Implicit and explicit learning gains in Alzheimer's

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Implicit and explicit learning gains in Alzheimer's patients: Effects of naming and information retrieval training a

b

Sharon M. Arkin , Chandelle Rose & Tammy Hopper

a c

a

Department of Speech and Hearing Sciences, University of Arizona, Tucson, AZ, USA b

Department of Physiological Science, University of Arizona, USA c

National Center for Neurogenic Communication Disorders, University of Arizona, USA Published online: 31 Aug 2010.

To cite this article: Sharon M. Arkin , Chandelle Rose & Tammy Hopper (2000) Implicit and explicit learning gains in Alzheimer's patients: Effects of naming and information retrieval training, Aphasiology, 14:7, 723-742, DOI: 10.1080/026870300410955 To link to this article: http://dx.doi.org/10.1080/026870300410955

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aphasiology, 2000, vol. 14, no. 7, 723±742

Implicit and explicit learning gains in Alzheimer’s patients : Eåects of naming and information retrieval training


SH AR O N M. AR K IN" , CHA ND E LLE R OS E# , and T AM MY H OP P E R" $ " Department of Speech and Hearing Sciences, University of Arizona, Tucson, AZ, USA # Department of Physiological Science, University of Arizona, USA $ National Center for Neurogenic Communication Disorders, University of Arizona, USA

(Received 14 December 1998; accepted 9 July 1999)

Abstract The purpose of this study was to examine the eåects of repeated exposure to words from a target category on implicit and explicit learning of seven mild to moderate Alzheimer’s patients. Following 18±20 baseline ¯uency tests on the target category, subjects participated in eight sessions of a picture naming exercise and related quiz (study task) which exposed them to 33 words from the target category (exposure words). One hour after each study task session, the ¯uency test used at baseline was administered again (experimental ¯uency test). All subjects increased correct responses on the study task, demonstrating signi®cant explicit learning. Six subjects produced exposure words on the experimental ¯uency tests that they had never named during the multiple baseline tests and all subjects unexpectedly named novel words (not exposure words and not produced at baseline) on the experimental ¯uency tests. Taken together, these results provide evidence of implicit and explicit learning and semantic activation. Implications for management and direction for future research are discussed.

Introduction Memory de®cits are the major de®ning symptom of Alzheimer’s disease (AD), and contribute to the functional decline that patients experience, including communication di¬culties (Molloy and Lubinski 1995). The disruption in semantic memory that occurs in Alzheimer’s Disease may result in naming impairments that are evident on category ¯uency or confrontation naming tests, as well as in conversation (Salmon et al. 1995). As a result of these de®cits and their impact on functioning, memory processes are logical targets of behavioural interventions with Alzheimer’s patients. Researchers attempting remediation of memory impairment in Alzheimer’s disease often distinguish between explicit and implicit memory. Schacter (1992) describes explicit memory as relying on conscious or intentional recall of speci®c past information or experiences, whereas implicit memory is mediated by unconscious retrieval of past experiences that does not require cognitive eåort or Address correspondence to : Sharon M. Arkin, Department of Speech and Hearing Sciences, University of Arizona, Tucson, AZ 85721, USA. Email : arkinaz! earthlink.net ’ 2000 Psychology Press Ltd http:}}www.tandf.co.uk}journals}pp}02687038.html

S. M. Arkin et al.


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recollection of a speci®c learning event. Tests of implicit memory provide opportunity for demonstration of skills or improved performance on a task that is attributable to information acquired during a previous study episode (Schacter 1987). According to Camp and colleagues (1995), interventions with dementia patients involving explicit memory have been mostly abandoned due to the popular belief that dementia patients generally cannot use conscious processing to store and retrieve information. Therefore, interventions relying on unconscious learning processes to perform implicit memory tasks have been more widely accepted (Camp et al. 1995). According to Rybash (1996), implicit memory can be assessed through priming tasks in which subjects make judgments about stimuli that may or may not have been presented previously. `Priming is demonstrated if exposure to items during a study phase results in enhanced performance (e.g. reduced latency of response, or increased accuracy of response) relative to control items during a test phase ’ (Rybash 1996a). In this experiment, the study phase involved repeated presentations of pictured items from a target category, followed by semantically related questions. The test phase consisted of a 60 second ¯uency test, administered one distraction-®lled hour after each study session, in which the subject was asked to spontaneously generate exemplars from the target category. Ènhanced performance ’ was de®ned as production on the test phase ¯uency tests of category items to which participants had been exposed on the study task, but had never produced during baseline testing. The intervention in the present experiment (i.e. the study task) meets Rybash’s de®nition of `retrieval-dependent ’ priming, in that the task seems to be facilitated by conceptually driven processes such as semantic elaboration. Pilot studies Arkin (1994) had a series of category ¯uency tests administered to a subject, Bee, who was at the early moderate stage of Alzheimer’s disease. Bee was tested in three categories (colours, fruits and modes of transportation), during 24 practice sessions, held in a 10 week period. The number of words produced in the three categories increased by 14%, 57% and 83 % respectively from pretest to ®nal test. The total number of diåerent exemplars that Bee produced in the three categories was double the number produced on her best single trial for the three categories and triple the number produced at baseline. For the category `things people wear ’, the subject was given a clothing and jewellery picture naming task and a related quiz similar to that in the present experiment. Ten twice-weekly training sessions in ®ve weeks resulted in a doubled number of correct quiz responses, which provides evidence for explicit learning. In the experimental ¯uency tests administered two days after each session of the naming and quiz task, a total of 45 diåerent exemplars was produced during training and the post-test. Sixteen of the 45 words were new words which had been included in the picture naming and quiz exercise, but had never been produced during three baseline tests, evidence of implicit learning. Cutcher (1996) repeated Arkin’s study with Mary, another moderate Alzheimer’s disease patient. Corrective feedback provided for each unknown or incorrectly answered question resulted in improved naming of jewellery and clothing pictures and improved performance on the corresponding quiz. As evidence of implicit

Learning gains in AD

725

learning, Mary produced seven exposure words in the experimental ¯uency tests that she had not produced on the baseline tests. Although an increase in single occasion output was not found, the study analysis did yield evidence of a larger lexical repertoire than was shown by any single ¯uency test ; the total number of exemplars produced during multiple tests exceeded the best one-time production by 346%.


