Cited by 924Sleep and Wakefulness ResearchNeural dynamics and brain functionSleep and related disorders

Regional Slow Waves and Spindles in Human Sleep

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Nir, Yuval, Staba, Richard J., Andrillon, Thomas, Vyazovskiy, Vladyslav V., Cirelli, Chiara, Fried, Itzhak, Tononi, Giulio·2011·Neuron

Abstract

The most prominent EEG events in sleep are slow waves, reflecting a slow (<1 Hz) oscillation between up and down states in cortical neurons. It is unknown whether slow oscillations are synchronous across the majority or the minority of brain regions--are they a global or local phenomenon? To examine this, we recorded simultaneously scalp EEG, intracerebral EEG, and unit firing in multiple brain regions of neurosurgical patients. We find that most sleep slow waves and the underlying active and inactive neuronal states occur locally. Thus, especially in late sleep, some regions can be active while others are silent. We also find that slow waves can propagate, usually from medial prefrontal cortex to the medial temporal lobe and hippocampus. Sleep spindles, the other hallmark of NREM sleep EEG, are likewise predominantly local. Thus, intracerebral communication during sleep is constrained because slow and spindle oscillations often occur out-of-phase in different brain regions.

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Crossref · 10.1016/j.neuron.2011.02.043

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  • EEG slow frequencies between 1 and 4 Hz during sleep are associated with neuronal down-states and bistability, which prevent the emergence of stable causal interactions among cortical areas, and have been linked to the loss of consciousness.

    “EEG slow frequencies between 1 and 4 Hz during sleep are associated with neuronal down-states and bistability 11 , which prevent the emergence of stable causal interactions among cortical areas 12 , and have been linked to the loss of consciousness 13,14 .”

    From The neural correlates of dreaming (2017) · cites this paper as [11]

    Split into 2 atoms — 0 confirmed, 2 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.

    Experimental — accuracy not yet measured
  • Encoding of information during waking enhances subsequent SWA in specific brain regions.

    “in demonstrating that the encoding of information during waking enhances subsequent SWA in specific brain regions, these studies provide compelling evidence that SWA is regulated locally in addition to its global regulation by brain stem and diencephalic structures (672, 859, 975, 1267).”

    From About Sleep's Role in Memory (2013) · cites this paper as [859]

    The Introduction (page unavailable) says prolonged waking increases SWA, most strongly over frontal cortex, and reports that sleep slow waves vary locally with prior use and plastic processes. It does not specifically say that encoding information during waking enhances subsequent SWA in the regions involved; the paper's own recordings establish that slow waves are often local, not that encoding caused a regional increase. (LLM, conf=0.84)

    Experimental — accuracy not yet measured
  • SWA is regulated locally in addition to its global regulation by brain stem and diencephalic structures.

    “these studies provide compelling evidence that SWA is regulated locally in addition to its global regulation by brain stem and diencephalic structures (672, 859, 975, 1267).”

    From About Sleep's Role in Memory (2013) · cites this paper as [859]

    The Introduction (page unavailable) states that SWA can be locally regulated, and the Results describe a continuum from local to global slow waves. The passages do not identify brain stem or diencephalic structures as regulators of global SWA, so that part of the sentence is not supported by this source. (LLM, conf=0.84)

    Experimental — accuracy not yet measured
  • In the neocortex, single spindles typically express as local phenomena and are restricted to specific regions and circuits, regardless of whether or not they are synchronized in phase with central thalamic spindle generation.

    “Importantly, this research revealed that in the neocortex, single spindles typically express as a local phe-nomena and are restricted to specific regions and circuits, regardless of whether or not they are synchronized in phase with central thalamic spindle generation.”

    From About Sleep's Role in Memory (2013) · cites this paper as [859]

    The Results (Extent of Local Sleep Spindles) and Discussion (Local Sleep Spindles) report that most spindles occur locally, often in only a minority of recorded brain regions. The paper says spindles are generated in the thalamus and that the neocortex governs their synchronization, but it does not establish that cortical spindles remain local regardless of their phase synchronization with thalamic spindle generation. (LLM, conf=0.88)

    Experimental — accuracy not yet measured

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Research works printed but not linked: 85

