1. Neuroscience

Neural correlates and reinstatement of recent and remote memory in children and young adults

  1. Iryna Schommartz  Is a corresponding author
  2. Philip F Lembcke
  3. Javier Ortiz-Tudela
  4. Martin Bauer
  5. Angela M Kaindl
  6. Claudia Buss
  7. Yee Lee Shing  Is a corresponding author
  1. Department of Psychology, Goethe University Frankfurt, Germany
  2. Center for Individual Development and Adaptive Education of Children at Risk (IDeA), Germany
  3. Charité – Universitätsmedizin Berlin, Department of Medical Psychology, Germany
  4. Charité – Universitätsmedizin Berlin, Department of Pediatric Neurology, Germany
  5. Charité – Universitätsmedizin Berlin, Center for Chronically Sick Children, Germany
  6. Charité – Universitätsmedizin Berlin, Institute of Cell- and Neurobiology, Germany
  7. Charité – Universitätsmedizin Berlin, Department of Pediatric Surgery, Germany
  8. Development, Health and Disease Research Program, Department of Pediatrics, University of California, Irvine, United States
https://doi.org/10.7554/eLife.89908.4
Share this article
Cite this article
  1. Iryna Schommartz
  2. Philip F Lembcke
  3. Javier Ortiz-Tudela
  4. Martin Bauer
  5. Angela M Kaindl
  6. Claudia Buss
  7. Yee Lee Shing
(2025)
Neural correlates and reinstatement of recent and remote memory in children and young adults
eLife 12:RP89908.
https://doi.org/10.7554/eLife.89908.4
  2. Download BibTeX
  3. Download .RIS
12 figures, 2 tables and 19 additional files

Figures

Figure 1
Download asset Open asset
Experimental Task and Procedure.

(A) Trial structures in the experimental task. (i) Initial encoding: Participants memorized object-location pairs by creating a story or forming a ‘mental photo’ of each scene, focusing on the exact location of the object within the scene. (ii) Learning phase: Participants selected one of three possible object locations and received feedback: a happy face for correct responses, a sad face for incorrect ones, and a sleeping face for missed responses. The correct object-location pairing was then displayed again. (iii) Retrieval phase: Conducted inside the MR scanner, participants chose the object’s location in the scene from three options without receiving feedback. (B) Experimental procedure. Testing took place across 3 days. On day 0, participants learned 60 object-location associations (remote items). On day 1 (short delay), they learned 30 new object-location associations (recent items) and retrieved 30 remote and 30 recent items. On day 14 (long delay), participants learned another 30 new associations and retrieved 30 remote and 30 recent items. Throughout all sessions, participants also completed socio-demographic and psychometric questionnaires, which were distributed across sessions. Note: RT – reaction time; s – second, fMRI – functional magnetic resonance imaging.

Figure 2
Download asset Open asset
Learning Performance.

(A) Overview of learning performance. Individual learning trajectories across up to four encoding-retrieval cycles for children and young adults on day 0, day 1, and day 14. Each colored dot represents a participant’s accuracy (percentage of correct responses) at a given cycle. Transparent connecting lines illustrate within-person changes in accuracy across cycles. Across all sessions, children needed on average between two to four learning-retrieval cycles to reach the criterion of 83% correct responses, while young adults typically reached it within two cycles. (B) Final learning performance. Final learning accuracy is calculated as the percentage of correct responses during the last learning cycle for both children and young adults. For each group and session, distributions are visualized using half-eye plots (smoothed density estimates), overlaid with boxplots indicating the median and interquartile range. The shape and spread of the density plot reflect individual data variability. Gray dashed line indicates the criteria of 83% correctly learned items.

Figure 3 with 1 supplement
Download asset Open asset
Retention rates for initially correctly learned items.

