Department of Cognitive, Perceptual and Brain Sciences, University College London, England;
Christopher J. Berry
Department of Cognitive, Perceptual and Brain Sciences, University College London, England
David R. Shanks
Department of Cognitive, Perceptual and Brain Sciences, University College London, England
Acknowledgement: Emma V. Ward is now at the Department of Psychology, University of York, and Christopher J. Berry is now at the School of Psychology, Plymouth University.
This research was supported by an ESRC studentship award. We thank Qizhang Sun for help with data collection in Experiments 3b and 3c.
Memory can be measured directly or indirectly. Direct or explicit tests (e.g., recognition) require deliberate recollection of specific information from a prior study episode, whereas indirect or implicit tests measure memory of previously studied information in a seemingly unrelated task (e.g., perceptual identification). Priming is a commonly used index of implicit memory. It refers to a long-term change in behavioral response to an item as a result of prior exposure to it, and usually takes the form of facilitated processing. For example, previously studied words or pictures are usually identified more quickly than new ones.
The question of whether there are distinct memory systems driving explicit and implicit memory has provoked extensive research over the past few decades. Performance on explicit and implicit tests has been shown to dissociate under numerous experimental manipulations (reviewed in
Age-invariant priming has been reported on tests of word-stem completion (e.g.,
How convincing are prior reports of spared priming in old age? Most published demonstrations of age-invariant priming rest on a null result (a failure to find a statistically significant difference between groups), and it is possible that many studies lacked the required statistical power to detect a significant priming difference. Indeed, priming is usually numerically lower in older relative to young adults, and a meta-analysis by
Prior conclusions have also been limited because samples of explicit and implicit memory have traditionally been measured in separate experimental phases. Scores may dissociate because there is a longer study-test delay for one task than the other, and/or because participants adopt different response strategies or levels of motivation in the two tasks when they are presented separately. For samples of explicit and implicit memory to be truly comparable, they need to be taken for the same items at around the same point in time (see
Computational models can offer considerable theoretical insights regarding empirical dissociations. Formal single-system models have successfully reproduced several dissociations that have previously been taken as support for multiple memory systems (e.g.,
Until recently, there have been few attempts to test formal multiple-systems models.
More robust evidence for multiple systems would come from a demonstration that priming is completely preserved in old age (i.e., equivalent in young and older adults), despite a clear group difference in recognition memory when the two are measured consecutively on each test trial. The present study aimed to establish whether such a pattern can be produced. This study is the first to our knowledge to compare recognition and priming in young and older individuals using the continuous identification with recognition (CID-R) paradigm (e.g.,
We compared the performance of young and older adults on the CID-R task. Participants studied pictures of everyday objects both immediately and 60 min prior to the test. The delay was included to reduce the strength of memory for a subset of items as much as possible. We anticipated reductions in recognition memory as a function of age and delay, and the question of whether priming would be similarly affected was of primary interest.
Participants
Twenty young (seven men) and 20 older (two men) adults participated for a small payment. The young adults were students from University College London (UCL), recruited through an advertisement on an internal website. The older adults were members of the University of the Third Age (U3A) organization. All were native English speakers who reported good health. Participant demographic information is summarized in
Materials
The stimuli were pictures of everyday objects from 10 categories: animals, clothing, fruit and vegetables, electrical appliances, musical instruments, transportation vehicles, kitchen utensils, insects, tools, and furniture. Items within these categories were selected based on the category norms collected by
Design and procedure
The experiment used a mixed factorial design with the between-subjects factor age group (young/older adult) and the within-subjects factor delay (60 min/no delay).
The experimental procedure, identical for both groups, consisted of four parts: an initial study phase, a 60-min interval, a second study phase, and finally the CID-R test. Participants were tested individually, and the duration of the experiment was approximately 90 min. In this and subsequent experiments, the task was programmed in Matlab 6 using the Cogent 2000 toolbox, and administered on a PC with a screen resolution of 1024 × 768 pixels. Viewing distance was approximately 50 cm.