  1. Amaral DG Price JL Pitkanen A Carmichael ST Aggleton JP Anatomical organization of the primate amygdala The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction 1992 New York Wiley-Liss 1 66
  2. Amzica F Steriade M Disconnection of intracortical synaptic linkages disrupts synchronization of a slow oscillation J. Neurosci 1995a 15 4658 4677 7790931 PMC6577695
  3. Amzica F Steriade M Short- and long-range neuronal synchronization of the slow (< 1 Hz) cortical oscillation J. Neurophysiol 1995b 73 20 38 7714565
  4. Amzica F Steriade M Cellular substrates and laminar profile of sleep K-complex Neuroscience 1998 82 671 686 9483527
  5. Anderer P Klosch G Gruber G Trenker E Pascual-Marqui RD Zeitlhofer J Barbanoj MJ Rappelsberger P Saletu B Low-resolution brain electromagnetic tomography revealed simultaneously active frontal and parietal sleep spindle sources in the human cortex Neuroscience 2001 103 581 592 11274780
  6. Bassetti C Vella S Donati F Wielepp P Weder B SPECT during sleepwalking Lancet 2000 356 484 485 10981896
  7. Borbely AA Achermann P Sleep homeostasis and models of sleep regulation J. Biol. Rhythms 1999 14 557 568 10643753
  8. Buzsaki G Memory consolidation during sleep: A neurophysiological perspective J. Sleep Res 1998 7 Suppl 1 17 23 9682189
  9. Caderas M Niedermeyer E Uematsu S Long DM Nastalski J Sleep spindles recorded from deep cerebral structures in man Clin. Electroencephalogr 1982 13 216 225 7172452
  10. Campbell IG EEG recording and analysis for sleep research Curr. Protoc. Neurosci. Chapter 2009 10 Unit 10.2. PMC2824445 19802813
  11. Cash SS Halgren E Dehghani N Rossetti AO Thesen T Wang C Devinsky O Kuzniecky R Doyle W Madsen JR The human K-complex represents an isolated cortical down-state Science 2009 324 1084 1087 19461004 PMC3715654
  12. Cavada C Company T Tejedor J Cruz-Rizzolo RJ Reinoso-Suarez F The anatomical connections of the macaque monkey orbitofrontal cortex A review. Cereb. Cortex 2000 10 220 242 10731218
  13. Chauvette S Volgushev M Timofeev I Origin of active states in local neocortical networks during slow sleep oscillation Cereb, Cortex 2010 20 2660 2674 20200108 PMC2951844
  14. Chrobak JJ Buzsaki G High-frequency oscillations in the output networks of the hippocampal-entorhinal axis of the freely behaving rat J. Neurosci 1996 16 3056 3066 8622135 PMC6579047
  15. Clemens Z Molle M Eross L Barsi P Halasz P Born J Temporal coupling of parahippocampal ripples, sleep spindles and slow oscillations in humans Brain 2007 130 2868 2878 17615093
  16. Colrain IM The K-complex: A 7-decade history Sleep 2005 28 255 273 16171251
  17. Contreras D Destexhe A Sejnowski TJ Steriade M Control of spatiotemporal coherence of a thalamic oscillation by corticothalamic feedback Science 1996 274 771 774 8864114
  18. Contreras D Destexhe A Steriade M Spindle oscillations during cortical spreading depression in naturally sleeping cats Neuroscience 1997 77 933 936 9130774
  19. Contreras D Steriade M Cellular basis of EEG slow rhythms: A study of dynamic corticothalamic relationships J. Neurosci 1995 15 604 622 7823167 PMC6578315
  20. Dang-Vu TT Desseilles M Laureys S Degueldre C Perrin F Phillips C Maquet P Peigneux P Cerebral correlates of delta waves during non-REM sleep revisited Neuroimage 2005 28 14 21 15979343
  21. Dang-Vu TT Schabus M Desseilles M Albouy G Boly M Darsaud A Gais S Rauchs G Sterpenich V Vandewalle G Spontaneous neural activity during human slow wave sleep Proc. Natl. Acad. Sci. USA 2008 105 15160 15165 18815373 PMC2567508
  22. Dehghani N Cash SS Chen CC Hagler DJ Jr Huang M Dale AM Halgren E Divergent cortical generators of MEG and EEG during human sleep spindles suggested by distributed source modeling PLoS ONE 2010 5 e11454 20628643 PMC2898804
  23. Destexhe A Contreras D Neuronal computations with stochastic network states Science 2006 314 85 90 17023650
  24. Destexhe A Hughes SW Rudolph M Crunelli V Are corticothalamic “up” states fragments of wakefulness? Trends Neurosci 2007 30 334 342 17481741 PMC3005711
  25. Diekelmann S Born J The memory function of sleep Nat. Rev. Neurosci 2010 11 114 126 20046194
  26. Dinner DS Lüders ders HO Epilepsy and Sleep: Physiological and Clinical Relationships 2001 San Diego, CA Academic Press
  27. Ermentrout GB Kleinfeld D Traveling electrical waves in cortex: insights from phase dynamics and speculation on a computational role Neuron 2001 29 33 44 11182079
  28. Esser SK Huber R Massimini M Peterson MJ Ferrarelli F Tononi G A direct demonstration of cortical LTP in humans: a combined TMS/EEG study Brain Res. Bull 2006 69 86 94 16464689
  29. Finelli LA Borbely AA Achermann P Functional topography of the human nonREM sleep electroencephalogram Eur. J. Neurosci 2001 13 2282 2290 11454032
