[go: up one dir, main page]
Wikipedia

Sleep spindle

For other uses, see Spindle (disambiguation).

Sleep spindles are bursts of neural oscillatory activity that are generated by interplay of the thalamic reticular nucleus (TRN) and other thalamic nuclei during stage 2 NREM sleep in a frequency range of ~11 to 16 Hz (usually 12–14 Hz) with a duration of 0.5 seconds or greater (usually 0.5–1.5 seconds).[1][2][3] After generation as an interaction of the TRN neurons and thalamocortical cells,[4] spindles are sustained and relayed to the cortex by thalamo-thalamic and thalamo-cortical feedback loops regulated by both GABAergic and NMDA-receptor mediated glutamatergic neurotransmission.[5] Sleep spindles have been reported (at face value) for all tested mammalian species. Considering animals in which sleep-spindles were studied extensively (and thus excluding results mislead by pseudo-spindles[6]), they appear to have a conserved (across species) main frequency of roughly 9–16 Hz. Only in humans, rats and dogs is a difference in the intrinsic frequency of frontal and posterior spindles confirmed, however (spindles recorded over the posterior part of the scalp are of higher frequency, on average above 13 Hz).[7]

Research supports that spindles (sometimes referred to as "sigma bands" or "sigma waves") play an essential role in both sensory processing and long term memory consolidation. Until recently, it was believed that each sleep spindle oscillation peaked at the same time throughout the neocortex. It was determined that oscillations sweep across the neocortex in circular patterns around the neocortex, peaking in one area, and then a few milliseconds later in an adjacent area. It has been suggested that this spindle organization allows for neurons to communicate across cortices. The time scale at which the waves travel at is the same speed it takes for neurons to communicate with each other.[8] Doubts, however, remain whether a link exists between sleep spindles and memory with a recent meta-review of 53 studies concluding that "there is no relationship between sleep spindles and memory, and thus it is unlikely that sleep spindles are indeed generally implicated in learning and plasticity".[9]

Although the function of sleep spindles is unclear, it is believed that they actively participate in the consolidation of overnight declarative memory through the reconsolidation process. The density of spindles has been shown to increase after extensive learning of declarative memory tasks and the degree of increase in stage 2 spindle activity correlates with memory performance.

Among other functions, spindles facilitate somatosensory development, thalamocortical sensory gating, synaptic plasticity, and offline memory consolidation.[10] Sleep spindles closely modulate interactions between the brain and its external environment; they essentially moderate responsiveness to sensory stimuli during sleep.[11] Recent research has revealed that spindles distort the transmission of auditory information to the cortex; spindles isolate the brain from external disturbances during sleep.[12] Another study found that re-exposure to olfactory cues during sleep initiate reactivation, an essential part of long term memory consolidation that improves later recall performance.[13] Spindles generated in the thalamus have been shown to aid sleeping in the presence of disruptive external sounds. A correlation has been found between the amount of brainwave activity in the thalamus and a sleeper's ability to maintain tranquility.[14] Spindles play an essential role in both sensory processing and long term memory consolidation because they are generated in the TRN.

During sleep, these spindles are seen in the brain as a burst of activity immediately following muscle twitching. Researchers think the brain, particularly in the young, is learning about what nerves control what specific muscles when asleep.[15][16]

Sleep spindle activity has furthermore been found to be associated with the integration of new information into existing knowledge[17] as well as directed remembering and forgetting (fast sleep spindles).[18]

During NREM sleep, the brain waves produced by people with schizophrenia lack the normal pattern of slow and fast spindles.[19] Loss of sleep spindles are also a feature of familial fatal insomnia, a prion disease.[20] Changes in spindle density are observed in disorders. There are some studies that show a change in sleep spindles in autistic children.[21] Also some studies suggest a lack of sleep spindles in epilepsy.[22][23]

Research is currently underway to develop a web-based automatic sleep spindle detection system by using machine learning techniques. The results of the present study show that the automatic sleep spindle detection system has great potential in practical application.[24]

