Sleep Spindle Density and Temporal Clustering Are Associated with Sleep-dependent Memory Consolidation in Parkinson's Disease

Overview

Journal J Clin Sleep Med

Specialties Neurology
Psychiatry

Date 2024 Mar 1

PMID 38427318

Authors

Soraya Lahlou

Marta Kaminska

Julien Doyon

Julie Carrier

Madeleine Sharp

Affiliations

Soon will be listed here.

Abstract

Study Objectives: Sleep is required for successful memory consolidation. Sleep spindles, bursts of oscillatory activity occurring during non-rapid eye movement sleep, are known to be crucial for this process and, recently, it has been proposed that the temporal organization of spindles into clusters might additionally play a role in memory consolidation. In Parkinson's disease, spindle activity is reduced, and this reduction has been found to be predictive of cognitive decline. However, it remains unknown whether alterations in sleep spindles in Parkinson's disease are predictive of sleep-dependent cognitive processes such as memory consolidation, leaving open questions about the possible mechanisms linking sleep and a more general cognitive state in Parkinson's patients.

Methods: The current study sought to fill this gap by recording overnight polysomnography and measuring overnight declarative memory consolidation in a sample of 35 patients with Parkinson's. Memory consolidation was measured using a verbal paired-associates task administered before and after the night of recorded sleep.

Results: We found that lower sleep spindle density at frontal leads during non-rapid eye movement stage 3 was associated with worse overnight declarative memory consolidation. We also found that patients who showed less temporal clustering of spindles exhibited worse declarative memory consolidation.

Conclusions: These results suggest alterations to sleep spindles, which are known to be a consequence of Parkinson's disease, might represent a mechanism by which poor sleep leads to worse cognitive function in Parkinson's patients.

Citation: Lahlou S, Kaminska M, Doyon J, Carrier J, Sharp M. Sleep spindle density and temporal clustering are associated with sleep-dependent memory consolidation in Parkinson's disease. . 2024;20(7):1153-1162.

References

Rasch B, Born J . About sleep's role in memory. Physiol Rev. 2013; 93(2):681-766. PMC: 3768102. DOI: 10.1152/physrev.00032.2012. View

Christensen J, Kempfner J, Zoetmulder M, Leonthin H, Arvastson L, Christensen S . Decreased sleep spindle density in patients with idiopathic REM sleep behavior disorder and patients with Parkinson's disease. Clin Neurophysiol. 2013; 125(3):512-9. DOI: 10.1016/j.clinph.2013.08.013. View

Pushpanathan M, Loftus A, Thomas M, Gasson N, Bucks R . The relationship between sleep and cognition in Parkinson's disease: A meta-analysis. Sleep Med Rev. 2015; 26:21-32. DOI: 10.1016/j.smrv.2015.04.003. View

Hawkes C, Del Tredici K, Braak H . A timeline for Parkinson's disease. Parkinsonism Relat Disord. 2009; 16(2):79-84. DOI: 10.1016/j.parkreldis.2009.08.007. View

Schmidt C, Peigneux P, Muto V, Schenkel M, Knoblauch V, Munch M . Encoding difficulty promotes postlearning changes in sleep spindle activity during napping. J Neurosci. 2006; 26(35):8976-82. PMC: 6675334. DOI: 10.1523/JNEUROSCI.2464-06.2006. View

Latreille V, Carrier J, Lafortune M, Postuma R, Bertrand J, Panisset M . Sleep spindles in Parkinson's disease may predict the development of dementia. Neurobiol Aging. 2014; 36(2):1083-90. DOI: 10.1016/j.neurobiolaging.2014.09.009. View

Fogel S, Vien C, Karni A, Benali H, Carrier J, Doyon J . Sleep spindles: a physiological marker of age-related changes in gray matter in brain regions supporting motor skill memory consolidation. Neurobiol Aging. 2016; 49:154-164. DOI: 10.1016/j.neurobiolaging.2016.10.009. View