  30. Gottselig JM Bassetti CL Achermann P Power and coherence of sleep spindle frequency activity following hemispheric stroke Brain 2002 125 373 383 11844737
  31. Hahn TT Sakmann B Mehta MR Differential responses of hippocampal subfields to cortical up-down states Proc. Natl. Acad. Sci. USA 2007 104 5169 5174 17360347 PMC1829281
  32. Huber R Ghilardi MF Massimini M Ferrarelli F Riedner BA Peterson MJ Tononi G Arm immobilization causes cortical plastic changes and locally decreases sleep slow wave activity Nat. Neurosci 2006 9 1169 1176 16936722
  33. Isomura Y Sirota A Ozen S Montgomery S Mizuseki K Henze DA Buzsaki G Integration and segregation of activity in entorhinal-hippocampal subregions by neocortical slow oscillations Neuron 2006 52 871 882 17145507
  34. Ji D Wilson MA Coordinated memory replay in the visual cortex and hippocampus during sleep Nat. Neurosci 2007 10 100 107 17173043
  35. Jones BE From waking to sleeping: Neuronal and chemical substrates Trends Pharmacol. Sci 2005 26 578 586 16183137
  36. Jones EG Synchrony in the interconnected circuitry of the thalamus and cerebral cortex Ann. N Y Acad. Sci 2009 1157 10 23 19351352
  37. Khazipov R Sirota A Leinekugel X Holmes GL Ben-Ari Y Buzsaki G Early motor activity drives spindle bursts in the developing somato-sensory cortex Nature 2004 432 758 761 15592414
  38. Kristiansen K Courtois G Rhythmic electrical activity from isolated cerebral cortex Electroencephalogr. Clin. Neurophysiol 1949 1 265 272 18135418
  39. Krueger JM Rector DM Roy S Van Dongen HP Belenky G Panksepp J Sleep as a fundamental property of neuronal assemblies Nat. Rev. Neurosci 2008 9 910 919 18985047 PMC2586424
  40. Landsness EC Crupi D Hulse BK Peterson MJ Huber R Ansari H Coen M Cirelli C Benca RM Ghilardi MF Tononi G Sleep-dependent improvement in visuomotor learning: A causal role for slow waves Sleep 2009 32 1273 1284 19848357 PMC2753806
  41. Le Van Quyen M Staba R Bragin A Dickson C Valderrama M Fried I Engel J Large-scale microelectrode recordings of high-frequency gamma oscillations in human cortex during sleep J. Neurosci 2010 30 7770 7782 20534826 PMC3842470
  42. Loomis AL Harvey EN Hobart G Potential rhythms of the cerebral cortex during sleep Science 1935 81 597 598 17739875
  43. Magnin M Rey M Bastuji H Guillemant P Mauguiere F Garcia-Larrea L Thalamic deactivation at sleep onset precedes that of the cerebral cortex in humans Proc. Natl. Acad. Sci. USA 2010 107 3829 3833 20142493 PMC2840430
  44. Mahowald MW Schenck CH Insights from studying human sleep disorders Nature 2005 437 1279 1285 16251953
  45. Maquet P Functional neuroimaging of normal human sleep by positron emission tomography J. Sleep Res 2000 9 207 231 11012860
  46. Marshall L Helgadottir H Molle M Born J Boosting slow oscillations during sleep potentiates memory Nature 2006 444 610 613 17086200
  47. McCormick DA Bal T Sleep and arousal: Thalamocortical mechanisms Annu. Rev. Neurosci 1997 20 185 215 9056712
  48. McCormick DA Pape HC Properties of a hyperpolarization-activated cation current and its role in rhythmic oscillation in thalamic relay neurones J. Physiol 1990 431 291 318 1712843 PMC1181775
  49. McDonald AJ Cortical pathways to the mammalian amygdala Prog. Neurobiol 1998 55 257 332 9643556
  50. Mohajerani MH McVea DA Fingas M Murphy TH Mirrored bilateral slow-wave cortical activity within local circuits revealed by fast bihemispheric voltage-sensitive dye imaging in anesthetized and awake mice J. Neurosci 2010 30 3745 3751 20220008 PMC6632233
  51. Molle M Marshall L Gais S Born J Grouping of spindle activity during slow oscillations in human non-rapid eye movement sleep J. Neurosci 2002 22 10941 10947 12486189 PMC6758415
  52. Molle M Yeshenko O Marshall L Sara SJ Born J Hippocampal sharp wave-ripples linked to slow oscillations in rat slow-wave sleep J. Neurophysiol 2006 96 62 70 16611848
  53. Mukhametov LM Supin AY Polyakova IG Interhemispheric asymmetry of the electroencephalographic sleep patterns in dolphins Brain Res 1977 134 581 584 902119
  54. Nir Y Mukamel R Dinstein I Privman E Harel M Fisch L Gelbard-Sagiv H Kipervasser S Andelman F Neufeld MY Interhemispheric correlations of slow spontaneous neuronal fluctuations revealed in human sensory cortex Nat. Neurosci 2008 11 1100 1108 19160509 PMC2642673
  55. Noda H Adey WR Firing of neuron pairs in cat association cortex during sleep and wakefulness J. Neurophysiol 1970 33 672 684 4318175
  56. Pare D Collins DR Pelletier JG Amygdala oscillations and the consolidation of emotional memories Trends. Cogn. Sci 2002 6 306 314 12110364
  57. Rattenborg NC Amlaner CJ Lima SL Unilateral eye closure and interhemispheric EEG asymmetry during sleep in the pigeon (Columba livia) Brain Behav. Evol 2001 58 323 332 12016351
