Impairments In Prospective And Retrospective Memory Following Stroke
1. Impairments in prospective and retrospective
memory following stroke
Authors: Hyun Jung Kim a; Fergus I. M. Craik b; Lin Luo b; Jon Erik Ween c
a
Affiliations: Department of Rehabilitation Medicine, Eulji General Hospital, Eulji University School
of Medicine, Seoul, Republic of Korea
b
Rotman Research Institute, Baycrest and Department of Psychology, University of
Toronto, Toronto, Canada
c
Posluns Centre for Stroke and Cognition, Kunin-Lunenfeld Applied Research Unit,
Baycrest, Toronto, Canada
DOI: 10.1080/13554790802709039
Publication Frequency: 6 issues per year
Published in: Neurocase, Volume 15, Issue 2 April 2009 , pages 145 - 156
First Published: April 2009
Abstract
Prospective memory (PM) is the ability to carry out a planned intention at a future
time. We studied PM deficits in a group of community-dwelling stroke survivors
compared with normal controls. Twelve stroke patients and 12 matched controls
performed a series of tests assessing executive function, prospective (PM) and
retrospective memory (RM). Patients performed less well than controls on
laboratory measures of PM and associative RM; they also showed deficits on
standard tests of RM and executive control. The groups did not differ on more
structured clinical measures of executive function, RM, PM or self-rated PM and
RM. The results are discussed in terms of an impairment in the ability to 'self-
initiate' effortful cognitive processes.
Keywords: Stroke; Prospective memory; Cognition; Executive function; Retrospective memory
INTRODUCTION
Prospective memory (PM), the ability to plan future actions and execute them
successfully, is a central part of daily living (Cohen, 1996; Kliegel & Martin, 2003;
Martin & McDaniel, 2003). PM function has been postulated to depend heavily on
frontal lobe areas (Burgess, 2000; Goldstein, Bernard, Fenwick, Burgess, &
McNeil, 1993; McDaniel, Glisky, Rubin, Guynn, & Routhieaux, 1999; Okuda et
al., 1998; Shallice & Burgess, 1991; West & Covell, 2001; West, Jakubek, &
Wymbs, 2002) and has been studied extensively in normal aging (Cohen, West,
& Craik, 2001; Einstein & McDaniel, 1990; Henry, MacLeod, Phillips, & Crawford,
2004; Rendell & Craik, 2000) and in traumatic brain injury (Kliegel, Eschen, &
Thone-Otto, 2004; Mathias & Mansfield, 2005; Schmitter-Edgecombe & Wright,
2004). PM deficits following stroke (Brooks, Rose, Potter, Jayawardena, &
Morling, 2004) have been studied much less frequently, despite the high
2. prevalence of stroke in the adult population (Hachinski, 2007) and the significant
impact of stroke on frontal-executive functions (Reed, Eberling, Mungas, Weiner,
& Jagust, 2001; Reed et al., 2004).
PM requires the formation of an intention to act following a delay filled with other
activities. Typically, the planned action is triggered either by an event (e.g.,
'When you meet James, give him this information') or by a specified time (e.g.,
'Please phone home at 4:30 pm'). 'Time-based PM' is typically more difficult than
'event-based PM', since no explicit cue is given in the time-based case (Einstein
& McDaniel, 1990; Kvavilashvili & Ellis, 1996), with the consequent need for
more effortful 'self-initiated processing' (Craik, 1983, 1986; Einstein, McDaniel,
Richardson, Guynn, & Cunfer, 1995). Successful PM requires both that the
person 'remembers to remember' - the PM component of the overall performance
- and also recollects what is to be done. This latter aspect is assumed to involve
episodic or 'retrospective' memory (RM). Dissociation of the PM and RM
components have been clearly established (Cohen et al., 2001; Kliegel & Martin,
2003; West & Krompinger, 2005).
Studies of PM have utilized laboratory tasks, naturalistic observations and self-
rated questionnaires. In the present study, we used all three methods of
assessment. We used two laboratory tasks. The first was the Virtual Week (VW)
task developed by Rendell and Craik (2000) as a naturalistic laboratory task. VW
uses a board game to provide attentional load and occasions for PM cues (times
and events). It also allows the embedding of a realistic time-based PM task, and
provides a reasonably high number of measurable events for statistical power.
The second was the Memory for Intentions (MI) task (Cohen et al., 2001) in
which participants are given a series of real-life intentions (e.g., 'make a doctor's
appointment') to associate with a series of pictures. When the pictures are re-
presented later, embedded in a standard memory task, the subject must identify
the original pictures as cues, and recall the associated intentions. In addition to
these tasks, we used the Remembering a Belonging subtest from the Rivermead
Behavioural Memory Test (RBMT) (Wilson, Cockburn, & Baddeley, 1985) which
is a standard clinical event-based PM task. We also used the Prospective and
Retrospective Memory Questionnaire (PRMQ) (Crawford, Smith, Maylor, Della
Sala, & Logie, 2003) - a 16-item questionnaire measuring self-rated memory
failures as a way to quantify an individual's memory complaints. Finally, we also
3. administered a short battery of standard neuropsychological tests, as described
in the Methods section.