Initial study
Participants performed an incidental encoding task that involved matching briefly presented pictures to object categories. Each trial was presented as follows: (a) a fixation point (+) was presented in center screen for 500 ms, (b) a picture (e.g., a dog) was presented for 250 ms, (c) The instruction “Which category was the object from?” appeared at the top center of the screen, and two category options were displayed (e.g., F = animal/J = musical instrument). Participants were instructed to use the ‘F’ and ‘J’ keyboard keys to select the correct option. No time limit was imposed on participants to respond, and the choice categories remained on the screen until a keypress was made. (d) Finally, there was a 1,000-ms blank screen prior to the start of the next trial. There were 30 randomized trials in total, plus 5 practice trials.
Interval testing
The interval between the initial and second study phases was 60 minutes. The following battery of tests was administered: (a) Demographic and health questionnaire, (b) Near Vision Test, (c) Wechsler Test of Adult Reading, (d) Wechsler Adult Intelligence Scale–III (WAIS-III) subtests: Vocabulary and Digit Symbol Substitution, (e) Mini Mental State Exam (older adults only). Breaks were provided.
Second study
Next, participants performed the second study phase, which was identical in format to the initial study task, but comprised a different set of 30 critical items.
CID-R test
Immediately following the second study phase, participants were given instructions for the CID-R task. Participants were not informed of this task in advance. Each trial consisted of a speeded masked-picture identification in which response times (reaction times [RTs]) were measured, and a recognition judgment. Each trial was self-initiated by the participant, and began with the identification task: A mask was initially presented in center screen for 500 ms. A picture (old or new) was then presented for 17 ms, followed immediately by the mask for 233 ms (making a 250-ms block). These block presentations were repeated, with the duration of picture presentations increasing by 17 ms on every alternate block while the total block duration remained constant, thus making the picture gradually more visible (
The recognition segment of the trial immediately followed each identification. The picture was presented once more, and participants were required to make a judgment as to whether they thought it was shown in either of the study phases using a 6-point scale where 1 = very sure no; 2 = fairly sure no; 3 = guess no; 4 = guess yes; 5 = fairly sure yes; 6 = very sure yes. No time limit was imposed in making recognition judgments, and no feedback was provided. There were 120 randomized trials in total—60 old (30 items from each study phase) and 60 new.
In this and subsequent experiments, an alpha level of .05 was used, and all t tests were two-tailed unless otherwise stated.
Study phases
Mean categorization accuracy was at 98.3% (SD = 2.29) for young and 96.5% (SD = 4.77) for older adults on the initial study phase, and 97.7% (SD = 3.26) for young adults and 98.5% (SD = 2.53) for older adults on the second study phase. Performance was not statistically different between groups in either phase: t(38) = 1.55, p = .13, and t = 0.90, p = .37, for the initial and second study phases, respectively. In this and subsequent experiments, items associated with incorrect study phase responses were removed from further analysis.
Recognition
Ratings 4–6 (“yes” – old) and 1–3 (“no” – new) on the 6-point scale were collapsed. For each participant, the proportion of hits (old pictures judged old) and false alarms (new pictures judged old) were used to calculate d′ (
Discrimination was significantly greater than chance (i.e., d′ > 0) for young and older adults, for items studied immediately prior to testing and those studied 60 min prior to testing (all ts(19) > 7, ps < .001, d′s > 1.72). There was a significant main effect of age group, F(1, 38) = 4.26, p = .04, ηp
Priming
The following steps were performed on each participant’s raw RT data (
Priming was strong and significantly above chance (i.e., >0 ms) for items studied immediately prior to testing, t(19) = 3.68, p = .002, and t(19 = 2.79, p = .01, for young and older adults, respectively), and items studied 60 min prior to testing, t(19) = 4.60, p < .001, and t(19 = 2.78, p = .01, for young and older adults, respectively, all d′s > 0.62). However, a repeated measures ANOVA with the between-subjects factor age group revealed no significant main effect of age group, F(1, 38) = 1.78, p = .19, or delay, F(1, 38) = 0.02, p = .89, and no significant interaction, F(1, 38) = 0.04, p = .85.
Recognition memory was reduced by age and delayed testing, while priming was not significantly affected. There was, however, a clear numerical trend—priming was lower in older adults compared with young, so we are reluctant to conclude that priming is preserved in old age. There are two possible explanations for this pattern (other than it being because of sampling error): First, there is a genuine decline in priming with age which this experiment failed to detect statistically, and second, priming was reduced in older individuals compared with young because of explicit contamination in the priming (CID) task.
