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. Author manuscript; available in PMC: 2020 Oct 1.
Published in final edited form as: Sleep Med Rev. 2019 Jun 5;47:39–50. doi: 10.1016/j.smrv.2019.05.004

Table 1:

Summary of studies reviewed in the systematic analysis.

Learning Type Task Rule Type Study N Subjects Design Sleep Time Implicit Effect Explicit effect Sleep correlates
Insight NRT T Wagner et al., 2004 [9] 106 Adults Sleep vs. Wake Overnight No Yes -
NRT T Yordanova et al., 2008 [31]; 2009a [90], 2009b [91], 2010 [92], 2012 [12] 55 Adults SWS-rich vs. REM-rich Overnight No Yes SWS
NRT T Debarnot et al., 2017 [93] 74 Adults, Elderly Sleep vs. Wake
Young vs. Old
Overnight - Yes (young)
No (elderly)
-
Virtual Map Insight T Lerner & Gluck, 2018 [32] 20 Adults Single Sleep Group Multiple Nights Yes No SWS
Surveillance T Lerner et al., 2019 [33] 24 Adults Cue vs. sham Overnight Yes Indirect a nREM
Visuo-Motor Sequence Learning SRTT T Maquet et al., 2000 [37]; Peigneux et al., 2003 [94] 31 Adults Sleep vs. Wake b
Structured vs. Random
Overnight Yes No REM
SRTT T Robertson et al., 2004 [34] (implicit instructions condition) 36 Adults Sleep vs. Wake Overnight No No -
SRTT T Robertson et al., 2005 [95] 44 Adults Sleep vs. Wake Overnight Yes (some conditions) c No -
SRTT T Spencer et al., 2006 [76], (implicit instructions condition) 50 Adults Sleep vs. Wake Overnight Yes (some conditions) d No -
SRTT T Spencer et al., 2007 [96], (implicit instructions condition) 16 Elderly Sleep vs. Wake Overnight No No -
SRTT T Ertelt et al., 2012 [97] 37 Adults Sleep vs. Wake Overnight Yes No -
SRTT T Pace-Schott & Spencer, 2013 [98] 112 Adults, Elderly Sleep vs. Wake Overnight Yes (young)
No (elderly)
No -
SRTT T Wilhelm et al., 2013 [39] 161 Children, Adults Sleep vs. Wake Overnight - Yes SWS
SRTT T Song et al., 2014 [99] (unintentional group) 40 Adults Sleep vs. Wake Overnight No No -
SRTT T Cousins et al., 2014 [100] 32 Adults Cueing before vs. during sleep Overnight Yes Yes SWS, Spindles
SRTT T Kirov et al., 2015 [101] 53 Adults Single sleep group Overnight - Yes nREM-REM tr.
SRTT T Diekelmann et al., 2016 [40] 36 Men, Women Cue vs. sham Overnight No Yes (men)
No (women)
SWS
SRTT T Cousins et al., 2016 [64] 22 Adults Single sleep group, cued vs. uncued target Overnight Yes Indirect e SWS, REM
SRTT T Zinke et al., 2017 [102] 25 Children Single sleep group Overnight No Yes Spindles
SRTT T Yordanova et al., 2017 [103] 53 Adults Single sleep group Overnight No Yes Spindles
SRTT T Lutz et al., 2018 [104] 117 Adults Sleep vs. Wake Overnight Yes Yes f -
Ocular SRTT T Albouy et al., 2006 [105] 49 Adults Sleep vs. Wake Overnight Yes No -
ASRT T Song et al., 2007 [36] 36 Adults Sleep vs. Wake Overnight No No -
ASRT T Nemeth et al., 2010 [41] 25 Adults, Elderly Sleep vs. Wake Overnight No No -
ASRT T Hallgato et al., 2013 [106] 102 Adults Sleep vs. Wake Overnight No No -
ASRT T Csabi et al., 2014 [107] 34 Adults OSA vs. control Overnight No No -
High-order SRTT T Fischer et al., 2006 [11] 20 Adults Sleep vs. Wake Overnight No Yes -
High-order SRTT T Fischer et al., 2007 [35] 25 Children, Adults Sleep vs. Wake Overnight No (children)
Yes (adults)
- -
High-order SRTT T Drosopoulos et al., 2011 [81] 40 Adults Sleep vs. SD Overnight - Yes -
Statistical Learning Tone Learning T Durrant et al., 2011 [14] 36 Adults Sleep vs. Wake Overnight Yes - SWS
Tone Learning T Durrant et al., 2012 [49], 2016 [50] 48 Adults Sleep vs. Wake Nap Yes - SWS
Tone Learning T Hennies et al., 2017 [108] 42 Adults Cue at sleep vs. wake Overnight Yes - SWS
WPT S Djonlagic et al., 2009 [28] 99 Adults Sleep vs. Wake Overnight Yes (some conditions) Indirect (some conditions) g REM
WPT S Barsky et al., 2015 [47] 51 Adults Sleep vs. Wake Nap Yes - REM
WPT S Kemeny & Lukacs, 2016 [109] 44 Adults Sleep vs. Wake Overnight No -
WPT S Lerner et al., 2016 [48] (experiment 2) 20 Adults Single sleep group Multiple Nights Yes - SWS, N1/N2
Artificial Grammar Learning (AGL) AXB words T Gomez et al., 2006 [5] 48 Infants Sleep vs. Wake Nap Yes - -
AXB words T Hupbach et al., 2009 [61] 48 Infants Sleep vs. Wake Nap Yes - -
AXB words T Frost & Monaghan et al., 2017 [62] 72 Adults Sleep vs. Wake Overnight Yes - -
Syllable regularity S h Gaskell et al., 2014 [45] 38 Adults Single cued sleep group Nap Yes No SWS
“Reber”-like Grammar 1 T Nieuwnhuis et al., 2013 [110] 81 Adults Sleep vs. Wake Overnight Yes - -
“Reber”-like Grammar 2 T Kemeny & Lukacs, 2016 [109] 45 Adults Sleep vs. Wake Overnight No - -
“Reber”-like Grammar 3 S g Batterink & Paller, 2017 [44] 44 Adults Single cued sleep group Nap Yes No SWS
Segmentation T Simon et al., 2017 [46] 37 Infants Sleep vs. Wake Nap Yes - SWS
Relational Memory Transitive Inference S Ellenbogen et al., 2007 [4] 56 Adults Sleep vs. Wake Overnight Yes No -
Transitive Inference S Werchen & Gomez, 2013 [42] 64 Adults Sleep vs. Wake Overnight Yes No -
Associative Inference S Lau et al., 2010 [13] 31 Adults Sleep vs. Wake Nap Yes - SWS
Associative Inference S Alger & Payne, 2016 [43] 58 Adults Sleep vs. Wake Nap Yes - REM
Information-Integration Frequency-Orientation Associations S Maddox et al., 2009 [30] 49 Adults Sleep vs. SD Overnight Yes - -
Visual-Audio Associations S Hennies et al., 2014 [29] 52 Adults Sleep vs. Wake Overnight No No i -
Tone-Density Associations S Ashton et al., 2018 [51] 95 Adults Sleep vs. Wake Overnight Yes j No -
Generalization of Categorical Learning Prototypes (AB task) S Maddox et al, 2011 [58] 18 Adults Sleep vs. SD Overnight No - -
Objects S Werchan & Gomez, 2014 [60] 27 Infants Sleep vs. Wake Nap No - -
Dot Pattern S Graveline & Wamsley, 2017 [56] 73 Adults Sleep vs. Wake Overnight Yes - -
Satellites S Schapiro et al., 2017 [59] (novel items condition) 193 Adults Sleep vs. Wake Overnight, Nap - No REM k
Abstract images S Lutz et al., 2017 [57] 28 Adults Sleep vs. Wake Overnight No l - REM k
Movies T Sandoval et al., 2017 [55] 79 Children Sleep vs. Wake Nap Yes - -
Novel objects S Friedrich et al., 2015 [52] 90 Infants Sleep vs. Wake Nap Yes - Spindles
Novel objects S Friedrich et al., 2017 [53] 107 Infants Sleep vs. Wake Nap Yes - Spindles, N2
Novel objects S Friedrich et al., 2019 [54] 30 Infants Single sleep group Nap Yes - Spindles