  58. Rubio-Garrido P Perez-de-Manzo F Porrero C Galazo MJ Clasca F Thalamic input to distal apical dendrites in neocortical layer 1 is massive and highly convergent Cereb. Cortex 2009 19 2380 2395 19188274
  59. Sanchez-Vives MV McCormick DA Cellular and network mechanisms of rhythmic recurrent activity in neocortex Nat. Neurosci 2000 3 1027 1034 11017176
  60. Sejnowski TJ Destexhe A Why do we sleep? Brain Res 2000 886 208 223 11119697
  61. Shu Y Hasenstaub A McCormick DA Turning on and off recurrent balanced cortical activity Nature 2003 423 288 293 12748642
  62. Sirota A Buzsaki G Interaction between neocortical and hippo-campal networks via slow oscillations Thalamus Relat. Syst 2005 3 245 259 18185848 PMC2180396
  63. Sirota A Csicsvari J Buhl D Buzsaki G Communication between neocortex and hippocampus during sleep in rodents Proc. Natl. Acad. Sci. USA 2003 100 2065 2069 12576550 PMC149959
  64. Steriade M Corticothalamic resonance, states of vigilance and mentation Neuroscience 2000 101 243 276 11074149
  65. Steriade M Neuronal substrates of sleep and epilepsy 2003 Cambridge, UK Cambridge University Press
  66. Steriade M Contreras D Curro Dossi R Nunez A The slow (< 1 Hz) oscillation in reticular thalamic and thalamocortical neurons: Scenario of sleep rhythm generation in interacting thalamic and neocortical networks J. Neurosci 1993a 13 3284 3299 8340808 PMC6576531
  67. Steriade M Nunez A Amzica F Intracellular analysis of relations between the slow (< 1 Hz) neocortical oscillation and other sleep rhythms of the electroencephalogram J. Neurosci 1993b 13 3266 3283 8340807 PMC6576520
  68. Steriade M Nunez A Amzica F A novel slow (< 1 Hz) oscillation of neocortical neurons in vivo: Depolarizing and hyperpolarizing components J. Neurosci 1993c 13 3252 3265 8340806 PMC6576541
  69. Steriade M Timofeev I Grenier F Natural waking and sleep states: A view from inside neocortical neurons J. Neurophysiol 2001 85 1969 1985 11353014
  70. Stickgold R Walker MP Sleep-dependent memory consolidation and reconsolidation Sleep Med 2007 8 331 343 17470412 PMC2680680
  71. Terzaghi M Sartori I Tassi L Didato G Rustioni V LoRusso G Manni R Nobili L Evidence of dissociated arousal states during NREM parasomnia from an intracerebral neurophysiological study Sleep 2009 32 409 412 19294961 PMC2647795
  72. Timofeev I Grenier F Bazhenov M Sejnowski TJ Steriade M Origin of slow cortical oscillations in deafferented cortical slabs Cereb. Cortex 2000 10 1185 1199 11073868
  73. Timofeev I Grenier F Steriade M Disfacilitation and active inhibition in the neocortex during the natural sleep-wake cycle: An intracellular study Proc. Natl. Acad. Sci. USA 2001 98 1924 1929 11172052 PMC29358
  74. Timofeev I Steriade M Low-frequency rhythms in the thalamus of intact-cortex and decorticated cats J. Neurophysiol 1996 76 4152 4168 8985908
  75. Tononi G Cirelli C Sleep function and synaptic homeostasis Sleep Med. Rev 2006 10 49 62 16376591
  76. Tononi G Massimini M Riedner BA Sleepy dialogues between cortex and hippocampus: Who talks to whom? Neuron 2006 52 748 749 17145497
  77. Volgushev M Chauvette S Mukovski M Timofeev I Precise long-range synchronization of activity and silence in neocortical neurons during slow-wave oscillations J. Neurosci 2006 26 5665 5672 16723523 PMC6675259
  78. Vyazovskiy V Borbely AA Tobler I Unilateral vibrissae stimulation during waking induces interhemispheric EEG asymmetry during subsequent sleep in the rat J. Sleep. Res 2000 9 367 371 11123523
  79. Vyazovskiy VV Faraguna U Cirelli C Tononi G Triggering slow waves during NREM sleep in the rat by intracortical electrical stimulation: Effects of sleep/wake history and background activity J. Neurophysiol 2009a 101 1921 1931 19164101 PMC2695630
  80. Vyazovskiy VV Olcese U Lazimy YM Faraguna U Esser SK Williams JC Cirelli C Tononi G Cortical firing and sleep homeostasis Neuron 2009b 63 865 878 19778514 PMC2819325
  81. Wagner T Axmacher N Lehnertz K Elger CE Fell J Sleep-dependent directional coupling between human neocortex and hippocampus Cortex 2010 46 256 263 19552899
  82. Werth E Achermann P Borbely AA Fronto-occipital EEG power gradients in human sleep J. Sleep Res 1997 6 102 112 9377529
  83. Wierzynski CM Lubenov EV Gu M Siapas AG State-dependent spike-timing relationships between hippocampal and prefrontal circuits during sleep Neuron 2009 61 587 596 19249278 PMC2701743
  84. Wolansky T Clement EA Peters SR Palczak MA Dickson CT Hippocampal slow oscillation: A novel EEG state and its coordination with ongoing neocortical activity J. Neurosci 2006 26 6213 6229 16763029 PMC6675178
  85. Wyler AR Ojemann GA Ward AA Jr Neurons in human epileptic cortex: Correlation between unit and EEG activity Ann. Neurol 1982 11 301 308 7092182

