The Sleep Slow Oscillation as a Traveling Wave

By Marcello Massimini, Reto Huber, F. Ferrarelli, Sean L. Hill, Giulio Tononi. Journal of Neuroscience, 2004

1,198 citations recorded by the source corpus.

During much of sleep, virtually all cortical neurons undergo a slow oscillation (<1 Hz) in membrane potential, cycling from a hyperpolarized state of silence to a depolarized state of intense firing. This slow oscillation is the fundamental cellular phenomenon that organizes other sleep rhythms such as spindles and slow waves. Using high-density electroencephalogram recordings in humans, we show here that each cycle of the slow oscillation is a traveling wave. Each wave originates at a definite site and travels over the scalp at an estimated speed of 1.2-7.0 m/sec. Waves originate more frequently in prefrontal-orbitofrontal regions and propagate in an anteroposterior direction. Their rate of occurrence increases progressively reaching almost once per second as sleep deepens. The pattern of origin and propagation of sleep slow oscillations is reproducible across nights and subjects and provides a blueprint of cortical excitability and connectivity. The orderly propagation of correlated activity along connected pathways may play a role in spike timing-dependent synaptic plasticity during sleep.

Subfields: Cellular and Molecular Neuroscience, Cognitive Neuroscience

View Paper: https://www.semanticscholar.org/paper/c11ff925a3d829436f15a26aafb8594c6386e477

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Citations in the corpus

Precise Long-Range Synchronization of Activity and Silence in Neocortical Neurons during Slow-Wave Sleep (2006, background): “, 2004) and synchronization of weaker activity, originating at multiple locations (Timofeev et al., 2000; Massimini et al., 2004).”
Scaling Brain Size, Keeping Timing: Evolutionary Preservation of Brain Rhythms (2013, neutral): “Within the same hemisphere, slow oscillations typically originate in prefrontal– orbitofrontal regions and propagate in a fronto-occipital direction at a speed of 1.2–7.0 m/sec in humans (Massimini et al., 2004) but only at 0.02-0.1 m/sec in rats (Luczak et al., 2007).”
Rhythms of the brain (2006, background): “Such a rare form of traveling wave is the so-called K-complex of light sleep (Massimini et al., 2004).”
Synaptic Mechanisms of Memory Consolidation during Sleep Slow Oscillations (2016, background): “During slow oscillations, the transition from a Down to Up state of oscillations occurs in a form of traveling waves (Massimini et al., 2004; Volgushev et al., 2006), possibly initiated at many independent network locations.”
Electrophysiological correlates of the brain's intrinsic large-scale functional architecture (2008, background): “(19) is responsible both for the fading of consciousness and for the collapse of gamma power correlations.”
About sleep's role in memory. (2013, background): “High-density EEG recordings in humans as well as depth recordings in epileptic patients and cats indicate that the slow oscillation behaves like a travelling wave, which originates most frequently in the frontal regions and propagates towards posterior regions, although other origins and directions ”
Cortical travelling waves: mechanisms and computational principles (2018, background): “This pattern would sleep has been reported to be a travelling wave that moves globally from anterior to posterior regions 44 .”
The memory function of sleep (2010, background): “that also contribute to the generation of slow oscillation”
Imaging human EEG dynamics using independent component analysis. (2006, background): “, 1996), as do some EEG phenomena such as epileptic seizures, very slow spreading depressions associated with migraine headaches (Lauritzen, 1994), and sleep spindles (Massimini et al., 2004).”
Cortical firing and sleep homeostasis. (2009, background): “During non-rapid eye movement (NREM) sleep the electroencephalogram (EEG) shows characteristic slow waves that can be recorded over the entire cortical surface (Massimini et al., 2004).”
Auditory closed-loop stimulation of the sleep slow oscillation enhances memory. (2013, methodology): “Topographical maps of SO origins and their delays were generated with regard to the SO negative half-wave peaks (subdivided into SOs emerging in frontal, central, and parietal areas) by third-order spherical spline interpolation (Massimini et al., 2004).”
Regional slow waves and spindles in human sleep. (2011, neutral): “Slow waves propagate along major anatomical pathways (Massimini et al., 2004; Murphy et al., 2009) so that individual waves may be driven by distinct cortical origins (Riedner et al., 2007).”
Neural basis of global resting-state fMRI activity (2010, background): “Alternatively, spontaneous fluctuations could have their genesis in the cortex itself, perhaps taking the form of spatiotemporal waves upon the cortical sheet in a manner analogous to cortical slow waves (55).”
Spontaneous events outline the realm of possible sensory responses in neocortical populations (2009, background): “Cortical circuits both in vitro and in vivo during resting and sleep spontaneously produce periods of activity known as ‘‘upstates’’ (Battaglia et al., 2004; Luczak et al., 2007; Massimini et al., 2004; Petersen et al., 2003; Sirota et al., 2003; Steriade et al., 1993a).”