Hypotheses of present study The present study is a modi®ed group replication of the Arkin (1994) and Cutcher (1996) single-subject experiments. Experimenters attempted to foster explicit learning by means of a repeated study task in which subjects were asked to identify picture cards and answer a related question for each item. The subjects participated in eight sessions of the confrontational naming and quiz study task, which exposed them to a total of 33 words from the target category, `things people wear ’. The experimental test phase consisted of eight trials of a category ¯uency test of the target category, each trial occurring approximately one hour after each single presentation of the study task. The purpose of the category ¯uency tests was to determine if exposure to the study task served as `priming ’ and resulted in subsequent ¯uency test production of words encountered in the study task, but never produced on baseline testing. Research hypotheses were that : (1) the number of correct responses to the study task would increase with practice ; (2) on the experimental category ¯uency tests, subjects would name words that were presented during the study task (i.e. exposure words) but never named during baseline testing ; (3) the percentage of exposure words named during baseline testing (i.e. baseline exposure words) and produced at least once during the experimental ¯uency tests would be greater than the percentage of baseline words not presented during the study task (i.e. baseline non-exposure words); and (4) the average number of words produced during the eight experimental category ¯uency tests would exceed the average number produced in the series of baseline tests. Method1 Participants Research subjects Subjects were seven very mild to moderate stage Alzheimer’s patients who were participants in an NIA-funded longitudinal rehabilitation study.# Baseline MiniMental State Examination (MMSE ; Folstein et al. 1975) scores ranged from 15±29, with a mean of 23, SD ¯ 4.75. Verbal ¯uency for the category ànimals ’ and confrontational naming scores ranged from normal to moderately impaired. Selected test scores and demographic data are displayed in table 1. Subjects were tested, diagnosed, and staged according to criteria used by the Consortium to Establish a Registry for Alzheimer’s Disease (CERAD) (Morris et al. 1989). Testers were clinicians trained and certi®ed by CERAD staå. CERAD eligibility criteria corresponded to NINCDS-ADRDA (National Institute of Neurological and Communicative Disorders and Stroke-Alzheimer’s Disease and Related Disorders Association) work group criteria, described by McKhann et al. (1984). CERAD criteria also require patients to be at least 50 years old, community

M

F

F

F

F

F

F

Alfred

Blanche

Doris

Dorothy

Helen

Ida

Winifred

80

84

83

80

84

87

79

Age

16

19

11

21

27

28

22

MMSE

1

2

2

1

0.5

1

1

CDR StageŒ

12 (mild) 5 (moderate) 2 (moderate to severe) 5 (moderate)

12 (mild) 14 (normal) 13 (very mild) 15}15 (no dementia) 11}15 (mild to moderate) 14}15 (no dementia) 11}15 (mild to moderate)

15}15 (no dementia) 15}15 (no dementia) 15}15 (no dementia)

12

14

18

12

12

12

15

Education (in years)

Mobile home park operator School bus driver for children with disabilities Sales person

Musician}drummer

Lifetime occupation

Assisted living Nurse facility Home w}day-time Homemaker caregiver Home w}relatives Cook’s helper

Home alone

Group home

Home alone

Group home

Residence

‹ MMSE scores were from January 1998 for 5 subjects. Winifred’s score was from June 1998 and Helen’s score from March 1998. CERAD and CDR scores were from baseline tests in June 1997. Study took place in February, March and April 1998. Œ Stage 0.5 ¯ questionable dementia Stage 1 ¯ mild dementia Stage 2 ¯ moderate dementia Stage 3 ¯ severe dementia

Sex

Subjects

Boston naming test (CERAD version) (confrontational naming)

Subject characteristics‹

Verbal ¯uency of animals (CERAD)

Table 1.


726 S. M. Arkin et al.


727

dwelling (not in a nursing home), English speaking and not on an experimental or approved Alzheimer drug at intake. They must have an involved caregiver or informant and have no depression or psychiatric disorders that impair cognitive function.


Student partners Each subject in the rehabilitation study is matched with a series of undergraduate university students. Each student serves as a rehabilitation partner for one semester. This experiment took place during the subjects’ second semester. The second semester student partners administered both the study task and the experimental category ¯uency tests. Baseline data were gathered by subjects’ ®rst semester student partners. Student participants earned academic credit for their participation. Interest in the study was generated through an article in the university newspaper and through recruiting visits to undergraduate classes. Students were matched with subjects based on common interests, geographic location and personality. Setting Study task sessions were conducted in conjunction with student-supervised physical ®tness workouts at the University of Arizona Medical Center’s cardio-rehab }employee wellness center and with volunteer service or recreational activities at various community locations. Sessions occurred at various times during the day and early evening, according to the students’ availability. Varying degrees of distraction were present, including music and other people at the wellness center or volunteer site. Procedures Baseline testing During the previous semester, the subjects had been given 18±20 60 second category ¯uency tests in which they were asked to name as many items as they could think of in the category `things that people wear, such as clothing and jewellery ’. Baseline testing was conducted before and after ten weekly exercise sessions at the wellness center. The purpose of the multiple baseline tests was to obtain an exhaustive list of each subject’s repertoire of exemplars in that category. This repertoire was used as baseline data (baseline list) for the present study. The combined baseline list for the seven subjects is included in appendix A. Baseline exposure words are de®ned as those words from an individual’s baseline list that were selected to be practised as study task items. Baseline nonexposure words are de®ned as words that were produced during an individual’s baseline testing, but were not included in the study task. Novel words are de®ned as words that were not on an individual’s baseline list, nor on the study task, but were produced during the experimental test phase. Experimental intervention The experimental intervention (study task) consisted of a 50 item exercise : 25 coloured pictures of `things people wear ’, plus 25 related short answer questions. Eight of the related questions had a word from the target category as the correct

