Cited by 79Memory Processes and InfluencesMemory and Neural MechanismsCognitive Functions and Memory

Spaced learning enhances episodic memory by increasing neural pattern similarity across repetitions

Open access
Feng, Kanyin, Zhao, Xiao, Liu, Jing, Cai, Ying, Ye, Zhifang, Chen, Chuansheng, Xue, Gui·2019·The Journal of Neuroscience

Abstract

Spaced learning has been shown consistently to benefit memory compared with massed learning, yet the neural representations and processes underlying the spacing effect are still poorly understood. In particular, two influential models (i.e., the encoding variability hypothesis and the study-phase retrieval hypothesis) could both model behavioral performance very well, but they make opposite hypotheses regarding the spacing effect9s neural mechanisms. The present study attempted to provide empirical neural evidence to adjudicate these competing hypotheses. Using spatiotemporal pattern similarity (STPS) analysis of EEG data, this study investigated whether and how repetition lags (massed/short-spaced/long-spaced) modulated the STPS9s contribution to episodic memory encoding in male and female human participants. The results revealed that greater item-specific STPS in the right frontal electrodes at 543–727 ms after stimulus onset was associated with better memory performance. More importantly, this STPS was larger under the spaced-learning condition than the massed-learning condition and partially mediated the spacing effect on memory performance. In addition, we found that massed learning was associated with stronger repetition suppression in the N400 component that reflected momentary retrieval strength, but reduced activity in the late positive component that was associated with memory retrieval. These results suggest that spaced learning improves long-term memory by increasing retrieval effort and enhancing the pattern reinstatement of prior neural representations, which may be achieved by reducing the momentary retrieval strength as the extended repetition lags might help to eliminate the residual representation in working memory. SIGNIFICANCE STATEMENT As one of the most ubiquitous and fundamental phenomena in the history of memory research, the spacing effect provides an important window into understanding how enduring memory is formed in the brain and how different practice strategies could modulate these mechanisms to affect memory performance. By leveraging the neural representational analysis on scalp EEG data, the current study provides the first empirical data to show that spaced learning enhances memory by improving the spatiotemporal similarity that occurs at a late time window. Our results support the study-phase retrieval hypothesis but not the encoding variability hypothesis and emphasize the role of neural pattern reinstatement in strengthening memory via repeated study.

AI snapshot

Written from the paper’s full text.

TL;DR

Using EEG spatiotemporal pattern similarity (STPS), this study tested whether spaced learning improves episodic memory by changing neural pattern reinstatement across repetitions. Spaced learning increased item-specific STPS in a late right frontal window, and this STPS partially mediated the spacing effect on memory.

Key findings

  • Spaced learning improved recognition memory: mean high-confidence hit rates were 40.08% (massed), 42.94% (short-spaced), and 44.75% (long-spaced); d′ was 0.41, 0.53, and 0.55, respectively.
  • Item-specific STPS in right frontal electrodes at 543–727 ms was greater for subsequently remembered than forgotten items (F(1,32)=10.98, p=0.002), with no between-item STPS difference.
  • In the 606–652 ms window, short-spaced learning produced greater within-item STPS than massed learning (t(32)=2.43, p=0.02), and this STPS partially mediated the spacing effect on memory (indirect effect=0.0047, 95% CI=0.001–0.0093).
  • Massed learning showed stronger N400 repetition suppression and reduced late positive component (LPC) activity; LPC was associated with subsequent memory but did not carry item-specific information.

Methods

  • Thirty-three healthy Chinese college students (19 females; mean age 19.8±1.8 years) studied 288 Chinese faces twice under massed (IRI 0–1 trials), short-spaced (IRI 4–8 trials), or long-spaced (IRI 94–96 trials) conditions, then completed a surprise recognition test after a 30 min distractor task.
  • EEG was recorded with a 64-channel system; STPS was computed using Pearson correlations between single-trial spatiotemporal feature vectors, converted to Fisher’s Z, and analyzed with cluster-based permutation tests.
  • Mixed-effects models and mediation analysis tested whether STPS related to subsequent memory and mediated the spacing effect, controlling for univariate ERP amplitude.

