Lesser neural pattern similarity across repeated tests is associated with better long-term memory retention.
Open accessAbstract
Encoding and retrieval processes enhance long-term memory performance. The efficiency of encoding processes has recently been linked to representational consistency: the reactivation of a representation that gets more specific each time an item is further studied. Here we examined the complementary hypothesis of whether the efficiency of retrieval processes also is linked to representational consistency. Alternatively, recurrent retrieval might foster representational variability--the altering or adding of underlying memory representations. Human participants studied 60 Swahili-Swedish word pairs before being scanned with fMRI the same day and 1 week later. On Day 1, participants were tested three times on each word pair, and on Day 7 each pair was tested once. A BOLD signal change in right superior parietal cortex was associated with subsequent memory on Day 1 and with successful long-term retention on Day 7. A representational similarity analysis in this parietal region revealed that beneficial recurrent retrieval was associated with representational variability, such that the pattern similarity on Day 1 was lower for retrieved words subsequently remembered compared with those subsequently forgotten. This was mirrored by a monotonically decreased BOLD signal change in dorsolateral prefrontal cortex on Day 1 as a function of repeated successful retrieval for words subsequently remembered, but not for words subsequently forgotten. This reduction in prefrontal response could reflect reduced demands on cognitive control. Collectively, the results offer novel insights into why memory retention benefits from repeated retrieval, and they suggest fundamental differences between repeated study and repeated testing. SIGNIFICANCE STATEMENT: Repeated testing is known to produce superior long-term retention of the to-be-learned material compared with repeated encoding and other learning techniques, much because it fosters repeated memory retrieval. This study demonstrates that repeated memory retrieval might strengthen memory by inducing more differentiated or elaborated memory representations in the parietal cortex, and at the same time reducing demands on prefrontal-cortex-mediated cognitive control processes during retrieval. The findings contrast with recent demonstrations that repeated encoding induces less differentiated or elaborated memory representations. Together, this study suggests a potential neurocognitive explanation of why repeated retrieval is more beneficial for long-term retention than repeated encoding, a phenomenon known as the testing effect.
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Retrieval practice reduces demands on left prefrontal brain regions implicated in cognitive control functions.
“In our prior fMRI studies we found support for that retrieval practice, as measured across three consecutive tests with (Wiklund-Hörnqvist et al., 2017) or without feedback (Karlsson Wirebring et al., 2015), reduces demands on left prefrontal brain regions implicated in cognitive control functions.”
From Retrieval Practice Is Effective Regardless of Self-Reported Need for Cognition - Behavioral and Brain Imaging Evidence (2022) · cites this paper as Karlsson Wirebring et al., 2015
The Day 1 BOLD signal repetition-effects section reports a decline in left dorsolateral prefrontal activity across repeated tests for words later remembered and suggests this could reflect reduced demands on cognitive control. The citing sentence presents that interpretation as a finding without noting that the effect did not pass the paper’s chosen statistical threshold or that the decline differed by later retention. (LLM, conf=0.88)
Experimental — accuracy not yet measuredTwo studies observed greater activations related to memory enhanced by the testing effect in parietal, frontal, insular, temporal, and thalamic regions.
“Two studies observed greater activations related to memory enhanced by the testing effect in parietal, frontal, insular, temporal, and thalamic regions (Keresztes et al., 2014; Wirebring et al., 2015).”
From Neural Correlates of Long-Term Memory Enhancement Following Retrieval Practice (2021) · cites this paper as Wirebring et al., 2015
The Day 1 BOLD results report greater activity in parietal and medial prefrontal regions for repeatedly retrieved words retained one week later. The Day 7 results also report greater activity in parietal, temporal, and frontal regions. Our copy does not report insular or thalamic activations for this comparison; those parts of the two-study claim are not supported by this source. (LLM, conf=0.85)
Experimental — accuracy not yet measuredWirebring et al. (2015) showed reduced prefrontal cortex activation during repeated correct retrieval at the encoding phase tests, only for words subsequently remembered but not subsequently forgotten at the final test.
“This study showed reduced prefrontal cortex activation during repeated correct retrieval at the encoding phase tests, only for words subsequently remembered but not subsequently forgotten at the final test.”
From Neural Correlates of Long-Term Memory Enhancement Following Retrieval Practice (2021) · cites this paper as Wirebring et al., 2015
The Abstract reports decreasing dorsolateral prefrontal BOLD response across repeated successful Day 1 retrievals for words remembered on Day 7, but not for words forgotten. However, the Day 1 BOLD signal repetition-effects section says the interaction did not pass the chosen statistical threshold and should be considered preliminary; the claim omits that uncertainty. (LLM, conf=0.85)
Experimental — accuracy not yet measuredThe Test Group also showed greater activation for successful recall in bilateral putamen, which is consistent with a study examining successful recall for studied and tested word pairs.