S. M. Arkin et al.


728

answer. Thus, subjects were exposed to a total of 33 items from the target category during the study task. These words are referred to as èxposure words ’. Pictures selected for use were of items named least frequently or not named at all during the baseline ¯uency tests. All subjects encountered some of their baseline words on the study task. The number of items included in each subject’s study task varied, ranging from 3 to 16 (see table 3). Most of the pictures were taken from the `communications skill builders ’ boxed set of photo cue cards (Kerr 1988); others were from magazines and catalogues. A copy of the study task protocol is presented as appendix B, and an alphabetical list of the 33 exposure words is contained in appendix A. During administration of the study task, the student pointed to each picture and asked the subject to name it. (Sometimes, the student just pointed and the subject responded.) The student recorded the response and repeated the correct answer. Then a question was asked that related to that item. For example, the subjects were asked to identify a picture of a belt. Then they were asked, `What do you call the elastic straps that can also hold up pants ? ’ (correct response : suspenders). Again, the response was recorded and the student repeated the correct answer. Subjects could obtain bonus points by providing multiple answers to two questions. For example, after the picture of a dress was shown, the subjects were asked, `What are some kinds of material that are shiny like that dress appears to be? ’ Any correct response in addition to the ®rst was awarded a bonus point. The study task was the ®rst activity of the rehab session during which it was administered. It was followed by either a physical ®tness workout or an hour of volunteer work, after which the experimental category ¯uency test was administered. The training sessions occurred twice a week, once at the wellness center and once at the volunteer activity site, until eight sessions were completed. Training lasted from four to eight weeks because of variations in students’ schedules. An increase in the number of correct responses produced on the study task from trial 1 to trial 8 was de®ned as explicit learning, as answering the questions required conscious, intentional recall of studied material. Experimental ¯uency tests The experimental category ¯uency tests were the same 60 second tests that had been administered to subjects during baseline testing the previous semester. Each test was administered approximately one hour after each of the eight study task sessions, at the end of the rehab session. Performance on these tests was considered a measure of implicit learning. Roediger and McDermott (1993) diåerentiate between explicit and implicit memory tests according to the instructions that subjects are given during the test : On priming tests of implicit memory, subjects are not directed to recollect past events. Rather, they are asked to complete some task as well as possible; retention is inferred from how well the task has been aåected by recent experience (Roediger and McDermott 1993 : 64).

In the experimental ¯uency tests, subjects were not asked to name words they had been exposed to during the study task, but rather any words they could think of from the category `things people wear, such as clothing and jewellery ’. Evidence of implicit learning was de®ned as : (1) production, during any of the eight experimental ¯uency tests, of exposure words that had never been produced


729

Table 2. Total correct responses achieved during study task trials Subjects (MMSE) Alfred (22) Blanche (28) Doris (27) Dorothy (21) Helen (11) Ida (19) Winifred (16)

Trial 1

Trial 2

Trial 3

Trial 4

Trial 5

Trial 6

Trial 7

Trial 8

46.5 43.5 49 44 21.5 39 22

46.5 42 51.5 48.5 27.5 35.5 21

49.5 50.5 50 48.5 31.5 40.5 20.5

48 50.5 51 50.5 35 38 21.5

49 51.5 53 46.5 31 41 27.5*

49 54* 53.5 47.5 39* 44.5 22

51* 52.5 55 51.5 36 49* 20.5

49 54* 56* 52.5* 35.5 44 26


* Indicates each subject’s best trial.

on baseline tests ; and (2) production of a higher percentage of baseline than of nonbaseline exposure words during the experimental ¯uency tests. Scoring All study task protocols were scored by the second author. One point was given for each correct answer. Half credit was given for some responses if a portion of the answer, but not the whole answer, was stated. For example, if boots was stated instead of cowboy boots (an exposure item), half-a-point was awarded. For each correct bonus answer given, a point was awarded. Appendix B contains the study task items. The odd-numbered questions represent picture naming questions and were tallied separately. Even-numbered questions represent questions relating to the picture and were tallied separately. The number of odd, even, bonus and total points was recorded on a tally sheet. The ®rst, best, and eighth score are presented for each subject in table 3. Results Three of the four research hypotheses were supported. The ®rst hypothesis, that the number of correct responses to the study task would increase, was supported. Every subject increased the number of correct responses to the picture naming and quiz study task from the ®rst trial to the last one (see table 2). The improvement of the group as a whole, as measured by a paired t-test of the diåerence in mean scores between trial 1 and trial 8, was signi®cant : [t (6) ¯ 4.870, * p ! 0.002]. The scores ¯uctuated among trials for all subjects, with the best performance achieved between trials 5 and 8. Every subject improved on the confrontational naming and related quiz items, and all but one improved on the number of bonus items named (see table 3). There was a signi®cant positive correlation between MMSE scores and performance on the confrontational naming and related quiz task : [r ¯ 0.7678, * p ! 0.05]. The second hypothesis, that exposure words never named at baseline would be produced on the 60 second experimental ¯uency tests, also was supported. After eight sessions of the study task, six of the seven subjects produced exposure items never named before during the 18±20 baseline tests (see table 4). The third hypothesis, that the percentage of baseline exposure words named at least once during the 60 second experimental ¯uency tests would be greater than

46.5 43.5 49 44 21.5 39 22

Trial 1

49 54 56 52.5 35.5 44 26

Trial 8

51 54 56 52.5 39 49 27.5

Best trial

22.5 23 23 22 14.5 20.5 15

Trial 1 23 23.5 25 23.5 20 24 16

Trial 8 24 24 25 24.5 21.5 24 17.5

Best trial

Confrontational naming items correct

22 19.5 23 21 7 17.5 7

Trial 1 23 23.5 25 24 14.5 19 10

Trial 8

Related quiz items correct

Items answered correctly from the study task‹

24 24 25 25 16.5 22 10

Best trial

2 1 3 1 0 1 0

Trial 1

3 7 7 5 1 1 0

Trial 8

Bonus items named

4 8 7 5 2 4 0

Best trial

‹ For each subject, the number of study task items that were on his or her baseline list (i.e. baseline exposure words) is presented in parentheses after the subject’s name.

