items from a different taxonomic category. The extent to which performance on the shift trial increases relative to the preceding trial, as compared with the third and fourth trials in the non-shift condition, constitutes the release from PI measure. Studies have shown that the elderly sometimes show impairment on release from proactive interference relative to young controls although the reason for this variability is not clear [9]. However, some evidence points to a link between the release from PI effect and the intactness of frontal functioning [29]. Variability in the elderly’s performance on release from PI might therefore from stem from an associated variation in frontal dysfunction within the subject groups used. The second task was the Matched Recall and Recognition Task. It has been proposed a number of times that frontal lobe damage results in a disproportionate impairment of recall relative to recognition [14,24]. However, these claims have, until recently, been moderated by the problems raised by task sensitivity in that the apparent sparing of recognition memory might be an artefact of task difficulty-recognition being less affected simply because it is a less sensitive test of memory. This problem was successfully addressed by Calev [4] who devised recall and recognition procedures which produced remarkably similar levels of recall and recognition in normal populations. Using this procedure Calev further demonstrated a disproportionate impairment of recall in a group of schizophrenic patients. Many studies [see 26 for a recent review] have now associated schizophrenia with a characteristic pattern of hypofrontality and it thus reasonable to suppose that the selective disruption of recall shown by schizophrenics can be attributed to frontal dysfunction. More direct evidence for frontal involvement in the selective disruption of recall is reported by Hanley, Downes and Davies [14]. They adopted the Calev methodology and showed that, despite normal control performance, a patient with damage to the caudate produced substantially impaired recall relative to recognition. This finding has subsequently been replicated and extended by Parkin, Yeomans and Bindschaedler [24] in their investigation of CB who became memory impaired due to a frontal lesion arising from a ruptured aneurysm of the anterior communicating artery. The frontal tests used comprised the two tests used by Eslinger and Grattan, WCST and Alternate Uses, plus an additional test of spontaneous flexibility-the widely used FAS test of word fluency [2].

METHOD Subjects

The elderly group comprised 22 adults (18 female, 4 male) who lived independently in their own homes and who reported themselves to be in good health. Any volunteers with diabetes or a history of neurological illness were excluded. All subjects were screened for dementia using the Blessed Scale [I] and none were excluded on this basis. The characteristics of this group are described in Table 1. The measurement of age effects involved various young control groups whose characteristics are described at the appropriate points in the text.

1526

A J. PARKIN

and A. LAWRENCE

The elderly subjects were all tested in their own homes. Where data from younger controls is reported these data were gathered in the laboratory. The five tests were administered at different points across sessions spread over 2 or 4 days. The administration of tasks was arranged so as to minimise any effects of fatigue and to avoid interference from tasks of similar nature.

C&c-matched recull-recoy,zifion. In the recognition procedure 40 unrelated target words are individually presented every 4 set and the subject instructed to try and learn them. After the last word a 3-digit number is presented for 5 set and the subject instructed to recall it. A Yes No recognition procedure then follows in which the subject is shown a sheet of paper on which the 40 targets and 38 distracters are arranged randomly. Half of the distracters are either a rhyme or semantic associate of the targets. In the recall procedure 24 target words are presented followed bya 3-digit number. Recall is then immediately tested. This recall is relatively easy as the list comprises six sets ofcategorically related items, four in each, which are presented in 6 blocks each comprising items from one category. To compare recall and recognition, recall of the 24 target words is compared with 24 matched words from the recognition phase. The elderly group were compared with 23 younger subjects. mean age 48.45 years. Rrleusefiuorn PI. Subjects were presented with three words drawn from the same taxonomic category. They wcrc then requested to count backwards in ones (elderly) or three (young) for 9 set before recalling the words. This was then repeated three times using a ditrerent wjord triad on each trial. There were eight blocks of trials, on four of these the last triad was drawn from a different taxonomic category (shift condition) and on four it was drawn from the same taxonomic category (non-shift). The eight blocks of trials were spread over two sessions. Eleven elderly were presented trials in the order NS, S, NS, S, NS, S, NS, S; the other eleven elderly subjects were presented trials in the order S. NS. S. NS, S, NS, S, NS. Six young control subjects (mean age 30.8 years, NART FSIQ 122.X) were also tested.

