Coping with Sleep Deprivation: Shifts in Regional Brain Activity and Learning Strategy

Hagewoud, Roelina; Havekes, Robbert; Tiba, Paula Ayako; Novati, Arianna; Hogenelst, Koen; Weinreder, Pim; Zee, Eddy A. van der; Meerlo, Peter

doi:10.1093/sleep/33.11.1465

Cited by 79 publications

(83 citation statements)

References 48 publications

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“…We found that sleep deprivation following training during the late day impaired the consolidation of LTM. This is consistent with previous research in rodents demonstrating that posttraining sleep deprivation interferes with LTM 7,45,[88][89][90][91][92] and studies in Drosophila. 6,93 In contrast, when sleep deprivation occurred after the period of macromolecular synthesis necessary for 24 h memory, we found that long-term LFI memory was unaffected by sleep deprivation.…”

Section: Discussionsupporting

confidence: 93%

Acute Sleep Deprivation Blocks Short- and Long-Term Operant Memory inAplysia

Krishnan

Gandour

Ramos

et al. 2016

Sleep

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Study Objectives: Insufficient sleep in individuals appears increasingly common due to the demands of modern work schedules and technology use. Consequently, there is a growing need to understand the interactions between sleep deprivation and memory. The current study determined the effects of acute sleep deprivation on short and long-term associative memory using the marine mollusk Aplysia californica, a relatively simple model system well known for studies of learning and memory. Methods: Aplysia were sleep deprived for 9 hours using context changes and tactile stimulation either prior to or after training for the operant learning paradigm, learning that food is inedible (LFI). The effects of sleep deprivation on short-term (STM) and long-term memory (LTM) were assessed. Results: Acute sleep deprivation prior to LFI training impaired the induction of STM and LTM with persistent effects lasting at least 24 h. Sleep deprivation immediately after training blocked the consolidation of LTM. However, sleep deprivation following the period of molecular consolidation did not affect memory recall. Memory impairments were independent of handling-induced stress, as daytime handled control animals demonstrated no memory deficits. Additional training immediately after sleep deprivation failed to rescue the induction of memory, but additional training alleviated the persistent impairment in memory induction when training occurred 24 h following sleep deprivation. Conclusions: Acute sleep deprivation inhibited the induction and consolidation, but not the recall of memory. These behavioral studies establish Aplysia as an effective model system for studying the interactions between sleep and memory formation.

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Section: Discussionsupporting

confidence: 93%

Acute Sleep Deprivation Blocks Short- and Long-Term Operant Memory inAplysia

Krishnan

Gandour

Ramos

et al. 2016

Sleep

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“…Together, these findings support the notion that secondary working memory training has potential value to increase attentive performance on targeted tasks and skills despite extensive practice and experience (e.g., Di Nocera et al 2006;Youmans and Ohlsson 2008;Hagewoud et al 2010;Friederich and Herzog 2011;Gillan et al 2011;He et al 2011;Reichenbach et al 2011;Hogarth et al 2013). Consistent with this hypothesis, delay discounting has been shown to improve both with working memory training and instruction that shifts attention to focus on later rather than immediate rewards (Radu et al 2011).…”

Section: Discussionsupporting

confidence: 66%

A secondary working memory challenge preserves primary place strategies despite overtraining

et al. 2013

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Learning by repetition engages distinct cognitive strategies whose contributions are adjusted with experience. Early in learning, performance relies upon flexible, attentive strategies. With extended practice, inflexible, automatic strategies emerge. This transition is thought fundamental to habit formation and applies to human and animal cognition. In the context of spatial navigation, place strategies are flexible, typically employed early in training, and rely on the spatial arrangement of landmarks to locate a goal. Response strategies are inflexible, become dominant after overtraining, and utilize fixed motor sequences. Although these strategies can operate independently, they have also been shown to interact. However, since previous work has focused on single-choice learning, if and how these strategies interact across sequential choices remains unclear. To test strategy interactions across sequential choices, we utilized various two-choice spatial navigation tasks administered on the Opposing Ts maze, an apparatus for rodents that permits experimental control over strategy recruitment. We found that when a second choice required spatial working memory, the transition to response navigation on the first choice was blocked. Control experiments specified this effect to the cognitive aspects of the secondary task. In addition, response navigation, once established on a single choice, was not reversed by subsequent introduction of a secondary choice reliant on spatial working memory. These results demonstrate that performance strategies interact across choices, highlighting the sensitivity of strategy use to the cognitive demands of subsequent actions, an influence from which overtrained rigid actions may be protected.[Supplemental material is available for this article.]Whenever a subject engages in a repetitive task or behavior, with practice several aspects of performance undergo modification. Not only does overall performance tend to improve or become more effective, but the underlying cognitive strategies change. Specifically, the formation of habits is thought to result from an incremental progression away from the use of flexible, attentive performance strategies to the engagement of inflexible, automatic strategies. This strategy transition is observed in various cognitive domains, e. . Although the transition is robust, several factors internal and external to the subject alter the onset of automatic behaviors (Restle 1957;McDonald et al. 2004;Packard 2009). These factors seem to exert their effects by differentially engaging dissociable learning and memory systems which interact to recruit a distinct performance strategy at select time points during learning. Thus, an understanding of these interactions has important implications for decision-making at large.Much of the current evidence for the nature of these interactions stems from studies of spatial navigation. In these studies, flexible/attentive strategies, termed place (locale) strategies, rely on calibrated spatial information associated with ...

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“…A consistent finding in these studies is that the hippocampus-dependent version is more age-sensitive than the nonhippocampus-dependent version. Switches in learning strategy are also seen with sleep deprivation, which has adverse effects on hippocampus-dependent memory formation (Hagewoud et al 2010;Havekes et al 2011). We suspect that cTPL requires the plasticity of an intact hippocampus, while instead ordinal (noncircadian) TPL may depend more on a less age-sensitive memory system, presumably the striatum (Mulder et al 2013b).…”

Section: Switching Strategiesmentioning

confidence: 99%

Time–place learning over a lifetime: absence of memory loss in trained old mice

et al. 2015

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Time -place learning (TPL) offers the possibility to study the functional interaction between cognition and the circadian system with aging. With TPL, animals link biological significant events with the location and the time of day. This whatwhere-when type of memory provides animals with an experience-based daily schedule. Mice were tested for TPL five times throughout their lifespan and showed (re)learning from below chance level at the age of 4, 7, 12, and 18 mo. In contrast, at the age of 22 mo these mice showed preservation of TPL memory (absence of memory loss), together with deficiencies in the ability to update time-of-day information. Conversely, the majority of untrained (na€ ıve) mice at 17 mo of age were unable to acquire TPL, indicating that training had delayed TPL deficiencies in the mice trained over lifespan. Two out of seven na€ ıve mice, however, compensated for correct performance loss by adapting an alternative learning strategy that is independent of the age-deteriorating circadian system and presumably less cognitively demanding. Together, these data show the age-sensitivity of TPL, and the positive effects of repeated training over a lifetime. In addition, these data shed new light on aging-related loss of behavioral flexibility to update time-of-day information.

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Coping with Sleep Deprivation: Shifts in Regional Brain Activity and Learning Strategy

Cited by 79 publications

References 48 publications

Acute Sleep Deprivation Blocks Short- and Long-Term Operant Memory inAplysia

Acute Sleep Deprivation Blocks Short- and Long-Term Operant Memory inAplysia

A secondary working memory challenge preserves primary place strategies despite overtraining

Time–place learning over a lifetime: absence of memory loss in trained old mice

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