Age-related changes in fast spindle clustering during NREM sleep and their relevance for memory consolidation

Pierre Champetier; Claire André; Frederik D Weber; Stéphane Rehel; Valentin Ourry; Alice Laniepce; Antoine Lutz; Françoise Bertran; Nicolas Cabé; Anne-Lise Pitel; Géraldine Poisnel; Vincent de la Sayette; Denis Vivien; Gaël Chételat; Géraldine Rauchs

doi:10.1093/sleep/zsac282

Age-related changes in fast spindle clustering during NREM sleep and their relevance for memory consolidation

Pierre Champetier, Claire André, Frederik D Weber, Stéphane Rehel, Valentin Ourry, Alice Laniepce, Antoine Lutz, Françoise Bertran, Nicolas Cabé, Anne-Lise Pitel, Géraldine Poisnel, Vincent de la Sayette, Denis Vivien, Gaël Chételat, Géraldine Rauchs,

Onderzoeksoutput: Bijdrage aan wetenschappelijk tijdschrift/periodieke uitgave › Artikel › Wetenschappelijk › peer review

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Sleep plays a crucial role in memory consolidation. Recent data in rodents and young adults revealed that fast spindle band power fluctuates at a 0.02-Hz infraslow scale during non-rapid eye movement (NREM) sleep. These fluctuations result from a periodic temporal clustering of spindles and may modulate sleep maintenance and memory consolidation. With age, sleep undergoes substantial changes but age-related changes in spindle clustering have never been investigated. Polysomnography data were collected in 147 older (mean age ± SD: 69.3 ± 4.1 years) and 32 young-middle aged (34.5 ± 10.9 years) adults. Sleep-dependent memory consolidation was assessed in a subsample of 57 older adults using a visuospatial memory task. We analyzed power fluctuations in fast spindle frequency band, detected fast spindles and quantified their clustering during the night separating encoding and retrieval. Fast spindle band power fluctuated at a 0.02-Hz infraslow scale in young-middle aged and older adults. However, the proportion of clustered fast spindles decreased non-linearly with age (p < 0.001). This effect was not mediated by NREM sleep fragmentation. The clustering level of fast spindles modulated their characteristics (p < 0.001). Finally, the mean size of spindle clusters was positively associated with memory consolidation (p = 0.036) and negatively with NREM sleep micro-arousals density (p = 0.033). These results suggest that clusters of fast spindles may constitute stable sleep periods promoting off-line processes such as memory consolidation. We emphasize the relevance of considering spindle dynamics, obviously impaired during ageing, to understand the impact of age-related sleep changes on memory.

Originele taal-2	Engels
Artikelnummer	zsac282
Tijdschrift	Sleep
Volume	46
DOI's	https://doi.org/10.1093/sleep/zsac282
Status	Gepubliceerd - 2023

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10.1093/sleep/zsac282

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Champetier, P., André, C., Weber, F. D., Rehel, S., Ourry, V., Laniepce, A., Lutz, A., Bertran, F., Cabé, N., Pitel, A.-L., Poisnel, G., de la Sayette, V., Vivien, D., Chételat, G., Rauchs, G. (2023). Age-related changes in fast spindle clustering during NREM sleep and their relevance for memory consolidation. Sleep, 46, Artikel zsac282. https://doi.org/10.1093/sleep/zsac282

@article{0cee5c63d6474a2bb780c864347bf627,

title = "Age-related changes in fast spindle clustering during NREM sleep and their relevance for memory consolidation",

abstract = "Sleep plays a crucial role in memory consolidation. Recent data in rodents and young adults revealed that fast spindle band power fluctuates at a 0.02-Hz infraslow scale during non-rapid eye movement (NREM) sleep. These fluctuations result from a periodic temporal clustering of spindles and may modulate sleep maintenance and memory consolidation. With age, sleep undergoes substantial changes but age-related changes in spindle clustering have never been investigated. Polysomnography data were collected in 147 older (mean age ± SD: 69.3 ± 4.1 years) and 32 young-middle aged (34.5 ± 10.9 years) adults. Sleep-dependent memory consolidation was assessed in a subsample of 57 older adults using a visuospatial memory task. We analyzed power fluctuations in fast spindle frequency band, detected fast spindles and quantified their clustering during the night separating encoding and retrieval. Fast spindle band power fluctuated at a 0.02-Hz infraslow scale in young-middle aged and older adults. However, the proportion of clustered fast spindles decreased non-linearly with age (p < 0.001). This effect was not mediated by NREM sleep fragmentation. The clustering level of fast spindles modulated their characteristics (p < 0.001). Finally, the mean size of spindle clusters was positively associated with memory consolidation (p = 0.036) and negatively with NREM sleep micro-arousals density (p = 0.033). These results suggest that clusters of fast spindles may constitute stable sleep periods promoting off-line processes such as memory consolidation. We emphasize the relevance of considering spindle dynamics, obviously impaired during ageing, to understand the impact of age-related sleep changes on memory.",