Limitations

  • The paper states that it failed to replicate the detrimental effect of long inter-repetition intervals; the long-spaced interval may not have been long enough, and the design created imbalanced temporal distributions across spacing conditions, with a significant spacing (MA vs SS) by serial position interaction (F(3,96)=2.74, p=0.048).
  • The paper states that the LPC–STPS relationship was exploratory and requires replication, and that repetition priming or N400 repetition suppression could not quantitatively predict memory performance.
  • Evident from the text: the sample was small and restricted to Chinese college students, learning used faces in a single session, and EEG has limited spatial resolution; the mediation result is correlational rather than causal.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1523/jneurosci.2741-18.2019

Cites

66 of 66 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

0 of 50 cited sources checked · 0 supported · 0 flagged

  • Findingown data

    In the right frontal cluster, there was a significant item specificity by spacing (massed vs short-spaced) interaction in the 606-652 ms time window.

    “Focusing on the right frontal cluster that showed greater item-specific STPS for remembered items than forgotten items, we found a significant item specificity by spacing (MA vs SS) interaction in the 606 -652 ms time window (F (1,32)max ϭ 13.52, F clustersum ϭ 123.89, p cluster ϭ 0.016) (Fig. 2 E, F ).”
    Quote in the paperSubstantial claim
  • Findingown data

    In this study, spaced learning (short-spaced and long-spaced) was associated with better subsequent memory performance than massed learning, as indexed by higher hit rate and discriminability (d').

    “Consistent with previous observations, the current study revealed a significant spacing effect on subsequent memory performance (Fig. 1C) (hit rate: F (2,64) ϭ 6, p ϭ 0.004; dЈ: F (2,64) ϭ 8.63, p ϭ 0.0005).”
    • Also stated in: § Results · plain
      “Compared with MA, the hit rate was significantly higher under SS (t (32) ϭ 2.5, p ϭ 0.02) and LS (t (32) ϭ 3.39, p ϭ 0.002).”
    • Also stated in: § Results · plain
      “Similarly, the dЈ was also higher under SS (0.53, t (32) ϭ 3.96, p ϭ 0.0004) or LS (0.55, t (32) ϭ 3.46, p ϭ 0.002) than MA (0.41).”
    Quote in the paperSubstantial claim
  • Findingown data

    There was no time window showing a significant difference in item specificity between massed and long-spaced learning.

    “There was no time window showing significant difference in item specificity between MA and LS.”
    Quote in the paperNot a substantial claim
  • Findingown data

    The subsequent memory effect in within-item STPS remained significant after controlling for EEG amplitude.

    “The subsequent memory effect in WI STPS remained significant after controlling the EEG amplitude ( ͑1͒ 2 ϭ 7.99, p ϭ 0.005).”
    Quote in the paperSubstantial claim
  • Findingown data

    Response consistency between the two presentations was higher under massed learning than under short-spaced and long-spaced learning.

    “Further paired sample t test revealed significantly higher consistency for MA (82.65%) than SS (76.45%) (t (32) ϭ 4.4, p ϭ 0.0001) and LS (72.41%) (t (32) ϭ 6.85, p Ͻ 0.0001) and for SS than LS (t (32) ϭ 3.35, p ϭ 0.0021)”
    Quote in the paperNot a substantial claim
  • The quote only partly states this claim. 3
  • Classified as probably not a substantial claim. 24
  • May combine two claims. 29
  • The quote only partly states this claim.

    Findingown data

    In a 543-727 ms cluster in the right frontal region, within-item STPS was greater for subsequently remembered items than forgotten items.