Evolution

edit

No sleep spindles have been observed in reptiles and birds so far.[25][26][27] In most mammals sleep spindles were described at face value, but the existence of pseudo-spindles[6] invites uncertainty around these observations. Spindle-like oscillations, that show additional analogies (e.g. apparent involvement in learning or thalamic dependence) are currently only known from humans, rats, mice, cats, and dogs.[7] In these species spindles invariantly oscillate between 9 and 16 Hz, with minor variations (e.g. 7–14 Hz in the cat[28]). Clearly distinct frontal and posterior sleep spindles (i.e. "slow" and "fast") were only confirmed outside humans in rats[29] and dogs.[30]

Sex differences

edit

Sleep spindles play a crucial role in declarative memory consolidation and both sex and menstruation affect sleep[31] and online learning periods.[32] Studies have shown that the influence of sleep spindles during the declarative memory process may be affected by modulatory menstrual cycle effects in females.[33]

Humanlike sex differences in sleep spindle activity and sleep-dependent learning were observed in dogs.[30][34] A direct link to specific sexual hormones could not be established, but the effects were stronger in intact animals.[30]

Females tend to have 0.16 more sleep spindles per minute than males[35] ( ⁠i.e. roughly 9–⁠10 more over an hour's time). A female advantage has been found for episodic, emotional, and spatial memories as well as recognition of odours, faces, and pictures.[36] These differences are believed to be due to hormonal influence, especially that of estrogen. The female sex hormone estrogen primarily influences sexual maturation and reproduction, but has also been found to facilitate other brain functions, including cognition and memory. On verbal tasks where women scored higher than men, women scored higher during the mid-luteal phase, when females have higher estrogen levels, when compared to the menstrual phase.[31] A recent study found that local brain estrogen production within cognitive circuits may be important for the acquisition and consolidation of memories.[37] Recent experiments concerning the relationship between oestrogen and the process of offline memory consolidation have also focused on sleep spindles. Genzel and colleagues determined that there was a menstrual effect on declarative and motor performance, meaning that females in the mid-luteal phase (high estrogen) performed higher than the other female participants.[33] Females in the luteal phase were also the only participants to experience an increase in spindles after learning, which led to the conclusion that the effect of the menstrual cycle may be mediated by spindles and female hormones.[33]

