The Mitigating Effect of Repeated Memory Reactivations On Forgetting
The Mitigating Effect of Repeated Memory Reactivations On Forgetting
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Memory reactivation is a process whereby cueing or recalling a long-term memory makes it enter a new active and labile state.
Substantial evidence suggests that during this state the memory can be updated (e.g., adding information) and can become more
vulnerable to disruption (e.g., brain insult). Memory reactivations can also prevent memory decay or forgetting. However, it is
unclear whether cueing recall of a feature or component of the memory can benefit retention similarly to promoting recall of the
entire memory. We examined this possibility by having participants view a series of neutral images and then randomly assigning
them to one of four reactivation groups: control (no reactivation), distractor (reactivation of experimental procedures), component
(image category reactivation), and descriptive (effortful description of the images). The experiment also included three retention
intervals: 1 h, 9 days, and 28 days. Importantly, the participants received three reactivations equally spaced within their respective
retention interval. At the end of the interval, all the participants were given an in-lab free-recall test in which they were asked to
write down each image they remembered with as many details as possible. The data revealed that both the participants in the
descriptive reactivation and component reactivation groups remembered significantly more than the participants in the control
groups, with the effect being most pronounced in the 28-day retention interval condition. These findings suggest that memory
reactivation, even component reactivation of a memory, makes memories more resistant to decay.
npj Science of Learning (2018)3:9 ; doi:10.1038/s41539-018-0025-x
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Psychology Department, Trent University, Peterborough, ON, Canada
Correspondence: Hugo Lehmann ([email protected])
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Fig. 2 Mean (±SEM) number of correctly remembered images during the free-recall test for each reactivation group across all three retention
intervals: 1 h, 9 days, and 28 days. Retention performance significantly decreased across retention intervals (ps < 0.05), suggesting time-
dependent forgetting. Yet, overall, the participants in the Descriptive and Component groups recalled significantly more images than the
participants in the Distractor group (ps < 0.05). More strikingly, in the 28-day condition, the participants in both the Descriptive and
Component groups recalled significantly more images than the participants in the Distractor and Control groups (ps < 0.05), with an relative
enhancement exceeding 59%. Hence, the descriptive and component reactivations successfully mitigated forgetting on this index of memory
Fig. 3 Mean (±SEM) number of correctly remembered details during the free-recall test for each reactivation group across all three retention
intervals: 1 h, 9 days, and 28 days. Retention performance significantly decreased across retention intervals (ps < 0.05), again suggesting
forgetting over time. However, overall, both the Descriptive and Component groups recalled significantly more details than the participants in
the Distractor group (ps < 0.05). At the longest retention interval, the participants in both the Descriptive and Component groups recalled
significantly more details than the participants in both the Distractor and Control groups (ps < 0.05) and the relative retention enhancement
exceeded 100%. Thus, the descriptive and component reactivations successfully mitigated forgetting on this memory measure as well
Correct details per image determine whether the reactivation method increased the quality
The total number of details recalled may be confounded with the of the retained mnemonic representation. The ANOVA revealed a
number of images recalled, therefore Fig. 4 shows the average significant main effect of interval, F (2, 155) = 13.97, p < 0.001, and
number of details recalled per correctly recalled image for each a significant main effect of reactivation, F (3, 155) = 2.94, p = 0.04,
group across all three retention intervals. This was conducted to but no interaction, F (6, 155) = 0.59, p = 0.74.
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Fig. 4 Mean (±SEM) number of correctly remembered details per recalled image during the free-recall test for each reactivation group across
all three retention intervals: 1 h, 9 days, and 28 days. This index is more revealing of the quality/precision of the memory for each recalled
image. In the 28-day condition, the participants in the Descriptive group recalled significantly more details per image than the participants in
the Distractor and Control groups (ps < 0.05), a finding that was not observed in the Component group. Hence, only the descriptive
reactivation improved precision retention
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the other retention intervals using pairwise comparisons to results of our Descriptive group support this view, the component
examine group differences. Both the Descriptive and the reactivation findings, in which the reactivation process differs from
Component groups remembered significantly more images than that of the final test, do not. The component findings suggest that
the Distractor group (ps < 0.05) and the no reactivation Control promoting reactivation of the target memories, even in a different
group (ps < 0.05). Similarly, the Descriptive and Component retrieval form, is sufficient to promote long-term retention. Our
groups remembered significantly more correct details than the combined descriptive and component reactivation findings may
Distractor and no reactivation Control groups (ps < 0.05). These provide better support for theories such as the Elaborative
findings suggest that both types of reactivation mitigated Retrieval Hypothesis or the Construction-Integration Model, which
forgetting. The Descriptive and Component groups did not posits that retrieval, regardless of setting and features, causes
significantly differ from each other (ps > 0.05) nor did the widespread network activation that increases the number of
Distractor and no reactivation Control groups (ps > 0.05) on either traces supporting the memory and/or promotes more pathways to
of the two measures. In addition, the participants in the it.34,39,40 With this greater network, access to the target memories