    “This analysis revealed a 543-727 ms cluster in right frontal region (region 2) showing a significant subsequent memory by item-specificity interaction (F (1,32)max ϭ 12.84, F clustersum ϭ 391.75, p cluster ϭ 0.03; Fig. 2 B, C).”
    • Also stated in: § Subsequently remembered items showed greater item-specific STPS · plain
      “Post hoc tests showed significantly greater WI STPS for remembered items than forgotten items (F (1,32) ϭ 10.98, p ϭ 0.002), but no difference in BI STPS (F (1,32) ϭ 0.34, p ϭ 0.56).”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Findingown data

    There was a 676-710 ms time window showing a spacing (short-spaced vs long-spaced) by item specificity interaction, but it did not survive Bonferroni correction.

    “We also found a 676 -710 ms time window that showed a spacing (SS vs LS) by item specificity interaction (F (1,32)max ϭ 9.54, F clustersum ϭ 70.16, p cluster ϭ 0.036), but it did not survive Bonferroni correction.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingown data

    There was no significant difference between short-spaced and long-spaced conditions in hit rate or discriminability (d').

    “No significant difference between SS and LS was found for either hit rate (t (32) ϭ Ϫ1.18, p ϭ 0.25) or dЈ (t (32) ϭ Ϫ0.63, p ϭ 0.53).”
    Quote in the paperNot a substantial claim
  • May combine two claims. The quote only partly states this claim.

    Findingown data

    Subsequent memory performance was not significantly associated with reaction time or response consistency during encoding.

    “Three-way (spacing condition, subsequent memory performance, and repetition) repeated-measures ANOVA revealed no significant main effect of subsequent memory (remembered vs forgotten) on reaction time (F (1,32) ϭ 0.21, p ϭ 0.65), nor its interactions with other two factors (all p Ͼ 0.066)”
    • Also stated in: § Spaced learning reduced repetition priming and response consistency · plain
      “Results revealed a significant main effect of spacing condition (F (2,64) ϭ 25, p Ͻ 0.0001), but no effect of subsequent memory performance (F (1,32) ϭ 1.64, p ϭ 0.21) or the interaction between spacing condition and subsequent memory performance (F (2,64) ϭ 1.4, p ϭ 0.25).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    Compared with massed learning, short-spaced learning showed significantly greater within-item STPS in the right frontal cluster (606-652 ms), but comparable between-item STPS.

    “Post hoc tests revealed that, compared with MA, SS showed significantly greater WI STPS (t (32) ϭ 2.43, p ϭ 0.02), but comparable BI STPS (t (32) ϭ 0.46, p ϭ 0.66) (Fig. 2F ).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    In that right frontal cluster, within-item STPS was greater than between-item STPS only for subsequently remembered items, not for forgotten items.

    “In addition, significantly greater WI than BI STPS was only found for subsequently remembered items (F (1,32) ϭ 10.8, p ϭ 0.003), but not for forgotten items (F (1,32) ϭ 1.81, p ϭ 0.19) (Fig. 2D).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    The LPC and item-specific STPS in the right frontal region occurred at a similar time window but with different topographic distributions.

    “Interestingly, they occurred at a similar time window but with different topographic distributions.”
    Quote in the paperNot a substantial claim
  • The quote only partly states this claim.

    Findingown data

    Within-item STPS in the right frontal region (606-652 ms) partially mediated the spacing effect on memory.

    “Mediation analysis showed that the WI STPS partially mediated the spacing effect on memory (indirect effect ϭ 0.0047, 95% CI ϭ 0.001-0.0093)(Fig. 3).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    The LPC representation contained no item-specific information but was associated with memory performance.

    “Third, the LPC representation contained no item-specific information but was associated with memory performance.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    Under the MA learning condition, there were significant primacy and recency effects; trials studied in the first and last quartiles of a run were remembered better than those studied in the middle.