Recent studies have sharpened the general concept of self-initiation by
suggesting that successful performance of PM tasks typically involves the
maintenance of an intention or a strategic monitoring set in the interval preceding
the PM cue or designated time (Guynn, 2003). This maintenance consumes
attentional resources (Smith, 2003), and the ability to maintain the intention to
respond appropriately activates brain regions in the frontal pole, lateral frontal,
inferior parietal and precuneus (Burgess, Quayle, & Frith, 2001). We
hypothesized that PM tasks - particularly time-based tasks - require substantial
degrees of self-initiated processing (Craik, 1983) and that patients with anterior
lesions should show deficits in tasks requiring such self-initiated processing
(Burgess & Shallice, 1996). Our sample of post-stroke patients had lesions that
were predominantly anterior (see Subjects) so we had some expectation that
they would show PM deficits in at least some tests, despite the fact that they
were now living normal lives in the community and reporting no particular
cognitive difficulties. We chose patients with high levels of post-stroke functional
ability to minimize confounding effects of other cognitive impairments as much as
possible.
A second, more exploratory point, concerns the relations between PM and RM -
episodic memory for past events. The current literature is divided on the point of
whether PM is simply an aspect of RM (Crowder, 1996; Roediger, 1996) or
draws on different processes. A recent study of an individual with multiple
sclerosis (West, McNerney & Krauss, 2007) reported that the person
demonstrated poor performance on a number of PM tasks despite showing
superior levels of intelligence and average to superior RM. In this case, at least, it
appears that RM was intact whereas PM was negatively affected. The point at
issue in the present investigation is whether post-stroke patients will show
deficits in both PM and RM, or in one type of memory task and not in the other.
Such data could contribute to the debate on the similarity or otherwise of PM and
RM. A final purpose of the study was to compare levels of PM functioning
assessed by questionnaire and by a simple clinical test on the one hand, with PM
performance measured on laboratory tests on the other hand. The hope was that
both types of test would yield the same answer, but it also seemed possible that
4. the laboratory measures would be more sensitive, in which case they could be
used diagnostically to complement existing clinical batteries.
The aim of the present study was therefore to conduct a comprehensive
assessment of how PM is affected by stroke in non-demented chronic stroke
survivors who dwell independently in the community. Due to the complex nature
of PM performance, we wished to explore the effects of stroke on each type (i.e.,
event-based, time-based) and component (i.e., PM and RM components) of PM.
The two laboratory tasks were used to give separate measures for different types
and components of PM. The two neuropsychological assessments (Rivermead
and Questionnaire) were included to give a general measure of overall PM
functioning. For independently-dwelling stroke patients, a contrast between
laboratory task measures and general neuropsychological measures of PM might
reveal subtle impairments in stroke patients that are not readily detected by
existing assessment tools.
METHOD
Subjects
Twelve stroke patients and 12 neurologically normal control subjects were
included in this study. All stroke patients were recruited from the outpatient
Stroke and Cognition Clinic at the Brain Health Centre at Baycrest or the patient
database at Baycrest's Rotman Research Institute. The inclusion criteria were:
(1) diagnosis of stroke based on clinical assessment and imaging (CT, MRI), (2)
fluent English speaker, (3) independent in activities of daily living (ADLs) and
living at home, and (4) willing to participate.
The average length of time since stroke was 2.99 years (range 4.8 months to 9
years). There were five patients with right and five with left hemisphere lesions,
and two with bilateral lesions. All patients had received either an MRI or a CT
scan. The image processing was carried out by a stroke neurologist (JW) with
expertise in lesion analysis. All scans were visually rated according to Age
Related White Matter Changes (ARWMC) reported to be comparable for CT and
MRI (Wahlund et al., 2001). The ARWMC uses a 3-point scale (0 = normal, 1 =
isolated white matter hyperintensities, 2 = near confluence of lesions, 3 =
confluent lesions) in each of 10 compartments, 5 right and 5 left. The areas are
frontal, parieto-occipital, temporal, basal ganglia and infratentorial. Table 1 shows
5. the classification of lesion severity for all 12 patients in each of the 10 brain
regions. The majority of lesions are subcortical and in frontal, basal ganglia and
parieto-occipital areas. Given the intimate connections between frontal and basal
ganglia regions via frontal-striatal circuits (Cummings, 1993), the patients may be
described in general terms as having 'frontal' lesions.
TABLE 1 White matter lesion intensity (see text for explanation) for each
patient as a function of brain region
Brain Region
Patient RF LF RBG LBG RT LT RPO LPO RIT LIT
ID
P1 2 0 0 0 0 0 0 0 0 0
P2 0 1 0 1 0 0 0 0 0 0
P3 0 2 0 1 0 0 0 0 0 0
P4 1 3 1 2 0 0 1 1 0 0
P5 2 2 0 0 0 0 0 1 0 0
P6 3 3 3 3 3 3 3 3 0 0
P7 0 0 3 0 0 0 0 0 0 0
P8 1 0 2 0 0 0 0 0 0 0
P9 1 2 0 3 0 0 0 1 0 0
P10 0 0 0 0 0 3 0 0 0 0
P11 3 3 3 3 0 0 2 2 0 0
P12 2 2 1 1 0 0 2 2 0 0
Notes: R and L, right and left respectively; F, frontal; PO, parieto-occipital; T, temporal; BG, basal ganglia;
IT, infratentorial.