author = "Pierre Champetier and Claire Andr{\'e} and Weber, {Frederik D} and St{\'e}phane Rehel and Valentin Ourry and Alice Laniepce and Antoine Lutz and Fran{\c c}oise Bertran and Nicolas Cab{\'e} and Anne-Lise Pitel and G{\'e}raldine Poisnel and {de la Sayette}, Vincent and Denis Vivien and Ga{\"e}l Ch{\'e}telat and G{\'e}raldine Rauchs",

year = "2023",

doi = "10.1093/sleep/zsac282",

language = "English",

volume = "46",

journal = "Sleep",

issn = "0161-8105",

publisher = "American Academy of Sleep Medicine",

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T1 - Age-related changes in fast spindle clustering during NREM sleep and their relevance for memory consolidation

AU - Champetier, Pierre

AU - André, Claire

AU - Weber, Frederik D

AU - Rehel, Stéphane

AU - Ourry, Valentin

AU - Laniepce, Alice

AU - Lutz, Antoine

AU - Bertran, Françoise

AU - Cabé, Nicolas

AU - Pitel, Anne-Lise

AU - Poisnel, Géraldine

AU - de la Sayette, Vincent

AU - Vivien, Denis

AU - Chételat, Gaël

AU - Rauchs, Géraldine

PY - 2023

Y1 - 2023

N2 - Sleep plays a crucial role in memory consolidation. Recent data in rodents and young adults revealed that fast spindle band power fluctuates at a 0.02-Hz infraslow scale during non-rapid eye movement (NREM) sleep. These fluctuations result from a periodic temporal clustering of spindles and may modulate sleep maintenance and memory consolidation. With age, sleep undergoes substantial changes but age-related changes in spindle clustering have never been investigated. Polysomnography data were collected in 147 older (mean age ± SD: 69.3 ± 4.1 years) and 32 young-middle aged (34.5 ± 10.9 years) adults. Sleep-dependent memory consolidation was assessed in a subsample of 57 older adults using a visuospatial memory task. We analyzed power fluctuations in fast spindle frequency band, detected fast spindles and quantified their clustering during the night separating encoding and retrieval. Fast spindle band power fluctuated at a 0.02-Hz infraslow scale in young-middle aged and older adults. However, the proportion of clustered fast spindles decreased non-linearly with age (p < 0.001). This effect was not mediated by NREM sleep fragmentation. The clustering level of fast spindles modulated their characteristics (p < 0.001). Finally, the mean size of spindle clusters was positively associated with memory consolidation (p = 0.036) and negatively with NREM sleep micro-arousals density (p = 0.033). These results suggest that clusters of fast spindles may constitute stable sleep periods promoting off-line processes such as memory consolidation. We emphasize the relevance of considering spindle dynamics, obviously impaired during ageing, to understand the impact of age-related sleep changes on memory.

AB - Sleep plays a crucial role in memory consolidation. Recent data in rodents and young adults revealed that fast spindle band power fluctuates at a 0.02-Hz infraslow scale during non-rapid eye movement (NREM) sleep. These fluctuations result from a periodic temporal clustering of spindles and may modulate sleep maintenance and memory consolidation. With age, sleep undergoes substantial changes but age-related changes in spindle clustering have never been investigated. Polysomnography data were collected in 147 older (mean age ± SD: 69.3 ± 4.1 years) and 32 young-middle aged (34.5 ± 10.9 years) adults. Sleep-dependent memory consolidation was assessed in a subsample of 57 older adults using a visuospatial memory task. We analyzed power fluctuations in fast spindle frequency band, detected fast spindles and quantified their clustering during the night separating encoding and retrieval. Fast spindle band power fluctuated at a 0.02-Hz infraslow scale in young-middle aged and older adults. However, the proportion of clustered fast spindles decreased non-linearly with age (p < 0.001). This effect was not mediated by NREM sleep fragmentation. The clustering level of fast spindles modulated their characteristics (p < 0.001). Finally, the mean size of spindle clusters was positively associated with memory consolidation (p = 0.036) and negatively with NREM sleep micro-arousals density (p = 0.033). These results suggest that clusters of fast spindles may constitute stable sleep periods promoting off-line processes such as memory consolidation. We emphasize the relevance of considering spindle dynamics, obviously impaired during ageing, to understand the impact of age-related sleep changes on memory.

U2 - 10.1093/sleep/zsac282

DO - 10.1093/sleep/zsac282

M3 - Article

C2 - 36433753

SN - 0161-8105

VL - 46

JO - Sleep

JF - Sleep

M1 - zsac282

ER -

Age-related changes in fast spindle clustering during NREM sleep and their relevance for memory consolidation

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