    “There were significant primacy and recency effects under the MA learning condition; that is, trials studied in the first and last quartiles of a run were remembered better than those studied in the middle (t (32) ϭ 2.33, p ϭ 0.026).”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Interpretationcitation

    The finding of greater item-specific STPS for remembered items replicates previous results from a study that used foreign characters as learning stimuli.

    “This finding replicated previous results from a study that used foreign characters as learning stimuli (Lu et al., 2015).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Lu et al., 2015

      Not checked in the free run.

    • The authors state this as an assumption: A greater within-item similarity than between-item similarity reflects item-specific encoding.
  • May combine two claims.

    Premisecitation

    Due to the temporal autocorrelation of the BOLD response, neural pattern similarity between two trials is affected by their temporal distance, which seriously confounds the spacing effect.

    “First, due to the temporal autocorrelation of the BOLD response, the neural pattern similarity between two trials is affected by their temporal distance (Mumford et al., 2014), which seriously confounds the spacing effect.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Mumford et al., 2014

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductown data

    Corrections for multiple comparisons were performed using nonparametric cluster-based permutation tests.

    “Corrections for multiple comparisons were performed using a nonparametric statistical method based on cluster-level permutation tests implemented in Fieldtrip toolbox.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Study design and conductreasoning

    Twelve additional faces were added at the beginning and end of study lists to minimize primacy and recency effects, but were not tested in the recognition task.

    “To minimize the primacy and recency effects, 12 additional faces (four for each run) were added at the beginning and the end of the study lists, but were not tested in the recognition task.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Interpretationown data

    Spaced learning improves long-term memory by increasing retrieval effort and enhancing the pattern reinstatement of prior neural representations, which may be achieved by reducing the momentary retrieval strength as extended repetition lags might help eliminate the residual representation in working memory.

    “These results suggest that spaced learning improves long-term memory by increasing retrieval effort and enhancing the pattern reinstatement of prior neural representations, which may be achieved by reducing the momentary retrieval strength as the extended repetition lags might help to eliminate the residual representation in working memory.”
    Quote in the paperSubstantial claim
    • The authors state this as an assumption: A greater within-item similarity than between-item similarity reflects item-specific encoding.
    • Rests on an assumption: Only condition differences in neural pattern similarity that are linked to successful memory encoding would explain the spacing effect in memory.
  • May combine two claims.

    Interpretationown data

    The LPC might not carry item-specific representations, but rather may reflect general memory-related cognitive processes.

    “These results suggest that the LPC might not carry item-specific representations, but rather may reflect general memory-related cognitive processes.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Premisecitation

    EEG provides higher temporal resolution to differentiate a 350-450 ms component reflecting retrieval strength and a 500-700 ms component containing the neural pattern similarity that supports later memory.

    “Second, EEG provides higher temporal resolution to differentiate 350 -450 ms component reflecting retrieval strength (Rugg and Curran, 2007;Zhao et al., 2015), and the 500 -700 ms component containing the neural pattern similarity that supports later memory (Lu et al., 2015).”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Rugg and Curran, 2007

      Not checked in the free run.

    • cites Zhao et al., 2015

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    • cites Lu et al., 2015

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  • May combine two claims.

    Interpretationown data

    Both the LPC that reflects general cognitive processing and the item-specific STPS in the right frontal region were associated with the spacing effect on memory.

    “The above results suggest that both the LPC that reflects general cognitive processing and the item-specific STPS in the right frontal region were associated with the spacing effect on memory.”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    Pairwise comparisons between the three spacing conditions were further corrected for multiple comparisons using Bonferroni correction.

    “When pairwise comparisons between the three spacing conditions were conducted, the cluster-level tests were further corrected for multiple comparisons using Bonferroni correction.”
    Quote in the paperNot a substantial claim
  • Classified as probably not a substantial claim.

    Study design and conductreasoning

    To determine whether within-item similarity reflected item-specific representations, between-item pairs were matched to within-item pairs on memory performance, spacing condition, number of repetitions, and inter-repetition interval.