6. The exclusion criteria were (1) dementia diagnosed from the medical history or
from the Clinical Dementia Rating Scale (Morris, 1993) score of > 0.5; (2) history
of alcohol or substance abuse within 5 years of testing, (3) history of head
trauma with loss of consciousness, (4) significant other neurological or
psychiatric disorders, (5) medications (other than selective serotonin reuptake
inhibitors) that affect cognitive function (6) serious, unstable medical illness or
neurological impairment that would limit participation or completion of the
protocol. Control subjects (n = 12) were recruited from the Rotman Research
Institute database. They were all community-dwelling individuals with no history
of any neurological or psychiatric conditions. The two groups were matched for
age and education (Table 2). The Ethics Committee of Baycrest approved this
experiment and each participant gave informed consent.
TABLE 2 Demographics, clinical characteristics and neuropsychological
profiles for subject groups
Patients Controls t-Tests
M SD M SD t df p
Age (years) 69.33 7.02 69.08 4.94 0.10 19.75 .92
Education (years) 14.42 3.73 15.67 3.23 -0.88 21.56 .39
MMSE 28.67 1.07 29.00 1.13 -0.74 21.95 .47
Trail Making Time
A (s) 39.92 13.85 33.83 8.91 1.28 18.77 .22
B (s) 90.00 33.34 78.92 20.92 0.98 18.50 .34
Verbal Fluency
FAS (words) 35.67 10.05 45.25 9.37 -2.42 21.89 .02
Animal (words) 14.17 4.69 18.42 6.61 -1.82 19.83 .08
SART
Reaction Time (ms) 367.3 109.59 438.97 60.54 -1.98 17.14 .06
3
Error of Commission 10.92 7.19 4.58 2.87 2.83 14.43 .01
Error of Omission 7.42 14.06 3.50 3.68 0.93 12.50 .37
Verbal Paired Associates
Total Recall (words) 9.83 1.85 11.08 3.32 -1.14 17.25 .27
CVLT
Total learning score (1-5) 35.50 10.78 50.75 7.62 -4.08 19.12 .00
Long delay free recall 6.58 3.09 10.75 2.05 -3.89 19.12 .00
Recognition Hits - False 8.50 5.30 11.92 3.87 -1.80 20.14 .09
alarms
R-SAT
7. % Easy Items Completed 90 10 84 17 1.11 17.07 .28
Values reported are raw scores. M, mean, SD, standard deviation, df, degrees of freedom. Two-
tailed t-tests are reported. See methods section for abbreviations.
Neuropsychological profile
A battery of standard neuropsychological measures was administered to
participants to measure executive and immediate memory abilities. First, basic
demographics such as age, gender and educational level were recorded. The
Mini-mental State Examination (MMSE; Folstein, Folstein, & McHugh, 1975) was
administered to measure global cognitive function. The Trail Making Tests A & B
(Reitan, 1986) were given to assess speed and cognitive flexibility: The
measures of performance taken were the time taken to complete Trails A and
Trails B, respectively. Lexical and category verbal fluency abilities were assessed
by the Verbal Fluency phonemic (FAS) test and the semantic categories (animal)
test (Lezak, 1995). The measures of performance here are the total numbers of
items produced for the FAS test and the animal naming test, respectively. A
measure of attention and inhibitory capacity was provided by the Sustained
Attention to Response Task (SART) (Robertson, Manly, Andrade, Baddeley, &
Yiend, 1997). Performance was measured by the mean reaction time (RT), and
the number of errors of commission and errors of omission. Memory abilities
were assessed by two tests; first the Verbal Paired Associates (VPA) test from
the Wechsler Memory Scale-Third Edition (Wechsler, 1997) and second the
California Verbal Learning Test-Second Edition (CVLT-II, Delis DC, Kaplan, &
Ober, 2000). The measures we took included total correct recall from VPA, and
T-score, long delay free recall performance and recognition hits from CVLT-II.
Finally, the Revised Strategy Application Test (R-SAT) was administered for the
assessment of strategy function (Levine, Dawson, Boutet, Schwartz, & Stuss,
2000; Stuss & Levine, 2002). The main measure of performance was the
proportion of easy items completed out of the total number of items in the test.
High percentages indicate more efficient strategies.
The characteristics of the study groups are presented in Table 2. The groups did
not differ in terms of age and education, but the proportion of men was higher in
the stroke sample (Patient: M = 8, F = 4; Control: M = 3; F = 9). The scores on
the MMSE did not differ significantly between two groups. Control participants
generated more items in both the FAS test and the animal names test, although
only the former reached statistical significance. A marginally significant difference
between groups was found on SART reaction times (patients were faster than
controls), and a significant difference was found on errors of commission
(patients made more errors than controls). The stroke patients scored
significantly lower on the measures of CVLT-II learning and long-delay free recall
but not on recognition memory, as has been noted as a pattern characteristic of
8. vascular cognitive impairment (Roman et al., 2004).
