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Oscillating circuitries in the sleeping brain

Abstract

Brain activity during sleep is characterized by circuit-specific oscillations, including slow waves, spindles and theta waves, which are nested in thalamocortical or hippocampal networks. A major challenge is to determine the relationships between these oscillatory activities and the identified networks of sleep-promoting and wake-promoting neurons distributed throughout the brain. Improved understanding of the neurobiological mechanisms that orchestrate sleep-related oscillatory activities, both in time and space, is expected to generate further insight into the delineation of sleep states and their functions.

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Fig. 1: Sleep-state specificity of oscillations.
Fig. 2: Circuit mechanisms of NREM sleep-specific oscillations.
Fig. 3: Circuit mechanisms of REM sleep-specific oscillations.

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References

  1. Caton, R. The electric currents of the brain. Br. Med. J. 2, 278 (1875).

    Google Scholar 

  2. Berger, H. Über das elektrenkephalogramm des menschen [German]. Arch. Psychiatr. Nervenkr. 87, 527–570 (1929).

    Google Scholar 

  3. Wright, K. P. Jr., Badia, P. & Wauquier, A. Topographical and temporal patterns of brain activity during the transition from wakefulness to sleep. Sleep 18, 880–889 (1995).

    PubMed  Google Scholar 

  4. Vyazovskiy, V. V. et al. Local sleep in awake rats. Nature 472, 443–447 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Huber, R., Ghilardi, M. F., Massimini, M. & Tononi, G. Local sleep and learning. Nature 430, 78–81 (2004). The first demonstration of localized sleep oscillations in the human brain.

    CAS  PubMed  Google Scholar 

  6. Gent, T. C., Bandarabadi, M., Herrera, C. G. & Adamantidis, A. R. Thalamic dual-control of sleep and wakefulness. Nat. Neurosci. 21, 974–984 (2018). The first demonstration of thalamic control of frontal cortical slow waves and their brain-wide propagation via a thalamic relay.

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Poulet, J. F. & Petersen, C. C. Internal brain state regulates membrane potential synchrony in barrel cortex of behaving mice. Nature 454, 881–885 (2008).

    CAS  PubMed  Google Scholar 

  8. Krueger, J. M. et al. Sleep as a fundamental property of neuronal assemblies. Nat. Rev. Neurosci. 9, 910–919 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Weber, F. & Dan, Y. Circuit-based interrogation of sleep control. Nature 538, 51–59 (2016).

    CAS  PubMed  Google Scholar 

  10. Marzano, C. et al. Recalling and forgetting dreams: theta and alpha oscillations during sleep predict subsequent dream recall. J. Neurosci. 31, 6674–6683 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Molle, M., Marshall, L., Gais, S. & Born, J. Grouping of spindle activity during slow oscillations in human non-rapid eye movement sleep. J. Neurosci. 22, 10941–10947 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  12. Bastien, C. H., Crowley, K. E. & Colrain, I. M. Evoked potential components unique to non-REM sleep: relationship to evoked K-complexes and vertex sharp waves. Int. J. Psychophysiol. 46, 257–274 (2002).

    PubMed  Google Scholar 

  13. Bernardi, G. et al. Regional delta waves in human rapid eye movement sleep. J. Neurosci. 39, 2686–2697 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Tort, A. B. L. et al. Parallel detection of theta and respiration-coupled oscillations throughout the mouse brain. Sci. Rep. 8, 6432 (2018).

    PubMed  PubMed Central  Google Scholar 

  15. Zelano, C. et al. Nasal respiration entrains human limbic oscillations and modulates cognitive function. J. Neurosci. 36, 12448–12467 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Mensen, A., Zhang, Z., Qi, M. & Khatami, R. The occurrence of individual slow waves in sleep is predicted by heart rate. Sci. Rep. 6, 29671 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Perogamvros, L. et al. Increased heartbeat-evoked potential during REM sleep in nightmare disorder. Neuroimage Clin. 22, 101701 (2019).

    PubMed  PubMed Central  Google Scholar 

  18. Brown, S. A. Circadian metabolism: from mechanisms to metabolomics and medicine. Trends Endocrinol. Metab. 27, 415–426 (2016).

    CAS  PubMed  Google Scholar 

  19. Mang, G. M. & Franken, P. Genetic dissection of sleep homeostasis. Curr. Top. Behav. Neurosci. 25, 25–63 (2015).

    PubMed  Google Scholar 

  20. Schmidt, M. H. The energy allocation function of sleep: a unifying theory of sleep, torpor, and continuous wakefulness. Neurosci. Biobehav. Rev. 47, 122–153 (2014).

    PubMed  Google Scholar 

  21. Blumberg, M. S. Beyond dreams: do sleep-related movements contribute to brain development? Front. Neurol. 1, 140 (2010).

    PubMed  PubMed Central  Google Scholar 

  22. Bryant, P. A., Trinder, J. & Curtis, N. Sick and tired: does sleep have a vital role in the immune system? Nat. Rev. Immunol. 4, 457–467 (2004).

    CAS  PubMed  Google Scholar 

  23. Rechtschaffen, A. & Kales, A. A Manual of Standardized Terminology, Techniques and Scoring System for Sleep Stages of Human Subjects (NIH Publishing, 1968).

  24. Iber, C., Ancoli-Israel, S., Chesson, A. & Quan, S. F. The AASM Manual for the Score of Sleep and Associated Events: Rules, Terminology, and Technical Specifications (AASM, 2007).

  25. Schulz, H. Rethinking sleep analysis. J. Clin. Sleep Med. 4, 99–103 (2008).

    PubMed  PubMed Central  Google Scholar 

  26. Nielsen, T. et al. Partial REM-sleep deprivation increases the dream-like quality of mentation from REM sleep and sleep onset. Sleep 28, 1083–1089 (2005).

    PubMed  Google Scholar 

  27. Bodizs, R., Sverteczki, M., Lazar, A. S. & Halasz, P. Human parahippocampal activity: non-REM and REM elements in wake-sleep transition. Brain Res. Bull. 65, 169–176 (2005).

    PubMed  Google Scholar 

  28. Lacroix, M. M. et al. Improved sleep scoring in mice reveals human-like stages. Preprint at bioRxiv https://doi.org/10.1101/489005 (2018).

    Article  Google Scholar 

  29. Loomis, A. L., Harvey, N. & Hobart, G. A. 3rd Distribution and disturbance patterns in the human electroencephalogram, with special reference to sleep. J. Neurophysiol. 1, 413–430 (1938).

    Google Scholar 

  30. Davis, H., Davis, P. A., Loomis, A. L., Harvey, E. N. & Hobart, G. Changes in human brain potentials during the onset of sleep. Science 86, 448–450 (1937).

    CAS  PubMed  Google Scholar 

  31. Steriade, M., Nuñez, A. & Amzica, F. A novel slow (<1 Hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components. J. Neurosci. 13, 3252–3265 (1993). The seminal paper that differentiated slow and delta oscillations.

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Timofeev, I., Grenier, F., Bazhenov, M., Sejnowski, T. J. & Steriade, M. Origin of slow cortical oscillations in deafferented cortical slabs. Cereb. Cortex 10, 1185–1199 (2000). An important study showing spontaneous slow oscillations in cortical tissue devoid of thalamic inputs.

    CAS  PubMed  Google Scholar 

  33. Steriade, M., Nuñez, A. & Amzica, F. Intracellular analysis of relations between the slow (<1Hz) neocortical oscillation and other sleep rhythms of the electroencephalogram. J. Neurosci. 13, 3266–3283 (1993).

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Cash, S. S. et al. The human K-complex represents an isolated cortical down-state. Science 324, 1084–1087 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Csercsa, R. et al. Laminar analysis of slow wave activity in humans. Brain 133, 2814–2829 (2010).

    PubMed  PubMed Central  Google Scholar 

  36. Vyazovskiy, V. V., 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. 101, 1921–1931 (2009).

    PubMed  PubMed Central  Google Scholar 

  37. Panagiotou, M., Vyazovskiy, V. V., Meijer, J. H. & Deboer, T. Differences in electroencephalographic non-rapid-eye movement sleep slow-wave characteristics between young and old mice. Sci. Rep. 7, 43656 (2017).

    PubMed  PubMed Central  Google Scholar 

  38. Koike, B. D. V. et al. Electrophysiological evidence that the retrosplenial cortex displays a strong and specific activation phased with hippocampal theta during paradoxical (REM) sleep. J. Neurosci. 37, 8003–8013 (2017).

    PubMed  PubMed Central  Google Scholar 

  39. Einstein, M. C., Polack, P. O., Tran, D. T. & Golshani, P. Visually evoked 3-5 Hz membrane potential oscillations reduce the responsiveness of visual cortex neurons in awake behaving mice. J. Neurosci. 37, 5084–5098 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Funk, C. M. et al. Role of somatostatin-positive cortical interneurons in the generation of sleep slow waves. J. Neurosci. 37, 9132–9148 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Steriade, M., McCormick, D. A. & Sejnowski, T. J. Thalamocortical oscillations in the sleeping and aroused brain. Science 262, 679–685 (1993).