Diekelmann S, Biggel S, Rasch B, Born J . Offline consolidation of memory varies with time in slow wave sleep and can be accelerated by cuing memory reactivations. Neurobiol Learn Mem. 2012; 98(2):103-11. DOI: 10.1016/j.nlm.2012.07.002. View

Latreille V, Carrier J, Gaudet-Fex B, Rodrigues-Brazete J, Panisset M, Chouinard S . Electroencephalographic prodromal markers of dementia across conscious states in Parkinson's disease. Brain. 2016; 139(Pt 4):1189-99. PMC: 5841211. DOI: 10.1093/brain/aww018. View

10.

Lustenberger C, Wehrle F, Tushaus L, Achermann P, Huber R . The Multidimensional Aspects of Sleep Spindles and Their Relationship to Word-Pair Memory Consolidation. Sleep. 2015; 38(7):1093-103. PMC: 4481015. DOI: 10.5665/sleep.4820. View

11.

Mander B, Rao V, Lu B, Saletin J, Ancoli-Israel S, Jagust W . Impaired prefrontal sleep spindle regulation of hippocampal-dependent learning in older adults. Cereb Cortex. 2013; 24(12):3301-9. PMC: 4224242. DOI: 10.1093/cercor/bht188. View

12.

Barakat M, Doyon J, Debas K, Vandewalle G, Morin A, Poirier G . Fast and slow spindle involvement in the consolidation of a new motor sequence. Behav Brain Res. 2010; 217(1):117-21. DOI: 10.1016/j.bbr.2010.10.019. View

13.

Osorio-Forero A, Cardis R, Vantomme G, Guillaume-Gentil A, Katsioudi G, Devenoges C . Noradrenergic circuit control of non-REM sleep substates. Curr Biol. 2021; 31(22):5009-5023.e7. DOI: 10.1016/j.cub.2021.09.041. View

14.

Jacobs H, Priovoulos N, Poser B, Pagen L, Ivanov D, Verhey F . Dynamic behavior of the locus coeruleus during arousal-related memory processing in a multi-modal 7T fMRI paradigm. Elife. 2020; 9. PMC: 7343392. DOI: 10.7554/eLife.52059. View

15.

Solano A, Riquelme L, Perez-Chada D, Della-Maggiore V . Visuomotor Adaptation Modulates the Clustering of Sleep Spindles Into Trains. Front Neurosci. 2022; 16:803387. PMC: 8966394. DOI: 10.3389/fnins.2022.803387. View

16.

Bergmann T, Molle M, Diedrichs J, Born J, Siebner H . Sleep spindle-related reactivation of category-specific cortical regions after learning face-scene associations. Neuroimage. 2011; 59(3):2733-42. DOI: 10.1016/j.neuroimage.2011.10.036. View

17.

Zhang J, Yetton B, Whitehurst L, Naji M, Mednick S . The effect of zolpidem on memory consolidation over a night of sleep. Sleep. 2020; 43(11). PMC: 8064806. DOI: 10.1093/sleep/zsaa084. View

18.

Garcia-Borreguero D, Larrosa O, Bravo M . Parkinson's disease and sleep. Sleep Med Rev. 2003; 7(2):115-29. DOI: 10.1053/smrv.2002.0229. View

19.

Wamsley E, Shinn A, Tucker M, Ono K, McKinley S, Ely A . The effects of eszopiclone on sleep spindles and memory consolidation in schizophrenia: a randomized placebo-controlled trial. Sleep. 2013; 36(9):1369-76. PMC: 3738047. DOI: 10.5665/sleep.2968. View

20.

Maingret N, Girardeau G, Todorova R, Goutierre M, Zugaro M . Hippocampo-cortical coupling mediates memory consolidation during sleep. Nat Neurosci. 2016; 19(7):959-64. DOI: 10.1038/nn.4304. View