Figures and data in Bayesian meta-analysis reveals the mechanistic role of slow oscillation-spindle coupling in sleep-dependent memory consolidation

Figures
Tables
Additional files

14 figures, 15 tables and 8 additional files

Figures

Figure 1

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Measurement of phase-amplitude coupling (PAC) in slow oscillation and spindle events.

(A) The origin of neural oscillations during sleep. SO slow oscillation, *SP sleep spindle, SWR* sharp wave ripple. In each subgraph, the vertical line indicates the typical amplitude of that sleep wave, while the horizontal line indicates the typical frequency and duration. Note that SPs also propagate along the cortex, and the figure only displays the origin. (B) Electrophysiology representation diagram of the SO-SP coupling. SO and SP amplitudes are normalized. The phase of SOs when SPs are at their maximum instantaneous amplitude is recorded as the coupling phase. The occurrence of SPs and SO-SP coupling is not necessarily continuous as shown in the diagram. (C) Coupling preferred phase and strength diagram. (Left) The phase and strength used in the circular plot are simulated data from existing dataset for visualization purposes only. At the group level, the mean circular direction shows the preferred SO phase, while the mean vector length shows the strength of the precise coupling. (Right) The phase of SO peaks is noted as 0, while the phase of SO troughs is noted as $\pm π$ .

Figure 2

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Hierarchical diagram of coupling measures.

*PETH* peri-event time histogram, *MVL* mean vector length, MI modulation index. *SPcSO* Percentage of SPs coupled with SOs in all SP events. In contrast to the term ‘frequency’ used throughout the text in reference to the neural oscillation, the coupling prevalence in the diagram indicates the occurrence of SO–SP coupling events.

Figure 3

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Risk of bias assessment summary plot adapted from ROBINS-I (Sterne et al., 2016).

The most significant heterogeneity is revealed in the measurement of outcome, while the overall assessment indicated a moderate risk of bias across studies after requesting unreported results and data transformation. Based on the complexity of the type of measures involved in phase-amplitude coupling analysis, we believe that this degree of risk of bias is acceptable. Specific evaluations for each study were reported in Appendix 1.

Figure 4

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Forest and regression plots for the association between SO-SP coupling phase and memory retention.

(A) Overall model forest plot at study-level. Dashed lines indicate the 95% credible interval (CrI) of the pooled effect size. The black point and error bar for each study show the adjusted estimation of effect size and 95% CrI combining data and prior information. The gray dots under each distribution show raw effect sizes of each study. Effect size-level plots can be found in Supplementary file 3. (B) Meta regression plot with age as moderator. Blue lines represent 200 overplotted spaghetti fit lines to visualize predictions. (C) Moderator-level forest plot. Each box represents a type of moderator. Mixed effect sizes with mixed conditions from different factor levels listed above. *Weight* Stacked weight of each moderation model in the paired model performance comparison between the moderator and overall (intercept-only) model. The stacked weight of the overall model in each pair of comparisons can be calculated as 1 - weight of the moderation model.

Figure 4—source data 1 Subtable of effect size-level metadata included in the coupling phase–memory analysis.: https://cdn.elifesciences.org/articles/101992/elife-101992-fig4-data1-v1.zip
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Figure 5

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Preferred slow oscillation-fast spindle coupling phase and its association with memory retention.

(A) Quadratic regression of the phase-memory association under different regions of PSG channels aggregated from studies included in the meta-analysis. 0 peak of SO upstate; ±π trough of SO downstate; r circular-linear correlation coefficient; *r_z* standardized circular-linear correlation coefficient. Bars represent the mean memory retention scores per π/4 radian (45°). The dashed vertical line represents the mean preferred phase across studies. The colored quadratic fit line represents the direction of the relationship. The direction of their relationship gradually flips as the PSG channel moves from the front to the posterior area. Only under the frontal and central channels do fit lines display a quadratic relationship, with a peak of memory score near the up-state peak of SOs. In posterior channels, in contrast, the relationship is convex, although it is not significant. Non-significant quadratic regressions between SO-slow SP coupling and memory are reported in Appendix 6. (B) Posterior distributions of mean preferred phases from the Bayesian circular mixed-effect model. The circular posterior distribution is shown in the top-right corner, and the area between two black lines is projected on a linear scale in the main graph. The vertical line reflects the up-state peak of SOs. Points and error bars denote the mean and 95% credible intervals of phases detected from each channel cluster. Phase values are reported as radians. (C) Circular plot of the preferred coupling phase. From top to bottom, frontal, central, and posterior. The direction of each colored dot represents the preferred coupling phase of each subject recorded from PSG channels in each cluster. The direction of the mean resultant vector indicates the mean preferred coupling phase across subjects, the width indicates the 95% credible interval of the mean coupling phase, the length from 0 (center) to 1 (circumference) indicates the consistency of coupling phase across subjects.