Memory accuracy is operationalized as the percentage of correct responses in the retrieval task conducted during the magnetic resonance imaging (MRI) scanning sessions for items that were initially correctly learned, indicating strong initial memories. Memory accuracy for recently consolidated items did not differ between sessions in young adults and children and was collapsed across sessions. Overall, young adults show higher and more stable memory accuracy than children, with memory declining over time for both groups, particularly for long delay. All tests used Sidak correction for multiple comparisons. *p<0.05; **p<0.01; ***p<0.001(significant difference); nonsignificant differences were not specifically highlighted. The boxplot summarizes the distribution of accuracy scores across sessions and delay conditions. In each boxplot, the central line indicates the median, the box represents the interquartile range (25th to 75th percentile), and the whiskers extend to the range of values within 1.5 times the variability. The red dashed line at 34% indicates the threshold for chance-level performance.

Figure 3—figure supplement 1
Download asset Open asset
Retention rates for initially correctly learned items (for participants who needed only two learning cycles).

Memory accuracy is operationalized as the percentage of correct responses in the retrieval task conducted during the magnetic resonance imaging (MRI) scanning sessions for items that were initially correctly learned, indicating initially strong memories. Memory accuracy for recently consolidated items did not differ between sessions in young adults and children and was collapsed across recent memory accuracy on day 1, which was higher than on day 14. Memory accuracy for remotely consolidated items differed between sessions in both young adults and children, showing higher remote memory accuracy on day 1 than on day 14. All tests used Sidak correction for multiple comparisons. Red dashed line indicates the threshold for random performance. *p<0.05; **p<0.01; ***p<0.001 (significant difference); nonsignificant differences were not specifically highlighted. Error bars indicate standard error based on the underlying linear mixed effects (LME) model.

Figure 4 with 2 supplements
Download asset Open asset
Mean signal differences between correct remote and recent memories.

The figure presents mean signal difference for remote > recent contrast across sessions and groups during the object presentation time window in (A) anterior and posterior hippocampus; (B) anterior and posterior parahippocampal gyrus; (C) cerebellum; (D) medial prefrontal cortex; (E) ventrolateral prefrontal cortex; (F) precuneus; (G) retrosplenial cortex; (H) lateral occipital cortex. Note: Bars indicate the group mean for each session (solid lines for day 1, dashed lines for day 14), plotted separately for children and young adults. Error bars represent ± 1 standard error of the mean. The color indicated the age groups: purple for children and khaki yellow for young adults. Across all panels, the mean of individual subject data is shown with transparent points. The connecting faint lines reflect within-subject differences across sessions. Orange asterisks denote significant difference of remote > recent contrast from zero. An upward orange arrow indicates that this difference is greater than zero, while a downward arrow indicates that this is less than zero. *p<0.05; **p<0.01; ***p<0.001 (significant difference); nonsignificant differences were not specifically highlighted. Significant main and interaction effects are highlighted by the corresponding asterisks. All main and interaction p-values were false discovery rate (FDR)-adjusted for multiple comparisons.

Figure 4—figure supplement 1
Download asset Open asset
Mean blood oxygen level-dependent (BOLD) signal intensity.

The figure presents the mean BOLD signal intensity for recent and remote memories on day 1 and day 14 in children and adults in (A) anterior hippocampus; (B) posterior hippocampus; (C) anterior parahippocampal gyrus. Note: Bars represent the average BOLD signal intensity. The color indicated the age groups: purple for children and khaki yellow for young adults. Solid-lined bars represent recent data from day 1 or day 14, while dashed-lined bars depict remote data from day 1 and day 14. Error bars indicate standard error of the mean.

Figure 4—figure supplement 2
Download asset Open asset
Mean neural activation for correctly recalled memories during scene presentation time window.

