Expert and crowd-sourced validation of an individualized sleep spindle detection method employing complex demodulation and individualized normalization

Frontiers in Human Neuroscience

Volumn 9, Issue September, 2015, Pages

  Ray, Laura B ^a   Sockeel, Stéphane ^b   Soon, Melissa ^a   Bore, Arnaud ^b   Myhr, Ayako ^a   Stojanoski, Bobby ^a   Cusack, Rhodri ^a   Owen, Adrian M ^a   Doyon, Julien ^b,c   Fogel, Stuart M ^a,b,c  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b CENTRE DE RECHERCHE   (Canada)

^c UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Automated; Crowdsourcing; Detection; EEG; Sleep; Spindle

Indexed keywords

ADULT; ARTICLE; COMPLEX DEMODULATION; CONTROLLED STUDY; CROWDSOURCING; FEMALE; HUMAN; HUMAN EXPERIMENT; INTERMETHOD COMPARISON; MALE; NONREM SLEEP; NORMAL HUMAN; SIGNAL PROCESSING; SLEEP; SLEEP DEPRIVATION; SLEEP SPINDLE; SLOW WAVE SLEEP; SPINDLE AMPLITUDE; SPINDLE DENSITY; SPINDLE DURATION; SPINDLE FREQUENCY; VALIDATION STUDY; YOUNG ADULT;

EID: 84943196653     PISSN: 16625161     EISSN: 16625161     Source Type: Journal    
DOI: 10.3389/fnhum.2015.00507     Document Type: Article

References (62)