Note: T and S in the ‘Rule type’ column refers to Temporal and Stationary regularities, respectively; ASRT, Alternating Serial Response Time task; nREM, non-REM; NRT, Number Reduction Task; OSA, Obstructive sleep apnea; REM, Rapid Eye Movement; SD, Sleep Deprivation; SRTT, Serial Reaction Time Task; SWS, Slow Wave Sleep; tr, transitions; WPT, Weather Prediction Task;

a

Cueing during sleep was correlated to implicit measures, which themselves were strongly influenced by explicit rule detection;

b

Wake and sleep groups were compared in order to identify brain regions showing higher activation during REM sleep; then, those regions were used to detect correlations with performance improvement for a sleep group that trained on structured sequences compared to a group that trained on random sequences;

c

sleep was shown to prevent the obstruction of regularities extraction caused by Transcranial Magnetic Stimulation (TMS) delivered following training; without TMS, however, no sleep effect was found;

d

sleep effect found only in the ‘contextual’ condition where additional hidden hints regarding the regularity were present;

e

no effects of cueing on explicit behavioral measures, but existing correlations between explicit measures and brain measures;

f

Explicit effects found for confidence ratings of a generation task (‘triplet completion’), though not for generation accuracy;

g

explicit rule knowledge not examined, but sleep was shown to facilitate explicit evaluation of simple stimulus-response probabilities when conditions prevented pre-sleep training performance to approach ceiling levels;

h

stimuli were words presented visually that were also read aloud; thus, the hidden rule could be discovered based on extraction of either stationary or temporal regularities;

i

explicit measurements were based on metrics from three additional tests. Although none of these tests directly required to state the hidden two-dimensional rule, one was reminiscent of a generation test (i.e., requiring to generate new examples of the rule) as defined in Methods;

j

no effects immediately following sleep, but sleep affected the ability to relearn the stimuli a week later;

k

REM sleep was associated to performance in memory tests but not in generalization tests (which were absent);

l

Effects were not found immediately following sleep; some sleep effects were found a year later, but at that point the generalization items were not totally novel.