The figure presents mean signal intensity for correctly recalled recent, short-delay remote, and long-delay remote memories in children and adults in (A) anterior hippocampus; (B) posterior hippocampus; (C) anterior parahippocampal gyrus; (D) posterior parahippocampal gyrus; (E) medial prefrontal cortex; (F) ventrolateral prefrontal cortex; (G) precuneus; (H) retrosplenial cortex; (I) lateral occipital cortex; (J) cerebellum. Note: Bars represent the average signal difference. The color indicated the age groups: purple for children and khaki yellow for young adults. Solid-lined bars represent data from day 1, while dashed-lined bars depict data from day 14. Across all panels, the mean of individual subject data is shown with transparent points. The connecting faint lines reflect within-subject differences across sessions. Error bars indicate standard error of the mean. *p<0.05; **p<0.01; ***p<0.001 (significant difference); nonsignificant differences were not specifically highlighted. Significant main and interaction effects are highlighted by the corresponding asterisks. All main and interactions p-values were false discovery rate (FDR)-adjusted for multiple comparisons.

Figure 5
Download asset Open asset
Multivariate short- and long-delay brain profiles of neural upregulation (remote vs. recent neural activation differences) are associated with variations in memory accuracy.

(A) Short-delay brain profile. Latent variable weights or saliences for each ROI build up one latent variable that expresses a composite short-delay brain profile across both age groups. (B) Long-delay brain profile. Latent variable weights or saliences for each ROI build up one latent variable that expresses a composite long-delay brain profile across both age groups. The bar plot shows the bootstrap ration (BSR) values for the latent variable, reflecting the stability of the relationship between brain activation and memory performance. Stability of salience elements is defined by Z-scores depicted as red lines: a value larger/smaller than ±1.96 is treated as reliably robust at (a<0.05). (C) Short-delay brain scores by group. (D) Long-delay brain scores by group. Each box represents the distribution of brain scores within a group, with central lines indicating the median and boxes showing the interquartile range. Whiskers represent the full range of non-outlier values. Note: PHGa – anterior parahippocampal gyrus; PHGp – posterior parahippocampal gyrus; HCa – anterior hippocampus; HCp – posterior hippocampus; PC – precuneus; vlPFC – ventrolateral prefrontal cortex; mPFC – medial prefrontal cortex; RSC – retrosplenial cortex; LOC – lateral occipital cortex; CE – cerebellum; r – Spearman’s rank order correlation index.

Figure 6
Download asset Open asset
Scene-specific reinstatement.

(A) Index computation (scene). A representational similarity index was computed by calculating the average similarity between activation patterns in the fixation and scene time windows, separately for recent scenes, remote scenes on day 1, and remote scenes on day 14. (B) Scene-specific reinstatement. A corrected scene-specific reinstatement index was computed by assessing the average similarity within-trial similarity between the fixation and scene time windows and subtracting the average between-trial (set-based) similarity across all other trials. This controls for baseline similarity unrelated to specific scene content. S – scene time window; F – fixation time window; r – Pearson’s correlation index; Δz – difference between two Fisher-transformed r values. * – Activation patterns.

Figure 7 with 1 supplement
Download asset Open asset
Corrected scene-specific neural reinstatement.

Scene-specific neural reinstatement is defined as the difference between Fisher-transformed scene-specific and set-specific representational similarity. Scene-specific neural reinstatement index by group (children vs. adults) and session (day 0 – recent, day 1 – remote short delay, day 14 – remote long delay). Bars represent the mean reinstatement index for each session within each group, with error bars indicating standard error of the mean. Transparent dots show individual participant data points, jittered horizontally for visibility. The x-axis is grouped by group and displays (A) hippocampus anterior; (B) hippocampus posterior; (C) parahippocampal gyrus anterior; (D) parahippocampal gyrus posterior; (E) cerebellum; (F) medial prefrontal cortex; (G) ventrolateral prefrontal cortex; (H) precuneus; (I) retrosplenial cortex; (J) lateral occipital cortex. *p<0.05; **p<0.01; ***p<0.001 (significant difference). Error bars indicate standard error.

Figure 7—figure supplement 1
Download asset Open asset
Object-specific neural reinstatement.

Object-specific neural reinstatement is defined as the difference between Fisher-transformed scene-specific and set-specific representational similarity (for incorrectly remembered items). Scene-specific neural reinstatement index by group (children vs. adults) and session (day 0 – recent, day 1 – remote short delay, day 14 – remote long delay). HC_A – hippocampus anterior; HC_P – hippocampus posterior; PHG_A – parahippocampal gyrus anterior; PHG_P – parahippocampal gyrus posterior; mPFC – medial prefrontal cortex; vlPFC – ventrolateral prefrontal cortex; RSC – retrosplenial cortex; LOC – lateral occipital cortex. Error bars indicate standard error.