Prospective memory tasks
Virtual Week
Virtual Week (VW) is a board game developed to assess PM (Rendell & Craik,
2000). Each circuit of the game represents 1 day from 7 am to 10 pm and
participants move around the board with the roll of a die. They have to remember
to carry out activities either at specified 'times' (as they pass the relevant square
on the board) or in response to specified 'events' that are given on event cards
picked up in the course of the circuit. The PM tasks were either 'Regular' (the
same tasks on all circuits) or 'Irregular' (different tasks on each circuit). The same
four 'Regular' tasks were performed on every circuit of the board and were given
in instructions before the game started; two were in response to events (taking
antibiotics at breakfast and dinner) and two were in response to squares
indicating virtual times on the board (taking asthma medication at 11 am and 9
pm). Irregular tasks also included two tasks in response to events and two other
tasks in response to virtual time squares. These tasks are however different for
each circuit and were given by the 'start card' at the beginning of each circuit. As
participants moved around the board, they were required to pick up 'event cards'
as they passed 'event squares', make choices about daily activities (e.g., a
choice of foods for lunch) and remember to carry out the required activities. All
the activities written on cards indicated things that people normally do in a typical
day. Participants carried out the specified actions simply by telling the
experimenter (e.g., 'The event card tells me that my friend Jane phoned, so I
remember to ask her to lunch next week' or 'It is now 4 pm so I remember that I
should phone the doctor's office'). The third type of PM task was a time-check
task in which the participant had to indicate to the tester when 2 min 30 s and
also 4 min 15 s had elapsed from the start of the current circuit, supposedly 'to
check virtual lung capacity'. This 'real-life' time was given by a stopwatch placed
on the desk facing down and participants were informed that they could check
the stopwatch at any time. Therefore, 10 PM tasks were assessed on each day
(complete circuit around the board). Each group of 10 consisted of four regular,
four irregular and two time-check tasks.
The point of these different tasks was to assess PM for different levels of habit
9. and environmental support. Thus, the regular tasks should be easiest as they
occurred predictably on every circuit; the irregular tasks were less habitual as
they changed on each circuit; finally, the time-check task required the participant
to break out of the board-game mode and remember to check the actual time as
given by the stopwatch. Previous results (Rendell & Craik, 2000) have generally
confirmed this order of difficulty. Participants were encouraged to tell the
examiner the required action later if they failed to carry out the intention at the
designated time or event but remembered it later; they were also asked to report
if they remembered that they had some task to perform, but were unable to
retrieve the content of the task. Although Rendell and Craik attempted to capture
the notion of time-based PM in the Virtual Week task by asking participants to
respond at various 'times of day', these 'times' are signaled clearly on the board,
and are thus not too different from events. Accordingly, and to simplify analyses,
the time-based and event-based responses were combined into one measure of
PM in the present study. True time-based PM ability is better represented by
performance in the clock-checking task.
In this study, participants completed three virtual days per session, and the mean
measures over the three circuits were taken as scores. Responses were
categorized as 'Correct' or 'Incorrect' on each task. A 'Correct' response on
'Regular' or 'Irregular' trials indicated that the participant had remembered to
state the required action before the next roll of the die. A 'Correct' response for
the time-check task was within 10 seconds of the target time. Thus, 'Correct'
responses indicated correct recognition of the prospective cue and correct recall
of the intention. The experimenter recorded types of error as 'Wrong', 'Late', or
'Miss'; 'Wrong' responses indicated that recall of the content was incorrect or the
action was recalled simply as 'something' at the correct time. 'Late' responses
indicated that recall of the correct content occurred at the incorrect time of the
virtual day. A 'Miss' response indicated that the participant failed to recall the
target at any time.
Memory for intentions
The Memory for Intentions (MI) task developed by Cohen et al. (2001) was
modified by constructing a shorter version. Participants were presented with a
series of 48 pictures, each paired with a word related to the picture; their task
was to remember the pair for a later memory test. Each picture-word pair was
10. presented for 6 sec. This series served as the background 'ongoing activity' for
the PM task proper. During this learning phase, participants were shown a further
series of 16 pictures, each of which also had a related word to be learned, but
had in addition an intended action to be remembered and stated at a later stage
in the experiment. These 16 pictures with their accompanying intentions and
paired-associate words were each shown for 12 seconds, and were presented
randomly intermixed with the 48-item paired associate task. There were 8
intentions in each of two categories (1) highly related and (2) somewhat related
to the activity shown in the accompanying picture, and subjects were asked to
form the intentions as they would use memory strategies in everyday life. For
example, if the intention was 'I need to phone a friend', a highly related cue might
be a picture of a person using a telephone; a somewhat related cue might be a
picture of two friends hugging. We manipulated the degree of semantic
relatedness in order to investigate the efficiency of the prospective and
retrospective components of PM in a stroke population. In their aging study,
Cohen et al. (2001) concluded that the efficiency of the retrospective component
(that is, the ability to recollect the intention when shown the picture at a later
time) was influenced by conceptually driven processes, and when the picture and
intention were semantically related the efficiency of the retrospective component
was similar for older and younger adults.
During the test phase, participants were shown the series of 64 studied pictures
plus 16 new pictures as distracters. Participants were instructed to recall the
word initially paired with the picture, or to say 'new' if they did not recognize the
picture. Additionally, participants were instructed to recall the intentions
associated with the 16 PM pictures, which were presented randomly in the test
sequence, and not identified as ones with intentions. Participants were also
instructed to respond to the experimenter when they detected a PM picture in the
test phase even if they could not recall the associated intention. During the test
phase, pictures were presented at a subject controlled pace. Task performance
was measured in three categories: (1) prospective component, the proportion of
correctly recognized PM pictures to total PM pictures, regardless of whether
participants explicitly remembered the associated intention, (2) retrospective
component, the proportion of intentions remembered correctly as a function of
the total number of identified PM pictures, and (3) associative memory, the
proportion of words recalled correctly in response to the 48 paired-associate
11. picture cues.