Figure 6

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Forest and regression plots for the association between SP amplitude and memory retention.

(A) Overall model forest plot at study-level. The solid vertical line represents the mean Pearson correlation coefficient under the null hypothesis. Dashed lines indicate the 95% credible interval (CrI) of the pooled effect size. The black point and error bar for each study show the adjusted estimation of effect size and 95% CrI combining data and prior information. The gray dots under each distribution show raw effect sizes of each study. Effect size-level plots can be found in Supplementary file 3. (B) Meta regression plot with age as moderator. Blue lines represent 200 overplotted spaghetti fit lines to visualize predictions. (C) Moderator-level forest plot. Each box represents a type of moderator. Mixed effect sizes with mixed conditions from different factor levels listed above. *Weight* Stacked weight of each moderation model in the paired model performance comparison between the moderator and overall (intercept-only) model. The stacked weight of the overall model in each pair of comparisons can be calculated as 1 weight of the moderation model.

Figure 6—source data 1 Subtable of effect size-level metadata included in the spindle amplitude memory analysis.: https://cdn.elifesciences.org/articles/101992/elife-101992-fig6-data1-v1.csv
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Figure 7

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Forest and regression plots for the association between coupling strength and memory retention.

(A) Overall model forest plot at study-level. The solid vertical line represents the mean Pearson correlation coefficient under the null hypothesis. Dashed lines indicate the 95% credible interval (CrI) of the pooled effect size. The black point and error bar for each study show the adjusted estimation of effect size and 95% CrI combining data and prior information. The gray dots under each distribution show raw effect sizes of each study. Effect size-level plots can be found in Supplementary file 3. (B) Meta regression plot with age as moderator. Blue lines represent 200 overplotted spaghetti fit lines to visualize predictions. (C) Moderator-level forest plot. Each box represents a type of moderator. Mixed effect sizes with mixed conditions from different factor levels listed above. *Weight* Stacked weight of each moderation model in the paired model performance comparison between the moderator and overall (intercept-only) model. The stacked weight of the overall model in each pair of comparisons can be calculated as 1 weight of the moderation model.

Figure 7—source data 1 Subtable of effect size-level metadata included in the coupling strength–memory analysis.: https://cdn.elifesciences.org/articles/101992/elife-101992-fig7-data1-v1.zip
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Figure 8

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Forest and regression plots for the association between coupling percentage and memory retention.

(A) Overall model forest plot at study-level. The solid vertical line represents the mean Pearson correlation coefficient under the null hypothesis. Dashed lines indicate the 95% credible interval (CrI) of the pooled effect size. The black point and error bar for each study show the adjusted estimation of effect size and 95% CrI combining data and prior information. The gray dots under each distribution show raw effect sizes of each study. Effect size-level plots can be found in Supplementary file 3. (B) Meta regression plot with age as moderator. Blue lines represent 200 overplotted spaghetti fit lines to visualize predictions. (C) Moderator-level forest plot. Each box represents a type of moderator. Mixed effect sizes with mixed conditions from different factor levels listed above. *Weight* Stacked weight of each moderation model in the paired model performance comparison between the moderator and overall (intercept-only) model. The stacked weight of the overall model in each pair of comparisons can be calculated as 1 weight of the moderation model.

Figure 8—source data 1 Subtable of effect size-level metadata included in the coupling percentage–memory analysis.: https://cdn.elifesciences.org/articles/101992/elife-101992-fig8-data1-v1.zip
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Figure 9

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PRISMA flow diagram of literature search, screening, and inclusion for systematic review and meta-analysis.

Appendix 1—figure 1

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Risk of bias (ROB) assessment for individual studies.

Appendix 4—figure 1

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Funnel Plot and Egger regression for assessing publication bias.

Each colored dot represents one effect size and corresponding standard error. The outer border of the transparent triangle indicates the area where it is anticipated that 95% of the included studies would fall if there were no publication biases present. The red dashed line represents the superimposed Egger’s regression line. We noted that with sufficient sample sizes, the phase-memory association and strength-memory association tend towards a moderate magnitude.

Appendix 5—figure 1

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Comparison of sampling distributions of standardized Circlin *r_z* under null.

Appendix 5—figure 2

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Sampling distributions of standardized Circlin *r_z* drawn from population correlations.