Alfred (7.5) Blanche (10) Doris (12) Dorothy (16) Helen (6.5) Ida (3) Winifred (6)

Subjects

Total items correct

Table 3.


730 S. M. Arkin et al.

Alfred (22) Blanche (28) Doris (27) Dorothy (21) Helen (11) Ida (19) Winifred (16)

Subjects (MMSE)

Alfred (22) Blanche (28) Doris (27) Dorothy (21) Helen (11) Ida (19) Winifred (16)

Subjects (MMSE)

Table 5.

35 53 39 74 25 21 36

38 57 40 51 19 30 11

Number of diåerent exemplars produced following study task (8 trials) 20 39 23 31 10 18 9

Exemplars produced at baseline also produced during experimental ¯uency tests (exposure and non-exposure words) 8 4 4 6 2 5 0

Exemplars demonstrating priming eåect (never produced at baseline, but produced following exposure during study task) 10 14 13 14 7 7 2

Exemplars demonstrating semantic activation (novel [non-baseline, non-exposure] words) produced on experimental ¯uency tests 63 83 58 59 80 100 43

Percent of baseline exposure words produced at least once on experimental ¯uency tests

Number of `things we wear ’ items produced on 60 second category ¯uency tests

12.1 18.9 12.4 16.4 4.7 12.9 4.0

Average number of words produced in study phase tests 0 4 2 2 1 2 3

Diåerence between 1st and best trial (study phase tests)

12.5 18.1 12.4 21.4 5.8 12.9 7.4

Average number of words produced in baseline tests

13 12 2 4 2 5 5

Diåerence between 1st and best trial (baseline tests)

Total number of words produced during experimental ¯uency tests and baseline category ¯uency tests

Number of diåerent exemplars produced at baseline (18±20 trials)

Table 4.


56 71 63 38 35 78 28

Percent of baseline nonexposure words produced at least once on experimental ¯uency tests

Learning gains in AD 731

S. M. Arkin et al.


732

the percentage of baseline non-exposure words named, was supported. Six of the seven subjects produced a larger percentage of baseline exposure words than of baseline non-exposure words (see table 4). The percentage diåerence between exposure and non-exposure items produced by the six subjects ranged from 7 %±45%. The mean group percentage score diåerence between the two categories, as measured by a paired t-test, was signi®cant : [t (6) ¯ ® 2.857, * p ! 0.03]. No signi®cant correlation was found between the number of baseline words a subject encountered on the study task (i.e. baseline exposure words) and the number of these baseline exposure words produced on the experimental ¯uency tests. The fourth hypothesis, that the average number of words produced during the eight experimental ¯uency tests would exceed the average number produced in the baseline series, was not supported. Only one subject produced more words on average during the experimental tests than during baseline. Two subjects produced the same average number of words, and four subjects produced more words during baseline tests than during the experimental tests. Dorothy had the largest margin, producing an average of ®ve more words during baseline than she did during experimental tests (see table 5). Although the average number of words produced per trial remained the same, four subjects produced more diåerent exemplars in the eight experimental ¯uency trials than they did in 18±20 baseline trials. There also was a very positive and unanticipated ®nding. All subjects named words on the experimental ¯uency tests that were not exposure words and that had never been produced during baseline testing. These are referred to as `novel ’ items. The number of novel items produced ranged from 2 to 14 (see table 4). Appendix A contains the combined list of novel words produced by the seven subjects. (Words listed as novel were novel to the subject that produced them. They appear on the baseline list if they were produced by one or more of the other subjects during baseline testing.) There was a positive correlation between MMSE scores and number of novel words produced on the experimental ¯uency tests that approached signi®cance: [r ¯ 0.7485, p ¯ 0.0529]. Discussion Both explicit and implicit learning gains were demonstrated by seven Alzheimer’s patients during a confrontational naming and related quiz study task and subsequent category ¯uency tests. Exposure to the study task seems to have helped subjects access previously inaccessible contents of their lexical repertoire, but did not aåect speed of processing, i.e. the average number of words produced in speeded trials remained constant (see table 5). Although the second set of opportunities was much smaller (8 trials instead of 18±20 at baseline), four of the seven subjects produced a larger number of diåerent exemplars during the experimental ¯uency tests than they did during baseline testing (see table 4). Explicit learning All subjects demonstrated explicit learning by increasing the number of correct responses to confrontational naming and related quiz questions. This increase is explicit learning, according to Schacter’s (1987) de®nition, because the task



733

required a conscious and eåortful search in semantic memory for correct responses to speci®c questions about information that had recently been presented. Repeated presentation of the study task, which made consistent semantic information retrieval demands and provided immediate feedback in the form of the correct answer when an item was not answered correctly, was eåective in promoting signi®cant improvement by the study participants. This improvement is notable for subjects with Alzheimer’s disease who have particular di¬culty with consolidation of new information and retrieval of speci®c information from semantic memory (Salmon et al. 1995). Though there was some ¯uctuation in performance from session to session, the general trend was upward and a positive learning curve resulted. The positive correlation found between MMSE scores and amount of learning achieved re¯ects the increasing di¬culty AD patients have with new learning as their dementia progresses. A ceiling eåect may have prevented the demonstration of even greater learning gains among the higher functioning subjects. Five subjects correctly identi®ed more than 20}25 of the confrontational naming pictures on the ®rst trial; four correctly answered more than 20}25 of the related quiz items on the ®rst trial. Aside from the two bonus items, these subjects did not have much opportunity to improve. Thus, Blanche, the subject with the highest mental status score, (MMSE ¯ 29) only showed a 24% gain from her ®rst to her best trial. Conversely, the subject with the lowest mental status test score showed the largest gain. Helen (MMSE ¯ 9) improved by 17.5 items from her ®rst trial to her best trial, an 81 % increase. The results indicate that the types of explicit learning exercises used in this study are appropriate for both lower functioning and higher functioning patients. However, explicit interventions of a more challenging level may be needed for higher functioning patients. Implicit learning gains On the series of eight experimental ¯uency tests, implicit learning gains were demonstrated in two ways : (1) by production, by all subjects, of words to which they had been exposed on the study task, but had never produced on baseline tests ; and (2) by production of a signi®cantly higher percentage of baseline exposure words than of baseline non-exposure words. (Variability in the number and type of exemplars produced during multiple ¯uency tests had been expected. Therefore, the researchers administered the baseline test between 18 and 20 times, to allow approximation of each subject’s total lexical repertoire.) Evidence for priming in individuals with Alzheimer’s disease is mixed. Salmon et al. (1988) report that Alzheimer’s patients do not bene®t from verbal priming on semantic memory tasks, such as word associations, or perceptual priming tasks, such as stem completions. Other researchers (Nebes et al. 1986, Nebes et al. 1984) report that individuals with mild to moderate AD show positive semantic priming eåects. Results from the present study seem to be in accord with the positive priming studies. Exposure to target words in the naming and quiz study task in the present study was su¬cient to generate `transient memory traces ’ (Salmon et al. 1995 : 43) that resulted in priming of the study task words and the subsequent production of these words on the experimental category ¯uency tests. The more frequent re-production on the experimental ¯uency tests of baseline words that were on the study task than of baseline words that were not on the study task

