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• W2129658507 abstract "Mounting behavioral evidence in humans supports the claim that sleep leads to improvements in recently acquired, nondeclarative memories. Examples include motor-sequence learning [1Walker M.P. Brakefield T. Morgan A. Hobson J.A. Stickgold R. Practice with sleep makes perfect: Sleep-dependent motor skill learning.Neuron. 2002; 35: 205-211Abstract Full Text Full Text PDF PubMed Scopus (855) Google Scholar, 2Cohen D.A. Pascual-Leone A. Press D.Z. Robertson E.M. Off-line learning of motor skill memory: A double dissociation of goal and movement.Proc. Natl. Acad. Sci. USA. 2005; 102: 18237-18241Crossref PubMed Scopus (188) Google Scholar]; visual-discrimination learning [3Stickgold R. James L. Hobson J.A. Visual discrimination learning requires sleep after training.Nat. Neurosci. 2000; 3: 1237-1238Crossref PubMed Scopus (524) Google Scholar]; and perceptual learning of a synthetic language [4Fenn K.M. Nusbaum H.C. Margoliash D. Consolidation during sleep of perceptual learning of spoken language.Nature. 2003; 425: 614-616Crossref PubMed Scopus (288) Google Scholar]. In contrast, there are limited human data supporting a benefit of sleep for declarative (hippocampus-mediated) memory in humans (for review, see [5Stickgold R. Sleep-dependent memory consolidation.Nature. 2005; 437: 1272-1278Crossref PubMed Scopus (1058) Google Scholar]). This is particularly surprising given that animal models (e.g., [6Wilson M.A. McNaughton B.L. Reactivation of hippocampal ensemble memories during sleep.Science. 1994; 265: 676-679Crossref PubMed Scopus (1887) Google Scholar, 7Pavlides C. Winson J. Influences of hippocampal place cell firing in the awake state on the activity of these cells during subsequent sleep episodes.J. Neurosci. 1989; 9: 2907-2918PubMed Google Scholar, 8Nadasdy Z. Hirase H. Czurko A. Csicsvari J. Buzsaki G. Replay and time compression of recurring spike sequences in the hippocampus.J. Neurosci. 1999; 19: 9497-9507PubMed Google Scholar]) and neuroimaging studies (e.g., [9Peigneux P. Laureys S. Fuchs S. Collette F. Perrin F. Reggers J. Phillips C. Degueldre C. Del Fiore G. Aerts J. et al.Are spatial memories strengthened in the human hippocampus during slow wave sleep?.Neuron. 2004; 44: 535-545Abstract Full Text Full Text PDF PubMed Scopus (531) Google Scholar]) predict that sleep facilitates hippocampus-based memory consolidation. We hypothesized that we could unmask the benefits of sleep by challenging the declarative memory system with competing information (interference). This is the first study to demonstrate that sleep protects declarative memories from subsequent associative interference, and it has important implications for understanding the neurobiology of memory consolidation. Mounting behavioral evidence in humans supports the claim that sleep leads to improvements in recently acquired, nondeclarative memories. Examples include motor-sequence learning [1Walker M.P. Brakefield T. Morgan A. Hobson J.A. Stickgold R. Practice with sleep makes perfect: Sleep-dependent motor skill learning.Neuron. 2002; 35: 205-211Abstract Full Text Full Text PDF PubMed Scopus (855) Google Scholar, 2Cohen D.A. Pascual-Leone A. Press D.Z. Robertson E.M. Off-line learning of motor skill memory: A double dissociation of goal and movement.Proc. Natl. Acad. Sci. USA. 2005; 102: 18237-18241Crossref PubMed Scopus (188) Google Scholar]; visual-discrimination learning [3Stickgold R. James L. Hobson J.A. Visual discrimination learning requires sleep after training.Nat. Neurosci. 2000; 3: 1237-1238Crossref PubMed Scopus (524) Google Scholar]; and perceptual learning of a synthetic language [4Fenn K.M. Nusbaum H.C. Margoliash D. Consolidation during sleep of perceptual learning of spoken language.Nature. 2003; 425: 614-616Crossref PubMed Scopus (288) Google Scholar]. In contrast, there are limited human data supporting a benefit of sleep for declarative (hippocampus-mediated) memory in humans (for review, see [5Stickgold R. Sleep-dependent memory consolidation.Nature. 