(A) Sampling distributions of standardized Circlin drawn from populations with moderate correlations (*r_z* = 0.3–0.4). Vertical dashed lines indicate the true population values from which samples were generated. (B) Sampling distributions of standardized Circlin drawn from populations with strong correlations (*r_z* = 0.6–0.7).

Appendix 6—figure 1

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Preferred slow oscillation-slow spindle coupling phase and its association with memory retention.

(A) Quadratic regression of the phase-memory association under different regions of PSG channels aggregated from studies included in the meta-analysis. 0 peak of SO upstate; ±π trough of SO downstate; r circular-linear correlation coefficient; *r_z* standardized circular-linear correlation coefficient. Bars represent the mean memory retention scores per π/4 radian (45°). The dashed vertical line represents the mean preferred phase across studies. The colored quadratic fit line represents the direction of the relationship. None of the PSG channels displays a typical quadratic relationship around the down-state trough of SOs. (B) Posterior distributions of mean preferred phases from the Bayesian circular mixed-effect model. The circular posterior distribution is shown in the top right corner, and the area between two black lines is projected on a linear scale in the main graph. The vertical line reflects the down-state trough of SOs. Dots and error bars denote the mean and 95% credible intervals of phases detected from each channel cluster. Phase values are reported in radians. (C) Circular plot of the preferred coupling phase. From top to bottom, frontal, central, and posterior. The direction of each colored dot represents the preferred coupling phase of each subject recorded from PSG channels in each cluster. The direction of the mean resultant vector indicates the mean preferred coupling phase across subjects, the width indicates the 95% credible interval of the mean coupling phase, the length from 0 (center) to 1 (circumference) indicates the consistency of coupling phase across subjects.

Tables

Table 1

Result of directional hypothesis tests for each pair of factor levels (conditions) in overall and each moderation model of the coupling phase-memory association.

Moderator	Overall	Memory Task			Age	Spindle	PSG Channel			Stage	Bout
Condition	H₁	Verbal	Emotional	Spatial	Younger	Fast	Frontal	Frontal	Central	N2	Night
Control	H₀	Motor	Motor	Motor	Older	Slow	Central	Posterior	Posterior	SWS	Nap
BF₁₀	58.35	1.30	1.09	0.07	160.94	11.39	13.58	6.13	0.86	1.74	2.23
Probability	0.98	0.57	0.52	0.06	0.99	0.92	0.93	0.86	0.46	0.63	0.69

Condition conditions hypothesized to be associated with stronger phase-memory association than other factor levels; Control Variables hypothesized to be associated with weaker phase-memory association; BF₁₀ Bayes factor in favor of H₁ over H₀; N2 nREM2 stage; SWS slow-wave sleep.

Table 2

Result of directional hypothesis tests for each pair of factor levels (conditions) in overall and each moderation model of the SP amplitude-memory association.

Moderator	Overall	Memory Task			Age	Spindle	PSG Channel			Stage	Bout
Condition	H₁	Verbal	Emotional	Spatial	Younger	Fast	Frontal	Frontal	Central	N2	Night
Control	H₀	Motor	Motor	Motor	Older	Slow	Central	Posterior	Posterior	SWS	Nap
BF₁₀	8.28	22.19	1.50	9.30	3.70	12.21	1.88	24.67	13.65	5.37	2.54
Probability	0.89	0.96	0.60	0.90	0.79	0.92	0.65	0.96	0.93	0.84	0.72

Condition conditions hypothesized to be associated with stronger amplitude-memory association than other factor levels; Control Variables hypothesized to be associated with weaker amplitude-memory association; BF₁₀ Bayes factor in favor of H₁ over H₀; N2 nREM2 stage; SWS slow-wave sleep.

Table 3

Result of directional hypothesis tests for each pair of factor levels (conditions) in overall and each moderation model of the coupling strength-memory association.

Moderator	Overall	Memory Task			Age	Spindle	PSG Channel			Stage	Bout
Condition	H₁	Verbal	Emotional	Spatial	Younger	Fast	Frontal	Frontal	Central	N2	Night
Control	H₀	Motor	Motor	Motor	Older	Slow	Central	Posterior	Posterior	SWS	Nap
BF₁₀	111.04	2.77	10.62	1.10	9.97	1.91	2.81	1.57	0.70	0.33	2.66
Probability	0.99	0.73	0.91	0.52	0.91	0.66	0.74	0.61	0.41	0.25	0.73

Condition conditions hypothesized to be associated with stronger strength-memory association than other factor levels; Control Variables hypothesized to be associated with weaker strength-memory association; BF₁₀ Bayes factor in favor of H₁ over H₀; N2 nREM2 stage; SWS slow-wave sleep.

