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The Effects of Sleep on Episodic Memory in Older and Younger Adults

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The Effects of Sleep on Episodic Memory in Older and Younger Adults MEMORY, 0000, 00 (00), 1Á8 The effects of sleep on episodic memory in older and younger adults Mariam Aly and Morris Moscovitch University of Toronto, Canada Evidence on sleep-dependent benefits for episodic memory remains elusive. Furthermore we know little about age-related changes on the effects of sleep on episodic memory. The study we report is the first to compare the effects of sleep on episodic memories in younger and older adults. Memories of stories and personal events were assessed following a retention interval that included sleep and following an equal duration of wakefulness. Both older and younger adults have superior memory following sleep compared to following wakefulness for both types of material. Amount of forgetting of personal events was less during wakefulness in older adults than in younger adults, possibly due to spontaneous rehearsal. Amount of time spent sleeping correlated highly with sleep benefit in older adults, suggesting that quantity of total sleep, and/or time spent in some stages of sleep, are important contributors to age- related differences in memory consolidation or protection from interference during sleep. Keywords: Ageing; Episodic memory; Sleep; Memory consolidation. The notion that sleep may enhance our capacity Despite a plethora of research on the topic, for alert mental functioning is a widespread one, knowledge about the effects of sleep on memory reflected in the popularity of advice to ‘‘sleep is limited in two respects. First, while experiments tight and wake bright’’. Far from mere folk investigating procedural memory improvements wisdom, this idea has been given empirical have consistently shown benefits gained from validation with regard to memory in particular. sleep, evidence of sleep-dependent episodic mem- As early as 1924 the studies of Jenkins and ory consolidation has been more elusive (for Dallenbach demonstrated superior memory for examples see Plihal & Born, 1997; Yaroush, nonsense syllables following an interval contain- Sullivan, & Ekstrand, 1971; Walker, 2005). Sec- ing sleep, compared to an equivalent duration of ond, age-related changes in the effects of sleep on wakefulness. Since then many experiments em- memory have been largely ignored. Our paper ploying different paradigms and assessing differ- aims to rectify this situation. ent aspects of memory have been conducted, Sleep may have differential effects on memory providing support for both episodic and proce- for older and younger adults, due to a multitude dural memory consolidation during sleep (see of changes in sleep architecture that occur with Gais & Born, 2004; Paller & Voss, 2004; Payne & age (Hornung, Danker-Hopfe, & Heuser, 2005; Nadel, 2004; Walker, Brakefield, Morgan, Hob- Van Cauter, Leproult, & Plat, 2000; Wolkove, son, & Stickgold, 2002; Walker et al., 2003). In Elkholy, Baltzan, & Palayew, 2007). Most impor- this paper we examine for the first time the tant for the present research is the finding that effects of ageing on the benefit that sleep has there is a substantial decline in slow-wave sleep for episodic memory. with age, and eventually stages 3 and 4 are Address correspondence to: Mariam Aly, Department of Psychology, University of Toronto, 100 Saint George St., Toronto, ON M5S 3G3, Canada. E-mail: [email protected] This work was supported by a CIHR Grant to Morris Moscovitch and Gordon Winocur. # 2010 Psychology Press, an imprint of the Taylor & Francis Group, an Informa business http://www.psypress.com/memory DOI:10.1080/09658211003601548 2 ALY AND MOSCOVITCH completely absent (Rosenzweig, Breedlove, & memory for the material in older and younger Watson, 2005). Since these stages of sleep pre- adults, so that any age-related difference following sumably underlie the consolidation of episodic periods of sleep or wakefulness would reflect memories (Plihal & Born, 1997; Yaroush et al., only changes from a common baseline, rather 1971), deficits in SWS point to the possibility of than ones that would be confounded by baseline less sleep-dependent episodic memory consolida- differences. tion in older adults. Furthermore, older adults Although this is a strictly behavioural study, show impairments on hippocampus-dependent finding equivalent benefits of sleep in older and memory tasks (Lupien et al., 1998): changes in younger adults would suggest that those neurolo- the structure and function of the hippocampus gical processes that confer a beneficial effect on and prefrontal cortex may underlie memory memory during sleep are sufficiently intact, at deficits in older adults and affect the quality of least in healthy older adults, to allow them to sleep-dependent consolidation (Hornung et al., operate. If, however, even under conditions that 2005). promote encoding and retention, the age-related Two studies that investigated the effects of decline in memory consolidation persists, it would sleep on memory in older and younger adults suggest that it is related to neurological changes confirmed that older adults