    “To determine whether the WI similarity reflected item-specific representations or common cognitive processes, we calculated the similarity for between-item (BI) pairs that matched the WI pairs in terms of their memory performance, spacing condition, number of repetitions (one or two), and IRI.”
    Quote in the paperSubstantial claim
  • Classified as probably not a substantial claim.

    Study design and conductown data

    To determine whether key findings of pattern similarity were due to differences in univariate amplitude, linear mixed-effects models included EEG amplitude as a covariate.

    “To determine whether our key findings of pattern similarity were due to differences in univariate amplitude, we constructed linear mixed-effects models to examine the subsequent memory effect and spacing effect, by including the amplitude as covariate.”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    Participants were not told about the subsequent memory task during the encoding phase.

    “They were not told about the subsequent memory task.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductcitation

    All faces used in the study were unfamiliar to the subjects.

    “All faces were unfamiliar to the subjects and were drawn from the CAS-PEAL face database (Gao et al., 2008).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Gao et al., 2008

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  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductreasoning

    A fixed intertrial interval of 4000 ms was used in the recognition phase so that total duration was not affected by participants' response time.

    “We used a fixed intertrial interval (ITI) of 4000 ms in the recognition phase so that the total duration of this phase was not affected by participants' response time, which could help to discourage the participants from making hasty responses.”
    Quote in the paperNot a substantial claim
  • Classified as probably not a substantial claim.

    Study design and conductnone given

    The materials used in the three spacing conditions were fully counterbalanced across participants.

    “The materials used in the three conditions were fully counterbalanced across participants.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Premisecitation

    N400 increases with repetitions and reflects momentary retrieval strength.

    “our results are consistent with previous studies showing that the N400 increased with repetitions (Henson et al., 2003;Schweinberger and Neumann, 2016) and reflected the momentary retrieval strength (Zhao et al., 2015).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Henson et al., 2003

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    • cites Schweinberger and Neumann, 2016

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    • cites Zhao et al., 2015

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  • May combine two claims.

    Premisecitation

    Item-specific representation in visual cortex is only found during perception, whereas during memory retrieval it is found in the inferior parietal lobule and is more abstract and aligned to current goals.

    “Item-specific representation in the visual cortex was only found during perception, whereas item-specific representation during memory retrieval was found in the inferior parietal lobule (Xiao et al., 2017;Favila et al., 2018) and its representation was more abstract (Jeong and Xu, 2016;Ye et al., 2016) and more aligned to current goals (Favila et al., 2018).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Xiao et al., 2017

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    • cites Favila et al., 2018

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    • cites Jeong and Xu, 2016

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  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    LPC is related to recollection, particularly the retrieval of complex information about prior events.

    “Previous studies have shown that LPC is related to recollection (Rugg and Yonelinas, 2003;Rugg and Curran, 2007;Kappenman and Luck, 2012), in particular, the retrieval of complex information about prior events.”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Rugg and Yonelinas, 2003

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    • cites Rugg and Curran, 2007

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    • cites Kappenman and Luck, 2012

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  • Classified as probably not a substantial claim. May combine two claims.

    Premisecitation

    Early time window representations correspond to early visual cortex; later time window representations correspond to higher-order visual cortex.

    “A recent study combining MEG and fMRI suggests that, whereas the representation in the early time window corresponded to the repre-sentations in the early visual cortex, the representations in the later time window corresponded to the representations in the higher-order visual cortex (Cichy et al., 2014).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Cichy et al., 2014

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    Representations in early and late time windows might carry distinct information and have a differential effect on long-term memory formation.

    “These results also suggest that the representations in early and late time windows might carry distinct information and have a differential effect on long-term memory formation.”
    Quote in the paperSubstantial claim
  • Classified as probably not a substantial claim.

    Premisecitation

    According to the new theory of disuse, an item in memory can be characterized by two strengths: storage strength and retrieval strength.