Table 4

Results of directional hypothesis tests for each pair of factor levels (conditions) in overall and each moderation model of the coupling percentage–memory association.

Moderator	Overall	Memory Task			Age	Spindle	PSG Channel			Stage	Bout
Condition	H₁	Verbal	Emotional	Spatial	Younger	Fast	Frontal	Frontal	Central	N2	Night
Control	H₀	Motor	Motor	Motor	Older	Slow	Central	Posterior	Posterior	SWS	Nap
BF₁₀	0.38	0.05	0.17	0.22	2.16	0.28	5.15	3.38	1.24	2.02	0.44
Probability	0.28	0.05	0.14	0.18	0.68	0.22	0.84	0.77	0.55	0.67	0.31

Condition conditions hypothesized to be associated with stronger percentage-memory association than other factor levels; Control Variables hypothesized to be associated with weaker percentage memory association; BF₁₀ Bayes factor in favor of H₁ over H₀; N2 nREM2 stage; SWS slow-wave sleep.

Table 5

Descriptive table of the meta-analysis result of measures of SO-SP coupling characteristics.

Measure	n	k	Pooled Effect Size	BF₁₀	Influential Moderators
Coupling Phase	23	90	0.07 [0.01, 0.13]	58.35	Memory Type, Age, Channel, Spindle
Spindle Amplitude	18	78	0.07 [−0.04, 0.18]	8.28	Memory Type, Age, Channel, Spindle
Coupling Strength	22	86	0.08 [0.02, 0.15]	111.04	Age
Coupling Percentage	11	43	−0.03 [−0.15, 0.07]	0.38	None

n number of studies included; k number of effect sizes included; BF₁₀ Bayes factor in favor of H₁ over H₀ (see Table 8 for the interpretation).

Table 6

Interpretation of the standardized circular-linear correlation coefficient.

r_z	Strength
<0	No Effect
0	Null
0.1	Small
0.3	Moderate
0.5	Strong

Table 7

Summary of memory tasks.

Memory Task Domain	Memory Task Modality
Verbal Tasks (n=12)	Word-Pair (WP)
	Word List
	Novel Metaphor
	Word-Image Pair (WIP)
Emotional Task (n=3)	Picture-recognition (IMG)
Spatial Tasks (n=4)	Spatial Memory
	2D Object Location (2DL)
	Visuo-spatial (VS)
Motor Tasks (n=6)	Motor Sequence (MST)
	Gross-motor Juggle
	Mirror-tracing Task (MTT)
	Visuomotor Adaptation (VMA)

Table 8

Interpretation of Bayes Factor (BF₁₀) for the strength of evidence.

BF₁₀	Direction
<0.1	Strong, Favor alternative
0.1–0.33	Moderate, Favor alternative
0.33–1	Weak, Favor alternative
1–3	Weak, Favor hypothesis
3–10	Moderate, Favor hypothesis
>10	Strong, Favor hypothesis

Appendix 1—table 1

Risk of bias assessment supplemental criteria.

Domain	Supplemental Signaling Questions
Bias due to confounding variables	1.1 Was sufficient information provided to assess the presence of major potential confounding variables?
	1.2 Were major potential confounding variables not relevant to study controlled during the data collection and analysis? Were influences from other experimental tasks or stimuli existing?
	1.3 Were confounding factors (such as gender, age, etc.) added to models to calculate and interpret as the “corrected” effect size?
Bias due to subject selection	2.1 Was subject selection representative? Can subjects represent the population or community targeted by the experiment?
	2.2 Was a random sampling method applied during data collection? Are subjects recruited mostly from a single source (e.g., university) or at different times and caused biases?
	2.3 Are the subjects independent from each other? Are the subjects socially connected (e.g., patients and their relatives, between groups if there are multiple groups in the original study)? Have the same subjects been measured repeatedly in pretest-posttest designs?
Bias due to classification of groups	3.1 For studies with multiple groups, can group(s) containing only healthy human subjects without intervention be clearly classified?
Bias due to classification of groups	3.2 When reporting the effect size, did the authors report the effect size separately for different groups?
Bias due to missing outcome data	4.1 Were only scatterplots reported in the article, necessitating the use of graph tools to estimate the effect size?
	4.2 Was data including t statistics, p-values, β statistics, and η² the only data provided that could be used to estimate the correlation, or only imprecise data provided for non-significant correlation?
	4.3 Have pre-sleep/sleep/post-sleep memories and/or sleep data for individual participants been lost? If true, were missing outcome data interpolated, averaged, simulated, or deleted?
Bias in measurement of the outcome	5.1 Were measurements, units, and signal processing approaches (including slow oscillillation, spindle, and coupling detection) used by the paper reliable and consistent with others?
	5.2 Were only nonparametric effect sizes including Spearman’s rho (ρ), Kendall’s tau (τ), or subjective estimation reported instead of Pearson’s r, Fisher’s z, or circular linear r?
	5.3 Did the authors analyze, transform, or clarify non-normal data, introduce resampling techniques and/or exclude outliers?
Bias in selection of the reported result	6.1 For multiple groups measured, if only group(s) with the largest effect size, or supported their hypotheses were reported, while non-significant or contradictory results were omitted?
	6.2 Have the authors declared their research proposal and expected outcomes within the framework of pre-registration, or declared any conflict of interest in the paper?
Overall Bias	7.1 Does the article not fully meet the applicable expectations of the Risk Of Bias In Non-randomized Studies of Interventions (Robins-I) and the above supplementary criteria in multiple domains listed?
Overall Bias	7.2 Alternatively, does the article significantly conflict with the criteria in one of these domains?

