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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 of ~10 –12 Hz for at least 0.5 seconds.[1][2] After generation in the TRN, spindles are sustained and relayed to the cortex by a thalamo-thalamic and thalamo-cortical feedback loops regulated by both GABAergic and NMDA-receptor mediated glutamatergic neurotransmission.[3] Sleep spindles have been found in all tested mammalian species and in vitro cells.

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.

FunctionEdit

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.[4] Sleep spindles closely modulate interactions between the brain and its external environment; they essentially moderate responsiveness to sensory stimuli during sleep.[5] Recent research has revealed that spindles distort the transmission of auditory information to the cortex; spindles isolate the brain from external disturbances during sleep.[6] 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.[7] 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.[8] 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.[9][10]

Sleep spindle activity has furthermore been found to be associated with the integration of new information into existing knowledge[11] as well as directed remembering and forgetting (fast sleep spindles).[12]

During NREM sleep, the brain waves produced by people with schizophrenia lack the normal pattern of slow and fast spindles.[13] Loss of sleep spindles are also a feature of familial fatal insomnia, a prion disease.[14] Changes in spindle density are observed in disorders such as epilepsy and autism.[15][16]

Gender differencesEdit

Sleep spindles play a crucial role in declarative memory consolidation, however, most studies neglect to control for sex, although both sex and menstruation affect sleep [17] and online learning periods.[18]

As a whole, women tend to have twice as many sleep spindles as men and a female advantage has been found for episodic, emotional, and spatial memories as well as recognition of odours, faces, and pictures.[19] 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 women have higher estrogen levels, when compared to the menstrual phase.[17] A recent study found that local brain estrogen production within cognitive circuits may be important for the acquisition and consolidation of memories.[20] The potentially significant relationship between overnight declarative memory consolidation and the influence of estrogen has not been well established and should be further investigated.

Recent experiments concerning the relationship between estrogen 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 women in the mid-luteal phase (high estrogen) performed higher than the other female participants.[21] Women 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.[21]

Most studies neglect to control for sex and menstrual cycles in women, although both sex and menstruation have been implicated to affect sleep [17] and online learning periods.[18] Studies have shown that the influence of sleep spindles during the declarative memory process may be affected by modulatory menstrual cycle effects in females.[21] These findings have contributed to a proposed waxing and waning effect of estrogen on the memory performance of women due to fluctuating estrogen levels, which could potentially predict a decrease in memory performance during menses. Because of the novelty of these studies, the waxing and waning effect has been overlooked in every prior study.

Because sleep spindle production is synonymous with declarative memory consolidation, our understanding of declarative memory has potentially been corrupted by focusing solely on men or combining women and men into one category, which assumes that the results apply to both. The potentially significant relationship between overnight declarative memory consolidation and the influence of estrogen has not been well established and should be further investigated.

ReferencesEdit

  1. ^ 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.
  2. ^ De Gennaro, L.; Ferrara, M. (2003). Sleep spindles: an overview. Sleep medicine reviews, 7(5), 423–440
  3. ^ Pinault, Didier (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.
  4. ^ Holz, Johannes; Piosczyk, Hannah; Feige, Bernd; Spiegelhalder, Kai; Baglioni, Chiara; Riemann, Dieter; Nissen, Christoph (2012-12-01). "EEG sigma and slow-wave activity during NREM sleep correlate with overnight declarative and procedural memory consolidation". Journal of Sleep Research. 21 (6): 612–619. doi:10.1111/j.1365-2869.2012.01017.x. ISSN 1365-2869.
  5. ^ Lüthi, A (2013) Sleep spindles: where they come from, what they do. Neuroscientist 20:243–256. CrossRef Medline
  6. ^ Dang-Vu, T. T., Bonjean, M., Schabus, M., Boly, M., Darsaud, A., Desseilles, M.,et al. (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), 15438–15443.
  7. ^ Rihm, J., Diekelmann, S., Born, J., & Rasch, B. (2014). Reactivating memories during sleep by odors: Odor specificity and associated changes in sleep oscillations. Journal of Cognitive Neuroscience, 26(8), 1806-1818. http://dx.doi.org/:10.1162/jocn_a_00579
  8. ^ Thien Thanh Dang-Vu, Scott M. McKinney, Orfeu M. Buxton, Jo M. Solet, Jeffrey M. Ellenbogen. Spontaneous brain rhythms predict sleep stability in the face of noise. Current Biology - 10 August 2010 (Vol. 20, Issue 15, pp. R626-R627)
  9. ^ "To sleep, perchance to twitch"
  10. ^ "Wiring your brain at college – a new perspective on sleep" Archived 2010-06-19 at the Wayback Machine.
  11. ^ Tamminen, J.; Payne, J.D.; Stickgold, R.; Wamsley, E.J.; Gareth Gaskell, M. (2010). Sleep spindle activity is associated with the integration of new memories and existing knowledge. The Journal of Neuroscience, 30(43), 14356–60
  12. ^ Saletin, J.M.; Goldstein, A.N.; Walker, M.P (2011). The Role of Sleep in Directed Forgetting and Remembering of Human memories. Cerebral Cortex, 21, 2534–2541
  13. ^ Ferrarelli, F.; Huber, R.; Peterson, M.J.; Massimini, M.; Murphy, M.; Riedner, B.A.; Watson, A.; Bria, P.; Tononi, G. (2007). Reduced Sleep Spindle Activity in Schizophrenia Patients. The American Journal of Psychiatry, 164, A62
  14. ^ Niedermeyer E, Ribiero M. Considerations of nonconvulsive status epilepticus. Clin Electroencephalogr 2000; 31: 192-195.
  15. ^ Iranmanesh, Saam; Rodriguez-Villegas, Esther (2017). "An Ultralow-Power Sleep Spindle Detection System on Chip". IEEE Transactions on Biomedical Circuits and Systems. doi:10.1109/TBCAS.2017.2690908.
  16. ^ Warby, Simon C; Wendt, Sabrina L; Welinder, Peter; Munk, Emil G S; Carrilo, Oscar; Sorensen, Helge B D; Jennum, Paul; Pappard, Paul E; Perona, Pietro; Mignot, Emmanuel (2014). "Sleep-spindle detection: crowdsourcing and evaluating performance of experts, non-experts and automated methods". Nature Methods. 11: 385–392. doi:10.1038/nmeth.2855.
  17. ^ a b c Manber, R., Armitage, R., 1999. Sex, steroids and sleep: a review. Sleep 22, 540—555.
  18. ^ a b Maki, P.M., Rich, J.B., Shayna Rosenbaum, R., 2002. Implicit memory varies across the menstrual cycle: estrogen effects in young women. Neuropsychologia 40, 518—529.
  19. ^ Dzaja, A., Arber, S., Hislop, J., Kerkhofs, M., Kopp, C., Pollma¨cher, T., Polo-Kantola, P., Skene, D.J., Stenuit, P., Tobler, I., Porkka-Heiskanen, T., 2005. Women’s sleep in health and disease. J. Psychiatr. Res. 39, 55—76.
  20. ^ Vahaba, D. M., & Remage-Healey, L. (2016). Brain estrogen production and the encoding of recent experience. Curr Opin Behav Sci., 6, 148-153. http://dx.doi.org/10.1016/j.cobeha.2015.11.005
  21. ^ a b c Genzel, L., Kiefer, T., Renner, L., Wehrle, R., Kluge, M., Grozinger, M., Dresler, M. (2012). Sex and modulatory menstrual cycle effects on sleep related memory consolidation. Psychoneuroendocrinology, 37, 987-998. http://dx.doi.org/10.1016/j.psyneuen.2011.11.006