References

edit
  1. ^ Berry RB, Wagner MH (2015). Sleep Medicine Pearls. Elsevier. pp. 10–14. ISBN 978-1-4557-7051-9. Retrieved 5 June 2019.
  2. ^ Rechtschaffen A, Kales A (1968). A Manual of Standardized Terminology, Techniques and Scoring System For Sleep Stages of Human Subjects. US Dept of Health, Education, and Welfare; National Institutes of Health. OCLC 2518321.
  3. ^ De Gennaro L, Ferrara M (October 2003). "Sleep spindles: an overview". Sleep Medicine Reviews. 7 (5): 423–40. doi:10.1053/smrv.2002.0252. PMID 14573378.
  4. ^ McCormick, David A.; Bal, Thierry (March 1997). "SLEEP AND AROUSAL: Thalamocortical Mechanisms". Annual Review of Neuroscience. 20 (1): 185–215. doi:10.1146/annurev.neuro.20.1.185. PMID 9056712.
  5. ^ Pinault D (August 2004). "The thalamic reticular nucleus: structure, function and concept". Brain Research. Brain Research Reviews. 46 (1): 1–31. doi:10.1016/j.brainresrev.2004.04.008. PMID 15297152. S2CID 26291991.
  6. ^ a b Gottesmann, C. (1996). The transition from slow-wave sleep to paradoxical sleep: evolving facts and concepts of the neurophysiological processes underlying the intermediate stage of sleep. Neuroscience and Biobehavioral Reviews 20, 367–387.
  7. ^ a b Iotchev, I. B., & Kubinyi, E. (2021). Shared and unique features of mammalian sleep spindles–insights from new and old animal models. Biological Reviews, 96(3), 1021-1034.
  8. ^ Muller, Lyle; Piantoni, Giovanni; Koller, Dominik; Cash, Sydney S; Halgren, Eric; Sejnowski, Terrence J (2016-11-15). Skinner, Frances K (ed.). "Rotating waves during human sleep spindles organize global patterns of activity that repeat precisely through the night". eLife. 5: e17267. doi:10.7554/eLife.17267. ISSN 2050-084X. PMC 5114016. PMID 27855061.
  9. ^ Ujma, Péter Przemyslaw (2024). "Meta-analytic evidence suggests no correlation between sleep spindles and memory". Neuropsychologia. 198: 108886. doi:10.1016/j.neuropsychologia.2024.108886.
  10. ^ Holz J, Piosczyk H, Feige B, Spiegelhalder K, Baglioni C, Riemann D, Nissen C (December 2012). "EEG Σ and slow-wave activity during NREM sleep correlate with overnight declarative and procedural memory consolidation". Journal of Sleep Research. 21 (6): 612–9. doi:10.1111/j.1365-2869.2012.01017.x. PMID 22591117.
  11. ^ Lüthi A (June 2014). "Sleep Spindles: Where They Come From, What They Do". The Neuroscientist. 20 (3): 243–56. doi:10.1177/1073858413500854. PMID 23981852. S2CID 206658010.
  12. ^ Dang-Vu TT, Bonjean M, Schabus M, Boly M, Darsaud A, Desseilles M, et al. (September 2011). "Interplay between spontaneous and induced brain activity during human non-rapid eye movement sleep". Proceedings of the National Academy of Sciences of the United States of America. 108 (37): 15438–43. Bibcode:2011PNAS..10815438D. doi:10.1073/pnas.1112503108. PMC 3174676. PMID 21896732.
  13. ^ Rihm JS, Diekelmann S, Born J, Rasch B (August 2014). "Reactivating memories during sleep by odors: odor specificity and associated changes in sleep oscillations" (PDF). Journal of Cognitive Neuroscience. 26 (8): 1806–18. doi:10.1162/jocn_a_00579. PMID 24456392. S2CID 22066368.
  14. ^ Dang-Vu TT, McKinney SM, Buxton OM, Solet JM, Ellenbogen JM (August 2010). "Spontaneous brain rhythms predict sleep stability in the face of noise". Current Biology. 20 (15): R626-7. doi:10.1016/j.cub.2010.06.032. PMID 20692606.
  15. ^ Dingfelder SF (January 2006). "To sleep, perchance to twitch". Monitor. 37 (1). American Psychological Association: 51.
  16. ^ Harney É (April 1, 2009). "Wiring your brain at college – a new perspective on sleep". Blog at WordPress.com. Archived from the original on 2010-06-19.
  17. ^ Tamminen J, Payne JD, Stickgold R, Wamsley EJ, Gaskell MG (October 2010). "Sleep spindle activity is associated with the integration of new memories and existing knowledge". The Journal of Neuroscience. 30 (43): 14356–60. doi:10.1523/JNEUROSCI.3028-10.2010. PMC 2989532. PMID 20980591.
  18. ^ Saletin JM, Goldstein AN, Walker MP (November 2011). "The role of sleep in directed forgetting and remembering of human memories". Cerebral Cortex. 21 (11): 2534–41. doi:10.1093/cercor/bhr034. PMC 3183424. PMID 21459838.
  19. ^ Ferrarelli F, Huber R, Peterson MJ, Massimini M, Murphy M, Riedner BA, et al. (March 2007). "Reduced sleep spindle activity in schizophrenia patients". The American Journal of Psychiatry. 164 (3): 483–92. doi:10.1176/ajp.2007.164.3.483. PMID 17329474.