Figure 8
Download asset Open asset
Representational similarity analysis.

(A) Index computation (gist). A representational similarity index was computed by assessing the average similarity for fixation time window for within-category and between-category scenes separately for recent, remote (day 1), and remote (day 14) scenes based on both within-run and cross-run comparisons. The diagonal (similarity of fixation time window with itself) was excluded from the analysis. (B) Gist-like representation. A gist-like representation index was computed by assessing the average similarity in fixation time window for the same-category pairs and subtracting from it the any-other-category pairs. S – scene time window; F – fixation time window; r – Pearson’s correlation index. Δz – difference between two Fisher-transformed r values.

Figure 9
Download asset Open asset
Gist-like representations.

Bar plots show mean gist-like representation index (difference in Fisher’s z-transformed (Δz) similarity: within-category – between-category) in each group (children, young adults) and session (day 0, day 1, day 14), computed from combined within- and cross-run comparisons. Error bars indicate ± 1 standard error of the mean. A representation value above zero (denoted by red asterisks) reflects greater neural pattern similarity during fixation time window between items from the same category than across categories. Bar positions are grouped by age group (x-axis). Session-specific estimates (days 0, 1, 14) are differentiated by line of bar border. (A) Medial prefrontal cortex; (B) ventrolateral prefrontal cortex; (C) lateral occipital cortex; (D) precuneus; *p<0.05; **p<0.01; ***p<0.001 (significant difference; false discovery rate (FDR)-corrected for multiple comparisons); nonsignificant difference was not specifically highlighted.

Figure 10
Download asset Open asset
Multivariate short- and long-delay brain profiles of scene-specific reinstatement are associated with variations in memory accuracy.

(A) Recent delay brain profile. Latent variable weights or saliences for each region of interest (ROI) build up one latent variable that expresses a composite immediate-delay scene-specific reinstatement brain profile. (B) Short-delay brain profile. Latent variable weights or saliences for each ROI build up one latent variable that expresses a composite short-delay scene-specific reinstatement brain profile. (C) Long-delay brain profile. Latent variable weights or saliences for each ROI build up one latent variable that expresses a composite long-delay scene-specific reinstatement brain profile. Stability of salience elements is defined by Z-scores (depicted as red lines: a value larger/smaller than ± 1.96 is treated as reliably robust at (a<0.05)). The bar plot shows the bootstrap ration (BSR) values for the latent variable, reflecting the stability of the relationship between brain scene-specific neural reinstatement and memory performance. (D) Recent delay brain scores. (E) Short-delay brain scores. (F) Long-delay brain scores. Each box represents the distribution of brain scores within a group, with central lines indicating the median and boxes showing the interquartile range. Whiskers represent the full range of non-outlier values. Note: PHGa – anterior parahippocampal gyrus; PHGp – posterior parahippocampal gyrus; HCa – anterior hippocampus; HCp – posterior hippocampus; PC – precuneus; vlPFC – ventrolateral prefrontal cortex; mPFC – medial prefrontal cortex; RSC – retrosplenial cortex; LOC – lateral occipital cortex; CE – cerebellum; r – Spearman’s rank order correlation index.

Figure 11
Download asset Open asset
Multivariate short- and long-delay brain profiles of gist-like representations are associated with variations in memory accuracy.

(A) Short-delay brain profile. Latent variable weights or saliences for each region of interest (ROI) build up one latent variable that expresses a composite short-delay gist-like representations brain profile across age groups. (B) Long-delay brain profile. Latent variable weights or saliences for each ROI build up one latent variable that expresses a composite long-delay gist-like representations brain profile in child group. The bar plot shows the bootstrap ration (BSR) values for the latent variable, reflecting the stability of the relationship between brain gist-like neural representations and memory performance. Stability of salience elements is defined by Z-scores (depicted as red lines: a value larger/smaller than ± 1.96 is treated as reliably robust at (a<0.05)). Note: vlPFC – ventrolateral prefrontal cortex; mPFC – medial prefrontal cortex; LOC – lateral occipital cortex; r – Spearman’s rank order correlation index.