1. Barakat, M., Doyon, J., Debas, K., Vandewalle, G., Morin, A., Poirier, G., et al. (2011). Fast and slow spindle involvement in the consolidation of a new motor sequence. Behav. Brain Res. 217, 117–121. doi: 10.1016/j.bbr.2010. 10.019
2. Bergmann, T. O., Mölle, M., Diedrichs, J., Born, J., and Siebner, H. R. (2011). Sleep spindle-related reactivation of category-specific cortical regions after learning face-scene associations. Neuroimage 59, 2733–27
3. doi: 10.1016/j.neuroimage.2011.10.036
4. Bixler, E. O., and Rhodes, J. M. (1968). Spindle activity during sleep in cultural familial mildretardates. Psychophysiology 5, 212.
5. Bódizs, R., Kis, T., Lázár, A. S., Havrán, L., Rigó, P., Clemens, Z., et al. (2005). Prediction of general mental ability based on neural oscillation measures of sleep.J. Sleep Res.14,285–292.doi:10.1111/j.1365-2869.2005.00472.x
6. Bódizs, R., Körmendi, J., Rigó, P., and Lázár, A. S. (2009). The individual adjustment method of sleep spindle analysis: methodological improvements and roots in the fingerprint paradigm. J. Neurosci. Methods 178, 205–213. doi: 10.1016/j.jneumeth.2008.11.006
7. Bódizs, R., Lázár, A. S., and Rigó, P. (2008). Correlation of visuospatial memory ability with right parietal EEG spindling during sleep. Acta Physiol. Hung. 95, 297–306.doi:10.1556/APhysiol.95.2008.3.5
8. Bonjean, M., Baker, T., Lemieux, M., Timofeev, I., Sejnowski, T., and Bazhenov, M. (2011). Corticothalamic feedback controls sleep spindle duration in vivo. J.Neurosci.31,9124–9134.doi:10.1523/JNEUROSCI.0077-11.2011
9. Broughton, R., Healey, T., Maru, J., Green, D., and Pagurek, B. (1978). A phase locked loop device for automatic detection of sleep spindles and stage 2. Electroencephalogr. Clin. Neurophysiol. 44, 677–680. doi: 10.1016/00134694(78)90134-7
10. Campbell, K., Kumar, A., and Hofman, W. (1980). Human and automatic validationofaphase-lockedloopspindledetectionsystem.Electroencephalogr. Clin.Neurophysiol.48,602–605.doi:10.1016/0013-4694(80)90296-5
11. Clemens, Z., Mölle, M., Eross, L., Barsi, P., Halász, P., and Born, J.(2007).Temporal coupling of parahippocampal ripples, sleep spindles and slow oscillations in humans. Brain 130 (Pt11) ,2868–2878. doi:10.1093/brain/awm146
12. Cox, R., Hofman, W.F., deBoer, M., and Talamini, L.M. (2014).Localsleepspindle modulationsinrelationtospecificmemorycues. Neuroimage 99,103–110. doi: 10.1016/j.neuroimage.2014.05.028
13. Crowley, K., Trinder, J., Kim, Y., Carrington, M., and Colrain, I. M. (2002). The effects of normal aging on sleep spindle and k-complex production. Clin. Neurophysiol.113,1615–1622.doi:10.1016/S1388-2457(02)00237-7
14. Dang-Vu, T.T., McKinney, S.M., Buxton, O.M., Solet, J.M., and Ellenbogen, J.M. (2010). Spontaneous brain rhythms predict sleep stability in the face of noise. Curr.Biol.20,R626–R627.doi:10.1016/j.cub.2010.06.032
15. De Gennaro, L., and Ferrara, M. (2003). Sleep spindles: an overview. Sleep Med. Rev.7,423–440.doi:10.1053/smrv.2002.0252
16. DeGennaro, L., Ferrara, M., and Bertini, M. (2000).Topographicaldistributionof spindles: variations between and within nrem sleep cycles. Sleep Res. Online 3, 155–160.doi:10.1046/j.1365-2869.2000.00193.x
17. De Gennaro, L., Ferrara, M., Vecchio, F., Curcio, G., and Bertini, M. (2005). An electroencephalographic fingerprint of human sleep. Neuroimage 26, 114–122. doi:10.1016/j.neuroimage.2005.01.020
18. Ferrarelli, F., Huber, R., Peterson, M. J., Massimini, M., Murphy, M., Riedner, B. A., et al. (2007). Reduced sleep spindle activity in schizophrenia patients. Am. J.Psychiatry164,483–492.doi:10.1176/appi.ajp.164.3.483
19. Fogel, S., Albouy, G., King, B., Vien, C., Karni, A., Benali, H., etal.(2014).Motor memory consolidation depends upon reactivation driven by the action of sleep spindles. J. Sleep Res. 23, 47.
20. Fogel, S.M., Albouy, G., Vien, C., Popovicci, R., King, B.R., Hoge, R., etal. (2014). FMRI and sleep correlates of the age-related impairment in motor memory consolidation .Hum. Brain Mapp . 35, 3625–3645. doi:10.1002/hbm.22426
21. Fogel, S. M., Nader, R., Cote, K. A., and Smith, C. T. (2007). Sleep spindles and learningpotential.Behav.Neurosci.121,1–10.doi:10.1037/0735-7044.121.1.1