Remembering a belonging: the Remembering a Belonging subtest from the
Rivermead Behavioural Memory Test (RBMT, Wilson et al., 1985) was also used
to assess PM. At the beginning of the test session, the experimenter requests
that the subject give the experimenter a personal belonging (e.g., a watch), which
the experimenter then hides from view in an easily accessible place known to the
subject. Participants are requested, but not reminded, to ask for the belonging
back at the end of the test session and to remember where it was hidden. If
subjects do not ask voluntarily, the experimenter prompts them as to whether or
not an item had been relinquished. Parameters assessed were (1) remembering
to ask for the hidden item and (2) remembering where the item was hidden,
either with or without prompting.
Prospective and Retrospective Memory Questionnaire: the Prospective and
Retrospective Memory Questionnaire (PRMQ, Crawford et al., 2003), a 16-item
questionnaire, 8-items for each memory domain, was also included to measure
self-rated memory failure by participants. For the results of the PRMQ, we
converted the raw scores to T-scores using the program downloaded from the
web site address: www.psyc.abdn.ac.uk/homedir/jcrawford/prmq.htm. The T-
scores have a mean of 50 and a standard deviation of 10 in a normal population.
Predictions and statistical analysis
If 'frontal' stroke patients have a specific problem with prospective memory, we
should see group differences on all PM measures. On the VW task, we expected
to see largest effects on the time-check component, given that this aspect
requires the subject to break ongoing task set, and thus arguably requires the
most 'initiation' and degree of strategic monitoring. Similarly on the MI task we
expected to see largest effects on the PM component (remembering which
pictures were associated with intentions). With regard to RM, we expected that
the stroke group would again have greatest difficulty with tests involving least
environmental support (such as free recall), but relatively less difficulty with tests
involving more support, such as cued recall and recognition (Craik, 1983, 1986).
Statistical analyses were performed using the computer software SPSS version
11.0 for Windows (SPSS, Chicago, IL). Between-group differences in age,
education, MMSE, PRMQ, and other neuropsychological tests were examined
12. with independent samples t-tests. Performance on the RBMT was assessed with
the Chi-square test. Performance on the Virtual Week and Memory for Intentions
tasks in the stroke and control groups were compared by analysis of variance
(ANOVA). An alpha level of p < .05 was used for all the above a priori analyses.
If significant main effects were found, post-hoc analyses between groups were
applied with independent-samples t-tests using the Bonferroni correction.
RESULTS
Prospective memory performance
Virtual Week: the mean proportions of 'Correct' responses and different types of
error are presented in Table 3. The proportions of correct responses were first
analyzed with a 2 3 mixed ANOVA using group (patients vs. controls) as the
between-subject variable and type of task (regular, irregular, time-check) as the
within-subject variable. Both main effects were statistically significant: The control
group outperformed the patient group, mean proportions correct: 0.59 vs. 0.39;
F(1, 21) = 8.94, p < .01, ηp2 = .30; for type of task, F(2, 42) = 11.61, p < .001, ηp2
= .36, post-hoc Bonferroni tests revealed that participants were more accurate on
the regular than the irregular tasks (p < .001). Furthermore, the interaction
between group and type of task approached significance, F(2, 42) = 2.55, p =
.09, ηp2 = .11, suggesting that the pattern of group differences may differ as a
function of task. To further evaluate this possibility, post-hoc t-tests were
performed to test for group differences in each task. The results showed that the
group difference was significant in the time-check task, t(21) = -2.99, p = .007, r =
.55, but not in the irregular tasks, t(21) = -1.87, p = .076, r = .38, or the regular
tasks, t(21) = -0.787, p = .44, r = .16.
TABLE 3 Proportions of correct responses and different types of error in
the Virtual Week task
Regular Irregular Time-check
Stro Contro Stro Contro Stro Control
ke l ke l ke
Correct
0.61 0.69 0.26 0.41 0.30 0.67
M
13. 0.17 0.27 0.16 0.22 0.28 0.30
S
D
Wrong
0.06 0.05 0.21 0.17 0.08 0.00
M
0.07 0.07 0.08 0.14 0.20 0.00
S
D
Late
0.05 0.12 0.03 0.03 0.14 0.26
M
0.08 0.14 0.04 0.04 0.08 0.27
S
D
Miss
0.27 0.14 0.50 0.38 0.48 0.07
M
0.18 0.19 0.21 0.21 0.29 0.11
S
D
A separate 2 3 mixed ANOVA was performed on the proportions of 'Miss'
responses. Both main effects were again statistically significant: for groups, F(1,
21) = 18.58, p < .001, ηp2 = .47, stroke patients showed a higher proportion of
miss responses than the controls, group means: 0.42 vs. 0.20, for patients and
control, respectively; for type of task, F(2, 42) = 8.30, p < .001, ηp2 = .28, post-hoc
tests revealed that the miss rates were higher in the irregular tasks than the
14. regular and time-check tasks. The interaction between group and type of task
was also significant, F(2, 42) = 3.96, p = .03, ηp2 = .16. Consequently, post-hoc
tests were performed to test for group differences in each task. Again, the results
showed a significant difference in the time-check task, t(12.63) = 4.41, p = .001, r
= .78 (degrees of freedom corrected for unequal variances), but not in the regular
and irregular tasks, t(21) = 1.72, p = .099, r = .35, and t(21) = 1.38, p = .183, r =
.29, respectively. The results from the Miss responses point to the same
conclusion as with that from the Correct responses and suggests that stroke
patients show the greatest deficits in the time-check tasks, and that such deficits
are characterized by a combination of lower accuracy rates and higher miss
rates. The other two types of error ('Wrong' and 'Late') were not analyzed due to
the low numbers of observations.