Author response image 1
Download asset Open asset

Tables

Table 1
Sample characteristics by age group.
Children(CH; N=49)Young adults(YA; N=39)Group effect(CH vs. YA)
Demographic measuresMSDMSDp-Valueω2
Age6.340.4325.602.79***0.96
Sex (M/F)27/22–20/19–––
IQ score117.9012.92107.6412.49***0.13
Socioeconomic status
ISCED – father6.221.434.391.75***0.29
ISCED – mother6.171.344.081.85***0.24

  1. Notes: Income is based on a 1–7 scale (1=less than 15,000 €, 7=more than 100,000 €); ISCED = Institute for Statistics (UIS), 2011 (Institute for Statistics (UIS), 2011); IQ = intelligence quotient based on K-ABC (Kaufman and Kaufman, 2015) for children and WAIS-IV (Wechsler, 2015) for young adults; M=mean; SD = standard deviation; ω2=omega squared; *p<0.05; **<0.01, ***<0.001 (significant difference).

Table 2
Statistical overview of linear mixed effects (LME) model-based Sidak-corrected post hoc comparisons for scene-specific reinstatement analysis (based on LME model described in Supplementary file 9).
Model-based post hoc comparisons*
YC >YARecent >Remote day 1Remote day 1>day 14
ROIbt(DF)pbt(DF)pbt(DF)p
HCa–.071–5.15(89)<0.0010.0404.35(162)<0.0010.0959.60(167)<0.001
HCp–0.068–5.14(91)<0.0010.0404.29(162)<0.0010.0949.45(168)<0.001
PHGa–0.069–4.75(90)<0.0010.0394.05(162)<0.0010.0989.62(167)<0.001
PHGp–0.055–3.91(90)<0.0010.0403.77(178)<0.0010.0969.07(172)<0.001
mPFC–0.049–2.94(92)0.0040.0454.16(162)<0.0010.0937.91(169)<0.001
vlPFC–0.058–3.84(93)<0.0010.0534.55(179)<0.0010.0897.79(169)<0.001
CE–0.044–3.05(89)0.0030.0463.97(166)<0.0010.0867.19(170)<0.001
RSC–0.041–2.99(90)0.0030.0393.72(162)<0.0010.0948.56(169)<.001
PC–0.047–3.33(89)0.0010.0444.15(165)<0.0010.0867.89(168)<.001
LOC–0.017–1.09(103)0.2790.0453.97(173)<0.0010.0837.07(174)<.001

  1. Notes: Degrees of freedom were adjusted based on Kenward-Roger methods. p-Values were adjusted based on Sidak adjustment. YA – young adults; CH – children; ROI – region of interest; HCa – anterior hippocampus; HCp – posterior hippocampus; PHGa – anterior parahippocampal gyrus; PHGp – posterior parahippocampal gyrus; mPFC – medial prefrontal cortex; vlPFC – ventrolateral prefrontal cortex; CE – cerebellum; RSC – retrosplenial cortex; PC– precuneus; LOC – lateral occipital cortex; b – beta values; t – t-value; DF – degrees of freedom; p – p-value; CI – confidence interval; *p<0.05; **<0.01, ***<0.001 (significant difference).