2005; 437: 1272-1278Crossref PubMed Scopus (1058) Google Scholar]). This is particularly surprising given that animal models (e.g., [6Wilson M.A. McNaughton B.L. Reactivation of hippocampal ensemble memories during sleep.Science. 1994; 265: 676-679Crossref PubMed Scopus (1887) Google Scholar, 7Pavlides C. Winson J. Influences of hippocampal place cell firing in the awake state on the activity of these cells during subsequent sleep episodes.J. Neurosci. 1989; 9: 2907-2918PubMed Google Scholar, 8Nadasdy Z. Hirase H. Czurko A. Csicsvari J. Buzsaki G. Replay and time compression of recurring spike sequences in the hippocampus.J. Neurosci. 1999; 19: 9497-9507PubMed Google Scholar]) and neuroimaging studies (e.g., [9Peigneux P. Laureys S. Fuchs S. Collette F. Perrin F. Reggers J. Phillips C. Degueldre C. Del Fiore G. Aerts J. et al.Are spatial memories strengthened in the human hippocampus during slow wave sleep?.Neuron. 2004; 44: 535-545Abstract Full Text Full Text PDF PubMed Scopus (531) Google Scholar]) predict that sleep facilitates hippocampus-based memory consolidation. We hypothesized that we could unmask the benefits of sleep by challenging the declarative memory system with competing information (interference). This is the first study to demonstrate that sleep protects declarative memories from subsequent associative interference, and it has important implications for understanding the neurobiology of memory consolidation. Participants first learned a list of word-pair associates (Ai-Bi), followed by a 12 hr, off-line, retention period containing sleep or wakefulness. After this retention period, but prior to testing, the sleep and wake groups were each split into interference and no-interference conditions (Figure 1). Subjects in the interference conditions learned a new list of word pairs (Ai-Ci) 12 min prior to testing, whereas the no-interference subjects went directly to testing. For all participants, the primary outcome was mean percent cued recall of the target words (Bi). We performed pairwise comparisons of individual groups by using two-tailed t tests (assuming unequal variances). Statistical analyses for recall performance were conducted on data (proportion of correct answers) after arcsine transformation of all measures [10Kleinbaum D.G. Kupper L.L. Muller K.E. Nizam A. Applied Regression Analysis and Other Multivariable Methods.Third Edition. Duxbury Press, Pacific Grove, CA1998Google Scholar]. (Means, standard deviations, and standard errors are presented numerically and graphically in their untransformed form.) In the no-interference conditions, mean recall was marginally higher in the sleep group (mean [M] = 94%, standard deviation [SD] = 7), than in the wake group (M = 82%, SD = 17), t(18) = 1.97, p = .064. However, in the interference conditions, there was a large and highly significant difference between the sleep-interference group (M = 76%, SD = 17) and wake-interference (M = 32%, SD = 19), t(22) = 5.34, p < .0001 (Table 1). We also performed a two-way, between-subjects ANOVA (n = 48) demonstrating significant main effects of sleep [F (1,47) = 26.93, p <.0001] and interference [F (1,47) = 46.17, p <.0001], as well as a significant sleep-by-interference interaction [F (1,47) = 5.84, p = .02] (Figure 2).Table 1Mean Percent Recall of the First List and Second List in the Entire SampleRecall (SD)paStatistical analyses for recall performance were conducted on data after arcsine transformation of all measures, formula = [arcsine(sq-rt(accuracy proportion))] [10].Cohen's dConditionnBCbParticipants in these no-interference conditions did not undergo associative-interference testing.BBWake1282 (17)-0.0640.92Sleep1294 (7)-Wake-I1232 (19)94 (8)<.00013.07Sleep-I1276 (17)96 (6)Recall of the first list was recall of B of the A-B pair. Recall of the second list was recall of C of the A-C pair.a Statistical analyses for recall performance were conducted on data after arcsine transformation of all measures, formula = [arcsine(sq-rt(accuracy proportion))] 10Kleinbaum D.G. Kupper L.L. Muller K.E. Nizam A. Applied Regression Analysis and Other Multivariable Methods.Third Edition. Duxbury Press, Pacific Grove, CA1998Google Scholar.b Participants in these