Cited by

Sorted by citations

Authors
Nir, Y., Staba, R. J., Andrillon, T., Vyazovskiy, V. V., Cirelli, C., Fried, I., & Tononi, G.
Affiliations
  • University of Wisconsin–Madison (US)
  • University of California, Los Angeles (US)
Corresponding author
Tononi, Giulio
Venue
Neuron
Publisher
Elsevier BV
Published
2011-04
Volume
70
Issue
1
Pages
153-169
ISSN
0896-6273 (ISSN-L)
OpenAlex
W1973117088
Cited by
924
References
18
Citations by year
2026: 37 · 2025: 72 · 2024: 65 · 2023: 67 · 2022: 73 · 2021: 56 · 2020: 69 · 2019: 83 · 2018: 60 · 2017: 81 · 2016: 51 · 2015: 53 · 2014: 45 · 2013: 56 · 2012: 38
FWCI
25.51
Type
journal article
Language
en
Open access
Locations
  • Neuron (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
  • Open Research (University of Surrey) (submittedVersion)
  • Surrey Research Insight Open Access (The University of Surrey) (submittedVersion)
Funders
  • European Molecular Biology Organization
  • National Institutes of Health (5p20mh077967-04, DP1OD000579)
  • National Institute of Mental Health (P20MH-077967)
  • National Institute of Neurological Disorders and Stroke (R01NS055185, R01NS033221, R01NS071048)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
  • Social Sciences › Psychology › Experimental and Cognitive Psychology › Sleep and related disorders
Keywords
sleep slow waves, sleep spindles, slow oscillations, intracranial EEG, NREM sleep, up-down states, slow wave propagation, medial prefrontal cortex, medial temporal lobe, hippocampus, interregional communication, neurosurgical patients
MeSH terms
Brain, Electroencephalography, Epilepsy, Humans, Sleep, Polysomnography

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