Memory for intentions: patients correctly recalled fewer words than control
subjects in the paired associate task, t(22) = -2.66, p = .014, r = .49. To examine
the effects of group and semantic relatedness on the PM task, 2 2 mixed
ANOVAs (between: group, patient vs. control; within: semantic relatedness, high
vs. somewhat related) were performed on the prospective and retrospective
components separately. No main effect of relatedness was found for either the
prospective or the retrospective component, nor did relatedness interact with
group (all F values < 1.0); the data were therefore collapsed across relatedness
and are presented in Figure 1. For the prospective component, a main effect of
group was found, F(1, 22) = 21.25, p < .001, ηp2 = .491, showing that the stroke
group had a significantly smaller proportion of correct responses than the control
group. No group difference was found for the retrospective component. Overall
then, stroke patients showed a deficit on the relatively difficult paired-associate
task (remembering which word was paired with each picture) but performed as
well as controls on remembering the activity associated with PM pictures,
provided that they recognized the 'intention' pictures as PM cues. The patients
did show a deficit in this latter response, however. They were less able to identify
the pictures associated with an intention (means = 0.66 and 0.88 for patients and
controls, respectively).
[Enlarge Image]
15. Figure 1. Mean proportions of correct responses as a function of memory
measure in the Memory for Intention task. Error bars represent standard
error. *p < .05; **p < .01. PM, Prospective Memory; RM, Retrospective
Memory.
Since there was a significant difference in performance on the picture-word
paired-associate task between the two groups, performance on this task was
included in the analysis to control for the contribution of general associative
memory ability. We conducted ANCOVAs on prospective and retrospective
components as the dependent measures with group as the between-subject
factor, relatedness as the within-subjects factor and associative memory as the
covariate. For the prospective component, both associative memory, F(1, 21) =
5.85, p = .025, ηp2 = .218, and group, F(1,21) = 10.46, p = .004, ηp2 = .332,
showed significant effects. That is, patients still showed significant prospective
deficits after controlling for their lower performance on the paired-associate task.1
No significant effects were found for the retrospective component.
Remember a belonging: three control subjects and five stroke patients
remembered to ask for their belongings in the Rivermead Test. Ten subjects in
each group remembered where the belonging was hidden. Chi-square tests
revealed that there were no significant differences between stroke patients and
controls on this test (X2 = 0.83, p = .67).
Prospective and Retrospective Memory Questionnaire. There were no significant
differences in PRMQ T-scores between the groups, though patients scored
slightly lower than controls on both components. Mean T-scores for the
retrospective memory questions were 47.8 and 51.5 for patients and controls,
respectively (t = -1.46, ns); T-scores for the prospective questions were 47.6 and
52.0 for patients and controls, respectively (t = -1.16, ns).
DISCUSSION
Neuropsychological tests
Group differences in the executive tasks revealed mixed results, such that
patients showed deficits in some but not all subcomponents of executive
functioning. For example, stroke patients did not show deficits in perceptual
speed (Trails A and B), some aspects of sustained attention (SART: error of
omission), or strategy application (R-SAT). In contrast, tasks that involve
16. inhibitory control (SART: error of commission) and unguided retrieval (verbal
fluency) showed large stroke-related deficits. This pattern of results suggests that
impairments in this group of patients are associated with difficulties of 'self-
initiation' (Craik, 1983, 1986) and cognitive control, which in turn may reflect
inefficiencies of frontal lobe functioning (Grady & Craik, 2000). Despite equivalent
levels of education and basic cognitive functions (MMSE), patients showed
decreased performance in both immediate memory tasks, VPA and CVLT-II
(although only the latter tasks were statistically significant). Thus, the patients
exhibited some deficits in associative and item memory, both measured by recall;
the groups did not differ on the recognition test of the CVLT-II. Hence,
performance holds up well in situations where cognitive processes are supported
by the task, the external environment, or well-learned habits, but deficits emerge
when decision-making or retrieval processes are not so supported.
Prospective memory
Patients made as many correct responses as controls on the regular tasks in the
Virtual Week test, suffered a slight deficit on the irregular tasks and a large deficit
on the time-check task (r = .16, p = .44; r = .38, p = .076 and r = .55, p = .0007,
respectively). Patients also missed more responses than controls in the time-
check task, although there were no significant group differences in numbers of
misses in regular or irregular tasks. No explicit prospective cues are available in
the time-check task; for successful performance participants must therefore
break out of the set induced by the Virtual Week task and self-initiate the
decision to check the stopwatch. If the post-stroke patients had more trouble in
this respect it might be expected that they would check the clock less frequently.