    CAS  PubMed  Google Scholar 

  42. Steriade, M., Contreras, D., Curro Dossi, R. & Nuñez, 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. 13, 3284–3299 (1993).

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Blethyn, K. L., Hughes, S. W., Toth, T. I., Cope, D. W. & Crunelli, V. Neuronal basis of the slow (<1 Hz) oscillation in neurons of the nucleus reticularis thalami in vitro. J. Neurosci. 26, 2474–2486 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  44. Steriade, M. & Amzica, F. Intracortical and corticothalamic coherency of fast spontaneous oscillations. Proc. Natl Acad. Sci. USA 93, 2533–2538 (1996).

    CAS  PubMed  Google Scholar 

  45. Sanchez-Vives, M. V. & McCormick, D. A. Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat. Neurosci. 3, 1027–1034 (2000).

    CAS  PubMed  Google Scholar 

  46. Lorincz, M. L. et al. A distinct class of slow (approximately 0.2-2 Hz) intrinsically bursting layer 5 pyramidal neurons determines UP/DOWN state dynamics in the neocortex. J. Neurosci. 35, 5442–5458 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  47. Fellin, T. et al. Endogenous nonneuronal modulators of synaptic transmission control cortical slow oscillations in vivo. Proc. Natl Acad. Sci. USA 106, 15037–15042 (2009).

    CAS  PubMed  Google Scholar 

  48. Zucca, S. et al. An inhibitory gate for state transition in cortex. eLife 6, e26177 (2017).

    PubMed  PubMed Central  Google Scholar 

  49. Neske, G. T. & Connors, B. W. Distinct roles of SOM and VIP interneurons during cortical up states. Front. Neural Circuits 10, 52 (2016).

    PubMed  PubMed Central  Google Scholar 

  50. Contreras, D. & Steriade, M. Cellular basis of EEG slow rhythms: a study of dynamic corticothalamic relationships. J. Neurosci. 15, 604–622 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Maingret, N., Girardeau, G., Todorova, R., Goutierre, M. & Zugaro, M. Hippocampo-cortical coupling mediates memory consolidation during sleep. Nat. Neurosci. 19, 959–964 (2016).

    CAS  PubMed  Google Scholar 

  52. Mölle, M., Bergmann, T. O., Marshall, L. & Born, J. Fast and slow spindles during the sleep slow oscillation: disparate coalescence and engagement in memory processing. Sleep 34, 1411–1421 (2011).

    PubMed  PubMed Central  Google Scholar 

  53. David, F. et al. Essential thalamic contribution to slow waves of natural sleep. J. Neurosci. 33, 19599–19610 (2013). An important study showing the contribution of thalamic T-type calcium channels to cortical slow waves.

    CAS  PubMed  PubMed Central  Google Scholar 

  54. Crunelli, V. & Hughes, S. W. The slow (<1Hz) rhythm of non-REM sleep: a dialogue between three cardinal oscillators. Nat. Neurosci. 13, 9–17 (2010).

    CAS  PubMed  Google Scholar 

  55. Timofeev, I. & Steriade, M. Low-frequency rhythms in the thalamus of intact-cortex and decorticated cats. J. Neurophysiol. 76, 4152–4168 (1996).

    CAS  PubMed  Google Scholar 

  56. Honjoh, S. et al. Regulation of cortical activity and arousal by the matrix cells of the ventromedial thalamic nucleus. Nat. Commun. 9, 2100 (2018).

    PubMed  PubMed Central  Google Scholar 

  57. Baker, R. et al. Altered activity in the central medial thalamus precedes changes in the neocortex during transitions into both sleep and propofol anesthesia. J. Neurosci. 34, 13326–13335 (2014). First demonstration of disruption in connectivity between midline thalamus and frontal cortex, but not between sensory thalamus and cortex, occuring at loss of consciousness.

    PubMed  PubMed Central  Google Scholar 

  58. Magnin, M., Bastuji, H., Garcia-Larrea, L. & Mauguière, F. Human thalamic medial pulvinar nucleus is not activated during paradoxical sleep. Cereb. Cortex 14, 858–862 (2004).

    PubMed  Google Scholar 

  59. Lemieux, M., Chen, J. Y., Lonjers, P., Bazhenov, M. & Timofeev, I. The impact of cortical deafferentation on the neocortical slow oscillation. J. Neurosci. 34, 5689–5703 (2014). The first study to show transient reductions in cortical slow waves following thalamic lesioning.

    PubMed  PubMed Central  Google Scholar 

  60. Durkin, J. et al. Cortically coordinated NREM thalamocortical oscillations play an essential, instructive role in visual system plasticity. Proc. Natl Acad. Sci. USA 114, 10485–10490 (2017).

    CAS  PubMed  Google Scholar 

  61. Miyamoto, D. et al. Top-down cortical input during NREM sleep consolidates perceptual memory. Science 352, 1315–1318 (2016). Discovery of a mechanism that regulates memory consolidation during NREM sleep.

    CAS  PubMed  Google Scholar 

  62. Siclari, F. et al. Two distinct synchronization processes in the transition to sleep: a high-density electroencephalographic study. Sleep 37, 1621–1637 (2014).

    PubMed  PubMed Central  Google Scholar 

  63. Massimini, M., Huber, R., Ferrarelli, F., Hill, S. & Tononi, G. The sleep slow oscillation as a traveling wave. J. Neurosci. 24, 6862–6870 (2004). The first demonstration of anterior to posterior propagation of sleep slow waves in the human brain.

    CAS  PubMed  PubMed Central  Google Scholar 

  64. Nir, Y. et al. Regional slow waves and spindles in human sleep. Neuron 70, 153–169 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  65. Murphy, M. et al. Source modeling sleep slow waves. Proc. Natl Acad. Sci. USA 106, 1608–1613 (2009).

    CAS  PubMed  Google Scholar 

  66. Chauvette, S., Volgushev, M. & Timofeev, I. Origin of active states in local neocortical networks during slow sleep oscillation. Cereb. Cortex 20, 2660–2674 (2010).

    PubMed  PubMed Central  Google Scholar 

  67. 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. 26, 5665–5672 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  68. Riedner, B. A., Hulse, B. K., Murphy, M. J., Ferrarelli, F. & Tononi, G. Temporal dynamics of cortical sources underlying spontaneous and peripherally evoked slow waves. Prog. Brain Res. 193, 201–218 (2011).

    PubMed  PubMed Central  Google Scholar 

  69. Amzica, F. & Steriade, M. Short- and long-range neuronal synchronization of the slow (<1 Hz) cortical oscillation. J. Neurophysiol. 73, 20–38 (1995).

    CAS  PubMed  Google Scholar 

  70. Kaufmann, C. et al. Brain activation and hypothalamic functional connectivity during human non-rapid eye movement sleep: an EEG/fMRI study. Brain 129, 655–667 (2006).

    CAS  PubMed  Google Scholar 

  71. Czisch, M. et al. Acoustic oddball during NREM sleep: a combined EEG/fMRI study. PLOS ONE 4, e6749 (2009).

    PubMed  PubMed Central  Google Scholar 

  72. Tushaus, L. et al. In human non-REM sleep, more slow-wave activity leads to less blood flow in the prefrontal cortex. Sci. Rep. 7, 14993 (2017).

    PubMed  PubMed Central  Google Scholar 

  73. Halász, P. K-complex, a reactive EEG graphoelement of NREM sleep: an old chap in a new garment. Sleep Med. Rev. 9, 391–412 (2005).

    PubMed  Google Scholar 

  74. Massimini, M., Rosanova, M. & Mariotti, M. EEG slow (approximately 1 Hz) waves are associated with nonstationarity of thalamo-cortical sensory processing in the sleeping human. J. Neurophysiol. 89, 1205–1213 (2003).

    PubMed  Google Scholar 

  75. Sherman, S. M. Thalamus plays a central role in ongoing cortical functioning. Nat. Neurosci. 19, 533–541 (2016).

    CAS  PubMed  Google Scholar 

  76. Issa, E. B. & Wang, X. Sensory responses during sleep in primate primary and secondary auditory cortex. J. Neurosci. 28, 14467–14480 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  77. Nir, Y., Vyazovskiy, V. V., Cirelli, C., Banks, M. I. & Tononi, G. Auditory responses and stimulus-specific adaptation in rat auditory cortex are preserved across NREM and REM sleep. Cereb. Cortex 25, 1362–1378 (2015).

    PubMed  Google Scholar 

  78. Amzica, F. & Steriade, M. The K-complex: its slow (<1-Hz) rhythmicity and relation to delta waves. Neurology 49, 952–959 (1997).

    CAS  PubMed  Google Scholar 

  79. De Gennaro, L. & Ferrara, M. Sleep spindles: an overview. Sleep Med. Rev. 7, 423–440 (2003).

    PubMed  Google Scholar 

  80. Andrillon, T. et al. Sleep spindles in humans: insights from intracranial EEG and unit recordings. J. Neurosci. 31, 17821–17834 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  81. Halassa, M. M. et al. Selective optical drive of thalamic reticular nucleus generates thalamic bursts and cortical spindles. Nat. Neurosci. 14, 1118–1120 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  82. Bartho, P. et al. Ongoing network state controls the length of sleep spindles via inhibitory activity. Neuron 82, 1367–1379 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  83. Kim, A. et al. Optogenetically induced sleep spindle rhythms alter sleep architectures in mice. Proc. Natl Acad. Sci. USA 109, 20673–20678 (2012).