    “According to the new theory of disuse (Bjork and Bjork, 1992;Bjork, 1999), an item in memory can be characterized by two”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Bjork and Bjork, 1992

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    • cites Bjork, 1999

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    Premisecitation

    N400 supports familiarity judgment.

    “previous studies also suggested that the N400 supported the familiarity judgment (Curran and Cleary, 2003;Rugg and Curran, 2007;Kutas and Federmeier, 2011).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Curran and Cleary, 2003

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    • cites Rugg and Curran, 2007

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    • cites Kutas and Federmeier, 2011

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  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Interpretationcitation

    As the memory trace is updated, its similarity to other items decreases and becomes more distinguishable during retrieval.

    “As the memory trace is updated, its similarity to other items decreases and becomes more distinguishable during retrieval.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Interpretationreasoning

    Introducing variance in the massed repetitions could reduce the momentary retrieval strength, enhance the retrieval of later abstract representations, and improve memory.

    “Introducing variance in the massed repetitions could reduce the momentary retrieval strength, enhance the retrieval of later abstract representations, and improve memory.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Some behavioral studies found that the spacing effect could be effective in terms of days or months.

    “Some behavioral studies found that the spacing effect could be effective in terms of days or months (Cepeda et al., 2008).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Cepeda et al., 2008

      Not checked in the free run.

  • May combine two claims.

    Interpretationcitation

    When study-phase retrieval fails, recall depends on the new trace and performance is impaired.

    “Therefore, the probability of recalling the item mostly depended on the new trace and the performance is thus impaired (Raaijmakers, 2003).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Raaijmakers, 2003

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  • Classified as probably not a substantial claim.

    Interpretationreasoning

    The long-spaced interval might not be long enough to bend the curve.

    “It seems that this long-spaced interval might not be long enough to bend the curve.”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    According to the differentiation model of memory, repeated exposure to an item results in the storage of additional information in the single memory trace established during the first exposure.

    “According to the differentiation model of memory (Kılıc ¸et al., 2017), repeated exposure to an item results in the storage of additional information in the single memory trace established during the first exposure.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Kılıç et al., 2017

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  • May combine two claims.

    Study design and conductreasoning

    The design results in an imbalance in the temporal distributions of repetitions under different spacing conditions, which might have some effect on memory performance.

    “In addition, this design unavoidably results in an imbalance in the temporal distributions of repetitions under different spacing conditions, which might have some effect on memory performance.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Interpretationcitation

    Early pattern similarity might reflect more sensory information that did not predict later memory, whereas later item-specific pattern similarity might reflect more abstract information and contribute to long-term memory.

    “Because perceptual details might decay more rapidly than more abstract information such as semantics (Craik and Tulving, 1975), the early pattern similarity might reflect more sensory information that did not predict later memory, whereas the later item-specific pattern similarity might reflect more abstract information and contribute to long-term memory.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Craik and Tulving, 1975

      Not checked in the free run.

  • May combine two claims.

    Interpretationcitation

    Introducing variance under the spaced condition could increase the chance of retrieval failure, in which case a new trace might be formed.

    “However, introducing variance under the spaced condition could increase the chance of retrieval failure (Verkoeijen et al., 2005;Cepeda et al., 2006), in which case a new trace might be formed.”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Verkoeijen et al., 2005

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    • cites Cepeda et al., 2006

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  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    The optimal interval varies in different learning tasks, different repetition intervals, and different retention lags.

    “In addition, the optimal interval also varied in different learning tasks, different repetition intervals, and different retention lags (Cepeda et al., 2006;Pashler et al., 2009;Toppino and Gerbier, 2014).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Cepeda et al., 2006

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    • cites Pashler et al., 2009

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    • cites Toppino and Gerbier, 2014

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  • May combine two claims.

    Interpretationcitation

    The mechanism accounts for the inverted U-shaped relationship between lag and memory, as too long a lag could result in retrieval failure.

