Memory encoding is impaired after multiple nights of partial sleep restriction

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Sleep is important in learning and memory processing (Kopasz et al., 2010; Rasch and Born, 2013). While sleep after learning has garnered considerable attention because of its contributions to memory consolidation, relatively fewer studies have explored the influence of sleep before learning on the brain's ability to encode new information (Antonenko et al., 2013; Drummond et al., 2000; Mander et al., 2011; Van Der Werf et al., 2009; Yoo et al., 2007).
Many people obtain insufficient sleep throughout the working week (Watson et al., 2015), and this may be particularly important in adolescents (Eaton et al., 2010; Owens, 2014), whose brains are actively developing and constantly learning. To date, the impact of inadequate sleep on cognition has been explored primarily by observing behaviour after a night of total sleep deprivation (TSD). In adults this has been associated with picture‐encoding deficits attributed to impaired hippocampal function (Yoo et al., 2007). Impaired learning after sleep deprivation (Hagewoud et al., 2010; Li et al., 2009) has been linked to a reduced capacity for long‐term potentiation in animal studies (Campbell et al., 2002; Vyazovskiy et al., 2008). To account for reduced learning capacity, the synaptic homeostasis hypothesis (SHY) proposes that sustained wakefulness potentiates synapses to a point of saturation that requires slow wave sleep (SWS) to down‐scale synapses for the restoration of encoding ability (Kuhn et al., 2016; Tononi and Cirelli, 2014).
While a single night of sleep deprivation is well suited for laboratory studies, exposure to multiple nights of reduced sleep is the more common form of sleep loss. Several aspects of sleep physiology differ between these two forms of sleep loss. For example, unlike the case of total sleep deprivation, where slow wave sleep (SWS) is lost completely on the experimental night, SWS duration remains relatively intact following multiple nights of sleep restriction, even though other sleep stages are reduced (Ong et al., 22016 Voderholzer et al., 2011). It is currently unclear how multiple nights of partial sleep restriction impact on memory‐encoding processes.
This is a question that is particularly pertinent to adolescents, who must encode and retain declarative information regularly to succeed academically. Some studies show remarkable resilience in adolescents’ cognitive abilities after 1 night of sleep restriction (4 h) (Carskadon et al., 1981; Fallone et al., 2001). However, other studies have found that several consecutive nights of sleep restriction result in progressive deterioration of subjective alertness (Anderson et al., 2009; Wolfson and Carskadon, 1998) and mood (Lo et al., 2015), as well as objective measures of sustained attention, working memory and speed of processing (Lo et al., 2015).
In this study we asked whether the encoding deficit observed in young adults after a night of TSD (Yoo et al., 2007) appears in adolescents after several consecutive nights of partial sleep restriction. Our sleep‐restricted group consisted of 15 to 18‐year‐olds who were permitted only 5 h time in bed (TIB) for 5 consecutive nights prior to a picture‐encoding task, simulating a demanding school week. A control group with a 9‐h sleep opportunity each night followed the same protocol. Encoding success was measured via a delayed recognition test conducted after 3 nights of 9 h TIB recovery sleep. We predicted that picture recognition would be impaired in the sleep‐restricted group, indicating a deficit in prior encoding, and this would be independent of a more general deterioration in subjective alertness and vigilance.
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