Nruropsychologw Vol. 24. No. 5, Pp. 681-690. 1986. Prmted m Great Britain

00X-3932/86 ~~.CCI+O.W Pergamon Journals Ltd.

THE EFFECTS OF VARYING CUE-LOAD ON AMNESIC AND NORMAL CUED RECALL

HOWARD F. JACKSON

Department of Psychology, Moss Side Hospital, Maghull, Merseyside, U.K

(Accepted 27 January 1986)

Abstract-The effects ofcue-load and cue-type (category and rhyming) on the cued recall of word lists were examined in amnesic and control subjects under conditions where contextual information was either important or superfluous to recall. Results indicated that amnesics were differently impaired compared to controls with increasing levels of cue-load, regardless of cue-type or the importance of contextual information. Amnesics achieved normal recall when cues applied to only one item. The results are interpreted as providing contradictory evidence for the semantic encoding and contextual encoding deficit theories. It is argued that human amnesia may result from a specific, unitary deficit at the cue generation stage of recollection.

INTRODUCTION

AMNESIA in humans has been attributed to a specific deficit in encoding [224] or retrieval processes [14, 16, 18, 20, 21, 231. In addition, a third cognitive dysfunction has been suggested which claims that amnesics have little difficulty in remembering specific items but fail to utilize contextual information during recall [9-111. Despite many studies which provided supportive evidence for each of these theories, there have been few which have attempted to compare them within the same experimental paradigm and with the same amnesic subjects.

Retrieval deficit theories claim that abnormal levels of forgetting are due to an enhanced susceptibility to interference from prior information during cued recall when the same cues are used for both prior and current item recall [18, 231. Further investigations failed to support the interference hypothesis [ 171 although it is possible that floor effects may have led to misinterpretation of the data. Conversely, encoding deficit theories, based on the depth of processing theory [6], have arisen from studies exposing the amnesics’ impoverished use of semantic information [335]. However, Korsakoff patients have been shown to be capable of semantic encoding and storage and utilizing semantic cues to the same extent as normals [13]. Furthermore, ensuring deep initial processing fails to substantially aid amnesic recall

t-1, 7, 121. Since amnesics show little difficulty in determining whether or not an item had been

encountered before but display considerable impairment in assessing when the item was encountered, it was claimed that their memory difficulties may result from an impaired ability to either encode [9, lo] or retrieve [l l] contextual information. Critics of this theory have pointed out that:

(1) the context has not proven a very robust one for normal subjects [2]; (2) dramatic changes in contextual cues have little effect on the discrepancy between amnesic and control recall [22]; and

681

682 HOWARD F. JACKSON

(3) intrusion errors may be markedly reduced in amnesics by minor changes in contextual information [22].

Varying the number of prior-list items related to a cue (i.e. cue-load) allows for an investigation of the retrieval-interference hypothesis since this hypothesis would predict a greater disruption of amnesic recall compared to controls with increasing cue-load. A differential effect of semantic (category) but not phonemic (rhyming) cues on amnesics compared to controls would support the semantic encoding hypothesis. Comparison of performance under two experimental conditions, one which requires contextual discrimina- tion and the other which does not permit an exmination of contextual theories of amnesia. Since these three hypotheses are examined within the same experimental design possible important interactions may also be investigated.

METHODS

Ten male amnesic patients from the Mersey Region were selected on the basis of relatively normal cognitive and perceptual abilities and a clinical diagnosis and amnesic syndrome. Table 1 shows the age, Wechsler Adult Intelligence Scale (WAIS) vocabulary subtest scaled score, WAIS Verbal and Performance IQ Digit Span, Wechsler Memory Scale MQ together with Paired Associate Learning Sub-test scores, clinical diagnosis (aetiology), and Williams Delayed Recall Test. As can be seen all the amnesic subjects revealed a high degree of memory impairment on these tests and relatively normal WAIS scores. Other cognitive tests were included in the selection battery, but the results are not presented here. An equivalent number of controls matched for age, sex, and WAIS vocabulary score were included. Table 1 shows their age and WAIS vocabulary scaled scores.

Mater-i& and drsiyn

Three ii& of 30 words chosen from the Thorndike- Lorge count [lS] were printed individually on 20 x 12.5 cm white cards. Wherever possible, high frequency words were chosen and frequency of use was balanced across lists. Words were selected to match a rhyming or category cue (cue-type) such that mean frequency of use was balanced across cue-type conditions. In addition, 20 words unrelated to each other or to any of the cues on the basis of category or rhyme were included as ‘fillers’ for List 1.