Participants may use explicit processing in an implicit test if they become aware that some items were previously studied (termed test awareness or awareness), and such a strategy is said to “contaminate” the priming measure. In the CID-R paradigm, participants are made aware at test that some items were shown at study, so they may attempt to retrieve study items from memory in an effort to facilitate their identifications of the objects. If such a strategy can affect priming (e.g., by reducing identification speeds of old items, and/or increasing identification speeds of new items), it is likely to be of a greater benefit to the performance of young individuals, because of their superior explicit memory. That is, explicit processing is more likely to result in boosted priming in young individuals (see
All aspects of the design and procedure were the same as in Experiment 1, except that the CID and recognition tasks were presented separately, and we introduced a post-test awareness questionnaire. Thus, there were 6 distinct phases in this experiment: the initial study phase, a 60-min interval, the second study phase, the CID task, the recognition task, and finally the awareness questionnaire. The purpose of separating the CID and recognition phases was to minimize test awareness (and thus the likelihood of explicit processing) in the priming phase. We assumed that participants would be less likely to become aware in the CID task when no reference is made to the prior study episode and when they are not required to make a recognition judgment after every identification trial. Observing a similar age-differential pattern of priming as in Experiment 1 would suggest that the effect is not because of differences between groups in the successful use of an explicit strategy.
Participants
Eighteen young (seven men) and 18 older (two men) adults participated for payment of £5. The young adults were again recruited through the UCL participant database, and the older adults through the U3A. All were native English speakers who reported good health. Participant demographic information is summarized in
Materials and procedure
The picture stimuli, categories, and priming mask were the same as those used in Experiment 1, and the experimental procedure was the same, except that the CID and recognition tasks were presented separately as described above. All participants performed the CID task prior to the recognition task so as to maintain low levels of test awareness in the priming phase. Different critical items were presented in the CID and recognition tasks as we found ceiling recognition performance in a pilot study that used the same items in both phases. Thirty pictures from each study phase later served as old items in the CID task, and an additional 30 pictures which were included in the initial study phase served as old items in the recognition task, but were not presented in the CID phase. There were 60 new items in the CID task, and 30 in the recognition task.
At the end of the experiment, participants completed a questionnaire to gauge their awareness during the CID phase. The questionnaire was similar to that introduced by
Study phases
Categorization accuracy was at 98.4% correct for both young and older adults on the initial study phase (young SD = 1.93; older SD = 2.25), and at 98.7% (SD = 2.60) for young, and 99.1% (SD = 1.92) for older adults on the second study phase. Performance was not statistically different between groups in either study phase (immediate study: t(34) = 0.08, p = .94; delayed study: t(34) = 0.49, p = .63.
Recognition
Recognition (
Priming
Priming (
Post-test awareness
Ten out of 18 young participants (55.5%), and 9 out of 18 older participants (50%) were classified as aware during the CID phase. Collapsed across immediate and delayed items, priming did not significantly differ between aware (.12) and unaware (.13) young participants, t(34) = 0.21, p = .84, or aware (.08) and unaware (.08) older participants, t(34) = 0.14, p = .89. There was also no significant difference between aware young versus older participants, t(36) = 0.51, p = .61, or unaware young versus older participants, t(32) = 0.92, p = .36. It should be noted that, because participants completed the questionnaire after the task was completed in its entirety, their recollection of the awareness experienced during the CID phase may have been distorted, and more participants may have actually been unaware during this phase than is reflected here.
In sum, we replicated the results of Experiment 1—recognition was reliably reduced by age, and priming was numerically lowered. To test the possibility that the age difference in priming is genuine but failed to reach significance because of low power, we increased power by pooling and reanalyzing the data from our experiments.
Reanalysis of pooled priming data
This analysis included the data from Experiments 1 and 2, as well as that of an additional experiment. The latter was almost identical to Experiment 1, hence only a brief outline is presented here. We included these data to increase statistical power as much as possible.
Across experiments, we pooled the priming scores for young and older individuals for immediate and delayed items (n = 58 per group).