“The Test Group also showed greater activation for successful recall in bilateral putamen, which is consistent with a study examining successful recall for studied and tested word pairs (Wirebring et al., 2015).”
From Neural Correlates of Long-Term Memory Enhancement Following Retrieval Practice (2021) · cites this paper as Wirebring et al., 2015
The Day 7 BOLD results compare successfully recalled with forgotten word pairs after repeated testing. Table 2 lists greater activity in the left putamen for that comparison, but does not list the right putamen; the cited study therefore supports the putamen finding only in part, not its bilateral extent. Our copy provides no page number for the table. (LLM, conf=0.87)
Experimental — accuracy not yet measuredThe position of the correct answer relative to the lures was systematically varied to avoid item order effects.
“The position of the correct answer relative to the lures systematically varied to avoid item order effects (see Karlsson Wirebring et al., 2015; Wiklund-Hörnqvist et al., 2017, 2020; Jonsson et al., 2020; Stillesjö et al., 2021).”
From Retrieval Practice Is Effective Regardless of Self-Reported Need for Cognition - Behavioral and Brain Imaging Evidence (2022) · cites this paper as Karlsson Wirebring et al., 2015
Wirebring et al. (2015) evaluated whole-brain activations for repeatedly tested word pairs that were subsequently remembered vs. forgotten but did not compare tested vs. studied-only word pairs that were correctly recalled.
“For example, Wirebring et al. (2015) evaluated whole-brain activations for repeatedly tested word pairs that were subsequently remembered vs. forgotten but did not compare tested vs. studied-only word pairs that were correctly recalled.”
From Neural Correlates of Long-Term Memory Enhancement Following Retrieval Practice (2021) · cites this paper as Wirebring et al., 2015
Greater variability in patterns of activation in parietal cortex across retrieval tests was associated with subsequent memory success.
“One study has provided a potential mechanistic understanding of parietal cortex contribution to repeated testing whereby greater variability in patterns of activation in parietal cortex across retrieval tests was associated with subsequent memory success (Wirebring et al., 2015).”
From Neural Correlates of Long-Term Memory Enhancement Following Retrieval Practice (2021) · cites this paper as Wirebring et al., 2015
Our findings regarding the decreased activation of prefrontal areas in the Test Group for correct retrieval at the final test are consistent with the results of Wirebring et al. (2015).
“Our findings regarding the decreased activation of prefrontal areas in the Test Group for correct retrieval at the final test are consistent with the results of Wirebring et al. (2015).”
From Neural Correlates of Long-Term Memory Enhancement Following Retrieval Practice (2021) · cites this paper as Wirebring et al., 2015
This reduced reliance on the frontal cortex for successful retrieval in the Test Group is consistent with results from Wirebring et al. (2015).
“This reduced reliance on the frontal cortex for successful retrieval in the Test Group is consistent with results from Wirebring et al. (2015).”
From Neural Correlates of Long-Term Memory Enhancement Following Retrieval Practice (2021) · cites this paper as Wirebring et al., 2015
Successful retrieval at the final test is related to reduced prefrontal activation during repeated correct retrieval during encoding.
“Thus, successful retrieval at the final test is related to reduced prefrontal activation during repeated correct retrieval during encoding.”
From Neural Correlates of Long-Term Memory Enhancement Following Retrieval Practice (2021) · cites this paper as Wirebring et al., 2015
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References 61 · Cited by 65
- Authors
- Karlsson Wirebring, L., Wiklund-Hornqvist, C., Eriksson, J., Andersson, M., Jonsson, B., & Nyberg, L.
- Affiliations
- Umeå University (SE)
- Venue
- Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2015-07-01
- Volume
- 35
- Issue
- 26
- Pages
- 9595-9602
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6605150
- OpenAlex
- W1627964365
- Cited by
- 65
- References
- 61
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 5 · 2023: 4 · 2022: 6 · 2021: 10 · 2020: 11 · 2019: 7 · 2018: 6 · 2017: 7 · 2016: 5
- FWCI
- 3.61
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- DiVA at Umeå University (Umeå University) (submittedVersion, other-oa)
- Funders
- Knut och Alice Wallenbergs Stiftelse
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Cognitive Functions and Memory
- Keywords
- testing effect, long-term memory retention, superior parietal cortex, dorsolateral prefrontal cortex, cognitive control, memory encoding, BOLD signal, word pair learning, pattern similarity
- MeSH terms
- Adult, Analysis of Variance, Association Learning, Brain, Brain Mapping, Female, Humans, Image Processing, Computer-Assisted, Magnetic Resonance Imaging, Male, Oxygen, Reaction Time, Retention, Psychology, Time Factors, Vocabulary, Young Adult, Memory, Long-Term
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