Descriptive group remembered significantly more details per at the time of testing is facilitated and benefits retention
image than participants in the Distractor group (p < 0.05). There performance.39
was no effect of reactivation group on number of false images or Our findings also extend our knowledge about the Testing
false details recalled (ps > 0.05). Effect on other fronts. First, our demonstration that reactivations
To better depict the magnitude of the reactivation benefits on can improve memory by mitigating forgetting up to a month after
retention, we transformed the absolute retention score of each the initial learning goes beyond the typical retention intervals, of
participant in the Descriptive and Component groups into a hours to a few days, examined in most studies.35,41,42 Second,
relative score using the no reactivation Control group average learning only occurred once without the possibility of additional
(change relative to Control). This revealed that image recall was study in our experimental design, whereas other studies often
enhanced by 58.8% (SEM = 18.4) for the Descriptive group and intermix new study episodes with their reactivations.41,43,44 Third,
67.2% (SEM = 23.9) for the Component group. Similarly, for both the Testing Effect is typically demonstrated using word lists,45
groups the number of details recalled increased by 134.5% (SEM facts,46 word pairs,34,39 prose,47 and course material.41,43,44 Here,
= 27.34) and 113.1% (SEM = 43.4), respectively. The correct details we show that the benefits of reactivations on long-term retention
per image was also increased by 44.5% (SEM = 19.4) for the also applies to visual stimuli, such as pictures of scenes without
Descriptive group, but only by 16.6% (SEM = 17.6) for the the use of verbal information.48
Component group. All these increases were significantly above We believe that the reactivations in the current study, whether
what would be expected by chance (ps < 0.05), with the exception descriptive or component, strengthened long-term memory
of the Component group on the correct details per image (28 days) by initiating cellular/synaptic reconsolidation bouts.
measure (p > 0.05). Importantly, the Distractor group did not have When a memory is initially consolidated, it undergoes protein
any significant relative increases in performance on these synthesis resulting in neuronal changes that convert the memory
measures (ps > 0.05). Actually, all relative changes were negative to long-term storage.49,50 This process, called cellular consolida-
for this group. tion, takes place hours after an initial learning period and
strengthens the memory trace. Despite the original belief that
this was a one-time process,3,4 it has been convincingly
DISCUSSION demonstrated that each time a memory is reactivated it under-
The current study examined whether memory reactivations goes a new bout of consolidation.5 Though these reconsolidation
strengthen memory as indicated by mitigated forgetting. Impor- bouts involve plastic changes that differ from those of the initial
tantly, the effects of repeated memory reactivations on long-term consolidation,15,51 they contribute to memory maintenance.9,52 In
retention were assessed using two different approaches: descrip- contrast, the reactivation-induced memory enhancement within
tive and component reactivations. The descriptive reactivations the 1-h condition cannot be explained by the same plastic
required recall of as much information as possible about the changes because the interval was too short to benefit from
viewed images. The component reactivations, on the other hand, protein thesis. The reactivations, within this retention interval,
required partial recall of categorical features of the previously likely promoted short-term synaptic facilitation mechanisms
viewed images, with no detailed description. Both types of known to support working memory.53
reactivations mitigated forgetting. The benefits of the reactiva- The current reactivation findings have other important implica-
tions, however, were the most prominent at the 28-day interval tions for understanding the neural organization of long-term
when the memories were the weakest. In this instance, image memory. For instance, it has been strongly argued that memories
recall, relative to control performance, was increased by 59% and initially dependent on the hippocampus, such as episodic
67%, respectively, for the Descriptive and Component groups. The memories, become independent of the hippocampus over
relative effect was even greater for the number of recalled details time.54–56 Evidence supporting this argument comes from studies
with an increase exceeding 100% for both reactivation groups. reporting temporally graded retrograde amnesia in patients with
Thus, these findings confirm the view that reactivations hippocampal lesions, meaning that recently, but not remotely,
strengthen memories. acquired memories are lost following the damage.57,58 Distributed
The beneficial memory strengthening effects following the Reinstatement Theory, however, suggests that time may not be
descriptive reactivations are consistent with those of numerous the most critical factor involved in making memories independent
studies that have examined the Testing Effect, in which detailed of the hippocampus.59,60 With more remote memories, there are
effortful retrieval of previously studied information results in more opportunities for reactivations, and thus repeated bouts of
improved retention.34,35 Importantly, our component reactivation reconsolidation which strengthen the memory beyond the
findings add to this literature by demonstrating that cueing hippocampus. Indeed, it has been shown that repeated distrib-
category retrieval also benefits the memory. In addition, the uted reactivations can preserve a memory following hippocampal
component findings may elucidate some of the debated damage,26 but not in all situations.27 Moreover, evidence from
mechanisms supporting the Testing Effect. Transfer appropriate functional magnetic resonance imaging or functional studies in
processing has been proposed as one possible explanation for the human participants suggests that repeated retrievals (reactiva-
Testing Effect.38 This perspective suggests that effortful tions) of a memory increase neuronal activity in areas aside from
reactivation-induced retrievals must be similar in form to the final the hippocampus.24,25 Combined, the evidence from these studies
test to promote better retention performance. Although the suggest that reactivations extend the neural network supporting a
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S MacLeod et al.