Appendix 2—table 1

Summary of models for SO–SP coupling–memory association measures.

Model	Moderator	Model Purposes
M	None	Study associations between SP amplitude, coupling phase, coupling strength, and coupling percentage, each in relation to memory consolidation.
M1	Memory Task	Investigate potential distinctions in coupling and memory association mechanisms between declarative memory—including verbal, spatial, and emotional memory—as well as procedural memory.
M2	Mean Age	Understand the potential impact of development and aging in coupling and memory associations.
M3	Spindle Type	Explore how the coupling between SOs and fast or slow SPs predicts memory retention performance differently.
M4	PSG Channel	Study the relation between sleep brain oscillations and memory in different cortical regions, as the frontal, central, and parietal areas were reported to be the most active area for SO–SP coupling but might play different roles.
M5	Sleep Stage	Examine the impact of sleep stage on the relationship between SO–SP coupling and memory, considering that SPs are most active during N2 sleep, while SOs dominate cortical oscillation during SWS.
M6	Sleep Bout	Investigate the potential impact of sleep timing and circadian rhythms on the relationship between SO–SP coupling and memory.
M7	Age × Channel	Investigate interactions between age differences and PSG channels in the memory consolidation mechanism, considering the frontal lobe is the latest area of the brain to develop.
M8	Age × Task	Study whether age increase implies a difference in predictive power of SO–SP coupling in the development of declarative and procedural memory consolidation.
M9	Channel × Spindle	Examine interactions between SP types and cortical areas in models.
Mf	All predictors	Include all pre-specified moderators to the model as fixed effects to explore their explanatory power and potential collinearity.
Mc	None	Fitted controlled model for focal and sensitivity analysis.

Appendix 2—table 2

Main characteristics for each study included in the meta-analysis.