22. Fogel, S. M., and Smith, C. T. (2006). Learning-dependent changes in sleep spindles and stage 2 sleep. J. Sleep Res. 15, 250–255. doi: 10.1111/j.13652869.2006.00522.x
23. Fogel, S. M., and Smith, C. T. (2011). The function of the sleep spindle: a physiological index of intelligence and a mechanism for sleep-dependent memory consolidation. Neurosci. Biobehav. Rev. 35, 1154–1165. doi: 10.1016/j.neubiorev.2010.12.003
24. Frauscher, B., von Ellenrieder, N., Dubeau, F., and Gotman, J. (2015). Scalp spindles are associated with wide spread in tracranial activity with unexpectedly low synchrony. Neuroimage 105, 1–12. doi:10.1016/j.neuroimage.2014.10.048
25. Gais, S., Mölle, M., Helms, K., and Born, J. (2002). Learning-dependent increases insleepspindledensity.J.Neurosci.22,6830–6834.
26. Geiger, A., Huber, R., Kurth, S., Ringli, M., Jenni, O.G., and Achermann, P. (2011). The sleep EEG as a marker of intellectual ability in school age children. Sleep 34,181–189.
27. Gibbs, E. L., and Gibbs, F. A. (1962). Extreme spindles: correlation of electroencephalographic sleep pattern with mental retardation. Science 138, 1106–1107.doi:10.1126/science.138.3545.1106
28. Hao, Y. -L., Ueda, Y., and Ishii, N. (1992). Improved procedure of complex demodulationandanapplicationtofrequencyanalysisofsleepspindlesinEEG. Med.Biol.Eng.Comput.30,406–412.doi:10.1007/BF02446168
29. Himanen, S.L., Virkkala, J., Huhtala, H., and Hasan, J. (2002).Spindlefrequencies in sleep EEGs howu-shape with in first four NREM sleep episodes. J. Sleep Res. 11, 35–42. doi:10.1046/j.1365-2869.2002.00273.x
30. Huupponen, E., DeClercq, W., Gómez-Herrero, G., Saastamoinen, A., Egiazarian, K., Värri, A., et al. (2006). Determination of dominant simulated spindle frequency with different methods. J. Neurosci. Methods 156, 275–283. doi: 10.1016/j.jneumeth.2006.01.013
31. Iber, C. (2007). The AASM Manual for the Scoring of Sleep and Associated Events: Rules, Terminology and Technical Specifications. Westchester, IL: American AcademyofSleepMedicine.
32. Klonowski, W. (2007). From conformons to human brains: an informal overview of nonlinear dynamics and its applications in biomedicine. Nonlinear Biomed. Phys.1:5.doi:10.1186/1753-4631-1-5
33. Ktonas, P. Y., Golemati, S., Xanthopoulos, P., Sakkalis, V., Ortigueira, M. D., Tsekou, H., et al. (2009). Time-frequency analysis methods to quantify the time-varying microstructure of sleep EEG spindles: possibility for dementia biomarkers? J. Neurosci. Methods 185, 133–142. doi:10.1016/j.jneumeth.2009.09.001
34. Ktonas, P. Y., and Papp, N. (1980). Instantaneous envelope and phase extraction from real signals: theory, implementation, and an application to EEGanalysis. SignalProcessing 2,373–385.doi:10.1016/0165-1684(80)90079-1
35. Limoges, E., Mottron, L., Bolduc, C., Berthiaume, C., and Godbout, R. (2005). Atypical sleep architecture and the autism phenotype. Brain 128, 1049–1061. doi:10.1093/brain/awh425
36. Martin, N., Lafortune, M., Godbout, J., Barakat, M., Robillard, R., Poirier, G., etal. (2012). Topography of age-related changes in sleep spindles. Neurobiol. Aging 34,468–476.doi: 10.1016/j.neurobiolaging.2012.05.020
37. Mölle, M., Marshall, L., Gais, S., and Born, J. (2002). Grouping of spindle activity during slow oscillations in human non-rapid eye movement sleep. J. Neurosci. 22,10941–10947.
38. Nicolas, A., Petit, D., Rompré, S., and Montplaisir, J. (2001). Sleep spindle characteristics in healthy subjects of different age groups. Clin. Neurophysiol. 112,521–527.doi:10.1016/S1388-2457(00)00556-3
39. Nir, Y., Staba, R. J., Andrillon, T., Vyazovskiy, V. V., Cirelli, C., Fried, I., et al. (2011).Regionalslowwavesandspindlesinhumansleep.Neuron70,153–169. doi:10.1016/j.neuron.2011.02.043
40. Nishida, M., and Walker, M. P. (2007). Daytime naps, motor memory consolidation and regionally specific sleep spindles. PLoS ONE 2:e341. doi: 10.1371/journal.pone.0000341
41. O’Reilly, C., Gosselin, N., Carrier, J., and Nielsen, T. (2014). Montreal archive of sleep studies: an open-access resource for instrument benchmarking and exploratory research. J. Sleep Res. 23, 628–635. doi:10.1111/jsr.12169
42. Peters, K. R., Smith, V., and Smith, C. T. (2007). Changes in sleep architecture following motor learning depend on initial skill level. J. Cogn. Neurosci. 19, 817–829.doi:10.1162/jocn.2007.19.5.817