    CAS  PubMed  Google Scholar 

  84. O’Reilly, C. & Nielsen, T. Assessing EEG sleep spindle propagation. Part 2: experimental characterization. J. Neurosci. Methods 221, 215–227 (2014).

    PubMed  Google Scholar 

  85. Souza, R. T., Gerhardt, G. J., Schönwald, S. V., Rybarczyk-Filho, J. L. & Lemke, N. Synchronization and propagation of global sleep spindles. PLOS ONE 11, e0151369 (2016).

    PubMed  PubMed Central  Google Scholar 

  86. Purcell, S. M. et al. Characterizing sleep spindles in 11,630 individuals from the National Sleep Research Resource. Nat. Commun. 8, 15930 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  87. Ayoub, A. et al. Differential effects on fast and slow spindle activity, and the sleep slow oscillation in humans with carbamazepine and flunarizine to antagonize voltage-dependent Na+ and Ca2+ channel activity. Sleep 36, 905–911 (2013).

    PubMed  PubMed Central  Google Scholar 

  88. Knoblauch, V., Martens, W., Wirz-Justice, A., Krauchi, K. & Cajochen, C. Regional differences in the circadian modulation of human sleep spindle characteristics. Eur. J. Neurosci. 18, 155–163 (2003).

    PubMed  Google Scholar 

  89. Cox, R., Hofman, W. F., de Boer, M. & Talamini, L. M. Local sleep spindle modulations in relation to specific memory cues. Neuroimage 99, 103–110 (2014).

    PubMed  Google Scholar 

  90. Staresina, B. P. et al. Hierarchical nesting of slow oscillations, spindles and ripples in the human hippocampus during sleep. Nat. Neurosci. 18, 1679–1686 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  91. Klinzing, J. G. et al. Spindle activity phase-locked to sleep slow oscillations. Neuroimage 134, 607–616 (2016).

    PubMed  Google Scholar 

  92. Zeitlhofer, J. et al. Topographic distribution of sleep spindles in young healthy subjects. J. Sleep Res. 6, 149–155 (1997).

    CAS  PubMed  Google Scholar 

  93. Werth, E., Achermann, P., Dijk, D. J. & Borbely, A. A. Spindle frequency activity in the sleep EEG: individual differences and topographic distribution. Electroencephalogr. Clin. Neurophysiol. 103, 535–542 (1997).

    CAS  PubMed  Google Scholar 

  94. Ujma, P. P. et al. A comparison of two sleep spindle detection methods based on all night averages: individually adjusted vs. fixed frequencies. Front. Hum. Neurosci. 9, 52 (2015).

    PubMed  PubMed Central  Google Scholar 

  95. Schabus, M. et al. Hemodynamic cerebral correlates of sleep spindles during human non-rapid eye movement sleep. Proc. Natl Acad. Sci. USA 104, 13164–13169 (2007).

    CAS  PubMed  Google Scholar 

  96. Jobert, M., Poiseau, E., Jähnig, P., Schulz, H. & Kubicki, S. Topographical analysis of sleep spindle activity. Neuropsychobiology 26, 210–217 (1992).

    CAS  PubMed  Google Scholar 

  97. Piantoni, G., Halgren, E. & Cash, S. S. The contribution of thalamocortical core and matrix pathways to sleep spindles. Neural Plast. 2016, 3024342 (2016).

    PubMed  PubMed Central  Google Scholar 

  98. Bal, T., von Krosigk, M. & McCormick, D. A. Role of the ferret perigeniculate nucleus in the generation of synchronized oscillations in vitro. J. Physiol. 483, 665–685 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  99. Bonjean, M. et al. Corticothalamic feedback controls sleep spindle duration in vivo. J. Neurosci. 31, 9124–9134 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  100. Luthi, A. Sleep spindles: where they come from, what they do. Neuroscientist 20, 243–256 (2014).

    PubMed  Google Scholar 

  101. Mak-McCully, R. A. et al. Coordination of cortical and thalamic activity during non-REM sleep in humans. Nat. Commun. 8, 15499 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  102. Sarasso, S. et al. Hippocampal sleep spindles preceding neocortical sleep onset in humans. Neuroimage 86, 425–432 (2014).

    CAS  PubMed  Google Scholar 

  103. Csicsvari, J., Hirase, H., Mamiya, A. & Buzsaki, G. Ensemble patterns of hippocampal CA3–CA1 neurons during sharp wave-associated population events. Neuron 28, 585–594 (2000).

    CAS  PubMed  Google Scholar 

  104. Ylinen, A. et al. Sharp wave-associated high-frequency oscillation (200Hz) in the intact hippocampus: network and intracellular mechanisms. J. Neurosci. 15, 30–46 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  105. Chrobak, J. J. & Buzsaki, G. High-frequency oscillations in the output networks of the hippocampal–entorhinal axis of the freely behaving rat. J. Neurosci. 16, 3056–3066 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  106. Khodagholy, D., Gelinas, J. N. & Buzsaki, G. Learning-enhanced coupling between ripple oscillations in association cortices and hippocampus. Science 358, 369–372 (2017). Important demonstration of sleep functions being coordinated by localized regulation between brain regions.

    CAS  PubMed  PubMed Central  Google Scholar 

  107. Skaggs, W. E. et al. EEG sharp waves and sparse ensemble unit activity in the macaque hippocampus. J. Neurophysiol. 98, 898–910 (2007).

    PubMed  Google Scholar 

  108. Bragin, A., Engel, J. Jr, Wilson, C. L., Fried, I. & Mathern, G. W. Hippocampal and entorhinal cortex high-frequency oscillations (100-500 Hz) in human epileptic brain and in kainic acid-treated rats with chronic seizures. Epilepsia 40, 127–137 (1999).

    CAS  PubMed  Google Scholar 

  109. Colgin, L. L. Rhythms of the hippocampal network. Nat. Rev. Neurosci. 17, 239–249 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  110. Hulse, B. K., Moreaux, L. C., Lubenov, E. V. & Siapas, A. G. Membrane potential dynamics of CA1 pyramidal neurons during hippocampal ripples in awake mice. Neuron 89, 800–813 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  111. Oliva, A., Fernandez-Ruiz, A., Buzsaki, G. & Berenyi, A. Role of hippocampal CA2 region in triggering sharp-wave ripples. Neuron 91, 1342–1355 (2016).

    CAS  PubMed  Google Scholar 

  112. Stark, E. et al. Pyramidal cell-interneuron interactions underlie hippocampal ripple oscillations. Neuron 83, 467–480 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  113. Schlingloff, D., Káli, S., Freund, T. F., Hájos, N. & Gulyás, A. I. Mechanisms of sharp wave initiation and ripple generation. J. Neurosci. 34, 11385–11398 (2014).

    PubMed  PubMed Central  Google Scholar 

  114. Logothetis, N. K. et al. Hippocampal–cortical interaction during periods of subcortical silence. Nature 491, 547–553 (2012).

    CAS  PubMed  Google Scholar 

  115. Yang, M., Logothetis, N. K. & Eschenko, O. Occurrence of hippocampal ripples is associated with activity suppression in the mediodorsal thalamic nucleus. J. Neurosci. 39, 434–444 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  116. Diekelmann, S. & Born, J. The memory function of sleep. Nat. Rev. Neurosci. 11, 114–126 (2010).

    CAS  PubMed  Google Scholar 

  117. Miyawaki, H. & Diba, K. Regulation of hippocampal firing by network oscillations during sleep. Curr. Biol. 26, 893–902 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  118. Hughes, S. W., Lorincz, M. L., Parri, H. R. & Crunelli, V. Infraslow (<0.1Hz) oscillations in thalamic relay nuclei basic mechanisms and significance to health and disease states. Prog. Brain Res. 193, 145–162 (2011).

    PubMed  PubMed Central  Google Scholar 

  119. Lecci, S. et al. Coordinated infraslow neural and cardiac oscillations mark fragility and offline periods in mammalian sleep. Sci. Adv. 3, e1602026 (2017).

    PubMed  PubMed Central  Google Scholar 

  120. De Gennaro, L., Ferrara, M., Curcio, G. & Cristiani, R. Antero-posterior EEG changes during the wakefulness–sleep transition. Clin. Neurophysiol. 112, 1901–1911 (2001).

    PubMed  Google Scholar 

  121. Marzano, C. et al. How we fall asleep: regional and temporal differences in electroencephalographic synchronization at sleep onset. Sleep Med. 14, 1112–1122 (2013).

    PubMed  Google Scholar 

  122. Uchida, S., Maehara, T., Hirai, N., Okubo, Y. & Shimizu, H. Cortical oscillations in human medial temporal lobe during wakefulness and all-night sleep. Brain Res. 891, 7–19 (2001).