Author (Year)	N	M_Age	Stage	Condition	PSG Channels	Spindles	Task	Memory Type	Measures Included
Bastian et al., 2022	15	23.3	N2, SWS	nap	frontal, central	fast, slow	Spatial	declarative	phase, amp, str, pct
Cox et al., 2018	24	30.2	N2, SWS	overnight	frontal, central, posterior	fast, slow	MST	motor	phase, str
Denis et al., 2022	31	22.3	N2, SWS	overnight	frontal, central	fast	IMG	declarative	phase, str, pct
Denis et al., 2021	34	22	N2, SWS	nap	frontal, central, posterior	fast, slow	WP	declarative	phase, amp, str, pct
Donnelly et al., 2022	16	14.1	N2, SWS	overnight	frontal, central, posterior	fast, slow	2 DL	declarative	phase, amp, str
Hahn et al., 2020	33	CH: 9.5, AD: 16	SWS	overnight	frontal, central, posterior	fast, slow	WP	declarative	phase, amp, str, pct
Hahn et al., 2022	42	AD: 12.9, YA: 22.0	SWS	overnight	frontal, central, posterior	fast, slow	Juggle	motor	phase, amp, str
Halonen et al., 2021	27	22	N2, SWS	overnight	frontal, central	fast	Metaphor	declarative	phase, str, pct
Halonen et al., 2022	151	17	N2, SWS	overnight	frontal, central	fast, slow	IMG	declarative	phase, amp, str, pct
Helfrich et al., 2018	52	YA: 20.4, OA: 73.8	SWS	overnight	frontal	fast	WP	declarative	phase, str
Kurz et al., 2021	19	11.24	N2, SWS	overnight	frontal, central, posterior	fast, slow	IMG	declarative	phase, amp, str, pct
Kurz et al., 2023	30	11.43	N2, SWS	overnight	frontal, central, posterior	fast, slow	Word List	declarative	phase, amp, str
Ladenbauer et al., 2021	43	YA: 23, OA: 66	N2, SWS	nap	frontal, central	fast	WP, VS	declarative	phase, amp, str
Mikutta et al., 2019	20	27.1	N2, SWS	overnight	central	fast, slow	Word List, MTT	declarative, motor	phase, amp, str
Mylonas et al., 2020	28	30	N2	overnight	central	fast	MST	motor	phase, amp, str, pct
Mylonas et al., 2022	14	13	N2	overnight	central	fast, slow	Spatial	declarative	phase, amp, str, pct
Nicolas et al., 2022	24	21.9	N2, SWS	nap	frontal, central, posterior	fast	MST	motor	phase, amp
Niknazar et al., 2015	28	22	N2	nap	central	fast	WP	declarative	phase, amp, str
Perrault et al., 2019	16	23.4	N2, SWS	overnight	frontal, posterior	fast, slow	WP	declarative	phase, amp
Schreiner et al., 2021	20	20.8	N2, SWS	nap	central	fast	WIP	declarative	phase, amp, str, pct
Solano et al., 2022	10	24.3	N2, SWS	overnight	frontal, central, posterior	fast, slow	VMA	motor	phase, amp, str, pct
Weiner et al., 2024	25	69.1	N2, SWS	overnight	frontal, central	fast, slow	WP	declarative	phase, amp, str
Zhang et al., 2020	28	20.6	N2, SWS	overnight	frontal, central, posterior	fast, slow	WP	declarative	phase, str

Notes. N sample size, only includes groups in the meta-analysis; N2 Stage 2 nREM sleep; SWS slow wave sleep; amp spindle amplitude; str coupling strength; pct oupling percentage; CH children; AD adolescents; YA young adults; OA older adults; PSG posterior channels include both parietal and occipital electrodes. Details about memory task types are listed in Table 7; additional detailed information and data are listed in Source data 1 (study-level characteristics) and source data of Figures 4 and 6—8 (effect size-level characteristics of each coupling metric).

Appendix 3—table 1

Summary of interaction and sensitivity models for the coupling phase-memory association.

Models	Weight	Factors	Estimate (95% CrI)	Age/Year slope (95% CrI)
Age× Channel	0.17	Age × Frontal	0.11(−0.05, 0.27)	0.001(−0.005, 0.007)
		Age × Central	0.19 (0.04, 0.33)	−0.007 (−0.012, −0.001)
		Age × Posterior	0.12 (−0.18, 0.43)	−0.004(−0.019, 0.012)
Age× Task	0.06	Age × Verbal	0.10 (−0.01, 0.25)	−0.001 (−0.006, 0.004)
		Age × Spatial	0.16 (−0.21, 0.56)	−0.010 (−0.022, 0.002)
		Age × Emotional	0.22 (−0.33, 0.71)	0.010 (−0.048, 0.028)
		Age × Motor	0.27 (−0.14, 0.68)	0.009 (−0.028, 0.010)
Channel× Spindle	0.16	Frontal × Fast SP	0.18 (0.06, 0.29)
		Central × Fast SP	0.06 (−0.05,0.16)
		Posterior × Fast SP	−0.01 (−0.18, 0.16)
		Frontal × Slow SP	0.02 (−0.11, 0.14)
		Central × Slow SP	0.04 (−0.09, 0.17)
		Posterior × Slow SP	−0.05 (−0.23, 0.44)
Time-lag	0.00	Time-lag bias		−0.010 (−0.050, 0.026)
Prior sensitivity	0.02	N(0, 2.5), InvGamma(2, 0.5)	0.07 (−0.01, 0.14)
Prior sensitivity	1.00	Non-informative	0.07 (0.01, 0.13)
Main model	1 − Weight	None	0.07 (0.01, 0.13)

Appendix 3—table 2

Summary of interaction and sensitivity models for the SP amplitude–memory association.