no-interference conditions did not undergo associative-interference testing. Open table in a new tab Recall of the first list was recall of B of the A-B pair. Recall of the second list was recall of C of the A-C pair. We also examined a number of outcome variables that do not directly impact our hypothesis but that address a common concern in sleep research: circadian performance. We compared the total number of trials necessary for a subject to learn all the word pairs at different times of day and found no significant differences between training in the morning (a.m.) and evening (p.m.) [A-B lists – p.m.: M = 105, SD = 23; a.m.: M = 118, SD = 42; t(36) = −1.26, p = .22; and A–C lists – p.m.: M = 99, SD = 23; a.m.: M = 115, SD = 39; t(18) = −1.2, p = 0.23]. We also compared second-list recall (C of A–C) at 12 min after training and found no significant differences between the morning and evening performance [a.m.: M = 96%, SD = 6; p.m.: M = 94%, SD = 8; t(21) = 0.71, p = 0.49]. To further address the concern for time-of-day effects, we ran an additional, independent group: 24 hr pm to pm, with interference (24-hr-PM-I). Participants in this group (n = 12) underwent the same screening, training, and testing procedures as those in the two 12 hr interference groups, Sleep-I and Wake-I. However, unlike the Sleep-I and Wake-I groups, this 24-hr-PM-I group was tested and trained at the same time of day (9 p.m.). Performance in this 24-hour-PM-I group (M = 71%, SD = 25) was nearly identical to that in the Sleep-I group, t(20) = −0.32, p = 0.75, and significantly better than that in the Wake-I group, t(21) = 4,13, p < .001 (Figure 3). This is the first study to demonstrate that sleep protects declarative memories from subsequent, associative interference. Our data show a benefit of sleep for declarative memory and suggest that sleep actively strengthens declarative memories, which it renders resistant to interference. We showed that cued recall of paired associates after 12 hr retention intervals containing sleep or wakefulness yields small differences in recall (13% relative reduction in performance in the Wake group compared to Sleep), a trend consistent with previous studies (e.g., [11Ekstrand B.R. Effect of sleep on memory.J. Exp. Psychol. 1967; 75: 64-72Crossref PubMed Scopus (61) Google Scholar]), whereas introducing associative interference after the delay demonstrated robust, large differences (58% reduction). Thus, although a memory trace may appear only modestly improved after similar intervals of sleep compared to wakefulness, the pronounced, beneficial effects of sleep are unmasked by interference testing; after wakefulness, memories remain highly susceptible to associative interference, whereas memories after sleep are resilient to disruption. We propose that sleep plays an active role in consolidating declarative memories and makes them resistant to interference. It should be noted that the data from the no-interference sleep group approached ceiling, which might have caused us to underestimate the difference in recall of these groups. In addition, it remains unclear whether this sleep benefit is specific for associative processes (i.e., A-B resistant to A-C interference) or is a more general memory effect (i.e., A-B resistant to C-D). Finally, although time-of-day effects are always a concern in sleep studies, we find it unlikely that they account for the findings of this study. There was no difference, at either time of day, in the amount of training needed for subjects to learn all the word pairs, and the training mechanism itself is designed to account for inter-individual differences by providing more learning trials—for those who require it—to reach an equal level of learning. Results of the 24-hr-PM-I group additionally argue against a time-of-day effect because training and testing took place at the same time of day. In addition to arguing against time-of-day effects, results of the 24-hr-PM-I group demonstrate that sleep provides a benefit that persists throughout the subsequent waking day. Although we did not attempt to control waking mental activities in the wake