Odor cueing during slow-wave sleep benefits memory independently of low cholinergic tone

Klinzing, Jens G.; Kugler, Sabine; Soekadar, Surjo R.; Rasch, Björn; Born, Jan; Diekelmann, Susanne

doi:10.1007/s00213-017-4768-5

Cited by 31 publications

(21 citation statements)

References 52 publications

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“…Note that mathematical models of memory posit competition between items linked to a context 40 ; however, these models have focused on data from wake, not sleep, and it is possible that memory systems operate differently during sleep. For example, low levels of acetylcholine during slow-wave sleep may put the hippocampus into a strong retrieval mode that makes it possible to retrieve more traces at once 41,42 (but see 43 ).…”

Section: Discussionmentioning

confidence: 99%

Multiple memories can be simultaneously reactivated during sleep as effectively as a single memory

Schechtman¹,

Antony

Lampe³

et al. 2019

Preprint

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Memory consolidation during sleep involves reactivation of memory traces. Targeting specific memories by presenting learning-related cues during sleep selectively enhances memory, but the mechanism behind this benefit is not fully understood. To better characterize the consolidation process in humans, we tested whether multiple memories can be reactivated in parallel using a spatial-memory task. After learning the locations of images belonging to semantically related sets of one, two, or six items, half of the sets were reactivated during a nap. Results showed a selective benefit in location recall for cued versus non-cued items regardless of set size, implying that reactivation may occur in a simultaneous, promiscuous manner. Intriguingly, sleep spindles and delta power modulations were sensitive to set-size and reflected the extent of previous learning. Taken together, our results refute the notion that resource availability strictly reduces the capacity of simultaneous sleep-reactivation and bring forward alternative testable models for sleep-related consolidation.More than a century after researchers started to explore the beneficial effects of sleep on memory 1 , the mechanism by which this benefit is achieved in still debated 2 . The leading hypothesis, termed active systems consolidation 3 , postulates that memories are stored in the hippocampus and then reactivated during sleep, subsequently shaping neocortical memory traces. Reactivation of memories during sleep was first observed in rodents 4, 5 . Sequential learning-related spiking activity was shown to "replay" during sleep, and this phenomenon has since been connected to the off-line consolidation process 6 . In Humans, recent studies using multivariate pattern classification analysis in fMRI have also shown evidence for reactivation of cortical and hippocampal memory-related patterns during sleep and awake rest 7,8,9,10 .An important milestone in the study of sleep-related reactivation has been the development of targeted memory reactivation (TMR), a paradigm designed to reactivate specific memories by unobtrusively presenting learning-related cues during sleep 11 . TMR has been shown to improve various forms of learning, including spatial 12, 13 , skill 14, 15 and vocabulary 16 learning. A recent TMR-fMRI study 17 demonstrated that cuing reactivated category-level learning-related cortical activity, further establishing the link between TMR-related memory reactivation and spontaneous reactivation during sleep. TMR spatial-learning paradigms have predominantly used olfactory and auditory cues to reactivate memories. Whereas olfactory designs have associated multiple learned items to a single odor (e.g., 15items 13,18,19 ), auditory designs have commonly used sounds that were associated with a single item (and more recently, with two items 20, 21 ). Both techniques have consistently shown benefits for cued items, but the question of whether effect sizes rely on the number of items reactivated has never been directly addressed. The relationship betwee...

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Section: Discussionmentioning

confidence: 99%

Multiple memories can be simultaneously reactivated during sleep as effectively as a single memory

Schechtman¹,

Antony

Lampe³

et al. 2019

Preprint

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“…Slow oscillations and spindles were detected during NREM epochs (i.e., stage 2, and SWS) using established algorithms (spindles: Klinzing et al 2016Klinzing et al , 2018Mölle et al 2011;slow oscillations: Mölle et al 2002;Ngo et al 2013). The algorithms are described in detail in Muehlroth et al (in press).…”

Section: Spindle and Slow Oscillation Detectionmentioning

confidence: 99%

Memory quality modulates the effect of aging on memory consolidation during sleep: Reduced maintenance but intact gain