Models	Weight	Factors	Estimate (95% CrI)	Age/Year slope (95% CrI)
Age× Channel	0.00	Age × Frontal	0.17 (−0.02, 0.36)	−0.002 (−0.008, 0.003)
		Age × Central	0.15 (−0.05, 0.34)	−0.002 (−0.009, 0.004)
		Age × Posterior	0.13 (−0.28, 0.55)	−0.008 (−0.032, 0.016)
Age× Task	0.73	Age × Verbal	0.10 (−0.09, 0.31)	0.001 (−0.005, 0.007)
		Age × Spatial	0.38 (0.08, 0.67)	−0.009 (−0.016, −0.001)
		Age × Emotional	0.20 (−0.46, 0.73)	−0.015 (−0.058, 0.028)
		Age × Motor	−0.26 (−0.80, 0.35)	0.013 (−0.018, 0.044)
Channel× Spindle	0.00	Frontal × Fast SP	0.14 (-0.03, 0.32)
		Central × Fast SP	0.13 (−0.03, 0.23)
		Posterior × Fast SP	0.05 (−0.17, 0.28)
		Frontal × Slow SP	0.11 (−0.07, 0.28)
		Central × Slow SP	−0.01 (−0.20, 0.19)
		Posterior × Slow SP	−0.18 (−0.46, 0.10)
Time-lag	0.00	Time-lag bias		0.00 (−0.070, 0.070)
Prior sensitivity	0.00	N(0, 2.5), InvGamma(2, 0.5)	0.07 (−0.04, 0.18)
Prior sensitivity	1.00	Non-informative	0.07 (−0.04, 0.19)
Main model	1 − Weight	None	0.07 (−0.04, 0.18)

Appendix 3—table 3

Summary of interaction and sensitivity models for the coupling strength–memory association.

Models	Weight	Factors	Estimate (95% CrI)	Age/Year slope (95% CrI)
Age× Channel	0.00	Age × Frontal	0.14 (−0.03, 0.30)	−0.001 (−0.007, 0.004)
		Age × Central	0.18 (0.01, 0.33)	−0.005 (−0.011, 0.001)
		Age × Posterior	−0.06 (−0.38, 0.27)	0.009 (−0.009, 0.026)
Age× Task	0.00	Age × Verbal	0.11 (−0.04, 0.27)	−0.002 (−0.007, 0.003)
		Age × Spatial	0.13 (−0.18, 0.45)	−0.004 (−0.015, 0.007)
		Age × Emotional	0.17 (−0.39, 0.64)	−0.001 (-0.035, 0.035)
		Age × Motor	0.14 (−0.45, 0.67)	−0.004(−0.028, 0.023)
Channel× Spindle	0.00	Frontal × Fast SP	0.15 (0.01, 0.28)
		Central × Fast SP	0.02 (−0.09, 0.14)
		Posterior × Fast SP	0.08 (−0.12, 0.28)
		Frontal × Slow SP	0.04 (−0.11, 0.18)
		Central × Slow SP	0.05 (0.10, 0.20)
		Posterior × Slow SP	0.15 (−0.05, 0.35)
Time-lag	0.43	Time-lag bias		0.024 (−0.015, 0.060)
Prior sensitivity	0.26	N(0, 2.5), InvGamma(2, 0.5)	0.08 (0.00, 0.16)
Prior sensitivity	1.00	Non-informative	0.08 (0.02, 0.15)
Main model	1 − Weight	None	0.08 (0.02, 0.15)

Appendix 3—table 4

Summary of interaction and sensitivity models for the coupling percentage–memory association.

Models	Weight	Factors	Estimate (95% CrI)	Age/Year slope (95% CrI)
Age× Channel	0.40	Age × Frontal	−0.04 (−0.76, 0.72)	0.005 (−0.038, 0.045)
		Age × Central	−0.00 (−0.59, 0.63)	-0.001 (-0.036, 0.031)
		Age × Posterior	0.18 (−0.61, 0.98)	−0.014 (−0.062, 0.030)
Age× Task	0.65	Age × Verbal	0.42 (−0.24, 1.16)	−0.035 (−0.085, 0.008)
		Age × Spatial	−0.04 (−1.00, 1.07)	0.003 (−0.072, 0.072)
		Age × Emotional	0.21 (-0.54, 0.84)	−0.017 (−0.073, 0.034)
		Age × Motor	0.39 (−0.91, 1.49)	−0.015 (−0.085, 0.055)
Channel× Spindle	0.00	Frontal × Fast SP	0.02 (−0.16, 0.19)
		Central × Fast SP	−0.04 (−0.20, 0.13)
		Posterior × Fast SP	0.00 (−0.29, 0.27)
		Frontal × Slow SP	0.10 (−0.10, 0.29)
		Central × Slow SP	0.01 (−0.18, 0.19)
		Posterior × Slow SP	−0.07 (−0.36, 0.95)
Time-lag	NaN	Time-lag bias		Did not perform
Prior sensitivity	0.09	N(0, 2.5), InvGamma(2, 0.5)	−0.04 (−0.17, 0.09)
Prior sensitivity	1.00	Non-informative	−0.03 (−0.16, 0.07)
Main model	1 − Weight	None	−0.03 (−0.15, 0.07)