    CAS  PubMed  Google Scholar 

  123. Kobayashi, T. et al. Interhemispheric differences of the correlation dimension in a human sleep electroencephalogram. Psychiatry Clin. Neurosci. 56, 265–266 (2002).

    PubMed  Google Scholar 

  124. De Gennaro, L. et al. Changes in fronto-posterior functional coupling at sleep onset in humans. J. Sleep Res. 13, 209–217 (2004).

    PubMed  Google Scholar 

  125. Buckelmuller, J., Landolt, H. P., Stassen, H. H. & Achermann, P. Trait-like individual differences in the human sleep electroencephalogram. Neuroscience 138, 351–356 (2006).

    CAS  PubMed  Google Scholar 

  126. Vyazovskiy, V. V. et al. Cortical firing and sleep homeostasis. Neuron 63, 865–878 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  127. Nobili, L. et al. Local aspects of sleep: observations from intracerebral recordings in humans. Prog. Brain Res. 199, 219–232 (2012).

    PubMed  Google Scholar 

  128. Magnin, M. et al. Thalamic deactivation at sleep onset precedes that of the cerebral cortex in humans. Proc. Natl Acad. Sci USA 107, 3829–3833 (2010). The first demonstration of sleep-relevant changes in the thalamus preceeding those in the cortex at the onset of human sleep.

    CAS  PubMed  Google Scholar 

  129. Bastuji, H. et al. Thalamic responses to nociceptive-specific input in humans: functional dichotomies and thalamo-cortical connectivity. Cereb. Cortex 26, 2663–2676 (2016).

    PubMed  Google Scholar 

  130. Finelli, L. A., Borbély, A. A. & Achermann, P. Functional topography of the human nonREM sleep electroencephalogram. Eur. J. Neurosci. 13, 2282–2290 (2001).

    CAS  PubMed  Google Scholar 

  131. Luppi, P. H., Peyron, C. & Fort, P. Not a single but multiple populations of GABAergic neurons control sleep. Sleep Med. Rev. 32, 85–94 (2017).

    PubMed  Google Scholar 

  132. Saper, C. B., Fuller, P. M., Pedersen, N. P., Lu, J. & Scammell, T. E. Sleep state switching. Neuron 68, 1023–1042 (2010). Description of the flip-flop model of sleep.

    CAS  PubMed  PubMed Central  Google Scholar 

  133. Zhang, Z. et al. Neuronal ensembles sufficient for recovery sleep and the sedative actions of α2 adrenergic agonists. Nat. Neurosci. 18, 553–561 (2015). An important study showing activation of a population of hypothalamic cells that initiates sleep onset accompanied with a drop in body temperature.

    CAS  PubMed  PubMed Central  Google Scholar 

  134. Chung, S. et al. Identification of preoptic sleep neurons using retrograde labelling and gene profiling. Nature 545, 477–481 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  135. Kroeger, D. et al. Galanin neurons in the ventrolateral preoptic area promote sleep and heat loss in mice. Nat. Commun. 9, 4129 (2018).

    PubMed  PubMed Central  Google Scholar 

  136. Anaclet, C. et al. Identification and characterization of a sleep-active cell group in the rostral medullary brainstem. J. Neurosci. 32, 17970–17976 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  137. Anaclet, C. et al. The GABAergic parafacial zone is a medullary slow wave sleep-promoting center. Nat. Neurosci. 17, 1217–1224 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  138. Oishi, Y. et al. Slow-wave sleep is controlled by a subset of nucleus accumbens core neurons in mice. Nat. Commun. 8, 734 (2017).

    PubMed  PubMed Central  Google Scholar 

  139. Liu, K. et al. Lhx6-positive GABA-releasing neurons of the zona incerta promote sleep. Nature 548, 582–587 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  140. Takata, Y. et al. Sleep and wakefulness are controlled by ventral medial midbrain/pons GABAergic neurons in mice. J. Neurosci. 38, 10080–10092 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  141. Hayashi, Y. et al. Cells of a common developmental origin regulate REM/non-REM sleep and wakefulness in mice. Science 350, 957–961 (2015).

    CAS  PubMed  Google Scholar 

  142. Morairty, S. R. et al. A role for cortical nNOS/NK1 neurons in coupling homeostatic sleep drive to EEG slow wave activity. Proc. Natl Acad. Sci. USA 110, 20272–20277 (2013).

    CAS  PubMed  Google Scholar 

  143. Crunelli, V., David, F., Lőrincz, M. L. & Hughes, S. W. The thalamocortical network as a single slow wave-generating unit. Curr. Opin. Neurobiol. 31, 72–80 (2015).

    CAS  PubMed  Google Scholar 

  144. Sun, Y.-G. et al. Biphasic cholinergic synaptic transmission controls action potential activity in thalamic reticular nucleus neurons. J. Neurosci. 33, 2048–2059 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  145. Beierlein, M. Synaptic mechanisms underlying cholinergic control of thalamic reticular nucleus neurons. J. Physiol. 592, 4137–4145 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  146. Ni, K. M. et al. Selectively driving cholinergic fibers optically in the thalamic reticular nucleus promotes sleep. eLife 5, e10382 (2016).

    PubMed  PubMed Central  Google Scholar 

  147. Giber, K. et al. A subcortical inhibitory signal for behavioral arrest in the thalamus. Nat. Neurosci. 18, 562–568 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  148. Aston-Jones, G. & Bloom, F. E. Activity of norepinephrine-containing locus coeruleus neurons in behaving rats anticipates fluctuations in the sleep-waking cycle. J. Neurosci. 1, 876–886 (1981).

    CAS  PubMed  PubMed Central  Google Scholar 

  149. Jones, B. E. From waking to sleeping: neuronal and chemical substrates. Trends Pharmacol. Sci. 26, 578–586 (2005).

    CAS  PubMed  Google Scholar 

  150. Carter, M. E. et al. Tuning arousal with optogenetic modulation of locus coeruleus neurons. Nat. Neurosci. 13, 1526–1533 (2010). Demonstration of the rapid-arousal properties of noradrenergic neurons in the pons.

    CAS  PubMed  PubMed Central  Google Scholar 

  151. Eschenko, O., Magri, C., Panzeri, S. & Sara, S. J. Noradrenergic neurons of the locus coeruleus are phase locked to cortical up-down states during sleep. Cereb. Cortex 22, 426–435 (2012).

    PubMed  Google Scholar 

  152. Sara, S. J. Locus coeruleus in time with the making of memories. Curr. Opin. Neurobiol. 35, 87–94 (2015).

    CAS  PubMed  Google Scholar 

  153. Beas, B. S. et al. The locus coeruleus drives disinhibition in the midline thalamus via a dopaminergic mechanism. Nat. Neurosci. 21, 963–973 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  154. Lara-Vásquez, A., Espinosa, N., Durán, E., Stockle, M. & Fuentealba, P. Midline thalamic neurons are differentially engaged during hippocampus network oscillations. Sci. Rep. 6, 29807 (2016).

    PubMed  PubMed Central  Google Scholar 

  155. Jego, S. et al. Optogenetic identification of a rapid eye movement sleep modulatory circuit in the hypothalamus. Nat. Neurosci. 16, 1637–1643 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  156. Siclari, F., Bernardi, G., Cataldi, J. & Tononi, G. Dreaming in NREM sleep: a high-density EEG study of slow waves and spindles. J. Neurosci. 38, 9175–9185 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  157. Siclari, F. & Tononi, G. Local aspects of sleep and wakefulness. Curr. Opin. Neurobiol. 44, 222–227 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  158. Bodizs, R. et al. Rhythmic hippocampal slow oscillation characterizes REM sleep in humans. Hippocampus 11, 747–753 (2001).

    CAS  PubMed  Google Scholar 

  159. Jouvet, M. & Michel, F. Electromyographic correlations of sleep in the chronic decorticate & mesencephalic cat [French]. CR Seances Soc. Biol. Fil. 153, 422–425 (1959).

    CAS  Google Scholar 

  160. Shimazono, Y. et al. The correlation of the rhythmic waves of the hippocampus with the behaviors of dogs. Neurol. Med. Chir. 2, 82–88 (1960).

    Google Scholar 

  161. Cantero, J. L. et al. Sleep-dependent theta oscillations in the human hippocampus and neocortex. J. Neurosci. 23, 10897–10903 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  162. Kramis, R., Vanderwolf, C. H. & Bland, B. H. Two types of hippocampal rhythmical slow activity in both the rabbit and the rat: relations to behavior and effects of atropine, diethyl ether, urethane, and pentobarbital. Exp. Neurol. 49, 58–85 (1975).

    CAS  PubMed  Google Scholar 

  163. Boyce, R., Glasgow, S. D., Williams, S. & Adamantidis, A. Causal evidence for the role of REM sleep theta rhythm in contextual memory consolidation. Science 352, 812–816 (2016). First causal demonstration of the role of septal inhibitory cells in driving REM sleep theta rhythm and their role in REM sleep-dependent contextual memory consolidation.