Word lists were compiled such that one, two or four words matched to each cue. In the one word per cue condition (cue-load = I), the cue applied to only one word which appeared in List 3. In the cue-load =2 condition, two words matched lo a single cue, located in List 3 and List 2, repectively. In the cue-load = 4 condition, a single cue matched four words, one in List I, two in List 2 and one in List 3. There were five category and five rhyming cues for each of the three cue-load conditions. Frequency of use of stimulus words was balanced across all cue-load x cue-type conditions.

An example of the design is shown below. for the cue-load =4 conditions

List I List 2 List 3 Cue

turnip carrot x x x pea

case race x x x grace

x-indicates an item unrelated to the cue

cabbage x x

lace x x

type of vegetable

rhymes with pace

Words in all lists were presented randomly at the rate ofone word every 4 sec. with the proviso that words in List 2 which matched to the same cue were separated by at least two items. Stimulus words were shown to the subject. read aloud by the author and repeated aloud by the subject in order to ensure that the word was perceived and attention maintained. Beyond these measures, no other means of facilitating encoding was enforced.

Immediately following presentation of the final word in each list, subjects were required to count backwards from

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684 HOWARD F. JACKSON

a three-figure number for 60 sec. For Lists 1 and 2, subjects were asked to recall as many items as they could in any order from the last word list presented, immediately following the ‘filled’ 60 set interval. The procedure for List 3 was exactly the same as that for Lists 1 and 2, except that recall was elicited by the presentation of cues.

Condition 1, Cues were presented verbally and randomly in order to minimize possible interactions between cue- load, cue-type and delay between presentation and recall. Subjects were asked to recall the word from List 3 which matched the cue. If subjects claimed that they were unable to recall the word, they were then asked to guess at the most likely word they could think of. Semantic cues were in the form “One word in the last list was a type of. ,“. Phonemic cues were in the form “One word in the last list rhymed with ,“,

Condition 2. Only seven subjects from each group who had taken part in Condition I were included in this condition. These subjects are indicated by ‘*’ in Table I. Following the cued recall of List 3, cues were randomly presented again in much the same way, except that the subject was informed how many words from all three lists matched the cue. Subjects were required to recall as many words which matched each cue from all three lists regardless of presentation order. When subjects claimed to be unable to recall a word they were prompted to guess.

RESULTS

A two-way analysis of variance with repeated measures across lists was performed on the percentage of words recalled from each of the three word lists. Over all lists, controls (30.90%) recalled more words than amnesics (15.43%) and this difference was significant [F( 1, 18)= 29.75, P<O.OOl]. A significant difference between lists was also found [F (2, 36) = 46.33, P < O.OOl], but the groups x list interaction failed to achieve significance [F (2, 36) = 1.8 11. Figure 1 shows the mean percentage recall across Lists I,2 and 3. As can be seen, the provision of cues in List 3 aided amnesic and control overall recall to the same extent and both groups were equally impaired by the prior presentation of List 1 on the free recall of List 2, although a floor effect on amnesic List 2 recall may mask possible differences between groups.

b--__ /

/ ‘-4

FIG. I. The percentage of words recalled by amnesics and controls for each of the three word lists ~~ controls; amnesics.

ConditiotI 1

A three-way analysis of variance with repeated measures across cue-type (i.e. category and rhyming cues) and across cue-load was performed on List 3 recall. Overall, a significant difference between groups was found [F(l, 18)=7.50, P~O.053, with controls (41.3%) recalling more words on average than amnesics (28.7%). No difference between the effects of

VARYING CUE-LOAD 685

semantic and phonemic cues on recall was found [F (1, 18) = 3.601 and the cue-type x groups interaction also failed to achieve significance [F (1, 18) = 1.151.

A significant effect of cue-load was found [F (2, 36) = 56.26, P < O.OOl]. Similarly, cue-load was found to have significantly different effects on amnesics and controls [F (2, 36) = 5.48, P<O.Ol]. Figure 2 shows the percentage cued recall of List 3 across cue-load for amnesics and controls. As can be seen, an increase in cue-load had a detrimental effect on both groups, but amnesic cued recall was significantly more impaired by increasing levels of cue-load than control recall. Students’ t statistics were performed on amnesic and control performance at each of the three cue-load conditions. These analyses are shown in Fig. 2 and confirm the differential effects of cue-load on the two groups.

