Downloaded from learnmem.cshlp.org on September 23, 2021 - Published by Cold Spring Harbor Laboratory Press Research Retrieval and sleep both counteract the forgetting of spatial information James W. Antony1,2 and Ken A. Paller1,3 1Interdepartmental Neuroscience Program, Northwestern University, Evanston, Illinois 60208, USA; 2Princeton Neuroscience Institute, Princeton University, Princeton, New Jersey 08544, USA; 3Department of Psychology, Northwestern University, Evanston, Illinois 60208, USA Repeatedly studying information is a good way to strengthen memory storage. Nevertheless, testing recall often produces superior long-term retention. Demonstrations of this testing effect, typically with verbal stimuli, have shown that repeated retrieval through testing reduces forgetting. Sleep also benefits memory storage, perhaps through repeated retrieval as well. That is, memories may generally be subject to forgetting that can be counteracted when memories become reactivated, and there are several types of reactivation: (i) via intentional restudying, (ii) via testing, (iii) without provocation during wake, or (iv) during sleep. We thus measured forgetting for spatial material subjected to repeated study or repeated testing followed by retention intervals with sleep versus wake. Four groups of subjects learned a set of visual object-location associations and either restudied the associations or recalled locations given the objects as cues. We found the advantage for restudied over retested information was greater in the PM than AM group. Additional groups tested at 5-min and 1-wk retention intervals confirmed previous findings of greater relative benefits for restudying in the short-term and for retesting in the long-term. Results overall support the conclusion that repeated reactivation through testing or sleeping stabilizes information against forgetting. A fundamental aspect of memory is that it degrades over time. One wakefulness (Jenkins and Dallenbach 1924; Yaroush et al. 1971; way to prevent degradation is to repeatedly reengage with the same Benson and Feinberg 1977; Plihal and Born 1997). Predominant material after initial encoding. Numerous studies and memory the- models propose that memories are reactivated during sleep, lead- ories have focused on memory differences following two types of ing to their stabilization (Diekelmann and Born 2010; Oudiette reengagement—restudying and testing without feedback. For ex- and Paller 2013). Interestingly, sleep may preferentially aid weaker ample, a student might attempt to master some material learned memories that still need to be recalled (Norman et al. 2005; van de during a lecture by reading notes taken during the lecture or by at- Ven et al. 2016). For instance, greater encoding difficulty increases tempting to recall some of the material without the notes. Students benefits of sleep relative to wakefulness (Schmidt et al. 2006; Payne often prefer the former strategy, but it can produce inflated impres- et al. 2012a), and reactivating memories with cues during sleep re- sions of one’s mastery of the material (Karpicke and Roediger sults in greater benefits for memories of intermediate than high ac- 2008). Moreover, on tests taking place within an hour of learning, curacy prior to sleep (Creery et al. 2014). restudying typically produces superior retrieval compared to test- Though restudy often benefits memory relative to retrieval in ing without feedback (Roediger and Karpicke 2006a; Kornell et al. the short-term, the long-term benefits of retrieval suggest restudied 2011; Bai et al. 2015). After delays longer than a few hours, howev- information may be less stabilized. Therefore, sleep may benefitre- er, testing benefits memory more than restudying, a phenomenon studied more than retrieved information. Bäuml et al. (2014) con- known as the “testing effect” (Abbott 1909; Gates 1917; Spitzer vincingly showed across a series of experiments that restudied 1939; Carrier and Pashler 1992; Roediger and Karpicke 2006b; information benefits more than tested information over sleep Carpenter et al. 2008). than wake. They interpreted their findings to indicate that sleep de- With the passage of time after learning, memories can become creases the testing effect. However, they also noted an alternative less accessible, while exposure to interfering information is known interpretation—rather than crediting sleep, it could be that pro- to directly interfere with memory accessibility (i.e., retroactive in- longed wake enhances interference, resulting in an increased rela- terference). Interestingly, testing protects memories from retroac- tive preservation of tested items. Because they did not include a tive interference (Potts and Shanks 2012), and tasks that add 24-h condition, they were unable to directly test this possibility. retroactive interference between encoding and practice tests in- Here we investigated the interaction of learning strategy and crease the relative stability of tested, as