    “This mechanism could also account for the inverted U-shaped relationship between lag and memory (Verkoeijen et al., 2005;Cepeda et al., 2006), as too long a lag could also result in retrieval failure.”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Verkoeijen et al., 2005

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    • cites Cepeda et al., 2006

      Not checked in the free run.

  • Classified as probably not a substantial claim. May combine two claims.

    Study design and conductown data

    Serial position and spacing might interact to affect memory performance, which could potentially confound the result.

    “This sug-gests that the serial position and spacing might interact to affect memory performance, which could potentially confound the result.”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Interpretationown data

    Repetition priming might be a result of residual working memory representation, which might hinder later pattern reinstatement and impair memory.

    “Although our results suggest that repetition priming might be a result of residual working memory representation, which might hinder later pattern reinstatement and impair memory”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S2 (checkable), S3 (load-bearing).

    Interpretationreasoning

    The results highlight the complex interactions of multiple memory processes and representations in determining memory performance.

    “These results highlight the complex interactions of multiple memory processes and representations in determining memory performance.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Interpretationown data

    Better memory was associated with greater STPS that occurred at a late time window and spacing enhanced memory by increasing the STPS.

    “Contrary to the encoding variability hypothesis, better memory was associated with greater STPS that occurred at a late time window and spacing enhanced memory by increasing the STPS.”
    Quote in the paperSubstantial claim
47 of 47
  • The paper relies on this without support.

    No prior study has compared neural representations under spaced and massed learning conditions.

    “First, because no study has compared the neural representations under the spaced-and massed-learning conditions, it is still unclear whether spacing could enhance neural pattern reinstatement to improve subsequent memory.”
  • The paper relies on this without support.

    Whether and how neural representations contribute to the spacing effect remains unknown.

    “Although many cognitive theories and computational models have been proposed to account for the spacing effect, whether and how the neural representations contribute to it remain unknown.”
  • The authors state this as an assumption.

    A greater within-item similarity than between-item similarity reflects item-specific encoding.

    “A greater WI similarity than BI similarity should reflect item-specific encoding.”
  • The paper relies on this without support.

    Only condition differences in neural pattern similarity that are linked to successful memory encoding would explain the spacing effect in memory.

    “Instead, only the condition differences in neural pattern similarity that are linked to successful memory encoding would explain the spacing effect in memory.”
  • The paper relies on this without support.

    Spacing could only modulate the EEG response evoked by the second repetition.

    “Since spacing could only modulate the EEG response evoked by the second repetition, we separately compared MA versus SS, MA versus LS, and SS versus LS on the ERP evoked by the second repetition.”
5 of 5

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Additional neurophysiological data suggest associations between longer intervals and specific neural patterns, but these findings require further replication and do not allow for the establishment of universal causality.

    “Additional neurophysiological data suggest associations between longer intervals and specific neural patterns, although these findings require further replication and do not allow for the establishment of universal causality”

    From Systematic Review of the Effectiveness of Neurodidactic Spaced Learning Strategies in Long-Term Memory (2026) · cites this paper as Feng et al., 2019

    The Results report neural-pattern differences for spaced versus massed repetitions, but the item-specific pattern-similarity difference was significant for short-spaced versus massed trials, not long-spaced versus massed trials. The Discussion identifies a possible design confound and calls for further study, consistent with caution about universal causality; it does not specifically say these findings require replication. (LLM, conf=0.82)

    Experimental — accuracy not yet measured
  • The use of MMAT revealed a generally high level of internal validity in studies employing advanced neurophysiological markers or high-impact academic assessments.

    “The use of MMAT added an additional layer of methodological calibration, revealing a generally high level of internal validity in studies employing advanced neurophysiological markers (e.g., EEG, standardized performance metrics) (Feng et al., 2019;Katz et al., 2021;Katz & Wiseheart, 2025) or high-impact academic assessments (Gilbert et al., 2023;Burel et al., 2025;Azim et al., 2025).”