groups, this was equally true for all groups. If incidental interference (i.e., nonexperimental interference that occurs as a result of waking mental activity) were to account for differences seen in our study between the 12 hr Wake-I and Sleep-I groups, then the 24-hr-PM-I group should perform at least as poorly as the Wake-I because members of this group had more than 12 hr of wakefulness; however, they performed considerably better. These data collectively indicate that the benefit that sleep provides declarative memory is not a passive (i.e., transient) protection against interference while an individual is asleep (a perspective inherited from the work of Jenkins and Dallenbach [12Jenkins J.G. Dallenbach K.M. Obliviscence during sleep and waking.Am. J. Psychol. 1924; 35: 605-612Crossref Google Scholar]). Rather, sleep actively stabilizes memories such that they become resistant to interference in the subsequent day. This study clarifies and extends prior work attempting to understand the role of sleep in declarative-memory consolidation. Many studies have emphasized individual sleep stages, sleep deprivation, or both in their experimental paradigms (for a review of traditional study designs, and exemplary studies, see [13Smith C. Sleep states and memory processes in humans: Procedural versus declarative memory systems.Sleep Med. Rev. 2001; 5: 491-506Abstract Full Text PDF PubMed Scopus (271) Google Scholar]). Two recent studies extended the work of Barrett et al. [14Barrett T.R. Ekstrand B.R. Effect of sleep on memory: III. Controlling for time-of-day effects.J. Exp. Psychol. 1972; 96: 321-327Crossref PubMed Scopus (96) Google Scholar] and emphasized the role of slow wave sleep (SWS) in declarative-memory consolidation [15Plihal W. Born J. Effects of early and late nocturnal sleep on declarative and procedural memory.J. Cogn. Neurosci. 1997; 9: 534-547Crossref PubMed Scopus (677) Google Scholar, 16Gais S. Born J. Low acetylcholine during slow-wave sleep is critical for declarative memory consolidation.Proc. Natl. Acad. Sci. USA. 2004; 101: 2140-2144Crossref PubMed Scopus (311) Google Scholar]. They showed enhanced performance across the first half of the night (so-called “early sleep,” a portion of sleep with relatively large amounts of SWS) compared to a matched period of sleep deprivation. We have extended these findings by examining sleep across an entire night and comparing them to wakefulness across the daytime (i.e., without acute sleep deprivation). Ekstrand [11Ekstrand B.R. Effect of sleep on memory.J. Exp. Psychol. 1967; 75: 64-72Crossref PubMed Scopus (61) Google Scholar] demonstrated that cued recall receives a similar benefit of sleep as our no-interference groups. We demonstrated a much larger effect size, and more significant effect of sleep, when participants were tested after associative interference. By tapping a particular sleep-provided benefit—rendering memories resistant to interference—we were able to show a robust benefit of sleep across the entire night and even across 24 hr. Other studies have examined A-B/A-C learning paradigms and sleep. Norman et al. applied a computational, neural network (the complementary-learning-system model [17McClelland J.L. McNaughton B.L. O'Reilly R.C. Why there are complementary learning systems in the hippocampus and neocortex: Insights from the successes and failures of connectionist models of learning and memory.Psychol. Rev. 1995; 102: 419-457Crossref PubMed Scopus (2993) Google Scholar, 18O'Reilly R.C. Rudy J.W. Conjunctive representations in learning and memory: principles of cortical and hippocampal function.Psychol. Rev. 2001; 108: 311-345Crossref PubMed Scopus (603) Google Scholar]) to study the effects of REM sleep on semantic learning in neocortical architecture [19Norman K.A. Newman E.L. Perotte A.J. Methods for reducing interference in the complementary learning systems model: Oscillating inhibition and autonomous memory rehearsal.Neural Netw. 2005; 18: 1212-1228Crossref PubMed Scopus (58) Google Scholar]. This computational model demonstrates that semantic knowledge, represented by extensive A-B training, is “repaired” by REM sleep epochs that alternate with A-C learning. Ekstrand [11Ekstrand B.R. Effect of sleep on memory.J. Exp. Psychol. 