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Supplementary file 2 Model diagnostics. Example plots demonstrating the diagnostic process for each fitted Bayesian model, including posterior predictive checks, trace plots, and autocorrelation plots.: https://cdn.elifesciences.org/articles/101992/elife-101992-supp2-v1.pdf
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Supplementary file 3 Effect size-level forest plot.: https://cdn.elifesciences.org/articles/101992/elife-101992-supp3-v1.pdf
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Supplementary file 4 Pareto k diagnostic statistics.: https://cdn.elifesciences.org/articles/101992/elife-101992-supp4-v1.pdf
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Supplementary file 5 Frequentist analysis. Forest plots generated using frequentist analysis for each fitted overall Bayesian model.: https://cdn.elifesciences.org/articles/101992/elife-101992-supp5-v1.pdf
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Supplementary file 6 Posterior distributions of moderators.: https://cdn.elifesciences.org/articles/101992/elife-101992-supp6-v1.pdf
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Source data 1 Main table of study characteristics and participant demographics.: https://cdn.elifesciences.org/articles/101992/elife-101992-data1-v1.zip
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Thea Ng
Eunsol Noh
Rebecca MC Spencer

(2025)

Bayesian meta-analysis reveals the mechanistic role of slow oscillation-spindle coupling in sleep-dependent memory consolidation

eLife 13:RP101992.

https://doi.org/10.7554/eLife.101992.3

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Measurement of phase-amplitude coupling (PAC) in slow oscillation and spindle events.

Hierarchical diagram of coupling measures.

Risk of bias assessment summary plot adapted from ROBINS-I (Sterne et al., 2016).

Forest and regression plots for the association between SO-SP coupling phase and memory retention.

Figure 4—source data 1

Preferred slow oscillation-fast spindle coupling phase and its association with memory retention.

Forest and regression plots for the association between SP amplitude and memory retention.

Figure 6—source data 1

Forest and regression plots for the association between coupling strength and memory retention.

Figure 7—source data 1

Forest and regression plots for the association between coupling percentage and memory retention.

Figure 8—source data 1

PRISMA flow diagram of literature search, screening, and inclusion for systematic review and meta-analysis.

Risk of bias (ROB) assessment for individual studies.

Funnel Plot and Egger regression for assessing publication bias.

Comparison of sampling distributions of standardized Circlin rz under null.

Sampling distributions of standardized Circlin rz drawn from population correlations.

Preferred slow oscillation-slow spindle coupling phase and its association with memory retention.

Result of directional hypothesis tests for each pair of factor levels (conditions) in overall and each moderation model of the coupling phase-memory association.

Result of directional hypothesis tests for each pair of factor levels (conditions) in overall and each moderation model of the SP amplitude-memory association.

Result of directional hypothesis tests for each pair of factor levels (conditions) in overall and each moderation model of the coupling strength-memory association.

Results of directional hypothesis tests for each pair of factor levels (conditions) in overall and each moderation model of the coupling percentage–memory association.

Descriptive table of the meta-analysis result of measures of SO-SP coupling characteristics.

Interpretation of the standardized circular-linear correlation coefficient.

Summary of memory tasks.

Interpretation of Bayes Factor (BF10) for the strength of evidence.

Risk of bias assessment supplemental criteria.

Summary of models for SO–SP coupling–memory association measures.

Main characteristics for each study included in the meta-analysis.

Summary of interaction and sensitivity models for the coupling phase-memory association.

Summary of interaction and sensitivity models for the SP amplitude–memory association.

Summary of interaction and sensitivity models for the coupling strength–memory association.

Summary of interaction and sensitivity models for the coupling percentage–memory association.

MDAR checklist

Supplementary file 1

Supplementary file 2

Supplementary file 3

Supplementary file 4

Supplementary file 5

Supplementary file 6

Source data 1

Downloads (link to download the article as PDF)

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

Comparison of sampling distributions of standardized Circlin r_z under null.

Sampling distributions of standardized Circlin r_z drawn from population correlations.

Interpretation of Bayes Factor (BF₁₀) for the strength of evidence.