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Temporal dynamics of cortical sources underlying spontaneous and peripherally evoked slow waves

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Riedner, Brady A., Hulse, Bradley K., Murphy, Michael J., Ferrarelli, Fabio, Tononi, Giulio·2011·Progress in Brain Research
DOI 10.1016/b978-0-444-53839-0.00013-2PMC PMC3160723
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Abstract

Slow waves are the most prominent electroencephalographic feature of non-rapid eye movement (NREM) sleep. During NREM sleep, cortical neurons oscillate approximately once every second between a depolarized upstate, when cortical neurons are actively firing, and a hyperpolarized downstate, when cortical neurons are virtually silent (Destexhe et al., 1999; Steriade et al., 1993a, 2001). Intracellular recordings indicate that the origins of the slow oscillation are cortical and that corticocortical connections are necessary for their synchronization (Amzica and Steriade, 1995; Steriade et al., 1993b; Timofeev and Steriade, 1996; Timofeev et al., 2000). The currents produced by the near-synchronous slow oscillation of large populations of neurons appear on the scalp as electroencephalogram (EEG) slow waves (Amzica and Steriade, 1997). Despite this cellular understanding, questions remain about the role of specific cortical structures in individual slow waves. Early EEG studies of slow waves in humans were limited by the small number of derivations employed and by the difficulty of relating scalp potentials to underlying brain activity (Brazier, 1949; Roth et al., 1956). Functional neuroimaging methods offer exceptional spatial resolution, but lack the temporal resolution to track individual slow waves (Dang-Vu et al., 2008; Maquet, 2000). Intracranial recordings in patient populations are limited by the availability of medically necessary electrode placements and can be confounded by pathology and medications (Cash et al., 2009; Nir et al., 2011; Wenneberg 2010). Source modeling of high-density EEG recordings offers a unique opportunity for neuroimaging sleep slow waves. So far, the results have challenged several of the influential topographic observations about slow waves that had persisted since the original EEG recordings of sleep. These recent analyses revealed that individual slow waves are idiosyncratic cortical events and that the negative peak of the EEG slow wave often involves cortical structures not necessarily apparent from the scalp, like the inferior frontal gyrus, anterior cingulate, posterior cingulate, and precuneus (Murphy et al., 2009). In addition, not only do slow waves travel (Massimini et al., 2004), but they often do so preferentially through the areas comprising the major connectional backbone of the human cortex (Hagmann et al., 2008). In this chapter, we will review the cellular, intracranial recording, and neuroimaging results concerning EEG slow waves. We will also confront a long held belief about peripherally evoked slow waves, also known as K-complexes, namely that they are modality independent and do not involve cortical sensory pathways. The analysis included here is the first to directly compare K-complexes evoked with three different stimulation modalities within the same subject on the same night using high-density EEG.

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  • EEG-based source modeling located the main origins of the travelling waves in the cingulate gyrus and the left insula.

    “EEG-based source modeling located the main origins of the travelling waves in the cingulate gyrus and the left insula (841, 993).”

    From About Sleep's Role in Memory (2013) · cites this paper as [993]

  • Slow oscillations originating from thalamo-cortical neurons vanish when the thalamus is isolated from cortical inputs, indicating the slow oscillation is a primary cortical phenomenon.

    “Slow oscillations originating from thalamo-cortical neurons (586) vanish when the thalamus is isolated from cortical inputs (1200), indicating the slow oscillation is a primary cortical phenomenon (993).”

    From About Sleep's Role in Memory (2013) · cites this paper as [993]

  • In the scalp EEG, the negative peak of the slow oscillation coincides with the beginning of the down-to-up state transition, whereas the depolarizing phase of sustained firing correlates with the positive EEG deflection.

    “In the scalp EEG, the negative peak of the slow oscillation coincides with the beginning of the down-to-up state transition (281, 993, 1261), whereas the depolarizing phase of sustained firing corre-lates with the positive EEG deflection (33,998,1268).”

    From About Sleep's Role in Memory (2013) · cites this paper as [993]

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  1. Maquet P this volume Progress in Brain Research Elsevier Amsterdam p. xxx

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Authors
Riedner, B. A., Hulse, B. K., Murphy, M. J., Ferrarelli, F., & Tononi, G.
Affiliations
University of Wisconsin–Madison (US)
Corresponding author
Riedner, Brady A.
ORCID
Venue
Progress in Brain Research
Publisher
Elsevier
Published
2011
Volume
193
Pages
201-218
ISSN
0079-6123 (ISSN-L)
DOI
10.1016/b978-0-444-53839-0.00013-2
PMC
PMC3160723
OpenAlex
W1607424647
Cited by
130
References
74
Citations by year
2026: 2 · 2025: 7 · 2024: 6 · 2023: 8 · 2022: 17 · 2021: 8 · 2020: 13 · 2019: 8 · 2018: 13 · 2017: 7 · 2016: 5 · 2015: 8 · 2014: 10 · 2013: 9 · 2012: 8
FWCI
19.07
Type
book chapter
Language
en
Open access
Licence
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations
  • Progress in brain research (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • National Institutes of Health (5p20mh077967-04)
  • National Institute of Mental Health (P20MH-077967)
  • National Institute of General Medical Sciences (GM007507, T32GM007507)
  • National Institute of Diabetes and Digestive and Kidney Diseases (T90DK070079, T9DK070079)
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
slow waves, NREM sleep, cortical sources, source modeling, high-density EEG, slow wave propagation, corticocortical connections, slow oscillations, sleep spindles, REM sleep, temporal dynamics, inferior frontal gyrus, anterior cingulate cortex, posterior cingulate cortex, precuneus
MeSH terms
Cerebral Cortex, Electroencephalography, Humans, Magnetic Resonance Imaging, Models, Neurological, Neurons, Periodicity, Sleep, Positron-Emission Tomography, Functional Neuroimaging

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