S. M. Arkin et al.

734

provides additional evidence of a priming eåect. As the words were produced spontaneously, without a conscious search for speci®c words that were responses to practised study task items, the demonstrated learning may be attributed to implicit memory processes. In contrast to performance on the explicit learning task, the amount of demonstrated implicit learning was not signi®cantly correlated with mental status. In this study, the three subjects with moderate AD may have been advantaged by the previous semantic context of the study task in much the same way as the four mild AD patients.


`Semantic activation ’ An unanticipated result of this experiment was the production by all subjects of more novel (non-baseline, non-exposure) words on the experimental ¯uency tests than of non-baseline exposure words that could be attributed to implicit learning. Repeated exposure to the target concept `things people wear, such as clothing and jewellery,’ ®rst during the 18±20 baseline category ¯uency tests, then during the 8 sessions of the study task, may have activated once known, but dormant or inaccessible items in the subjects’ lexical repertoire and facilitated their retrieval as `novel’ items on the experimental ¯uency tests. The theory of spreading activation could account for the production of novel exemplars that occurred in this study. According to the spreading activation theory described by Collins and Loftus (1975), semantic memory consists of lexical concept nodes organized in a systematic interconnected network based on associations and similarities of meaning. When a concept is accessed, (as occurred in this study each time a picture was named or a question was answered correctly), other items that are closely related to that item are activated, facilitating their later retrieval. The duration of the facilitated retrieval eåect in the present study (i.e. 60 minutes) is not in accordance with this early theory of semantic activation. Traditionally, semantic priming assumed rapid decay of activated memory traces (i.e. after several seconds), and eåects that disappear after more than one item is interposed between the prime and target stimuli (Becker et al. 1997). In their more recent theory of semantic priming, Becker et al. (1997 : 1061) propose that long-term semantic priming involves ìncremental learning in semantic networks ’ as opposed to short-term lexical tasks. The repeated presentation of both the study task and the ¯uency tests in the present experiment would qualify as providing incremental learning. The category exemplar generation example of conceptual priming cited by Becker’s group (presentation of the word `dog ’, followed by the categorical cue ànimal’, leading to the production of the word `dog ’), relates to the present experiment’s study task and implicit learning outcome (the naming of words encountered in the study task, but never previously named), but does not account for the production of novel words. Other researchers also have provided evidence of semantic activation in clinical tasks with individuals with AD. Bourgeois (1992) noted that subjects who were trained to use memory wallets often produced novel untrained statements during practice sessions with conversation partners. Indeed, the subjects of the present study often are reported by their student rehab partners to initiate relevant elaborations of factual statements and responses to related quiz questions that appear on an interactive tape-recorded biographical


735

memory exercise that they are administered every week. (For a description of the biographical memory training system and outcome research about it, see Arkin 1992, 1997, 1998, in press).


Sample’s ¯uency pro®le Category ¯uency is a frequently measured index of semantic integrity among cognitively impaired persons (Lezak 1995) and scores on this task are a highly sensitive measure of the de®ciencies in semantic memory associated with Alzheimer’s disease (Butters et al. 1987). Huå et al. (1986) suggest that category ¯uency tests are superior to object or picture naming in discerning impairment in early stage demented subjects because, lacking visual stimuli, they require more eåortful retrieval. Few norms exist for persons as old as those in the present study sample (mean age at time of study was 80, SD ¯ 7.33, range : 60±87). As the research literature is mixed on the issue of selective impairment for categories of living versus nonliving things (Gonnerman et al. 1997), it seemed important to report the present study sample’s performance on the animal category subtest of the CERAD battery (Morris et al. 1989), as compared to their performance on the study’s target category of non-living things. The present group’s mean score at baseline and one year later on the animals category test was exactly the same : 9, only slightly lower than the 11.4 mean score of the mentally intact òld old ’ group of Rosen (1980) (mean age : 83.6). One subject went up from 2 to 7 ; one went down from 13 to 9 ; the rest ¯uctuated by one or two points. The mean score on the animals test was signi®cantly lower than the group’s mean score on all of the `things people wear ’ ¯uency tests : [t (6) ¯ 2.445, * p ! 0.03]. Three subjects named 4±6 more `wear ’ items than they did animal exemplars ; the others ¯uctuated a point or two in either direction. It is reasonable to attribute the better performance on the `things people wear ’ category to the fact that many of the items in the category were present in their immediate surroundings, either on their person or on the person of the examiner. Practice must be discounted as an explanation, though, as subjects did not produce more exemplars during the experimental ¯uency tests than they did during baseline testing. Spreen and Strauss (1991) list 15.09 as the mean number of animal exemplars produced by 55 normal elderly persons aged 75 and older. CERAD’s mean score for normals is 18, but the average age of the sample is relatively younger at 68.1 years of age (Morris undated). More signi®cant than the number of items produced on average by study participants is the quality and diversity of items they produced as a group, and the originality demonstrated by such wearable contributions as : name tag, false teeth, hearing aid, diapers, shoulder braces and smile ! Summary and clinical implications Frequently, individuals with AD are assumed to be unable to learn. As a result, prognosis for improvement on therapy tasks is considered poor, and clinicians may be hesitant to implement cognitive stimulation programs. The results of the present study provide evidence that mild and moderate AD patients can learn and bene®t from language and memory interventions that engage both explicit and