Additional files

MDAR checklist
https://cdn.elifesciences.org/articles/89908/elife-89908-mdarchecklist1-v1.docx
Supplementary file 1

Statistical overview of the linear mixed effects model for memory retention rates for initially correctly learned items (corrected for chance performance) based on participants who needed only two learning cycles (N = 28).

https://cdn.elifesciences.org/articles/89908/elife-89908-supp1-v1.docx
Supplementary file 2

Statistical overview of post hoc analysis of the Item Type x Group Interaction effects for the linear mixed effects model for memory retention rates for initially correctly learned items (corrected for chance performance) based on participants who needed only two learning cycles.

https://cdn.elifesciences.org/articles/89908/elife-89908-supp2-v1.docx
Supplementary file 3

Two-sided permutation t-tests were conducted to assess whether the mean signal difference of the contrast remote > recent significantly differed from zero for each combination of ROI, session, and group.

https://cdn.elifesciences.org/articles/89908/elife-89908-supp3-v1.docx
Supplementary file 4

Test of neural activation during object presentation separately for recent and remote memories for significance (higher than zero).

https://cdn.elifesciences.org/articles/89908/elife-89908-supp4-v1.docx
Supplementary file 5

Full statistical overview of LME model for univariate analysis (includes only ROI that show above or below zero upregulation).

https://cdn.elifesciences.org/articles/89908/elife-89908-supp5-v1.docx
Supplementary file 6

Statistical overview of the main and interaction effects of the linear mixed effects models recent and remote univariate results of correctly recognized items.

https://cdn.elifesciences.org/articles/89908/elife-89908-supp6-v1.docx
Supplementary file 7

fMRI univariate analysis.

https://cdn.elifesciences.org/articles/89908/elife-89908-supp7-v1.docx
Supplementary file 8

Full statistical overview of LME model for univariate analysis (sub-sampled to those participants who reached accuracy criteria after 2 encoding loops).

https://cdn.elifesciences.org/articles/89908/elife-89908-supp8-v1.docx
Supplementary file 9

Statistical overview of the main and interaction effects of the linear mixed effects model for scene-specific reinstatement.

https://cdn.elifesciences.org/articles/89908/elife-89908-supp9-v1.docx
Supplementary file 10

Statistical overview of the main and interaction effects of the linear mixed effects model for object-specific reinstatement.

https://cdn.elifesciences.org/articles/89908/elife-89908-supp10-v1.docx
Supplementary file 11

Statistical overview of the main and interaction effects of the linear mixed effects model for remote object-specific reinstatement.

https://cdn.elifesciences.org/articles/89908/elife-89908-supp11-v1.docx
Supplementary file 12

Statistical overview of the main and interaction effects of the linear mixed effects model for scene-specific reinstatement for corpus callosum subregions.

https://cdn.elifesciences.org/articles/89908/elife-89908-supp12-v1.docx
Supplementary file 13

Statistical overview of LME-model based Sidak corrected post hoc comparisons for scene-specific reinstatement analysis for corpus callosum subregions.

https://cdn.elifesciences.org/articles/89908/elife-89908-supp13-v1.docx
Supplementary file 14

Test of gist-like representations index for significance (higher than zero).

https://cdn.elifesciences.org/articles/89908/elife-89908-supp14-v1.docx
Supplementary file 15

Memory Strength across Time.

https://cdn.elifesciences.org/articles/89908/elife-89908-supp15-v1.docx
Supplementary file 16

Assessment of demographic and cognitive covariates and fMRI data pre-processing.

https://cdn.elifesciences.org/articles/89908/elife-89908-supp16-v1.docx
Supplementary file 17

Statistical overview of the main and interaction effects of the linear mixed effects models for remote > recent univariate results for correctly recognized items (based on the pipeline without global signal).

https://cdn.elifesciences.org/articles/89908/elife-89908-supp17-v1.docx
Supplementary file 18

Statistical overview of the main and interaction effects of the linear mixed effects model for scene-based univariate neural analysis.

https://cdn.elifesciences.org/articles/89908/elife-89908-supp18-v1.docx

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Iryna Schommartz
  2. Philip F Lembcke
  3. Javier Ortiz-Tudela
  4. Martin Bauer
  5. Angela M Kaindl
  6. Claudia Buss
  7. Yee Lee Shing
(2025)
Neural correlates and reinstatement of recent and remote memory in children and young adults
eLife 12:RP89908.
https://doi.org/10.7554/eLife.89908.4