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memory, and arguably did the same for the image memories in of 167. This resulted in a group sample size ranging between 12 and 16,
the current study. which is consistent with that of other studies in the field.19,29
The complex features pertaining to the images we used
provided the advantage of an in-depth recall assessment (e.g., Materials
gist vs. detailed information). The descriptive and component Twenty-six neutral images were selected from the IAPS. Specifically, all
reactivations increased the number of images and details recalled, images ranged, according to IAPS, between four and six on the emotional
suggesting improved persistence/duration of the memory. The valence dimension (M = 5.4, SD = 0.45) and below four on the emotional
number of correct details recalled per image, however, is arguably arousal dimension (M = 3.3, SD = 0.42). Nine images depicted landscapes,
a better measure of the qualitative properties (precision) of the 3 were of animals, and the other 14 images were of household objects. The
image memories and only the descriptive reactivations improved images were presented on a 15-in. Dell LED monitor, using a Dell computer
performance on this index. Thus, the descriptive reactivations and Microsoft PowerPoint 2013.
improved long-term memory for the gist as well as the content of
the images. This is consistent with the evidence suggesting that Procedure
more effortful and detailed recall shows better Testing Effect Acquisition phase. The participants were told they would view a series of
benefits,41,44 as well as the enhanced mnemonic precision images, and were asked to remember as much about each image as
reported in studies that examined the effects of reconsolidation possible. The participants sat in front of, and approximately 60 cm away
in non-human animal studies.27,28 In contrast, the component from, the monitor, and when ready, pressed the “enter” key on the
reactivation strengthened the memory for the gist of the images. computer keyboard to begin the experiment. The 26 images were
We cannot know how much of the target memory was reactivated presented individually for 10 s, with a black screen shown between each
image for 3 s.
in the component condition. However, because only one
categorical feature was cued at the time of each reactivation, Reactivation manipulation. Each participant was randomly assigned to
we can assume that the recall was partial and lacked detailed one of four different groups: Descriptive Reactivation (Testing Effect
content. The finding that a memory can be strengthened without condition), Component Reactivation (Cueing Effect condition), Distractor,
detail-specific enhancement may also lend support to the memory and Control (no reactivation).
transformation view, which states that episodic memories become The Descriptive Reactivation group received three separate memory
more semantically represented, at least in part, because of reactivations by asking them to describe the images they had previously
repeated reactivation of gist-like information.61,62 viewed. In each instance, they were asked the same question, “Please
The reactivation benefits, whether from the Descriptive or describe, in as much detail as you recall, the images you viewed in Part 1
(acquisition phase) of this experiment.” The aim of this question was to
Component group, were most prominent when contrasted with
promote explicit effortful recall of detailed information of the images,
the Distractor group than the Control (no reactivation) group. The similar to the process that is followed in studies examining the Testing
former provided a control for experimenter–participant interac- Effect.47
tions during the reactivation sessions. Perhaps reactivating The Component Reactivation group also received three separate
irrelevant information of the experimental procedures added memory reactivations, but by cueing a component/categorical feature of
“noise” to the original image memories similar to memory the images. In each instance, the participants needed to provide the
updating, meaning the incorporation of new information into number of images that included the component. The first question
the target memory. But the absence of a statistical differences participants received was, “How many images included animals? Please do
between the Distractor and Control groups as well as the null not describe the images, only state the number within the category,”
question two, “How many images included landscapes? Please do not
findings on the false memory measures fail to support this describe the images, only state the number within the category” and
argument. Most importantly, the fact that the distractor reactiva- question three “How many images include household objects? Please do
tions did not strengthen the memory of the viewed images, but not describe the images, only state then number within the category.”
that the descriptive and component reactivations did, suggests Importantly, these reactivations did not require an explicit description of
that the reactivation content needs to pertain to the target the target memory.
memory in order to enhance retention. The Distractor group received three questions related to the experi-
In conclusion, we have replicated the Testing Effect through mental procedure which were not intended to trigger image reactivation.
descriptive reactivations and, more importantly, we have shown The objective of this condition was to provide an image-irrelevant
reactivation control, meaning controlling for questioning of the partici-
that component reactivations, in which only categorical features pants during the retention phase. The first question was “What was the
are used to induce reactivation, can similarly mitigate forgetting. date and time when you completed Part 1 of this experiment?” question
This suggests that an effortful description of the target memory is two, “What form did the experimenter go through with you before
not critical to enhance retention, at least gist-like information beginning the experiment?,” and question three “Please describe the
retention. In addition, the findings suggest that memory reactiva- procedure for Part 1 of this experiment.”
tion, whether descriptive or component, leads to memory The Control group did not receive any questions throughout the period
strengthening, a process commonly proposed within the memory from viewing the images to completing the recall test. The objective of this
reconsolidation literature. control condition was to examine the typical rate of forgetting.
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9-day condition: In the 9-day condition, the participants left the lab Publisher's note: Springer Nature remains neutral with regard to jurisdictional claims
after viewing the images. Two days following the acquisition phase, the in published maps and institutional affiliations.
participants were sent a reactivation question via e-mail using the SONA
system. The question differed according to the reactivation group to which
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