S. M. Arkin et al.


736

implicit memory processes. The act of processing and retrieving visual and verbal information that is presented repeatedly in a consistent format and with immediate feedback not only results in enhanced performance regarding the material actually presented, but stimulates the production of semantically related output. All subjects produced a greater number of novel exemplars (i.e. items never produced during baseline trials and not presented as exposure words in the study task), than items demonstrating a priming eåect or implicit learning. The study task was a stimulating activity for the research subjects and could be used, as is, or adapted, using diåerent subject matter, as a clinical intervention. The role of the speech language pathologist would be to thoroughly evaluate the patient, design the study task, ®nd and train students or caregivers to administer the intervention, and conduct periodic patient re-evaluations. The stimulus materials needed for this type of activity, pictures (e.g. Kerr 1988, 1994) and related questions, are easily obtained or created for other categories and topics. Future research A replication of this study by the ®rst author is underway to see whether results diåer when the study task and category ¯uency tests involve living things, rather than inanimate objects, as in the present study. Prior research has suggested that some individuals with brain damage have particular di¬culty with biological classes of objects (Bub et al. 1993, Silveri et al. 1991, Warrington and Shallice 1984). Although the results of the present study are promising, data on the e¬cacy of memory and language interventions for individuals with AD need to be collected using controlled research designs. In order to determine whether the learning eåects obtained can be directly attributed to the study task, a subsequent study is planned that will have a control group that receives repeated category ¯uency tests but has no exposure to the experimental intervention. This study was a sub-experiment within the context of a longitudinal treatment research program that provided and is continuing to provide a combination of vigorous interventions. The combination of interventions has resulted in positive ®rst year outcomes for the subjects described in this study : signi®cant improvement in memory for and retention of biographical information (Arkin in press); signi®cant improvement in physical ®tness (Arkin 1999b); and maintenance of function on nine cognitive and language measures, including several functional discourse measures (Arkin 1999a). The present study was conducted during the second program year, for which outcome data are not yet available. Future research is planned that will dissociate the three student-supervised program components ± a battery of memory and language stimulation activities, physical exercise, and volunteer work plus unstructured conversation ± and test their relative eåectiveness at multiple sites. University researchers interested in testing any one of the three interventions are invited to contact the ®rst author. Acknowledgments Research was supported by a 5 year National Institute on Aging KO1 Mentored Research Scientist Development Award (S. Arkin) and by National Multipurpose Research and Training Center Grant DC±01409 from the National Institute on Deafness and Other Communication Disorders (T. Hopper).


737

Statistical analyses were done by Patricia Camp of the Rand Corporation. The contribution of the seven University of Arizona undergraduates who administered the 18±20 baseline tests to the study subjects : Andrea Arlotti, Elizabeth Chilcote, Maya Bar-Ness, Carolyn Bland, Decemna Chow, Heather Lang, Melissa Palmer, and the students who administered the study task and study tests : Jean Nez, Welby Nielsen, Jennifer Phillips, Corinna Simala, Christine Stum, Cara Turner and Sena Wilson, is gratefully acknowledged.


Notes " Because the experiment was conducted during an ongoing rehabilitation program, it is sometimes necessary to use the present tense to describe events. # Rehabilitation activities consist of twice weekly physical ®tness training sessions, supervised volunteer work, and memory and language stimulation exercises.

References Arkin, S., 1992, Audio-assisted memory training with early Alzheimer’s patients : Two single subject experiments. Clinical Gerontologist, 12, 77±95. Arkin, S., 1994, Naming and category ¯uency training with an Alzheimer patient: Direct practice and implicit learning tasks yield gains. Poster presented at the Third International Practical Aspects of Memory Conference. University of Maryland, College Park, August, 1994. Arkin, S., 1996, Volunteers in partnership : An Alzheimer’s rehabilitation program delivered by students. American Journal of Alzheimer’s Disease, 11, 12±23. Arkin, S., 1997, Alzheimer memory training : Quiz beats repetition, especially for more impaired. American Journal of Alzheimer’s Disease, 12, 147±158. Arkin, S., 1998, Alzheimer memory training : Positive successes replicated. American Journal of Alzheimer’s Disease, 13, 102±104. Arkin, S., 1999a, Elder Rehab : A student-supervised exercise program for Alzheimer’s patients. The Gerontologis t, 39, 729±735. Arkin, S., 1999b, Alzheimer rehab program maintains cognitive and language function, improves ®tness: First year results. Paper presented at International Neuropsychological Society conference, June 22±26, Durban, South Africa. Arkin, S., in press, Alzheimer memory training : Students replicate learning successes. American Journal of Alzheimer’s Disease, 15. Becker, S., Moscovitch, M., Behrmann, M. and Joordens, S., 1997, Long-term semantic priming : A computational account and empirical evidence. Journal of Experimental Psychology : Learning, Memory, and Cognition, 23, 1059±1082. Bourgeois, M. S., 1992, Evaluating memory wallets in conversations with persons with dementia. Journal of Speech and Hearing Research, 35, 1344±1357. Bub, D., Arguin, M. and Chertkow, H., 1993, Towards an interpretation of category-speci®c agnosia for biological kinds. Paper presented at the 31st Annual Meeting of the Academy of Aphasia, October 24±26, Tucson, Arixona. Butters, N., Granholm, E., Salmon, D. P., Grant, I. and Wolfe, J., 1987, Episodic and semantic memory: A comparison of amnesic and demented patients. Journal of Clinical and Experimental Neuropsychology, 9, 479±497. Camp, C. J., Foss, J. W., O’Hanlon, A. M. and Stevens, A. B., 1995, Memory interventions for persons with dementia. Applied Cognitive Psychology, 9, 347, 1±18. Collins, A. M. and Loftus, E. F., 1975, A spreading-activation theory of semantic processing. Psychological Review, 82, 407±428. Cutcher, K., 1996, Replication of Alzheimer ¯uency and naming experimental yields more explicit than implicit learning gains. Undergraduate honors thesis and colloquium, University of Arizona Department of Speech and Hearing Sciences, Spring, 1996.