FAS orrhalfturnc~ lest [2]. Subjects are asked to give orally as many words as they could beginning with the letters F. A and S in that order, allowing I min per letter. Subjects are informed that the names of people and places or the same root word with different suffixes arc inadmissible. AIfernute uses 1131. Subjects are instructed to consider six common objects [wooden pencil. car tyre, eyeglasses, shoe, key, button]. Each object has a common use which the examiner states. The subject’s task is to generate orally as many other uses for the object or its parts as they can. As an example, a newspaper is most commonly used for reading, but could alternatively be used for swatting flies. to line drawers or shelves, to make a paper hat. etc. Acceptable responses must meet the criteria of being conceivable uses that are different from each other and from the common use. Two trials are presented, each with three objects and a 4.min response period. The three object names are printed on a card left in full view of the subject during each trial. After the examiner states the common use for each object. subjects are instructed to generate alternate uses in any order. .Mod[fied W’iscmsin curd .sorf lcI.sl [IS]. A total of48 stimulus cards are used. Each card must be sorted in accord with one of four reference cards. The subject can sort by the categories of shape. number. or colour. The first category according to which the subject sorts ih scored as correct, and that category is maintained until six consecutive sorts are correct. The examiner then states “the rules have now changed. I want you to lind another rule”. The next category (in the order colour, form. number) is then counted as correct and remains so until six consecutive correct sorts are scored. The procedure is then repeated with the remaining category counted as correct. Two runs of 24

Table

I. Characterlstlcs

of elderly group Mean

Age Education IMC NART FSIQ

7 I .9 years 9.4 years 35.4 106.1

S.D. 4.x

1.3 2.4 12.6

IMC: Information Memory Concentration Score [l] max=37: NART FSIQ: full scale IQ estimated from performance on the National Adult Reading Test 1191; S.D. = standard deviation.

AGING AND MEMORY

Table 2. Performance

Young S.D. Elderly S.D.

1521

of young and elderly group on matched task-all scores are proportions

Recall

Recog

F.A.

RecoggA

0.78 0.12 0.50 0.14

0.78 0.15 0.56 0.20

0.04 0.04 0.12 0.10

0.74 0.1s 0.43 0.16

recall and recognition

Recog-A

- Recall

0.05 0.09 0.06 0.16

Recog = Hits; F.A. = false alarms; Recog-A = Hits minus false alarms; -Recall = Adjusted recognition score minus recall; S.D. = standard deviation.

cards are used. The test is discontinued is as Nelson [1X].

when all 48 stimulus cards have been used or six categories

Recog-A

achieved.

Scoring

RESULTS Matched

recall

and recognition

The number of correct recall and recognition responses were calculated for both elderly and younger subjects. For analytical purposes all scores, except recall intrusions (young; mean intrusions 0.3; S.D. 0.6; elderly; mean 1.2, S.D. 1.6) were converted into proportions. For recall this measure was proportion of total recall possible and the absolute number of intrusions. For recognition the proportion of matched items recognised was calculated. In addition a false alarm rate was calculated based on the proportion of false alarms made to the 38 distracters used in the recognition sequence. In order to provide a correction for response bias in recognition each subject’s proportional hit score was adjusted by subtracting the proportional false alarm score. Using these proportional values a recognitionrecall discrepancy score was also calculated based on the adjusted recognition score minus the recall score. These data are summarised in Table 2. Young subjects performed significantly better on both recall, t (42) = 7.12, P < 0.001, and recognition, t (42)=6.64, P
from

proactive

interference

The mean number of correctly recalled items and number of prior list intrusions were calculated for the elderly subjects and these data are summarised in Fig. 1. Data from young subjects were also collected but these approached ceiling and are not therefore reported. A 2 x 4 ANOVA was performed on the elderly data with Trial (1,2, 3,4) and condition (shift, non-shift) as fixed factors. There was a highly significant effect of trial, [F (3, 63)=30.71, PtO.OOOl], and a significant trial x condition interaction [F (3, 63)= 10.37, P
A. J. PARKIN

1528

and A. LAWRENCE

3.0 -

2.5 -

non-shift z

shift

2.0 -

1.5

!