  20. ^ Niedermeyer E, Ribeiro M (October 2000). "Considerations of nonconvulsive status epilepticus". Clinical EEG. 31 (4): 192–5. doi:10.1177/155005940003100407. PMID 11056841. S2CID 30679161.
  21. ^ Merikanto, Ilona; Kuula, Liisa; Makkonen, Tommi; Salmela, Liisa; Räikkönen, Katri; Pesonen, Anu-Katriina (2019-03-15). "Autistic Traits Are Associated With Decreased Activity of Fast Sleep Spindles During Adolescence". Journal of Clinical Sleep Medicine. 15 (3): 401–407. doi:10.5664/jcsm.7662. ISSN 1550-9389. PMC 6411178. PMID 30853050.
  22. ^ Iranmanesh S, Rodriguez-Villegas E (August 2017). "An Ultralow-Power Sleep Spindle Detection System on Chip". IEEE Transactions on Biomedical Circuits and Systems. 11 (4): 858–866. doi:10.1109/TBCAS.2017.2690908. hdl:10044/1/46059. PMID 28541914. S2CID 206608057.
  23. ^ Warby SC, Wendt SL, Welinder P, Munk EG, Carrillo O, Sorensen HB, et al. (April 2014). "Sleep-spindle detection: crowdsourcing and evaluating performance of experts, non-experts and automated methods". Nature Methods. 11 (4): 385–92. doi:10.1038/nmeth.2855. PMC 3972193. PMID 24562424.
  24. ^ L. Wei; S. Ventura; S. Mathieson; G. B. Boylan; M. Lowery; C. Mooney (Jan 2022). "Spindle-AI: Sleep Spindle Number and Duration Estimation in Infant EEG". IEEE Transactions on Biomedical Engineering. 69 (1): 465–474. doi:10.1109/TBME.2021.3097815. PMID 34280088. S2CID 236141540.
  25. ^ Rattenborg, N. C., Martinez-Gonzalez, D., Roth, T. C. & Pravosudov, V. V. (2011). Hippocampal memory consolidation during sleep: a comparison of mammals and birds. Biological Reviews 86, 658–691.
  26. ^ Shein-Idelson, M., Ondracek, J. M., Liaw, H. P., Reiter, S. & Laurent, G. (2016). Slow waves, sharp waves, ripples, and REM in sleeping dragons. Science 352, 590–595.
  27. ^ van der Meij, J., Martinez-Gonzalez, D., Beckers, G. J. L. & Rattenborg, N. C. (2019). Intra-"cortical" activity during avian non-REM and REM sleep: variant and invariant traits between birds and mammals. Sleep 42, zsy230.
  28. ^ Steriade, M., & Llinás, R. R. (1988). The functional states of the thalamus and the associated neuronal interplay. Physiological reviews, 68(3), 649-742.
  29. ^ Terrier, G., & Gottesmann, C. L. (1978). Study of cortical spindles during sleep in the rat. Brain research bulletin, 3(6), 701-706.
  30. ^ a b c Iotchev, I. B., Kis, A., Turcsán, B., Tejeda Fernández de Lara, D. R., Reicher, V., & Kubinyi, E. (2019). Age-related differences and sexual dimorphism in canine sleep spindles. Scientific reports, 9(1), 1-11.
  31. ^ a b Manber R, Armitage R (August 1999). "Sex, steroids, and sleep: a review". Sleep. 22 (5): 540–55. doi:10.1093/sleep/22.5.540. PMID 10450590.
  32. ^ Maki PM, Rich JB, Rosenbaum RS (2002). "Implicit memory varies across the menstrual cycle: estrogen effects in young women". Neuropsychologia. 40 (5): 518–29. doi:10.1016/S0028-3932(01)00126-9. PMID 11749982. S2CID 15133827.
  33. ^ a b c Genzel L, Kiefer T, Renner L, Wehrle R, Kluge M, Grözinger M, et al. (July 2012). "Sex and modulatory menstrual cycle effects on sleep related memory consolidation". Psychoneuroendocrinology. 37 (7): 987–98. doi:10.1016/j.psyneuen.2011.11.006. PMID 22153362. S2CID 19797939.
  34. ^ Iotchev, I. B., Kis, A., Bódizs, R., van Luijtelaar, G., & Kubinyi, E. (2017). EEG transients in the sigma range during non-REM sleep predict learning in dogs. Scientific reports, 7(1), 1-11.
  35. ^ Purcell SM, Manoach DS, Demanuele C, Cade BE, Mariani S, Cox R, et al. (June 2017). "Characterizing sleep spindles in 11,630 individuals from the National Sleep Research Resource". Nature Communications. 8 (1): 15930. Bibcode:2017NatCo...815930P. doi:10.1038/ncomms15930. PMC 5490197. PMID 28649997.
  36. ^ Dzaja A, Arber S, Hislop J, Kerkhofs M, Kopp C, Pollmächer T, et al. (January 2005). "Women's sleep in health and disease". Journal of Psychiatric Research. 39 (1): 55–76. doi:10.1016/j.jpsychires.2004.05.008. PMID 15504424.
  37. ^ Vahaba DM, Remage-Healey L (December 2015). "Brain estrogen production and the encoding of recent experience". Current Opinion in Behavioral Sciences. 6: 148–153. doi:10.1016/j.cobeha.2015.11.005. PMC 4955874. PMID 27453921.
Retrieved from "https://en.wikipedia.org/w/index.php?title=Sleep_spindle&oldid=1238972165"