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Folstein, M., Folstein, S. and McHugh, P., 1975, Mini-mental state examination. Journal of Psychiatry Research, 12, 189±198. Gonnerman, L. M., Andersen, E. S., Devlin, J. T., Kempler, D. and Seidenberg, M. S., 1997, Double dissociation of semantic categories in Alzheimer’s disease. Brain and Language, 57, 254±279. Huff, F. J., Corkin, S. and Growdon, J. H., 1986, Semantic impairment and anomia in Alzheimer’s disease. Brain and Language, 28, 235±249. Kerr, J. Y. K., 1988, Photo Cue Cards (San Antonio, TX : Communication Skill Builders, a division of the Psychological Corporation). Kerr, J. Y. K., 1994. More Photo Cue Cards (San Antonio, TX : Communication Skill Builders, a division of the Psychological Corporation). Lezak, M. D., 1995, Neuropsychologica l Assessment (3rd edition) (New York : Oxford University Press). McKhann, G., Drachman, D., Folstein, M., Katzman, R., Price, D. and Stadlan, E. M., 1984, Clinical diagnosis of Alzheimer’s disease: report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer’s Disease. Neurology, 34, 939±944. Molloy, D. W. and Lubinski, R., 1995, Dementia : impact and clinical perspectives. In R. Lubinski (Ed.) Dementia and Communication (San Diego : Singular Publishing). Morris, J. C. (Undated), Memory Diagnostic Centre Psychometric Score Results. Cover sheet for CERAD test battery packet. Washington University. St. Louis. Morris, J. C., Edland, S., Clark, C., Galasko, D., Koss, E., Mohs, R., van Belle, G., Fillenbaum, G. and Heyman, A., 1993. The consortium to establish a registry for Alzheimer’s disease (CERAD). Part IV. Rates of cognitive change in the longitudinal assessment of probable Alzheimer’s disease. Neurology, 43, 2457±2465. Morris, J. C., Heyman, A., Mohs, R. C., Hughes, M. S., van Belle, G., Fillenbaum, G., Mellits, E. D., Clark, C. and the CERAD investigators. 1989, The consortium to establish a registry for Alzheimer’s disease (CERAD). Part I. Clinical and neuropsychological assessment of Alzheimer’s disease. Neurology, 39, 1159±1165. Nebes, R. D., Boller, F. and Holland, A., 1986, Use of semantic context by patients with Alzheimer’s disease. Psychology and Aging, 1, 261±269. Nebes, R. D., Martin, D. C. and Horn, L. C., 1984, Sparing of semantic memory in Alzheimer’s disease. Journal of Abnormal Psychology, 93, 321±330. Roediger III, H. L. and McDermott, K. B., 1993, Implicit memory in normal human subjects. In H. Spinnler and F. Boller (Eds) Handbook of Neuropsychology (Vol. 8 (Amsterdam : Elsevier), pp. 63±131. Rosen, W. G., 1980, Verbal ¯uency in aging and dementia. Journal of Clinical Neuropsychology, 2, 135±146. Rybash, J. M., 1996, Implicit memory and aging : a cognitive neuropsychological perspective. Developmental Neuropsychology, 12, 127±179. Salmon, D. P., Heindel, W. C. and Butters, N., 1995, Patterns of cognitive impairment in Alzheimer’s disease. In R. Lubinski (Ed.) Dementia and Communication (San Diego : Singular Publishing). Salmon, D. P., Shimamura, A. P., Butters, N. and Smith, S., 1988, Lexical and semantic priming de®cits in patients with Alzheimer’s disease. Journal of Clinical and Experimental Neuropsycholog y, 10, 477±494. Schacter, D. L., 1987, Implicit memory : history and current status. Journal of Experimental Psychology : Learning, Memory, and Cognition, 13, 501±517. Schacter, D. L., 1992, Understanding implicit memory. American Psychologis t, 47, 559±569. Silveri, M-C., Daniele, A., Giustolisi, L. and Gainotti, G., 1991, Dissociation between knowledge of living and nonliving things in dementia of the Alzheimer type. Neurology, 41, 545±546. Spreen, O. and Strauss, E., 1991, A Compendium of Neuropsychologica l Tests (New York : Oxford University Press). Warrington, E. K. and Shallice, T., 1984, Category speci®c semantic impairment. Brain, 107, 829±853.


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Appendix A List of baseline words produced by subjects, exposure words from study task and novel words produced on experimental ¯uency tests.


Baseline words Anklet Bandages Bandanna Barrettes Bathing suit Beads Belts Blouses Bobby pins Boots Bikini Bottoms Bow tie Boxers Bracelets Bras Cap Chains Chemise Class ring Coat Combs Corset Crosses Crowns Diamonds Dress Dungarees Earrings Engagement ring False teeth Flowers in hair Formal wear Fur coat Galoshes Garters Girdles Glasses Gloves Gown Hair combs Hair pins Hair ribbons

Half slips Handkerchiefs Hats Headbands Hearing aids Heart charms Hi-tops Hosiery House dress House slippers Jackets Jersey top Jumpers Knee-highs Knee socks Knitted caps Lingerie Locket Long pants Long underwear Make up Mittens Moccasins Name tag Necklace Night gown Outerwear Overcoats Oxfords Panties Pants Pantyhose Pearls Petticoats Pins Pjs Pumps Rain hat Raincoat Ring Robes Rubbers