    CAS  PubMed  Google Scholar 

  164. Siegel, J. M. The REM sleep–memory consolidation hypothesis. Science 294, 1058–1063 (2001).

    CAS  PubMed  Google Scholar 

  165. Ognjanovski, N. et al. Parvalbumin-expressing interneurons coordinate hippocampal network dynamics required for memory consolidation. Nat. Commun. 8, 15039 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  166. Vertes, R. P. & Eastman, K. E. The case against memory consolidation in REM sleep. Behav. Brain Sci. 23, 867–876 (2000).

    CAS  PubMed  Google Scholar 

  167. Boyce, R., Williams, S. & Adamantidis, A. REM sleep and memory. Curr. Opin. Neurobiol. 44, 167–177 (2017).

    CAS  PubMed  Google Scholar 

  168. Buzsaki, G. Theta oscillations in the hippocampus. Neuron 33, 325–340 (2002).

    CAS  PubMed  Google Scholar 

  169. Clemens, Z. et al. Phase coupling between rhythmic slow activity and gamma characterizes mesiotemporal rapid-eye-movement sleep in humans. Neuroscience 163, 388–396 (2009).

    CAS  PubMed  Google Scholar 

  170. Sirota, A. et al. Entrainment of neocortical neurons and gamma oscillations by the hippocampal theta rhythm. Neuron 60, 683–697 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  171. Lubenov, E. V. & Siapas, A. G. Hippocampal theta oscillations are travelling waves. Nature 459, 534–539 (2009).

    CAS  PubMed  Google Scholar 

  172. Courtin, J. et al. Prefrontal parvalbumin interneurons shape neuronal activity to drive fear expression. Nature 505, 92–96 (2014).

    PubMed  Google Scholar 

  173. Popa, D., Duvarci, S., Popescu, A. T., Léna, C. & Paré, D. Coherent amygdalocortical theta promotes fear memory consolidation during paradoxical sleep. Proc. Natl Acad. Sci. USA 107, 6516–6519 (2010). Important study of the role of inter-area coherence of network oscillations in memory consolidation during REM sleep.

    CAS  PubMed  Google Scholar 

  174. Andrillon, T., Nir, Y., Cirelli, C., Tononi, G. & Fried, I. Single-neuron activity and eye movements during human REM sleep and awake vision. Nat. Commun. 6, 7884 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  175. Goutagny, R., Jackson, J. & Williams, S. Self-generated theta oscillations in the hippocampus. Nat. Neurosci. 12, 1491–1493 (2009).

    CAS  PubMed  Google Scholar 

  176. Amilhon, B. et al. Parvalbumin interneurons of hippocampus tune population activity at theta frequency. Neuron 86, 1277–1289 (2015).

    CAS  PubMed  Google Scholar 

  177. Varga, V. et al. The presence of pacemaker HCN channels identifies theta rhythmic GABAergic neurons in the medial septum. J. Physiol. 586, 3893–3915 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  178. Toth, K., Freund, T. F. & Miles, R. Disinhibition of rat hippocampal pyramidal cells by GABAergic afferents from the septum. J. Physiol. 500, 463–474 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  179. Unal, G., Joshi, A., Viney, T. J., Kis, V. & Somogyi, P. Synaptic targets of medial septal projections in the hippocampus and extrahippocampal cortices of the mouse. J. Neurosci. 35, 15812–15826 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  180. Vandecasteele, M. et al. Optogenetic activation of septal cholinergic neurons suppresses sharp wave ripples and enhances theta oscillations in the hippocampus. Proc. Natl Acad. Sci. USA 111, 13535–13540 (2014).

    CAS  PubMed  Google Scholar 

  181. Robinson, J. et al. Optogenetic activation of septal glutamatergic neurons drive hippocampal theta rhythms. J. Neurosci. 36, 3016–3023 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  182. Montgomery, S. M., Sirota, A. & Buzsaki, G. Theta and gamma coordination of hippocampal networks during waking and rapid eye movement sleep. J. Neurosci. 28, 6731–6741 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  183. Karashima, A., Katayama, N. & Nakao, M. Enhancement of synchronization between hippocampal and amygdala theta waves associated with pontine wave density. J. Neurophysiol. 103, 2318–2325 (2010).

    PubMed  Google Scholar 

  184. Datta, S. Cellular basis of pontine ponto-geniculo-occipital wave generation and modulation. Cell. Mol. Neurobiol. 17, 341–365 (1997).

    CAS  PubMed  Google Scholar 

  185. Datta, S. Avoidance task training potentiates phasic pontine-wave density in the rat: a mechanism for sleep-dependent plasticity. J. Neurosci. 20, 8607–8613 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  186. Mikiten, T., Niebyl, P. H. & Hendley, C. D. EEG desynchronization during behavioral sleep associated with spike discharges from the thalamus of the cat. Fed. Proc. 20, 327 (1961).

    Google Scholar 

  187. Peigneux, P., Laureys, S., Delbeuck, X. & Maquet, P. Sleeping brain, learning brain. The role of sleep for memory systems. Neuroreport 12, A111–A124 (2001).

    CAS  PubMed  Google Scholar 

  188. Datta, S., Siwek, D. F., Patterson, E. H. & Cipolloni, P. B. Localization of pontine PGO wave generation sites and their anatomical projections in the rat. Synapse 30, 409–423 (1998).

    CAS  PubMed  Google Scholar 

  189. Vanni-Mercier, G. & Debilly, G. A key role for the caudoventral pontine tegmentum in the simultaneous generation of eye saccades in bursts and associated ponto-geniculo-occipital waves during paradoxical sleep in the cat. Neuroscience 86, 571–585 (1998).

    CAS  PubMed  Google Scholar 

  190. Datta, S., Patterson, E. H. & Siwek, D. F. Brainstem afferents of the cholinoceptive pontine wave generation sites in the rat. Sleep Res. Online 2, 79–82 (1999).

    CAS  PubMed  Google Scholar 

  191. Datta, S., Mavanji, V., Patterson, E. H. & Ulloor, J. Regulation of rapid eye movement sleep in the freely moving rat: local microinjection of serotonin, norepinephrine, and adenosine into the brainstem. Sleep 26, 513–520 (2003).

    PubMed  Google Scholar 

  192. Amzica, F. & Steriade, M. Progressive cortical synchronization of ponto-geniculo-occipital potentials during rapid eye movement sleep. Neuroscience 72, 309–314 (1996).

    CAS  PubMed  Google Scholar 

  193. Wehrle, R. et al. Functional microstates within human REM sleep: first evidence from fMRI of a thalamocortical network specific for phasic REM periods. Eur. J. Neurosci. 25, 863–871 (2007).

    PubMed  Google Scholar 

  194. Gott, J. A., Liley, D. T. & Hobson, J. A. Towards a functional understanding of PGO waves. Front. Hum. Neurosci. 11, 89 (2017).

    PubMed  PubMed Central  Google Scholar 

  195. Sanchez-Lopez, A. & Escudero, M. Tonic and phasic components of eye movements during REM sleep in the rat. Eur. J. Neurosci. 33, 2129–2138 (2011).

    PubMed  Google Scholar 

  196. Jasper, H. H. & Andrews, H. L. Brain potentials and voluntary muscle activity in man. J. Neurophysiol. 1, 87–100 (1938).

    Google Scholar 

  197. Buzsaki, G. & Wang, X. J. Mechanisms of gamma oscillations. Annu. Rev. Neurosci. 35, 203–225 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  198. Yizhar, O. et al. Neocortical excitation/inhibition balance in information processing and social dysfunction. Nature 477, 171–178 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  199. Bazhenov, M., Rulkov, N. F. & Timofeev, I. Effect of synaptic connectivity on long-range synchronization of fast cortical oscillations. J. Neurophysiol. 100, 1562–1575 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  200. Cardin, J. A. et al. Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature 459, 663–667 (2009). Important causal demonstration of the role of gamma rhythms in sensory integration.

    CAS  PubMed  PubMed Central  Google Scholar 

  201. Kim, T. et al. Cortically projecting basal forebrain parvalbumin neurons regulate cortical gamma band oscillations. Proc. Natl Acad. Sci. USA 112, 3535–3540 (2015).

    CAS  PubMed  Google Scholar 

  202. Sohal, V. S., Zhang, F., Yizhar, O. & Deisseroth, K. Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature 459, 698–702 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  203. Buzsaki, G. & Schomburg, E. W. What does gamma coherence tell us about inter-regional neural communication? Nat. Neurosci. 18, 484–489 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  204. Maloney, K. J., Cape, E. G., Gotman, J. & Jones, B. E. High-frequency gamma electroencephalogram activity in association with sleep-wake states and spontaneous behaviors in the rat. Neuroscience 76, 541–555 (1997).

    CAS  PubMed  Google Scholar 

  205. Scheffzük, C. et al. Selective coupling between theta phase and neocortical fast gamma oscillations during REM-sleep in mice. PLOS ONE 6, e28489 (2011).

    PubMed  PubMed Central  Google Scholar 

  206. Emrick, J. J., Gross, B. A., Riley, B. T. & Poe, G. R. Different simultaneous sleep states in the hippocampus and neocortex. Sleep 39, 2201–2209 (2016).