opposed to restudied, infor- sleep on memory. Although most studies of testing effects have mation (Halamish and Bjork 2011). These studies show that used verbal information, we used spatial information, for which varying amounts of interference can modulate the relative strength testing effects have also been found (Carpenter and Kelly 2012). of tested versus restudied information while controlling for the In our study, learning occurred in the morning or evening, with passage of time. a final test after either a 12- or 24-h retention interval (Fig. 1A), al- Another way to vary interference while controlling for the lowing us to test the competing accounts posed above. passage of time involves measuring memory performance across a sleep or wake interval. Intervals of sleep have been repeatedly # 2018 Antony and Paller This article is distributed exclusively by Cold Spring shown to preserve declarative memories relative to intervals of Harbor Laboratory Press for the first 12 months after the full-issue publication date (see http://learnmem.cshlp.org/site/misc/terms.xhtml). After 12 months, it is available under a Creative Commons License (Attribution-NonCommercial Corresponding author: [email protected] 4.0 International), as described at http://creativecommons.org/licenses/by-nc/ Article is online at http://www.learnmem.org/cgi/doi/10.1101/lm.046268.117. 4.0/. 25:258–263; Published by Cold Spring Harbor Laboratory Press 258 Learning & Memory ISSN 1549-5485/18; www.learnmem.org Downloaded from learnmem.cshlp.org on September 23, 2021 - Published by Cold Spring Harbor Laboratory Press Sleep and the testing effect ABversus 24-h) × time of encoding (AM ver- sus PM) × memory strategy (S versus T) ANOVA. As expected, we found a main ef- fect of retention interval, such that mem- ory worsened between the 12- and 24-h groups [F(1,60) = 4.0, P = 0.04]. Memory was also superior for restudied versus re- tested information [F(1,60) = 22.2, P < 0.001], an effect we attribute to strong initial learning (as discussed further be- low). We found no main effect of time of day [F(1,60) = 0.46, P = 0.51]. No two-way interactions were significant [retention interval × time of encoding: F(1,60) = 0.158, P = 0.69; retention interval × strat- egy: F(1,60) = 0.836, P = 0.36; time of en- coding × strategy: F(1,60) = 1.20, P = 0.28]. Finally, there was a marginal three-way in- teraction between the factors [F(1,60) = Figure 1. Paradigm and experimental overview. (A) During learning, subjects encoded the location of 3.37, P = 0.07], to be revisited below in objects, took practice tests with feedback, and then either restudied or retested on each object again light of our a priori predictions. without feedback. An example test trial is shown below, with an object shown where it might have been placed on the grid, as well as in its original location (shown as feedback). After this learning session (L), they returned to the laboratory to take a final test (T), as shown in (B) for each of the six groups. Sleep aided restudied more than retested information, but only at the 12-h interval Immediately after initial learning, object-location associations We next followed up our main prediction that sleep compared to were restudied (S) or retested (T) thrice more before the final test. wake would preferentially benefit restudied versus retested infor- We thus contrasted retention as a function of both the testing ef- mation. We tested this with a two-way, time of encoding (AM ver- fect and whether the retention interval included sleep. In line sus PM) × memory strategy (S versus T) ANOVA within 12-h groups. fi with the ndings of Bäuml et al. (2014), we hypothesized a relative We found a significant main effect of memory strategy [F(1,29) = preservation of restudied versus retested items during sleep, giving 16.4, P < 0.001], no main effect of time of encoding [F(1,29) = 0.61, rise to a preferential benefit for restudied versus retested informa- P = 0.43], and, critically, a significant interaction between the fac- tion in the 12-h PM group (sleep during the retention interval) ver- tors [F(1,29) = 4.6, P = 0.040]. Follow-up t-tests featuring direct com- sus the 12-h AM group (no sleep during the retention interval). parisons between restudied items in the AM versus PM group were Results could thus be used to test the alternative interpretation not significant [t(29) = 1.6, P = 0.11, d = 0.6], nor were they signifi- fi that wake enhances the bene ts of testing, rather than that sleep cant for tested items [t(29) = 0.25, P = 0.81, d = 0.08; Fig. 2]. reduces them. We next asked whether relative PM restudy benefits extended Additionally, we hypothesized memory would be better for to the 24-h group. We found no benefits using same contrasts as restudied information after 5-min intervals and retested informa- above [restudy 24-h AM versus PM: t(31) = 0.03, P = 0.98, d = 0.01; tion at intervals longer than a few hours, as is typical for the testing effect (Wheeler et al.