Cue load

FIG. 2. The percentage of words recalled from List 3 across cue-load. ~ controls; ~~~~~- amnesics. r(18)=2.96, P<O.Ol; t(18)=2.72, P<O.Ol; t(l8)=0.

It is interesting to note that, under conditions where cue-load was only one item (cue- load = l), there were no significant differences between amnesic and control performance. Since both groups achieved approximately 54% recall of List 3 items under these conditions, the failure to find group difference can not be explained as an artifact of floor or ceiling effects. Cue-type did not influence significantly the effects of cue-load as shown by the non- significant cue-type x cue-load interaction [F(2, 36)= 1.83). Nor did cue-type influence the differential effects of cue-load across groups as shown by the non-significant groups x cue- type x cue-load interaction [F (2, 36) = 0.793.

Percentage intrusion errors were calculated per total number of errors for each subject and analysed by a three way analysis of variance with repeated measures across cue-type and cue- load. A significant effect of cue-type was detected [F (1, 18) = 4.46, PC 0.05] with a greater number of intrusion errors occurring following category cues (56.72%, S.D. 20.16) compared to rhyming cues (46.30%, S.D. 22.26). A significant cue-load effect was also found [F (1, 18) = 42.90, PC O.OOl] with over twice as many percentage intrusion errors occurring in the cue-load=4 condition (68.62%, S.D. 12.57) than in the cue-load= 2 condition (32.40%, S.D. 18.32). Surprisingly, there was no significant difference between controls and amnesics in percentage intrusion errors nor did any of the interaction terms achieve significance.

686 HOWARD F. JACKSON

Condition 2

The number of items correctly recalled for each of the seven amnesics and seven controls tested under Condition 2 (i.e. cued recall from all three lists) were scaled using the formula:

number of items correctly recalled Scales cued recall = ~~ ~~~ ~- ~~~~ ~~

cue-load These data were then subjected to a three-way analysis of variance with repeated measures across cue-type and cue-load.

The most important findings from this analysis are that the effects of cue-load [F(2, 24)= 11.47, P<O.Ol] and thegroups x cue-load interaction [F(2, 24)= 3.48, P<O.O5] maintained significance in the absence of response competition and the requirement of list differentiation. Figure 3 shows the percentage scaled cued recall for both subject groups across cue-load. As can be seen from this graph, the cued recall of items under conditions of cue-load = 1 did not differ between groups, as was found when the recall of List 3 items only was required (i.e. Condition 1). Similarly, amnesic cued recall was impaired compared to controls with increasing cue-load.

The apparently higher performance of both groups under cue-load =4 conditions compared to cue-load = 2 conditions may reflect a priming effect in both groups, but more probably was due to the chance effects of guessing and is, therefore, not considered further here.

FIG. 3. The percentage of words recalled from all three lists across cue-load. ~ controls: amnesics.

A significant groups x cue-type interaction was found [F=7.57, Pt0.051. Closer examination of the mean cued recall for amnesics and controls under each of the cue-type conditions revealed that amnesics achieved a mean percentage scaled score of 37.14% and 38.37% for category and rhyming cues, respectively; compared to 55.50% and 44.48%, respectively, for controls. Students’ t statistics of the differences between these four means revealed that the only significant differences occurred in the comparisons between control recall with category cues and (1) control recall with rhyming cues [t (12) = 1.93, P < 0.051; (2)

VARYING CUE-LOAD 687

amnesic recall with category cues [t (12)= 2.93, P<O.Ol]; and (3) amnesic recall with rhyming cues [t (12) = 2.53, P < 0.051. All other comparisons were non-significant. Thus, the significant groups x cue-type interaction noted previously may be considered to be due to the comparatively greater recall of controls with category cueing. It is noticeable that this interaction failed to achieve significance when the recall of List 3 items only was required (i.e. Condition 1).

Although no formal analyses of the differential performance of amnesics with different aetiologies were performed, Table 2 shows little difference between the Korsakoff patients and the head injury and CVA amnesics in either condition or in percentage intrusion errors in Condition 1. Korsakoff patients may have performed slightly better than the other amnesics when semantic cues were provided although it is unlikely that this difference would achieve significance. However, the major finding is that cue-load severely impaired recall in all the amnesics regardless of aetiology.