In fact, the median number of checks (total for the three 'days') was 8 for the
patients and 15.5 for the controls; the difference was not statistically significant,
however, owing to the small numbers and the large variance - one patient
checked the clock 26 times for example. The fact that there were only two
occasions to perform the time-check task per circuit, as opposed to four
occasions for both regular and irregular tasks may also have played a part in the
results. The observation that no stroke-related deficit was evident under the
simplest condition (i.e., the regular tasks) is similar to the findings of Rendell and
Craik (2000) who reported no effect of aging in the performance of regular tasks,
although age-related differences were found in the irregular and time-check
tasks. The authors argued that older adults were able to benefit from the
17. environmental support provided by reoccurrence and by explicit cues in the
regular tasks. The present findings suggest that 'frontal' stroke patients are also
able to do so, and that this preserved ability may account for the observation that
despite impaired performance in a majority of the memory measures and
laboratory PM tasks, the patients showed equivalent levels of performance in
simple PM tasks and in subjective reports such as the memory questionnaire.
Performance differences between the two groups were larger in the non-
repeated irregular task than in the repeated regular task. Compared to the other
two tasks, the irregular task is associated with an increased demand to
constantly update the intentions held in mind for each trial. However, the
performance of stroke patients was poorest in the time-check task despite the
fact that this task also repeats. It is suggested that the time-check task is
associated with an increased demand for self-initiation as a result of less salient
prospective cues relative to the other two tasks. Relative to the easiest condition
(regular tasks), controls showed decreased performance only when the
prospective demands varied from trial to trial (irregular tasks), whereas patients
showed decreased performance both with irregularity and with increased
demands for self-initiation. It should be acknowledged that meta-analyses of age-
related differences in PM (e.g., Henry et al., 2004) have shown that event-based
PM tasks that are high in strategic demand, and also some RM tasks such as
free recall, can show as large age-related deficits as those on time-based PM
tasks. This suggests that there is nothing particularly unique about PM, but that
age-related difficulties, and post-stroke difficulties according to the present
results, are more likely to be found on tasks that have a high demand for
initiation, strategic monitoring, and executive control.
In the memory for intentions task, we found that patients recalled fewer words
than controls in the word-picture paired-associate background task. The patients
also missed more prospective memory cues. For those pictures correctly
identified as cues, however, patients and controls recalled the associated
intentions with equivalent accuracy. The apparent discrepancy in retrospective
memory results between the paired-associate recall and recall of intentions may
be due partly to the somewhat greater difficulty of the former task (Figure 1) but
probably also to the fact that the patient group identified fewer picture cues, so
that the conditional recall of intentions was based on fewer (and possibly easier)
18. examples. The ANCOVA analysis showed that pathology has an additional effect
(poorer performance on the PM task) even after differences in associative
memory were accounted for. Although PM performance and associative memory
performance are related, our analysis showed that patients performed more
poorly in PM tasks not only because of their lower associative memory
functioning. In this MI task, the relatedness of the intention and picture cue had
no effect on either the prospective or retrospective component, nor did it interact
with any other factor. This may be because both the 'highly related' and
'somewhat related' items were fairly easy to associate. The patient group in this
study did not show any deficits in this regard, possibly reflecting their spared
semantic functions. The effects of stroke found in this task were very similar to
the effects of aging reported by Cohen et al. (2001, Exp. 1). In that study, older
adults showed lower PM scores for highly related and somewhat related items,
but equivalent RM scores for these items compared to younger adults.
Speculatively, it seems possible that both stroke and aging affect the frontal-
executive functions responsible for successful PM.
No group differences were found in either the Memory for Belongings task taken
from the Rivermead Behavioural Memory Test or in the Prospective and
Retrospective Memory Questionnaire. The Memory for Belongings task was
obviously difficult for all participants since only 3 control subjects and 5 patients
remembered to ask for the object; these are people in their 60s and 70s,
however, so perhaps this level of performance on a one-off task is not surprising.
Our main point here is that whereas the test is easy to administer, it is obviously
rather a blunt instrument, and did not reveal PM difficulties in the patients which
were shown on the experimental tasks. Similarly, there were no group
differences in either PM or RM as measured by the questionnaire. Both groups
scored close to the population average of 50. Our conclusions are that the stroke
patients' memory problems are relatively subtle, and are not sufficiently grave to
lead them to rate their performance as lower than normal in the questionnaire.
Nonetheless, these difficulties were picked up by the VW and MI tests.
Taken together, our assessment of PM functions in stroke patients suggests that
they are impaired by some but not all aspect of PM. Specifically, the patients
performed as well as the controls on the regular tasks in the VW task and on the
RM component of PM in the MI task; they performed less well, however, on the
19. irregular and time-check aspects of VW and on the PM component of the MI
task. We therefore suggest that these differences can only be detected by
carefully designed tasks that measure these aspects separately. Stroke patients
also showed impairments in some RM tasks such as associative memory and
free recall. However, our analysis suggests that their deficits in PM functioning
clearly involve additional stroke-related deficits beyond general memory ability,
possibly deficits related to executive functioning.
CONCLUSIONS AND LIMITATIONS
The main limitation of the study is that the group of stroke patients is small.