1

trial

I

1

Fig. 1. Performance

trial of elderly

I

2

subjects

trial

*

I

3

trial

on release from proactive error).

4

interference

(bars = 1 standard

Trials 3 and 4 in both the shift and non-shift conditions. In the shift condition produced significantly better recall [t (21) =2.6, P-cO.021, there was no difference Trials 3 and 4 in the non-shift condition [t (21)= 1.241. A significant release from was therefore obtained. Performance on the frontal lobe tasks is summarised in Table 3 and it can be seen elderly perform more poorly than young controls on all three measures. Correlational

Trial 4 between PI effect that the

analyses

The primary interest was the possibility of correlations between the frontal tasks and components of the memory tasks. However, because IQ has been shown to correlate with frontal tasks in a previous study [19], and this was also widely evident in the present data, it was decided to use partial correlations in which IQ, as estimated from NART, was partialled out of each correlation of interest. The pattern of correlations is shown in Table 4 and it can seen that a strong correlation was found between release from PI and Alternate Uses and that the size of the recognitionrecall discrepancy correlated with both WCST error measures. Applying the Bonferroni correction, which yields an adjusted P value of 0.0125, the correlations remain significant except for that between WCST perseverative errors and recognition-recall discrepancy. It should be noted, however, that the total error measure and the perseverative measure of the WCST are themselves highly correlated (r=0.852, P
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Table 3. Performance of elderly in comparison with young on tests of frontal lobe function

subjects

Young

Old

r

58.3 A 2.8

36.9 10.7

s.7***

14.5 B 5.3

8.0 4.8

2.33*t

WCSTc S.D.

6.0 A 0.0

3.6 1.7

6.3***

WCSTp S.D.

0.3 A 0.1

7.1 7.2

4.3***

WCSTt S.D.

1.7 A 0.5

17.0 8.6

7.9***

FAS S.D. Alternate S.D.

uses

FAS = word fluency, WCST = Wisconsin Card Sorting Test, c = categories, p = perseverative errors, t = total errors, S.D. = standard deviation. A=young control data from Parkin and Walter (1991). B =six young controls (mean age 30.8 years, NART FSIQ 122.8). ***P
Table 4. Correlations between frontal tests and memory measures with IQ (as estimated by NART) partialled out Release from PI FAS Alternate WCSTp WCSTt

uses

0.21 0.60*** -0.24 0.06

Recognition-Recall discrepancy 0.12 0.23 0.47** 0.55***

NART = National Adult Reading Test; FAS = word fluency; WCST = Wisconsin Card Sorting Test; p = perseverative errors, t = total errors. **P
between these tests and WCST measures approached significance (range of r: - 0.09 to 0.18). There was also no reliable correlation between the two memory measures, r=O.lO.

DISCUSSION The above study demonstrated older subjects also demonstrated used. The latter thus confirms the illustrating an age-related decline lobes [7, 20, 21, 281. However, within the elderly group, between tests.

age related impairments on two tests of memory and that substantial deficits on the three tests of frontal function widely known age decrement in memory ability and studies in neuropsychological functions associated with the frontal the factor of primary interest concerned the relationship, performance on the memory tasks and on the frontal lobe