Critically, the analysis confirms a reliable reduction in priming as a function of age (46% reduction collapsed across immediate and delayed items). Although the effect size is small, the findings are of considerable importance, as noted in the Introduction. If levels of priming in young and older individuals were equivalent, this would strongly suggest that priming and recognition are driven by distinct memory systems. In contrast, the results are consistent with the single-system view which predicts an age effect on priming that is weaker than that on recognition because of the lower reliability of priming measures. We estimated the reliability of the recognition and priming tasks across experiments using split-half correlations (see
Measure reliability
We computed two scores for recognition (d′) and priming (proportion) for each participant by extracting odd and even test trials. We expected the correlation between scores to be larger in recognition than priming, and this was observed in all cases (
It should be noted that these split-half correlations are merely reliability estimates and are likely to be noisy because of the small samples. They serve to demonstrate that the priming index is statistically less reliable than the recognition measure, as predicted by the single-system model. It is noteworthy, however, that many of the correlations for the priming measure were very low or even negative, and one might wonder how this is possible in a measure that plainly—at the aggregate level—captures a meaningful and robust construct. If, as assumed by the model, priming consists of a fixed, memorial, component as well as nonmemorial noise, then the pattern of data is not so surprising. For instance, the fixed component could be fairly similar across both trials and participants, yielding a strong aggregate priming effect. If at the same time the noise component is uncorrelated across trials and participants, then reliability measured across odd and even test trials will be low or even zero. It will be an important question for future research to analyze reliability data in other types of priming or implicit memory measures (see
Model analysis
We fit the Berry et al. single-system model to the data of Experiment 1 in order to gain further insight into the age effect in priming.
These observations provide evidence that low measure reliability coupled with low statistical power can mask a genuine reduction in priming with age. This has substantial implications for prior studies which have reported evidence of spared priming in old age. However, the conclusion that priming is reduced by age rests crucially on eliminating the possibility that our priming measure was contaminated by explicit processing. As outlined previously, if explicit processing in the CID task affects priming, it is likely to be of a greater benefit to the performance of young adults, and thus could explain the age effect. Because test awareness is a necessary condition for the use of explicit processing, in Experiment 2 we attempted to reduce awareness in the priming task by separating the CID and recognition phases. The results were identical to Experiment 1 when participants were test aware and the CID and recognition tasks were presented concurrently trial-by-trial. It therefore seems unlikely that the reliable age difference in priming we report was driven by explicit contamination, but we nevertheless conducted further experiments to clarify whether explicit processing in the CID task can enhance priming in young individuals.
We attempted to create optimal conditions for the successful use of an explicit strategy in the CID task. Groups of Informed participants were told prior to each CID trial whether the next item to be identified was previously studied (cued “old”) or new (cued “new”), and they were encouraged to use this information to help them identify the objects. The cues enabled participants to search memory of the previously studied items on appropriate trials (i.e., those cued “old” and not those cued “new”), and we were interested in the effect on identification speeds and priming in comparison to Uninformed participants who received no explicit information and were rigorously monitored for spontaneous test awareness. If explicit processing boosts performance in the CID task (e.g., by reducing identification times for old items), then we expect to see greater priming in Informed participants.
In Experiment 3b Informed participants were also given category information ahead of each old-item trial (e.g., “old—animal”). Thus these participants were guided to explicitly search memory of a particular (small) set of previously studied items, which arguably provides the best possible opportunity for them to produce a rapid identification time.
In Experiment 3a, we also varied the ratio of old to new test trials—half the participants were exposed to a high proportion of old trials (80% old and 20% new), and half to a low proportion (20% old and 80% new) with the assumption that this would create further differences in test awareness in the Uninformed group (for a similar manipulation see
Participants and design
A total of 107 first year undergraduate students from UCL took part in Experiment 3a as part of a course requirement. There were 24 men and 83 women with an overall mean age of 18.7 (SD = 0.8). The experiment used a 2 (Informed vs. Uninformed) × 2 (High vs. Low proportion old trials) between-subjects design, and participants were randomly distributed among the conditions—Informed High (n = 26), Informed Low (n = 27), Uninformed High (n = 27), Uninformed Low (n = 27). In Experiment 3b, there were 32 participants (11 men) with an overall mean age of 22.7 (SD = 3.3). All were UCL students who participated for a small payment. Participants were equally divided into the Informed and Uninformed groups.