Table 2. The mean percentage of words recalled in conditions 1 and 2 and intrusion errors in condition 1 by Korsakoff and closed head injury and CVA subjects across cue-load and cue-type

Amnesics Korsakoff Head injury and CVA

Cue-type Category Rhyme Category Rhyme

Cue-load 4 2 1 4 2 1 4 2 1 4 2 1

Condition 1 23.3 23.3 63.3 10.0 30.0 50.0 15.0 5.0 45.0 0.0 20.0 50.0 Condition 2 36.3 37.5 55.0 42.5 27.5 50.0 41.7 16.7 40.0 43.3 23.3 53.3

Intrusion errors 65.2 34.8 - 66.7 23.8 - 64.7 26.3 ~ 60.0 6.3 -

DISCUSSION

The major finding of the present study is that cued recall in amnesic subjects was detrimentally influenced to a greater extent than controls by increasing levels of cue-load. This finding supports the previously mentioned suspicion that the dismissal of the retrieval- interference hypothesis by WARRINGTON and WEISKRANTZ [31] was based on the misinterpretation of data which were subject to floor effects. The results here indicate clearly that prior items interfere with the cued recall of subsequent related items when floor and ceiling effects are avoided. Furthermore, when cues which encompassed a single item were provided, amnesic cued recall achieved normal levels. A major factor in amnesic recall, therefore, appears to be the number of items subsumed by a cue. The present study also shows that normals are adversely affected by cue-load [19].

Since amnesics achieved normal levels of recall with both semantic and phonemic cues semantic encoding would not appear to be impaired as CERMAK and co-workers have suggested (e.g. [SJ). Furthermore cue-load had the same degree of disruptive effect on amnesic cued recall regardless of cue-type. If semantic encoding was deficient in amnesics, then it may be expected that they would suffer less interference than controls when semantic cues were presented due to the relative absence of interfering semantic items in memory store.

Interference from related items alone may be insufficient to explain the present results.

688 HOWARD F. JACKSON

Since free recall of List 1 was impaired in amnesics even though distractor items were absent, it is clear that amnesics require the provision of an external cue at recall in order to retrieve an item. It is possible that amnesic subjects fail to initiate cue generation. Indeed, this single feature of the human amnesic syndrome may also explain the enhanced effect of interference

in amnesics. MCDOWELL [13] proposed that a similar deficit may underlie amnesic disorders. In his

study, it was noted that semantic cues provided at recall aided amnesics to the same extent as they did controls, regardless of encoding instructions. Although he suggested that these findings support a theory based on a specific disability to generate cues in the amnesic group, amnesics were still impaired when the cue to recall was externally provided by the examiner. The present findings suggest that this residual impairment may have been due to the use of cues which subsumed more than one item. In the McDowell study [ 131, five words were cued by a single category word, thus amnesics may have been differentially impaired by high levels of cue-load. It is suggested here that recollection may involve a process of multiple cue generation. The provision of a single cue in McDowell’s study and the present experiments may be insufficient to elevate amnesic recall to normal levels when the cue signals the recall of more than one item. Additional cue generation may be a necessary process in order to differentiate between competing items.

In general, then, the provision of an external cue to recall would be expected to aid recall to a greater extent for amnesics than for controls. The failure to find such an effect when comparing overall cued recall of List 3 with free recall of List 2 in the present study may be due to two factors. First, it was pointed out earlier that amnesic performance on List 2 may be subject to floor effects. Second, the comparatively greater aid of external cues for amnesic subjects may well be offset by their increased susceptibility to interference from previous items in List I and/or List 2 which were related to the cues and two-thirds of the items in List 3. It is clear that external cues did aid amnesic performance to a greater extent than control performance under conditions where cue-load was only one item.

An alternative explanation to the cue generation deficiency hypothesis for the differential effects of cue-load on amnesics is that they failed to encode contextual information 19, lo] thereby impairing their ability to determine from which list a particular item had been encountered. However, when the recall of items from all lists was required (Condition 2), and thus, the need to differentiate between lists eliminated, cue-load was still found to differentially impair amnesic recall. If the failure to utilize contextual information accounted for the enhanced effect of cue-load on amnesic recall in Condition 1, then such effects should have been abolished in Condition 2, which they were not.