1530

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and A. LAWRENCE

The study was successful in demonstrating significant release from PI in the elderly group, This release effect was, however, variable, and the extent of this release effect was strongly related to how well subjects performed on the Alternate Uses Test. Performance on WCST did not, however, show any reliable relationship with the release effect-a finding consistent with an earlier study showing that unmedicated Parkinson’s patients show normal release from PI despite impaired WCST performance 1271. The present data show that elderly subjects can demonstrate release from PI and that where poor performance on this task by the elderly has been found [9] it may be due to the presence of significant frontal disturbance in the groups investigated. On the Calev Task both young and old subjects showed little discrepancy between recall and recognition although the older group did show significant age decrements on both the recognition and recall components. Comparison with frontal test data showed that larger discrepancies between recognition and recall in the elderly were significantly associated with increased errors on the WCST. However, there was no correlation with performance on the measures of spontaneous flexibility. If, as the data from patients with frontal lesions indicate, increased discrepancy between recall and recognition on the Calev Test indicates frontal dysfunction, it seems paradoxical that the discrepancy scores of young and old in this study did not differ significantly. It should be noted, however, that the older group showed significantly greater variance in the size of this discrepancy. Examination of the data showed that six elderly subjects produced markedly better recall performance than recognition. The origin of this atypical pattern is not clear as yet but one interesting possibility is that it might reflect two kinds of frontallymediated memory impairment. We have already noted those studies in which frontal damage causes a disproportionate impairment of recall but we should also note the case of DelbecqDerousne, Beauvois and Shallice [S] in which a frontal patient exhibited better recall than recognition. This pattern has now been observed in a second frontal patient studied by Parkin et al. [25]. It is thus feasible that the breakdown of the relation between recall and recognition in the elderly also follows this dichotomous pattern. Moreover it would suggest that reduced reactive flexibility relates only to impairments in recall. Another notable feature of the data is that the FAS test produced no correlations with memory performance. There could be a number of reasons for this. In the case of FAS there is known to be a strong relationship with IQ and some have even argued that it is essentially an IQ measure rather than one of frontal function [15]. There is also evidence that relatively simple measures of fluency may not be so sensitive to frontal dysfunction. Butler et al. [3] tested patients with known frontal lesions on both simple and complex frontal tests (the former category included FAS and the latter Alternate Uses) and found that only complex tasks were sensitive to tumour presence. The lack of associations between memory performance and the simple fluency measures used here might therefore reflect test sensitivity. The present results indicate that the relationship between measures of frontal performance and memory tasks considered to have a frontal component is not likely to be simple but that different memory tasks are likely to have different correlates within the range of frontal lobe functions that can be measured. These data thus run contrary to approaches to frontal function that assume some form of unitary deficit [e.g. lo]. Although these data are preliminary it is worth considering possible explanations of the observed relationships. First the link between Alternate Uses and release from PI could reflect some common retrieval mechanism. Performance on Alternate Uses requires some

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flexibility in retrieving information from semantic store and there is also evidence that flexible retrieval process influence release from PI. Gardiner, Craik and Birtwhistle [12] found that cues provided at retrieval could induce release from PI in sets of stimuli when performance on those same stimuli failed to show any release when no retrieval cues were present. A further study also points toward a link between spontaneous fluency and retrieval. Parkin, Walter and Hunkin [22] demonstrated significant age decrements on a list discrimination task in which subjects had to remember which of two lists a recognised target had been presented. Performance on the task was related to WCST and three measures of spontaneous fluency. No correlations were found between discrimination and WCST measures but all three measures of spontaneous flexibility were positively correlated with list discrimination performance. The demonstration that increased discrepancy between recall and recognition correlates with poorer performance on WCST but not spontaneous flexibility measures is perhaps less readily explained. However, closer analysis of the task suggests a possible explanation. In the Calev Task recall is made easy by the blocked presentation of items from different taxonomic categories. These switches are determined by the experimental sequence rather than the subject so the test might plausibly be seen as some measure of reactivity and thus sensitive to other measures addressing a similar function. This argument is backed up by data from Parkin and his colleagues. They have demonstrated that the ability of subjects to attribute recollective experience to a recognised item correlates with correct responding on WCST and that the probability of recollective responding itself is directly determined by the time allowed to initiate a response to the stimulus during learning [23]. To conclude, the present data show that aging produces a decline in memory functions considered, on a priori grounds, to be sensitive to frontal dysfunction. This is consistent with known neuropathological changes in the aging brain and by the fact that performance on these tasks relates to performance on psychological indices of frontal function. However, the relationship between frontal measures and memory does not appear to be unitary. We have provided a preliminary explanation of the differing relationships observed but resolution of this complex problem requires a great deal of future research. Acknowledgements-The Lawrence was supported

authors are grateful to Louise Harsent for her help in running control subjects. by the U.K. Medical Research Council during the period of this study.

Andrew

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