Muehlroth

Sander

Fandakova

et al. 2019

Preprint

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Successful consolidation of associative memories relies on the coordinated interplay of slow oscillations and sleep spindles during non-rapid eye movement (NREM) sleep, enabling the transfer of labile information from the hippocampus to permanent memory stores in the neocortex.During senescence, the decline of the structural and functional integrity of the hippocampus and neocortical regions is paralleled by changes of the physiological events that stabilize and enhance associative memories during NREM sleep. However, the currently available evidence is inconclusive if and under which circumstances aging impacts memory consolidation. By tracing the encoding quality of single memories in individual participants, we demonstrate that previous learning determines the extent of age-related impairments in memory consolidation. Specifically, the detrimental effects of aging on memory maintenance were greatest for mnemonic contents of medium encoding quality, whereas memory gain of weakly encoded memories did not differ by age. Using multivariate techniques, we identified profiles of alterations in sleep physiology and brain structure characteristic for increasing age. Importantly, while both 'aged' sleep and 'aged' brain structure profiles were associated with reduced memory maintenance, inter-individual differences in neither sleep nor structural brain integrity qualified as the driving force behind age differences in sleep-dependent consolidation in the present study.

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“…Specifically, authors observed an increase in EEG power in the frontal delta (1.5–4.5 Hz) and parietal fast spindles (13–15 Hz), two EEG activities purported to coordinate the reactivation and consolidation of declarative memories from the hippocampus to the cortical networks . Interestingly, it has been recently suggested that the beneficial effect of olfactory‐induced TMR seems not to rely on the same neurophysiological mechanism underlying neural reactivation during sleep . Indeed, a recent pharmacological study observed a benefit of odor stimulation during SWS even when the cholinergic tone of the participants was increased using physostigmine, an acetylcholinesterase inhibitor that effectively increases the accumulation of acetylcholine at the synaptic level .…”

Section: Tmr and Declarative Memorymentioning

confidence: 99%

“…Interestingly, it has been recently suggested that the beneficial effect of olfactory‐induced TMR seems not to rely on the same neurophysiological mechanism underlying neural reactivation during sleep . Indeed, a recent pharmacological study observed a benefit of odor stimulation during SWS even when the cholinergic tone of the participants was increased using physostigmine, an acetylcholinesterase inhibitor that effectively increases the accumulation of acetylcholine at the synaptic level . These results were surprising, since the authors expected that physostigmine would block hippocampal–neocortical communication (i.e., systems consolidation).…”

Section: Tmr and Declarative Memorymentioning

confidence: 99%

Shaping memory consolidation via targeted memory reactivation during sleep

Cellini

Capuozzo

2018

Annals of the New York Academy of Sciences

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Recent studies have shown that the reactivation of specific memories during sleep can be modulated using external stimulation. Specifically, it has been reported that matching a sensory stimulus (e.g., odor or sound cue) with target information (e.g., pairs of words, pictures, and motor sequences) during wakefulness, and then presenting the cue alone during sleep, facilitates memory of the target information. Thus, presenting learned cues while asleep may reactivate related declarative, procedural, and emotional material, and facilitate the neurophysiological processes underpinning memory consolidation in humans. This paradigm, which has been named targeted memory reactivation, has been successfully used to improve visuospatial and verbal memories, strengthen motor skills, modify implicit social biases, and enhance fear extinction. However, these studies also show that results depend on the type of memory investigated, the task employed, the sensory cue used, and the specific sleep stage of stimulation. Here, we present a review of how memory consolidation may be shaped using noninvasive sensory stimulation during sleep.

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Odor cueing during slow-wave sleep benefits memory independently of low cholinergic tone

Cited by 31 publications

References 52 publications

Multiple memories can be simultaneously reactivated during sleep as effectively as a single memory

Multiple memories can be simultaneously reactivated during sleep as effectively as a single memory

Memory quality modulates the effect of aging on memory consolidation during sleep: Reduced maintenance but intact gain

Shaping memory consolidation via targeted memory reactivation during sleep

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