Sailor hat Sandals Scarves Shifts Shirt Shoes Shoulder braces Shower hats Skates Skirts Slacks Slippers Slips Sloppy caps Smile Sneakers Socks Stick pins Stocking caps Stockings Suits Supporters Sweater Sweatshirt Swim suits T-shirt Tams Tennis shoes Tie Tops Trousers Turbans Under blouse Under things Underclothes Underpants Underwear V-neck Vest Watch Wedding ring Wristband

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740 Exposure words


Bathing suit Bathrobe Belt Bib Bicycle helmet Bifocals Bikini Blue jeans Buckle Coat Cowboy boots

Dress Fur coat Galoshes Garters Glasses Gloves Hat Hosiery Leather jacket Long underwear Mittens

Nightgown Pajamas Panty girdles Pearls Raincoat Sandals Suspenders Sweatshirt Umbrella Veil Vest

Housecoat Jewellery Long pants Mu°er Overcoat Overshoes Panties Pants Petticoat Pins Pocket watch Pumps Purse Rain hat Rain shoes Rubbers Shirts

Shorts Skirts Slacks Stocking cap Straw hat Suits Sweat out®t Sweater Tams Ties Tops Trousers Underpants Undershirt Underwear Wedding ring

Novel words Anklets Arctics Bead necklace Beads Blouses Bonnet Bottoms Bows Bracelet Brooches Cardigans Cotton socks Diamond rings Diapers Earmuås Hair clips Handkerchief

Appendix B : Things we wear picture naming exercise 1. 2. 3. 4. * * 5. 6. 7. 8. * *

jjjjjjjj (bicycle helmet). What is this used for ? jjjjjjjj (to protect the head from accident or injury). jjjjjjjj (sweatshirt). In what sport did the Arizona wildcats win the national championship in 1997 ? jjjjjjjj (basketball). jjjjjjjj (bicycle helmet). What is this used for ? jjjjjjjj (to protect the head from accident or injury). jjjjjjjj (jeans, blue jeans, dungarees, Levi’s). What kind of material are jeans made of? jjjjjjjj (denim). jjjjjjjj (panty girdle). What are the things that hold the stockings up? jjjjjjjj (garters). jjjjjjjj (bicycle helmet). What is this used for ? jjjjjjjj (to protect the head from accident or injury).

Learning gains in AD 9. 10. 11. 12


13. 14. * * 15. 16. 17. 18. 19. 20. 21. 22. * * 23. 24. 25. 26. 27. 28. 29. 30. 31. 32. * * 33. 34. 35. 36. 37. 38. 39. 40. 41.

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jjjjjjjj (gloves). What are they made out of? jjjjjjjj (leather). jjjjjjjj (leather jacket). What do you call the knitted part at the end of the sleeves that keeps the wind out? jjjjjjjj (cuås). jjjjjjjj (jacket, sport jacket, sport coat, men’s suit jacket or coat). What do you call the part of the collar that is folded back above the buttons ? jjjjjjjj (lapels). jjjjjjjj (bicycle helmet). What is this used for ? jjjjjjjj (to protect the head from accident or injury). jjjjjjjj (pajamas). What might a woman wear to bed instead of pajamas ? jjjjjjjj (nightgown). jjjjjjjj (long underwear, longjohns). What is the part that covers the arms ? jjjjjjjj (sleeves). jjjjjjjj (nylon stockings, hose, hosiery). What do you call a damaged place on a stocking ? jjjjjjjj (run, snag, ladder). jjjjjjjj (dress). What are some kinds of material that are shiny like that dress appears to be? jjjjjjjj (silk, satin, rayon, polyester). jjjjjjjj (bicycle helmet). What is this used for ? jjjjjjjj (to protect the head from accident or injury). jjjjjjjj (fur coat). Name some kinds of animals used to make fur coats. jjjjjjjj (mink, fox, raccoon, Persian lamb, chinchilla, seal, beaver, rabbit, leopard). jjjjjjjj (bathing suit). What do you call a skimpy two piece bathing suit ? jjjjjjjj (bikini). jjjjjjjj (bathrobe). What do you call the towel material that many bathrobes are made out of? jjjjjjjj (terrycloth). jjjjjjjj (cowboy boots). What do you call the sharp pointy things that cowboys wear on their boots to kick their horses with ? jjjjjjjj (spurs). jjjjjjjj (glasses). What do you call the type of glasses that have a two part lens, one for seeing near and one for seeing far ? jjjjjjjj (bifocals). jjjjjjjj (bicycle helmet). What is this used for ? jjjjjjjj (to protect the head from accident or injury). jjjjjjjj (sandals). What do you call the metal fastener that holds the straps together on sandals ? jjjjjjjj (buckle). jjjjjjjj (pearls). Real pearls come from what shell®sh in the sea ? jjjjjjjj (oyster). jjjjjjjj (mittens). What is a common type of warm material that mittens are made of? jjjjjjjj (wool). jjjjjjjj (belt). What do you call the elastic straps that can also hold up pants ? jjjjjjjj (suspenders). jjjjjjjj (raincoat, mackinaw).


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42. What do people carry above their heads to keep the rain oå ? jjjjjjjj (umbrella). 43. jjjjjjjj (galoshes). 44. What is the waterproof material most galoshes and tires are made of? jjjjjjjj (rubber). * jjjjjjjj (bicycle helmet). * What is this used for ? jjjjjjjj (to protect the head from accident or injury). 45. jjjjjjjj (woman’s hat). 46. What do you call the part that is hanging down over her face ? jjjjjjjj (veil). 47. jjjjjjjj (apron). 48. What do you call the apron like thing that babies wear to keep food from spilling on their clothes ? jjjjjjjj (bib). 49. jjjjjjjj (vest). 50. What do you call the type of pattern on this vest that is very typical of Scotland? jjjjjjjj (plaid). * jjjjjjjj (bicycle helmet). * What is this used for ? jjjjjjjj (to protect the head from accident or injury). Note : Repeated presentation of the bicycle helmet item was included to test whether subjects would learn an unfamiliar item using the spaced-retrieval technique (Camp et al. 1995). These data were used clinically, but were not systemically analysed in this study.