Materials and procedure
In Experiment 3a, 120 critical pictures were presented at study and 150 in the CID phase. In the High conditions, all the pictures presented at study were shown again at test (old items), along with an additional 30 new items. In the Low conditions, 30 old items were presented at test, along with 120 new items. Five sets of 30 items were rotated among old/new status. In Experiment 3b there were 60 critical study trials and 120 CID trials (60 old and 60 new). There were six object categories in total (animals, clothing, electrical appliances, fruit and vegetables, kitchen utensils and furniture), thus in both conditions, 10 items within each category were previously studied and 10 were new. Two sets of items were rotated.
The procedure for the study and CID phases was the same as described previously, with the exception that, for participants in Informed groups, the word “old” or “new” was presented in center screen for 2000 ms prior to the start of each trial and participants were instructed to try to use the cues to help them identify the objects. Informed participants in Experiment 3b were also given a category cue prompt on old trials (e.g., “old—animal”; on new trials participants were just prompted with the word “new”). Participants in Uninformed groups witnessed a fixation cross for 2,000 ms prior to the start of each trial, and were not informed that some items were previously studied. They were given the awareness questionnaire described previously at the end of the experiment.
Study phase
Categorization accuracy ranged from 95.7% to 98.3%, and performance did not significantly differ between groups in either experiment (greatest t = 1.51, p = .14).
Priming and post-test awareness
Priming was significantly greater than chance in all groups (all ts > 2, ps < .05, all d′s > 0.46). A two-way ANOVA indicated no main effect of informing participants in Experiment 3a, F(1, 103) = 0.11, p = .74 (
Of the participants in the Uninformed groups in Experiment 3a, 25/27 (92.6%) in the High condition, and 14/27 (51.9%) in the Low condition were deemed test aware. Priming in these participants did not significantly differ from that in unaware participants (High: aware M = .09, unaware M = .11, t(25) = 0.18, p = .86; Low: aware M = .06, unaware M = .05, t(25) = 0.33, p = .74). Eight out of 16 (50%) participants in the Uninformed group in Experiment 3b were deemed aware, but, again, priming did not significantly differ between aware (.10) and unaware (.11) participants, t(14) = 0.48, p = .64.
Providing old/new status and category information about items yields no speeding of RTs or enhancement of priming relative to uninformed conditions, but a stronger test is to compare a correctly informed condition with a misinformed condition. If explicit processing can affect priming then we would expect correct cues (e.g., “old” before an old picture) to induce particularly faster identifications relative to incorrect cues (e.g., “new” before an old picture), in which participants would be positively discouraged from engaging in a search of explicit memory. As such, we compared identification times in the CID task in two groups of participants who received incorrect cues on a subset of trials (the majority of items were correctly cued—90 out of 120 total—so as to ensure the overall validity of the cues). Participants were given an ‘old/new’ prompt before each trial as described previously, but one group (Misinformed New) received “old” cues prior to 30 (out of 60 total) new-item trials, and the other group (Misinformed Old) received “new” cues prior to 30 (out of 60 total) old-item trials. The critical comparisons were the identification speeds for items correctly cued relative to those incorrectly cued.
Thirty-two UCL students (15 men) with an overall mean age of 22.9 years (SD = 3.6) participated in this experiment for a small payment. They were equally divided between the two groups. The stimuli were those used in Experiment 3b, and in total there were 60 study trials and 120 CID trials (60 old and 60 new).
Study phase performance (categorization accuracy) did not significantly differ between groups (M = 95.8%; SD = 3.9, and M = 97.9%; SD = 4.7, for the Misinformed New and Misinformed Old groups, respectively), t(30) = 1.38, p = .18.
RTs were recorded for items for which participants received correct information (correctly cued old and correctly cued new items) and those for which they received incorrect information (incorrectly cued new items in the Misinformed New group and incorrectly cued old items in the Misinformed Old group;
In sum, providing participants with explicit information (correct or incorrect) does not affect the speed of identification of items in the CID task, nor the magnitude of priming. Even with a cue that should have created a small search set in explicit memory (Experiment 3b), no benefit to identification speed was observed.