    PubMed  PubMed Central  Google Scholar 

  207. Durán, E., Oyanedel, C. N., Niethard, N., Inostroza, M. & Born, J. Sleep stage dynamics in neocortex and hippocampus. Sleep 41, zsy060 (2018).

    Google Scholar 

  208. Vyazovskiy, V. V., Achermann, P., Borbely, A. A. & Tobler, I. The dynamics of spindles and EEG slow-wave activity in NREM sleep in mice. Arch. Ital. Biol. 142, 511–523 (2004).

    CAS  PubMed  Google Scholar 

  209. Broughton, R. & Hasan, J. Quantitative topographic electroencephalographic mapping during drowsiness and sleep onset. J. Clin. Neurophysiol. 12, 372–386 (1995).

    CAS  PubMed  Google Scholar 

  210. Renouard, L. et al. The supramammillary nucleus and the claustrum activate the cortex during REM sleep. Sci. Adv. 1, e1400177 (2015).

    PubMed  PubMed Central  Google Scholar 

  211. Funk, C. M., Honjoh, S., Rodriguez, A. V., Cirelli, C. & Tononi, G. Local slow waves in superficial layers of primary cortical areas during REM sleep. Curr. Biol. 26, 396–403 (2016). Demonstration of highly localized oscillations in the neocortex.

    CAS  PubMed  PubMed Central  Google Scholar 

  212. 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 98, 1924–1929 (2001).

    CAS  PubMed  Google Scholar 

  213. Niethard, N. et al. Sleep-stage-specific regulation of cortical excitation and inhibition. Curr. Biol. 26, 2739–2749 (2016).

    CAS  PubMed  Google Scholar 

  214. Grosmark, A. D., Mizuseki, K., Pastalkova, E., Diba, K. & Buzsáki, G. REM sleep reorganizes hippocampal excitability. Neuron 75, 1001–1007 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  215. Cisse, Y. et al. Discharge and role of acetylcholine pontomesencephalic neurons in cortical activity and sleep-wake states examined by optogenetics and juxtacellular recording in mice. eNeuro 5, ENEURO.0270-18.2018 (2018).

  216. Boucetta, S. & Jones, B. E. Activity profiles of cholinergic and intermingled GABAergic and putative glutamatergic neurons in the pontomesencephalic tegmentum of urethane-anesthetized rats. J. Neurosci. 29, 4664–4674 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  217. Billwiller, F., Renouard, L., Clement, O., Fort, P. & Luppi, P. H. Differential origin of the activation of dorsal and ventral dentate gyrus granule cells during paradoxical (REM) sleep in the rat. Brain Struct. Funct. 222, 1495–1507 (2017).

    PubMed  Google Scholar 

  218. Pedersen, N. P. et al. Supramammillary glutamate neurons are a key node of the arousal system. Nat. Commun. 8, 1405 (2017).

    PubMed  PubMed Central  Google Scholar 

  219. Ferrara, M. et al. The electroencephalographic substratum of the awakening. Behav. Brain Res. 167, 237–244 (2006).

    PubMed  Google Scholar 

  220. Lee, M. G., Hassani, O. K., Alonso, A. & Jones, B. E. Cholinergic basal forebrain neurons burst with theta during waking and paradoxical sleep. J. Neurosci. 25, 4365–4369 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  221. Anaclet, C. et al. Basal forebrain control of wakefulness and cortical rhythms. Nat. Commun. 6, 8744 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  222. Shi, Y. F., Han, Y., Su, Y. T., Yang, J. H. & Yu, Y. Q. Silencing of cholinergic basal forebrain neurons using archaerhodopsin prolongs slow-wave sleep in mice. PLOS ONE 10, e0130130 (2015).

    PubMed  PubMed Central  Google Scholar 

  223. McCormick, D. A. Neurotransmitter actions in the thalamus and cerebral cortex and their role in neuromodulation of thalamocortical activity. Prog. Neurobiol. 39, 337–388 (1992).

    CAS  PubMed  Google Scholar 

  224. Chen, N., Sugihara, H. & Sur, M. An acetylcholine-activated microcircuit drives temporal dynamics of cortical activity. Nat. Neurosci. 18, 892–902 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  225. Verret, L. et al. A role of melanin-concentrating hormone producing neurons in the central regulation of paradoxical sleep. BMC Neurosci. 4, 19 (2003).

    PubMed  PubMed Central  Google Scholar 

  226. Konadhode, R. R. et al. Optogenetic stimulation of MCH neurons increases sleep. J. Neurosci. 33, 10257–10263 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  227. Trotti, L. M. Waking up is the hardest thing I do all day: sleep inertia and sleep drunkenness. Sleep Med. Rev. 35, 76–84 (2017).

    PubMed  Google Scholar 

  228. Vallat, R., Meunier, D., Nicolas, A. & Ruby, P. Hard to wake up? The cerebral correlates of sleep inertia assessed using combined behavioral, EEG and fMRI measures. Neuroimage 184, 266–278 (2018).

    PubMed  Google Scholar 

  229. Marzano, C., Ferrara, M., Moroni, F. & De Gennaro, L. Electroencephalographic sleep inertia of the awakening brain. Neuroscience 176, 308–317 (2011).

    CAS  PubMed  Google Scholar 

  230. Gorgoni, M. et al. EEG topography during sleep inertia upon awakening after a period of increased homeostatic sleep pressure. Sleep Med. 16, 883–890 (2015).

    PubMed  Google Scholar 

  231. Tassi, P. & Muzet, A. Sleep inertia. Sleep Med. Rev. 4, 341–353 (2000).

    PubMed  Google Scholar 

  232. Gervasoni, D. et al. Electrophysiological evidence that noradrenergic neurons of the rat locus coeruleus are tonically inhibited by GABA during sleep. Eur. J. Neurosci. 10, 964–970 (1998).

    CAS  PubMed  Google Scholar 

  233. Poulet, J. F. A. & Crochet, S. The cortical states of wakefulness. Front. Syst. Neurosci. 12, 64 (2019).

    PubMed  PubMed Central  Google Scholar 

  234. Herrera, C. G. et al. Hypothalamic feedforward inhibition of thalamocortical network controls arousal and consciousness. Nat. Neurosci. 19, 290–298 (2016). The first demonstration of hypothalamic influence over thalamocortical networks in sleep–wake control.

    CAS  PubMed  Google Scholar 

  235. Economo, C. V. Sleep as a problem of localization. J. Nerv. Ment. Dis. 71, 249–259 (1930).

    Google Scholar 

  236. Lineberry, C. G. & Siegel, J. EEG synchronization, behavioral inhibition, and mesencephalic unit effects produced by stimulation of orbital cortex, basal forebrain and caudate nucleus. Brain Res. 34, 143–161 (1971).

    CAS  PubMed  Google Scholar 

  237. Massimini, M. et al. Triggering sleep slow waves by transcranial magnetic stimulation. Proc. Natl Acad. Sci. USA 104, 8496–8501 (2007).

    CAS  PubMed  Google Scholar 

  238. Ngo, H. V., Martinetz, T., Born, J. & Mölle, M. Auditory closed-loop stimulation of the sleep slow oscillation enhances memory. Neuron 78, 545–553 (2013).

    CAS  PubMed  Google Scholar 

  239. Fontanini, A. & Bower, J. M. Slow-waves in the olfactory system: an olfactory perspective on cortical rhythms. Trends Neurosci. 29, 429–437 (2006).

    CAS  PubMed  Google Scholar 

  240. Bayer, L. et al. Rocking synchronizes brain waves during a short nap. Curr. Biol. 21, R461–R462 (2011).

    CAS  PubMed  Google Scholar 

  241. Amici, R. et al. Changes in REM sleep occurrence due to rhythmical auditory stimulation in the rat. Brain Res. 868, 241–250 (2000).

    CAS  PubMed  Google Scholar 

  242. Adamantidis, A. R., Zhang, F., Aravanis, A. M., Deisseroth, K. & De Lecea, L. Neural substrates of awakening probed with optogenetic control of hypocretin neurons. Nature 450, 420–424 (2007). First use of in vivo optogenetics in mice to establish a causal link between electrical activity in orexin neurons and arousal from sleep.

    CAS  PubMed  PubMed Central  Google Scholar 

  243. Mölle, M., Eschenko, O., Gais, S., Sara, S. J. & Born, J. The influence of learning on sleep slow oscillations and associated spindles and ripples in humans and rats. Eur. J. Neurosci. 29, 1071–1081 (2009).

    PubMed  Google Scholar 

  244. Clemens, Z. et al. Temporal coupling of parahippocampal ripples, sleep spindles and slow oscillations in humans. Brain 130, 2868–2878 (2007).

    PubMed  Google Scholar 

  245. Sirota, A., Csicsvari, J., Buhl, D. & Buzsaki, G. Communication between neocortex and hippocampus during sleep in rodents. Proc. Natl Acad. Sci. USA 100, 2065–2069 (2003).

    CAS  PubMed  Google Scholar 

  246. Cox, R., van Driel, J., de Boer, M. & Talamini, L. M. Slow oscillations during sleep coordinate interregional communication in cortical networks. J. Neurosci. 34, 16890–16901 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  247. Rothschild, G., Eban, E. & Frank, L. M. A cortical–hippocampal–cortical loop of information processing during memory consolidation. Nat. Neurosci. 20, 251–259 (2017).