    From Systematic Review of the Effectiveness of Neurodidactic Spaced Learning Strategies in Long-Term Memory (2026) · cites this paper as Feng et al., 2019

    The Introduction and Behavioral data analysis section identify Feng et al. as a study using EEG, so it supports the citation's role as an example of a study employing a neurophysiological marker. The paper does not report an MMAT appraisal or establish a generally high level of internal validity; those parts of the citing sentence are not supported by this source. Page numbers were not available in our copy. (LLM, conf=0.84)

    Experimental — accuracy not yet measured
  • This review synthesizes a heterogeneous corpus by design, combining ecological classroom interventions with highly controlled mechanistic laboratory studies.

    “This review synthesizes a heterogeneous corpus by design, combining ecological classroom interventions with highly controlled mechanistic laboratory studies (e.g., Litman & Davachi, 2008;Feng et al., 2019).”
  • Reliability was reinforced through neurophysiological mapping (such as EEG pattern similarity analysis) and, in studies involving qualitative components, the application of abductive coding and inter-rater reliability checks.

    “Reliability was further reinforced through neurophysiological mapping (such as EEG pattern similarity analysis) (Feng et al., 2019) and, in studies involving qualitative components such as student reflections, the application of abductive coding and inter-rater reliability checks (Azim et al., 2025).”

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

Each contradiction between two passages listed here was confirmed by an independent check.

  • Encoding trials cannot fit into the reported run duration

    Minor

    The 288 learning faces were each presented twice, yielding 576 encoding trials across three runs. Even at the minimum stated trial duration of 4 seconds (500 ms fixation, 1000 ms stimulus, and 2500 ms blank), those trials require at least 38.4 minutes, not three 10-minute runs.

1 of 1

Cites

Flagged first, then by citations

Research works printed but not linked: 1

  1. Bates D, Mächler M, Bolker B, Walker S (2015) Fitting Linear Mixed-Effects Models Usinglme4. Journal of Statistical Software. Available at https:// www.jstatsoft.org/article/view/v067i01.

Cited by

Sorted by citations

Authors
Feng, K., Zhao, X., Liu, J., Cai, Y., Ye, Z., Chen, C., & Xue, G.
Affiliations
  • Beijing Normal University (CN)
  • University of California, Irvine (US)
Venue
The Journal of Neuroscience
Published
2019-04-29
Volume
39
Issue
27
Pages
5351-5360
ISSN
  • 0270-6474 (ISSN-L)
  • 1529-2401
OpenAlex
W2943106217
Cited by
78
References
66
Citations by year
2026: 10 · 2025: 14 · 2024: 14 · 2023: 11 · 2022: 12 · 2021: 10 · 2020: 7
FWCI
4.21
Type
journal article
Language
en
Open access
Locations
  • Journal of Neuroscience (publishedVersion)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • eScholarship (California Digital Library) (submittedVersion)
Funders
  • Deutsche Forschungsgemeinschaft (DFG TRR 169, NSFC 61621136008/DFG TRR-169, TRR169, 61621136008, NSFC 61621136008, 61621136008/DFG TRR-169)
  • National Natural Science Foundation of China (111 Project, 61621136008, NSFC 61621136008, TRR-169, 31730038, 2016ZT06S220, 61621136008/DFG TRR-169)
  • Higher Education Discipline Innovation Project (B07008)
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
spaced learning, spacing effect, episodic memory, N400, late positive component, memory retrieval, working memory, sex differences
MeSH terms
Adolescent, Adult, Electroencephalography, Evoked Potentials, Female, Humans, Learning, Male, Neurons, Mental Recall, Time Factors, Young Adult, Memory, Long-Term, Memory, Episodic

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Claims read by deepseek-v4.1-flash under definition version 3 (extract-v3) on 2026-10-10.

Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-10-10.

Statistics and arithmetic are recomputed, not judged.

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