When recall of all items related to the cue was required regardless of list (i.e. Condition 2), it was found that control subjects recalled more items with an external semantic cue than with the provision of an external phonemic cue, whereas the efficiency of different cue-types did not differ significantly for amnesic patients. At first sight, this finding seems to contradict the results found in Condition 1, where the groups x cue-type interaction failed to achieve significance. However, the test requirements of these two conditions were distinct in a number of ways.

First, Condition 2, was enforced after Condition 1. Therefore, it is possible that semantic memory traces decay at a faster rate in amnesics than in controls. This suggestion seems unlikely since the time lag for each subject between the beginning of Condition 2 was comparatively small in comparison to the time taken for the experiment overall. Second, Condition 2 required the recall of 40 more items than Condition I and was. perhaps, more

VARYING CUE-LOAD 689

sensitive to group differences in semantic encoding. This suggestion seems possible, but it would imply that the deficits in semantic encoding in the amnesic group played a relatively

minor contributory role towards their memory impairment.

Despite attempts to exclude those amnesics who suffered from other cognitive deficits, it is noticeable that Korsakoff subjects performed slightly better than CVA and head injury subjects when semantic cues were presented. It is possible that this difference (1) can be attributed to a failure to detect more subtle cognitive deficits in the screening assessment for the CVA and head injury amnesics and (2) may account for the significant groups x cue-type interaction found in the more sensitive Condition 2. Although important semantic encoding deficits may be found in some amnesics the present study was unable to detect any significant dysfunction in this process which could account for the severity of the amnesic disorder

suffered by Korsakoff, CVA and head injury subjects. Although amnesics may have been expected to make more intrusion errors than controls,

no such differences were found. However, intrusion errors may not measure prior-item interference accurately. Prior-item interference may disrupt the search process such that subjects abandon episodic memory search relying more on semantic memory mechanisms to respond to the cues presented. It is interesting to note that other studies (e.g. [ 173) have also failed to find greater intrusion errors amongst their amnesic sample when using similar experimental paradigms. Both amnesics and controls made more intrusion errors under category than rhyming cue conditions. Thus, intrusion errors may reflect the strength or depth at which items were encoded. That is, subjects may be more likely to retrieve prior-list items in response to semantic cues than phonemic cues since semantic memory traces are more permanent. This being the case, the intrusion data adds support to the contention that semantic encoding processes were relatively normal in the present amnesic sample. Furthermore, they infer that the rate of long-term memory decay was also normal in these amnesics. The relationship between intrusion errors, encoding processes and pro-active interference clearly requires further investigation, but it is argued that the non-significant group differences in instrusion errors found here do not weaken the retrieval-interference hypothesis substantially.

By assuming an active cue generation-recognition model of recollection where subjects generate multiple cues in order to locate the item to be remembered and differentiate that item from irrelevant items in storage, it may be possible to account for both the superiority of semantic processing in normals [S] and findings which have suggested impaired semantic encoding in amnesics. The semantic mode clearly provides the possibility of a greater number of effective cues than phonemic or orthographic modes. Thus, the superiority of semantic processing in normals may reflect this greater number and variability. If amnesics are deficient in their ability to generate retrieval cues then they would not benefit from the greater number of potentially effective cues available in the semantic mode. In addition, it is possible that the failure to generate contextual cues, especially when items have been encountered in more than one context and when more than one item has been encountered within a single context, may explain findings which have suggested that amnesics are impaired in their ability to encode contextual information.

The above arguments have a number of implications for future theoretical and clinical research. The present results would suggest that if amnesics were provided with multiple cues which together eliminated the effects of cue-load then they should attain normal recall. Mnemonic aids, which have proved effective in facilitating amnesic recall under certain conditions, may have their effects by providing the amnesic (a) with an external cue and (b)

690 HOWARD F. JACKWN

cues unique to the item to be recalled. In the clinical setting, the present author has found that the efficacy of mnemonic aids decreases rapidly with the number of different items for which those aids are used. Future development of such an approach to memory retraining may be advised to concentrate on the development of a system which allows unique mnemonic cues for unique items or events.

Acknowledgements-I am indebted to Dr P. D. Slade, Dr R. G. Owens and Mr E Ghadiali for their useful criticisms of earlier drafts of this paper. Many thanks are also due to the portering staff of Fazakerley Hospital and all the subjects who permitted investigation of their memory. Finally, I wish to express my gratitude to the medical, para- medical and professional National Health Service staff of the Mersey Region for the efforts in locating appropriate subjects and providing the facilities for testing.

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