    CAS  PubMed  Google Scholar 

  248. Latchoumane, C. V., Ngo, H. V., Born, J. & Shin, H. S. Thalamic spindles promote memory formation during sleep through triple phase-locking of cortical, thalamic, and hippocampal rhythms. Neuron 95, 424.e6–435.e6 (2017).

    Google Scholar 

  249. Helfrich, R. F., Mander, B. A., Jagust, W. J., Knight, R. T. & Walker, M. P. Old brains come uncoupled in sleep: slow wave-spindle synchrony, brain atrophy, and forgetting. Neuron 97, 221.e4–230.e4 (2018).

    Google Scholar 

  250. Fell, J. & Axmacher, N. The role of phase synchronization in memory processes. Nat. Rev. Neurosci. 12, 105–118 (2011).

    CAS  PubMed  Google Scholar 

  251. Fogel, S. M. & Smith, C. T. 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 (2011).

    PubMed  Google Scholar 

  252. Lustenberger, C. et al. Feedback-controlled transcranial alternating current stimulation reveals a functional role of sleep spindles in motor memory consolidation. Curr. Biol. 26, 2127–2136 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  253. Wimmer, R. D. et al. Thalamic control of sensory selection in divided attention. Nature 526, 705–709 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  254. Totty, M. S., Chesney, L. A., Geist, P. A. & Datta, S. Sleep-dependent oscillatory synchronization: a role in fear memory consolidation. Front. Neural Circuits 11, 49 (2017).

    PubMed  PubMed Central  Google Scholar 

  255. Jensen, O. & Colgin, L. L. Cross-frequency coupling between neuronal oscillations. Trends Cogn. Sci. 11, 267–269 (2007).

    PubMed  Google Scholar 

  256. Tort, A. B., Komorowski, R. W., Manns, J. R., Kopell, N. J. & Eichenbaum, H. Theta-gamma coupling increases during the learning of item-context associations. Proc. Natl Acad. Sci. USA 106, 20942–20947 (2009).

    CAS  PubMed  Google Scholar 

  257. Cohen, M. X., Elger, C. E. & Fell, J. Oscillatory activity and phase-amplitude coupling in the human medial frontal cortex during decision making. J. Cogn. Neurosci. 21, 390–402 (2009).

    PubMed  Google Scholar 

  258. Canolty, R. T. et al. High gamma power is phase-locked to theta oscillations in human neocortex. Science 313, 1626–1628 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  259. Schomburg, E. W. et al. Theta phase segregation of input-specific gamma patterns in entorhinal-hippocampal networks. Neuron 84, 470–485 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  260. Bandarabadi, M. et al. Dynamical modulation of theta-gamma coupling during REM sleep. Preprint at bioRxiv https://doi.org/10.1101/169656 (2017).

    Article  Google Scholar 

  261. Botella-Soler, V., Valderrama, M., Crépon, B., Navarro, V. & Le Van Quyen, M. Large-scale cortical dynamics of sleep slow waves. PLOS ONE 7, e30757 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  262. Jackson, J. et al. Reversal of theta rhythm flow through intact hippocampal circuits. Nat. Neurosci. 17, 1362–1370 (2014).

    CAS  PubMed  Google Scholar 

  263. Tagliazucchi, E. et al. Automatic sleep staging using fMRI functional connectivity data. Neuroimage 63, 63–72 (2012).

    PubMed  Google Scholar 

  264. Gibbs, S. A. et al. Sleep-related epileptic behaviors and non-REM-related parasomnias: insights from stereo-EEG. Sleep Med. Rev. 25, 4–20 (2016).

    PubMed  Google Scholar 

  265. Saper, C. B., Chou, T. C. & Scammell, T. E. The sleep switch: hypothalamic control of sleep and wakefulness. Trends Neurosci. 24, 726–731 (2001).

    CAS  PubMed  Google Scholar 

  266. Lu, J., Sherman, D., Devor, M. & Saper, C. B. A putative flip-flop switch for control of REM sleep. Nature 441, 589–594 (2006).

    CAS  PubMed  Google Scholar 

  267. Pace-Schott, E. F. & Hobson, J. A. The neurobiology of sleep: genetics, cellular physiology and subcortical networks. Nat. Rev. Neurosci. 3, 591–605 (2002).

    CAS  PubMed  Google Scholar 

  268. Luppi, P. H. et al. Paradoxical (REM) sleep genesis: the switch from an aminergic-cholinergic to a GABAergic-glutamatergic hypothesis. J. Physiol. Paris 100, 271–283 (2006).

    CAS  PubMed  Google Scholar 

  269. Llinas, R. R. & Steriade, M. Bursting of thalamic neurons and states of vigilance. J. Neurophysiol. 95, 3297–3308 (2006).

    PubMed  Google Scholar 

  270. Chauvette, S., Crochet, S., Volgushev, M. & Timofeev, I. Properties of slow oscillation during slow-wave sleep and anesthesia in cats. J. Neurosci. 31, 14998–15008 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  271. Ferrarelli, F. et al. Breakdown in cortical effective connectivity during midazolam-induced loss of consciousness. Proc. Natl Acad. Sci. USA 107, 2681–2686 (2010).

    CAS  PubMed  Google Scholar 

  272. Tononi, G., Boly, M., Massimini, M. & Koch, C. Integrated information theory: from consciousness to its physical substrate. Nat. Rev. Neurosci. 17, 450–461 (2016).

    CAS  PubMed  Google Scholar 

  273. Franks, N. P. General anaesthesia: from molecular targets to neuronal pathways of sleep and arousal. Nat. Rev. Neurosci. 9, 370–386 (2008).

    CAS  PubMed  Google Scholar 

  274. Nelson, L. E. et al. The sedative component of anesthesia is mediated by GABAA receptors in an endogenous sleep pathway. Nat. Neurosci. 5, 979–984 (2002).

    CAS  PubMed  Google Scholar 

  275. Lioudyno, M. I. et al. Shaker-related potassium channels in the central medial nucleus of the thalamus are important molecular targets for arousal suppression by volatile general anesthetics. J. Neurosci. 33, 16310–16322 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  276. Mohajerani, M. H., McVea, D. A., Fingas, M. & Murphy, T. H. Mirrored bilateral slow-wave cortical activity within local circuits revealed by fast bihemispheric voltage-sensitive dye imaging in anesthetized and awake mice. J. Neurosci. 30, 3745–3751 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  277. Borbely, A. A. A two process model of sleep regulation. Hum. Neurobiol. 1, 195–204 (1982). Original description of the two-process model that supports sleep homeostasis.

    CAS  PubMed  Google Scholar 

  278. Donlea, J. M., Alam, M. N. & Szymusiak, R. Neuronal substrates of sleep homeostasis; lessons from flies, rats and mice. Curr. Opin. Neurobiol. 44, 228–235 (2017).

    CAS  PubMed  Google Scholar 

  279. Greene, R. W., Bjorness, T. E. & Suzuki, A. The adenosine-mediated, neuronal-glial, homeostatic sleep response. Curr. Opin. Neurobiol. 44, 236–242 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  280. Porkka-Heiskanen, T. Sleep regulatory factors. Arch. Ital. Biol. 152, 57–65 (2014).

    CAS  PubMed  Google Scholar 

  281. Xie, L. et al. Sleep drives metabolite clearance from the adult brain. Science 342, 373–377 (2013).

    CAS  PubMed  Google Scholar 

  282. Fattinger, S., Jenni, O. G., Schmitt, B., Achermann, P. & Huber, R. Overnight changes in the slope of sleep slow waves during infancy. Sleep 37, 245–253 (2014).

    PubMed  PubMed Central  Google Scholar 

  283. Kattler, H., Dijk, D. & Borbély, A. Effect of unilateral somatosensory stimulation prior to sleep on the sleep EEG in humans. J. Sleep Res. 3, 159–164 (1994).

    CAS  PubMed  Google Scholar 

  284. Huber, R. et al. Arm immobilization causes cortical plastic changes and locally decreases sleep slow wave activity. Nat. Neurosci. 9, 1169–1176 (2006).

    CAS  PubMed  Google Scholar 

  285. Huber, R. et al. TMS-induced cortical potentiation during wakefulness locally increases slow wave activity during sleep. PLOS ONE 2, e276 (2007).

    PubMed  PubMed Central  Google Scholar 

  286. Rodriguez, A. V. et al. Why does sleep slow-wave activity increase after extended wake? Assessing the effects of increased cortical firing during wake and sleep. J. Neurosci. 36, 12436–12447 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  287. Benington, J. H. & Heller, H. C. REM-sleep timing is controlled homeostatically by accumulation of REM-sleep propensity in non-REM sleep. Am. J. Physiol. 266, R1992–R2000 (1994).

    CAS  PubMed  Google Scholar 

  288. Fort, P., Bassetti, C. L. & Luppi, P. H. Alternating vigilance states: new insights regarding neuronal networks and mechanisms. Eur. J. Neurosci. 29, 1741–1753 (2009).