Further studies are clearly needed to confirm and extend the present results. In
addition, such further studies should seek to specify the brain areas principally
concerned with failures of PM. Our speculative assumption is that these areas
are typically frontal in general, as the lesions in our patient group were primarily
anterior, but this assumption must be tested by further studies. Importantly, it is
also unclear at present whether the present pattern of results is associated with
stroke as such, or whether it may be found in a variety of cases involving anterior
lesions. Despite the relatively small numbers of subjects in each group, however,
the results showed substantial differences between patients and controls in many
but not all tests. This differential pattern gives some clues as to the nature of
cognitive difficulties experienced by stroke patients with anterior lesions. The
present results suggest, first, that difficulties such patients experience arise in
situations where the needed action is not well supported by well-practiced habits
or by environmental cues. Executive actions or retrieval processes must
therefore be 'self-initiated' by the subjects themselves. Second, the stroke
patients studied here seemed to have greatest difficulties with spontaneously
switching from one (ongoing) activity to another. This is evident in the MI task by
their reduced ability to spontaneously recognize pictures as prospective cues
rather than associative cues (i.e., the ongoing task), and by their reduced
likelihood of spontaneously checking the clock when playing the virtual week
board game. In line with this observation, stroke patients had shorter reaction
times on the SART and also made more errors of commission, suggesting that
they were less able than controls to inhibit a habitual activity. It is also noteworthy
that the present sample of patients reported no difficulties in everyday living, and
that the groups did not differ in their questionnaire responses. This discrepancy
suggests that patients' insight into the nature of their deficits is not complete.
20. Indeed, the disturbances in executive deficits that lead to memory retrieval
problems are often 'misinterpreted' by patients as 'short term memory' issues,
thus leading them to clinical attention with fears that they suffer from a
degenerative dementia. It is quite possible that some of the real-life difficulties
experienced by these patients may be embedded in the kind of PM deficits
reported here. A larger study would be required to settle this issue.
Acknowledgments
This work was supported by the Korea Research Foundation Grant (KRF-2006-
013-E00133) to H. J. Kim and by a grant from the Natural Sciences and
Engineering Research Council of Canada to F. I. M. Craik. We also wish to thank
HeeSun Lim for research assistance.
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Notes
1
The group covariate interaction was significant F(1, 20) = 5.04, p < .05, showing
that the assumption of homogeneous regression slope for ANCOVA was
violated. However, the violation of assumption has little effect on the conclusion
from ANCOVA when the group sizes are equal (Hamilton, 1977). So it seems
safe to conclude that the patient and control groups differed after controlling for
associative memory performance.
List of Figures
[Enlarge Image]
Figure 1. Mean proportions of correct responses as a function of memory
measure in the Memory for Intention task. Error bars represent standard
error. *p < .05; **p < .01. PM, Prospective Memory; RM, Retrospective
Memory.
List of Tables
TABLE 1 White matter lesion intensity (see text for
explanation) for each patient as a function of brain region
26. Patients Controls t-Tests
M SD M SD t df p
Age (years) 69.33 7.02 69.08 4.94 0.10 19.75 .92
Education (years) 14.42 3.73 15.67 3.23 -0.88 21.56 .39
MMSE 28.67 1.07 29.00 1.13 -0.74 21.95 .47
Trail Making Time
A (s) 39.92 13.85 33.83 8.91 1.28 18.77 .22
B (s) 90.00 33.34 78.92 20.92 0.98 18.50 .34
Verbal Fluency
FAS (words) 35.67 10.05 45.25 9.37 -2.42 21.89 .02
Animal (words) 14.17 4.69 18.42 6.61 -1.82 19.83 .08
SART
Reaction Time 367.33 109.59 438.97 60.54 -1.98 17.14 .06
(ms)
Error of 10.92 7.19 4.58 2.87 2.83 14.43 .01
Commission
Error of Omission 7.42 14.06 3.50 3.68 0.93 12.50 .37
Verbal Paired Associates
Total Recall 9.83 1.85 11.08 3.32 -1.14 17.25 .27
(words)
CVLT
Total learning 35.50 10.78 50.75 7.62 -4.08 19.12 .00
score (1-5)
27. Long delay free 6.58 3.09 10.75 2.05 -3.89 19.12 .00
recall
Recognition Hits - 8.50 5.30 11.92 3.87 -1.80 20.14 .09
False alarms
R-SAT
% Easy Items 90 10 84 17 1.11 17.07 .28
Completed
Values reported are raw scores. M, mean, SD, standard deviation, df, degrees of
freedom. Two-tailed t-tests are reported. See methods section for abbreviations.
TABLE 3 Proportions of correct responses and different
types of error in the Virtual Week task
Regular Irregular Time-check
Stro Contro Stro Contro Stro Control
ke l ke l ke
Correct
0.61 0.69 0.26 0.41 0.30 0.67
M
0.17 0.27 0.16 0.22 0.28 0.30
S
D
Wrong
0.06 0.05 0.21 0.17 0.08 0.00
M
0.07 0.07 0.08 0.14 0.20 0.00
S
28. D
Late
0.05 0.12 0.03 0.03 0.14 0.26
M
0.08 0.14 0.04 0.04 0.08 0.27
S
D
Miss
0.27 0.14 0.50 0.38 0.48 0.07
M
0.18 0.19 0.21 0.21 0.29 0.11
S
D