1967; 75: 64-72Crossref PubMed Scopus (61) Google Scholar] demonstrated that disruption of A-B learning by immediate A-C learning—all before sleep—can be recovered by subsequent sleep (although in a subsequent Ekstrand concluded that the interference effects he observed were not due to sleep [20Ekstrand B.R. Sullivan M.J. Parker D.F. West J.N. Spontaneous recovery and sleep.J. Exp. Psychol. 1971; 88: 142-144Crossref PubMed Scopus (36) Google Scholar]). Our findings extend these studies by demonstrating that sleep leads to the protection of episodic memories from subsequent interference; when we sleep after learning new, episodic information, the memories become resistant to disruption by subsequent learning. Evidence from animal models and human neuroimaging studies predicts the active participation of sleep in hippocampus-mediated memory consolidation. Several animal studies demonstrate that recently acquired, hippocampus-based memories are “replayed” during sleep (e.g.,[6Wilson M.A. McNaughton B.L. Reactivation of hippocampal ensemble memories during sleep.Science. 1994; 265: 676-679Crossref PubMed Scopus (1887) Google Scholar, 7Pavlides C. Winson J. Influences of hippocampal place cell firing in the awake state on the activity of these cells during subsequent sleep episodes.J. Neurosci. 1989; 9: 2907-2918PubMed Google Scholar, 8Nadasdy Z. Hirase H. Czurko A. Csicsvari J. Buzsaki G. Replay and time compression of recurring spike sequences in the hippocampus.J. Neurosci. 1999; 19: 9497-9507PubMed Google Scholar]) and that this reverberation is coherent with associated neocortex (e.g., [21Qin Y.L. McNaughton B.L. Skaggs W.E. Barnes C.A. Memory reprocessing in corticocortical and hippocampocortical neuronal ensembles.Philos. Trans. R. Soc. Lond. B Biol. Sci. 1997; 352: 1525-1533Crossref PubMed Scopus (204) Google Scholar, 22Sirota A. Csicsvari J. Buhl D. Buzsaki G. Communication between neocortex and hippocampus during sleep in rodents.Proc. Natl. Acad. Sci. USA. 2003; 100: 2065-2069Crossref PubMed Scopus (579) Google Scholar]). Recent neuroimaging findings in humans further demonstrate increased hippocampal activity during sleep after spatial learning [9Peigneux P. Laureys S. Fuchs S. Collette F. Perrin F. Reggers J. Phillips C. Degueldre C. Del Fiore G. Aerts J. et al.Are spatial memories strengthened in the human hippocampus during slow wave sleep?.Neuron. 2004; 44: 535-545Abstract Full Text Full Text PDF PubMed Scopus (531) Google Scholar]. Collectively, these studies suggest that hippocampus-dependent memories are repeatedly reactivated during sleep and that coherent networks form within and between appropriate brain regions. This sleep-dependent, reiterative process orchestrates the strengthening of memories and thereby renders them less vulnerable to interference. It is plausible that such biological mechanisms underlie the critical role we observed for sleep in declarative-memory consolidation. This is the first study to demonstrate that sleep protects declarative memories from associative interference in the subsequent day, and it thereby provides key evidence that sleep does not passively (i.e., transiently) protect declarative memories; rather, sleep plays an active role in declarative-memory consolidation. Our study provides a source of convergence among human behavior, animal research, computational models, and neuroimaging studies for investigations of declarative-memory consolidation. Although further research is needed to define the empirical limits and physiological correlates of this sleep and memory interaction, our study provides a new framework for considering the effects of sleep on human memory: sleep helps consolidate declarative memories and renders them resistant to associative interference." @default.
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• W2129658507 title "Interfering with Theories of Sleep and Memory: Sleep, Declarative Memory, and Associative Interference" @default.
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