    CAS  PubMed  Google Scholar 

  289. Luppi, P. H., Clément, O. & Fort, P. Paradoxical (REM) sleep genesis by the brainstem is under hypothalamic control. Curr. Opin. Neurobiol. 23, 786–792 (2013).

    CAS  PubMed  Google Scholar 

  290. Millstein, J. et al. Identification of causal genes, networks, and transcriptional regulators of REM sleep and wake. Sleep 34, 1469–1477 (2011).

    PubMed  PubMed Central  Google Scholar 

  291. Grosmark, A. D. & Buzsáki, G. Diversity in neural firing dynamics supports both rigid and learned hippocampal sequences. Science 351, 1440–1443 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  292. Kim, B. et al. Differential modulation of global and local neural oscillations in REM sleep by homeostatic sleep regulation. Proc. Natl Acad. Sci. USA 114, E1727–E1736 (2017).

    CAS  PubMed  Google Scholar 

  293. Maquet, P. et al. Human cognition during REM sleep and the activity profile within frontal and parietal cortices: a reappraisal of functional neuroimaging data. Prog. Brain Res. 150, 219–227 (2005).

    PubMed  Google Scholar 

  294. Stephenson, R., Caron, A. M. & Famina, S. Behavioral sleep-wake homeostasis and EEG delta power are decoupled by chronic sleep restriction in the rat. Sleep 38, 685–697 (2015).

    PubMed  PubMed Central  Google Scholar 

  295. Fernandez-Ruiz, A. et al. Long-duration hippocampal sharp wave ripples improve memory. Science 364, 1082–1086 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  296. Roumis, D. K. & Frank, L. M. Hippocampal sharp-wave ripples in waking and sleeping states. Curr. Opin. Neurobiol. 35, 6–12 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  297. Girardeau, G., Benchenane, K., Wiener, S. I., Buzsáki, G. & Zugaro, M. B. Selective suppression of hippocampal ripples impairs spatial memory. Nat. Neurosci. 12, 1222–1223 (2009). First perturbational study showing the importance of SWRs in spatial memory consolidation.

    CAS  PubMed  Google Scholar 

  298. Ego-Stengel, V. & Wilson, M. A. Disruption of ripple-associated hippocampal activity during rest impairs spatial learning in the rat. Hippocampus 20, 1–10 (2010).

    PubMed  PubMed Central  Google Scholar 

  299. van de Ven, G. M., Trouche, S., McNamara, C. G., Allen, K. & Dupret, D. Hippocampal offline reactivation consolidates recently formed cell assembly patterns during sharp wave-ripples. Neuron 92, 968–974 (2016). Important study showing that novel information is preferentially consolidated during NREM sleep.

    PubMed  PubMed Central  Google Scholar 

  300. Feld, G. B. & Born, J. Sculpting memory during sleep: concurrent consolidation and forgetting. Curr. Opin. Neurobiol. 44, 20–27 (2017).

    CAS  PubMed  Google Scholar 

  301. Lansink, C. S. et al. Preferential reactivation of motivationally relevant information in the ventral striatum. J. Neurosci. 28, 6372–6382 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  302. Valdes, J. L., McNaughton, B. L. & Fellous, J. M. Offline reactivation of experience-dependent neuronal firing patterns in the rat ventral tegmental area. J. Neurophysiol. 114, 1183–1195 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  303. Peyrache, A., Khamassi, M., Benchenane, K., Wiener, S. I. & Battaglia, F. P. Replay of rule-learning related neural patterns in the prefrontal cortex during sleep. Nat. Neurosci. 12, 919–926 (2009).

    CAS  PubMed  Google Scholar 

  304. Tononi, G. & Cirelli, C. Sleep and the price of plasticity: from synaptic and cellular homeostasis to memory consolidation and integration. Neuron 81, 12–34 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  305. Bushey, D., Tononi, G. & Cirelli, C. Sleep- and wake-dependent changes in neuronal activity and reactivity demonstrated in fly neurons using in vivo calcium imaging. Proc. Natl Acad. Sci. USA 112, 4785–4790 (2015).

    CAS  PubMed  Google Scholar 

  306. de Vivo, L. et al. Ultrastructural evidence for synaptic scaling across the wake/sleep cycle. Science 355, 507–510 (2017).

    PubMed  PubMed Central  Google Scholar 

  307. Calais, J. B., Ojopi, E. B., Morya, E., Sameshima, K. & Ribeiro, S. Experience-dependent upregulation of multiple plasticity factors in the hippocampus during early REM sleep. Neurobiol. Learn. Mem. 122, 19–27 (2015).

    CAS  PubMed  Google Scholar 

  308. Yang, G. et al. Sleep promotes branch-specific formation of dendritic spines after learning. Science 344, 1173–1178 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  309. Watson, B. O., Levenstein, D., Greene, J. P., Gelinas, J. N. & Buzsáki, G. Network homeostasis and state dynamics of neocortical sleep. Neuron 90, 839–852 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  310. Puentes-Mestril, C. & Aton, S. J. Linking network activity to synaptic plasticity during sleep: hypotheses and recent data. Front. Neural Circuits 11, 61 (2017).

    PubMed  PubMed Central  Google Scholar 

  311. Dumoulin, M. C. et al. Extracellular signal-regulated kinase (ERK) activity during sleep consolidates cortical plasticity in vivo. Cereb. Cortex 25, 507–515 (2015).

    PubMed  Google Scholar 

  312. Hengen, K. B., Torrado Pacheco, A., McGregor, J. N., Van Hooser, S. D. & Turrigiano, G. G. Neuronal firing rate homeostasis is inhibited by sleep and promoted by wake. Cell 165, 180–191 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The authors thank all the Tidis laboratory members and M. Schmidt for their helpful comments on a previous version of the manuscript. A.R.A. was supported by the Human Frontier Science Program, Inselspital University Hospital Bern, Swiss National Science Foundation, European Research Council and the University of Bern. T.C.G. was supported by the University of Zürich Forschungskredit. C.G.H. was supported by the Swiss National Science Foundation and the University of Bern.

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The AASM Manual for the Scoring of Sleep and Associated Events: https://aasm.org/clinical-resources/scoring-manual/

Glossary

Electroencephalography

(EEG). The gross electrical activity non-invasively recorded from dipoles at the level of the skull or scalp; this activity is largely considered as a proxy of neocortical activity.

Local field potentials

(LFPs). Oscillations recorded directly from the extracellular space, resulting from the firing of localized groups of neurons.

Slow oscillations

Bimodal oscillations (<1 Hz) of the cell resting membrane potential, typically cortical or thalamic neurons, between hyperpolarized (DOWN) and depolarized (UP) states.

Thalamus

A symmetrical collection of nuclei in the diencephalon, with functions including sensory relaying to neocortex, alertness, consciousness and motoric output, which is heavily implicated in the genesis of sleep oscillations.

Resonance

The natural frequency of an oscillating circuit without any external inputs.

State transitions

Changes from one vigilance state to another (that is, from wakefulness to non-rapid eye movement sleep), which are associated with transient network activity.

Polysomnography

A multiparametric test, including the electroencephalogram, electromyogram, electrooculogram and electrocardiogram, commonly used to measure sleep.

Slow waves

A term often used to define low frequency high amplitude electroencephalography events (0.5–4.0 Hz) predominating during deeper non-rapid eye movement sleep and including both slow and delta oscillations.

Bursts

Neuronal firing pattern consisting of regular periods of intense activity interspersed with periods of relative quiescence (also referred to as phasic activity).

Tonic activity

Neuronal firing pattern in which each action potential occurs at a regular sustained interval with no quiescent period.

Arousal threshold

The level of external stimulation (that is, acoustic or somatosensory) to produce behavioural arousal from sleep.

Circadian rhythm

Oscillations of physiology and behaviour with a 24-hour periodicity, synchronized to the revolution of the Earth.

Synaptic scaling

Refers to a non-Hebbian form of homeostatic plasticity that adjusts synapse strength (synaptic ‘renormalization’) in a network or neuron up or down in response to global changes in activity so that total synaptic inputs are tuned whilst the relative strength of all synapses is constant.

Ocular dominance plasticity

Refers to the plastic rearrangement of cortical visual areas following monocular deprivation, which triggers a shift in the response of individual neurons towards the non-deprived eye. Sleep is required for the expression of plasticity in the developing visual cortex.

Electro-oculography

The electrical activity resulting from eye movement used to help determine sleep stage.

Electromyography

Electrical activity of musculature, which shows distinct patterns dependent on behavioural state and is used to help determine sleep stage.

Inhibitory interneurons

GABAergic or glycinergic cells with localized feedback and modulatory control of excitatory neurons.

Synaptic strength

The degree of influence that the input of one neuron has on the activity of its target neuron.

Unsupervised sleep staging

Algorithm-defined sleep scoring methods, which are supposedly more objective than the subjective visual scoring of EEG or polysomnography recordings.

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Adamantidis, A.R., Gutierrez Herrera, C. & Gent, T.C. Oscillating circuitries in the sleeping brain. Nat Rev Neurosci 20, 746–762 (2019). https://doi.org/10.1038/s41583-019-0223-4

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