43. Principe, J.C., and Smith, J.R. (1982). Sleepspindlecharacteristicsasafunctionof age. Sleep 5, 73.
44. Ray, L. B., Fogel, S. M., Smith, C. T., and Peters, K. R. (2010). Validating an automatedsleepspindledetectionalgorithmusinganindividualizedapproach. J.SleepRes.19,374–378.doi:10.1111/j.1365-2869.2009.00802.x
45. Rechtschaffen, A., and Kales, A. (1968). A Manual of Standardized Terminology, Techniques and Scoring System for Sleep Stages of Human Subjects. Los Angeles, CA: Brain Information Service/ Brain Research Institute, University ofCalifornia.
46. Schabus, M., Dang-Vu, T. T., Albouy, G., Balteau, E., Boly, M., Carrier, J., et al. (2007).Hemo dynamic cerebral correlates of sleep spindles during human on rapid eye movement sleep. Proc. Natl. Acad. Sci. U.S.A. 104, 13164–13169. doi: 10.1073/pnas.0703084104
47. Schabus, M., Dang-Vu, T. T., Heib, D. P. J., Boly, M., Desseilles, M., Vandewalle, G., etal. (2012).ThefateofincomingstimuliduringNREMsleepisdetermined by spindles and the phase of the slow oscillation. Front. Neurol. 3:40. doi: 10.3389/fneur.2012.00040
48. Schabus, M., Gruber, G., Parapatics, S., Sauter, C., Klösch, G., Anderer, P., et al. (2004). Sleep spindles and their significance for declarative memory consolidation. Sleep 27, 1479–1485.
49. Schabus, M., Hödlmoser, K., Gruber, G., Sauter, C., Anderer, P., Klösch, G., et al. (2006). Sleep spindle-related activity in the human EEG and its relation to general cognitive and learning abilities. Eur. J. Neurosci. 23, 1738–1746. doi: 10.1111/j.1460-9568.2006.04694.x
50. Schimicek, P., Zeitlhofer, J., Anderer, P., and Saletu, B. (1994). Automatic sleep-spindle detection procedure: aspects of reliability and validity. Clin. Electroencephalogr. 25, 26–29. doi: 10.1177/1550059494025 00108
51. Shibagaki, M., Kiyono, S., and Watanabe, K. (1982). Spindle evolution in normal and mentally retarded children:areview. Sleep 5, 47–57.
52. Silverstein, L. D., and Levy, C. M. (1976). The stability of the sigma sleep spindle. Electroencephalogr. Clin. Neurophysiol. 40, 666–670.doi:10.1016/00134694(76)90142-5
53. Smith, C. T., Nixon, M. R., and Nader, R. S. (2004). Posttraining increases in REM sleep intensity implicate REM sleep in memory processing and provide a biological marker of learning potential. Learn. Mem. 11, 714–719. doi: 10.1101/lm.74904
54. Steriade, M. (2005). Sleep, epilepsy and thalamic reticular inhibitory neurons. TrendsNeurosci.28,317–324.doi:10.1016/j.tins.2005.03.007
55. Steriade, M. (2006). Grouping of brain rhythms in corticothalamic systems. Neuroscience 137, 1087–1106. doi: 10.1016/j.neuroscience.2005.10.029
56. Uchida, S., Atsumi, Y., and Kojima, T. (1994).Dynamicrelationshipsbetweensleep spindles and delta waves during a NREM period. Brain Res. Bull. 33, 351–355. doi:10.1016/0361-9230(94)90205-4
57. Ujma, P.P., Konrad, B.N., Genzel, L., Bleifuss, A., Simor, P., Pótári, A., etal.(2014). Sleep spindles and intelligence: evidence for a sexual dimorphism. J. Neurosci. 34,16358–16368.doi:10.1523/JNEUROSCI.1857-14.2014
58. Walter, D. O. (1968). The method of complex demodulation. Electroencephalogr. Clin.Neurophysiol.Suppl.27,53–57.
59. Wamsley, E.J., Tucker, M.A., Shinn, A.K., Ono, K.E., McKinley, S.K., Ely, A.V., et al. (2012). Reduced sleep spindles and spindle coherence in schizophrenia: mechanisms of impaired memory consolidation? Biol. Psychiatry 71, 154–161. doi:10.1016/j.biopsych.2011.08.008
60. Warby, S. C., Wendt, S. L., Welinder, P., Munk, E. G. S., Carrillo, O., Sorensen, H. B. D., et al. (2014). Sleep-spindle detection: crowdsourcing and evaluating performance of experts, non-experts and automated methods. Nat. Methods 11, 385–392. doi:10.1038/nmeth.2855
61. Werth, E., Achermann, P., Dijk, D.J., and Borbély, A.A. (1997).Spindlefrequency activity in the sleep EEG: individual differences and topographic distribution. Electroencephalogr. Clin. Neurophysiol. 103, 535–542. doi: 10.1016/S00134694(97)00070-9
62. Zeitlhofer, J., Gruber, G., Anderer, P., Asenbaum, S., Schimicek, P., and Saletu, B. (1997). Topographic distribution of sleep spindles in young healthy subjects. J.SleepRes.6,149–155.doi:10.1046/j.1365-2869.1997.00046.x