We investigated whether implicit memory is preserved in normal aging despite reduced explicit memory. To overcome the problems associated with measuring these memory phenomena in separate experimental phases, each test item was appraised for a recognition and priming judgment in a single trial (Experiment 1). Recognition memory was significantly lower in older relative to young adults, and priming was numerically reduced. These observations were replicated in Experiment 2 when the priming and recognition tasks were presented separately to reduce test awareness. In both experiments the priming task was statistically less reliable than recognition, thus it was more difficult to detect effects in priming. However, the age difference in priming reached significance in a combined analysis of our data which increased statistical power. The findings present a challenge to the notion of multiple memory systems, as the age-related dissociation between recognition and priming is often cited as evidence for independent systems. Moreover, the Berry et al. single-system model provided an excellent fit to the data of Experiment 1.
Other studies have observed an age effect in priming, but this is often attributed to explicit contamination. Explicit processing during an implicit test could feasibly contribute to an age effect in priming, because young and older adults may differ in their ability to use such a strategy.
Several other studies have examined the effect of test awareness and explicit processing on priming in young individuals, but results have been mixed.
Some may argue that explicit processing may have hindered the performance of older individuals in the CID task, resulting in lower priming in this group. This is unlikely given the evidence that the CID task is unaffected by both optimal and adverse explicit processing: performance was not improved when correct explicit information was provided to support performance (Experiments 3a and 3b), and it was not worsened when explicit processing was disadvantageous because incorrect cues were provided (Experiment 3c). Thus, although some priming tasks may be more susceptible to the effects of explicit contamination, we suggest that this does not pose a concern in the CID-R task. As
The current study revealed an effect of varying the number of old trials in the priming task (Experiment 3a). A high proportion of old trials resulted in stronger priming relative to a low proportion. A handful of prior studies have also varied the ratio of old/new test items, but because this has typically been done to bolster an instructional manipulation (i.e., uninformed participants are exposed to fewer old trials), it is impossible to unravel the differential contributions of the factors to outcomes.
The present investigation leads to the conclusion that the age-related reduction in priming is genuinely the result of a decline in memory function rather than explicit contamination in the priming task. The issue of ‘implicit contamination’ is also interesting—that is, the extent to which fluent processing because of prior exposure to test stimuli affects performance on explicit tasks. Generally, it is believed that the contribution of fluency from priming to recognition memory in the CID-R paradigm is very minor (
Finally, the delay effects in Experiment 1 deserve some consideration. We observed a weak delay effect on recognition in both groups (significant only at the one-tailed level). Priming was unaffected by the delay, but the small effect size coupled with the lower reliability of the CID task renders this unsurprising. The numerical priming patterns mirrored those in recognition, meaning it would be difficult to interpret this finding as support for multiple-systems. Furthermore, the single-system model predicted a very small change in priming across the delay.
To conclude, we provide evidence that priming and recognition are reduced by normal aging on a task that is immune to explicit contamination. This suggests that normal age-related memory decline leads to the compromise of a single system that supports both explicit and implicit expressions of memory, and accordingly our formal model fits the data closely.
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A full description of the single-system model and data fitting procedures is given in
Each item’s value of f is also used to calculate the item’s priming measure (this is what makes the model a single-system model). Importantly, f is combined with a different, independent source of noise, and is scaled to produce an identification RT. Greater values of f are assumed to produce shorter identification RTs:
A consequence of modeling recognition and priming in this manner is that changes in μold will tend to produce changes in both recognition and priming. However, because of the different ways in which recognition and priming measures are generated, and because of the greater variance of the noise typically associated with priming, the effect of changing μold will tend to be greater for recognition than priming.
The model was fit to each individual’s data in Experiment 1, using the data from each trial at test. Immediate and delayed items were modeled by assuming that there were separate distributions of f for each type of item. There were six free parameters: These were μImmediate, the mean f of Immediate items; μDelay, the mean f of Delayed items; b, the RT intercept; s the rate of change of RT with f; σp, the variance of the noise associated with the priming measure, and C, the old/new recognition judgment criterion. Certain parameter values were fixed (as in
The likelihood for a pair of observations, Z and RT, where Z denotes the recognition judgment on a given trial and RT denotes the identification RT, is given as
An optimization routine was used to find the parameter values that maximized the log likelihood of the model given the data. The summed log likelihoods across trials and participants are given in
The expected values for recognition and priming for each participant were calculated using the formulae in
Submitted: April 10, 2012 Revised: January 3, 2013 Accepted: January 3, 2013