benefited less from that accompany old age, such as the reduction of sleep (Spencer, Gouw, & Ivry, 2007; Spencer, SWS or hippocampal deterioration. Sumn, & Ivry, 2006). Explicit and implicit con- textual sequence learning tasks were used. Both tasks were presumed to engage hippocampal METHOD activity. These tasks are therefore similar to episodic memory tasks, which similarly depend Participants on the hippocampus. Younger adults showed greater memory im- A total of 10 younger (19Á29 years old) and 12 provements on these tasks following a 12-hour older (69Á80 years old) adults participated for $10 interval that included sleep, compared to an equal per hour. Younger adults were recruited through duration spent awake. Older adults showed no flyers placed around the University of Toronto. such sleep-dependent benefits, pointing to an age- Older adults were volunteers in the Adult Volun- related decline of sleep-dependent memory con- teer Pool, and were recruited by phone. The data solidation. Since this task presumably engaged of two older adults were discarded because they hippocampal activity, the findings suggest the did not follow instructions, leaving a sample of 10 possibility that episodic memories, which simi- older adults. Participants were fluent in English, larly depend on the hippocampus, may also be did not have any self-reported neurological, differentially affected by sleep in older and psychological, or severe medical conditions (e.g. younger adults. epilepsy, traumatic brain injury), and were not on Research has suggested, however, that age- any medication that affects sleep. Ethics approval related memory deficits may disappear when the was granted by the Department of Psychology studied material engages the older adults’ interest Ethics Review Committee at the University of rather than being neutral and indifferent (Car- Toronto. stensen & Turk-Charles, 1994; Rahhal, May, & Hasher, 2002). Because the material used in the above studies*word lists and sequences of Materials lights*resemble the latter more than the former, it is possible that using material that is inherently Two measures of episodic memory were used. more interesting for the older adults would elim- The first was the Logical Memory section of the inate the age-related decline in sleep-dependent Wechsler Memory Scale III (WMS-III), which memory consolidation. We decided, therefore, to consists of two short-paragraph-length stories use stories and personally experienced events, (Story A and Story B). The stories were scored both because such material would engage the in terms of the number of story units recalled, as older adults’ interest, and because memory for specified in the WMS-III scoring protocol. details of stories and personally experienced The second measure was a list of 12 questions events is dependent on the hippocampus. We to assess personal episodic memories for the first also thought it important to equate the initial (or last) conversation the participant had that AGEING, SLEEP, AND EPISODIC MEMORY 3 morning (or the previous evening), as well as immediately, in as much detail as they could memory for the first (or last) thing they read or remember. This was done to ensure that partici- saw on the news, radio, or television (see Appendix). pants paid attention to the story, and also to The questions were the same for each session with equate older and younger adults on initial mem- the exception of the final two, of which one version ory. In cases where older adults’ memory was was made to be appropriate for the morning and the significantly poorer than the average of younger other for the evening. adults, the story was repeated until they approxi- Finally, to gather information about partici- mated or passed the average (in all cases, only pants’ sleep the previous night and over the one repetition was required). preceding week, the St. Mary’s Hospital Sleep Participants were then asked the 12 questions Questionnaire (Ellis et al., 1981) and the Pitts- about events that happened the previous evening. burgh Sleep Quality Index (Buysse, Reynolds, They were told to answer them in as much detail Monk, Berman, & Kupfer, 1989) were adminis- as they could, taking their time to think about the tered. Questions assess sleep latency, sleep qual- answer if that was needed, but at the same time ity, amount of sleep, and sleep satisfaction. This keeping their answer limited to what the question information was obtained to ensure that partici- is asking. pants slept reasonably well the night before, and Finally, the participants were given the St. did not experience any unusual sleep problems. Mary’s Hospital Sleep Questionnaire. Only the measure of sleep duration was used in Participants were called again in the evening, the data analysis. 12 hours later, and were tested for recall of the story they heard that morning. Following this, the same procedure was followed as in the previous Procedure session except the second WMS-III story was used, and the 12 questions they were asked pertained to events of that morning. Lastly, since The study was conducted in three telephone there is an increase in daytime napping with age sessions separated by 12-hour intervals.
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