A novel slow (< 1 Hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components

By Mircea Steriade, A. Nuñez, F. Amzica. 1993

We describe a novel slow oscillation in intracellular recordings from cortical association areas 5 and 7, motor areas 4 and 6, and visual areas 17 and 18 of cats under various anesthetics. The recorded neurons (n = 254) were antidromically and orthodromically identified as corticothalamic or callosal elements receiving projections from appropriate thalamic nuclei as well as from homotopic foci in the contralateral cortex. Two major types of cells were recorded: regular- spiking (mainly slow-adapting, but also fast-adapting) neurons and intrinsically bursting cells. A group of slowly oscillating neurons (n = 21) were intracellularly stained and found to be pyramidal-shaped cells in layers III-VI, with luxuriant basal dendritic arbors. The slow rhythm appeared in 88% of recorded neurons. It consisted of slow depolarizing envelopes (lasting for 0.8–1.5 sec) with superimposed full action potentials or presumed dendritic spikes, followed by long- lasting hyperpolarizations. Such sequences recurred rhythmically at less than 1 Hz, with a prevailing oscillation between 0.3 and 0.4 Hz in 67% of urethane-anesthetized animals. While in most neurons (approximately 70%) the repetitive spikes superimposed on the slow depolarization were completely blocked by slight DC hyperpolarization, 30% of cells were found to display relatively small (3–12 mV), rapid, all-or-none potentials after obliteration of full action potentials. These fast spikes were suppressed in an all-or-none fashion at Vm more negative than -90 mV. The depolarizing envelope of the slow rhythm was reduced or suppressed at a Vm of -90 to -100 mV and its duration was greatly reduced by administration of the NMDA blocker ketamine. In keeping with this action, most (56%) neurons recorded in animals under ketamine and nitrous oxide or ketamine and xylazine anesthesia displayed the slow oscillation at higher frequencies (0.6–1 Hz) than under urethane anesthesia (0.3–0.4 Hz). In 18% of the oscillating cells, the slow rhythm mainly consisted of repetitive (15–30 Hz), relatively short-lasting (15–25 msec) IPSPs that could be revealed by bringing the Vm at more positive values than -70 mV. The long-lasting (approximately 1 sec) hyperpolarizing phase of the slow oscillation was best observed at the resting Vm and was reduced at about -100 mV. Simultaneous recording of another cell across the membrane demonstrated synchronous inhibitory periods in both neurons. Intracellular diffusion of Cl- or Cs+ reduced the amplitude and/or duration of cyclic long- lasting hyperpolaryzations.(ABSTRACT TRUNCATED AT 400 WORDS)

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Citations in the corpus

Replay in Deep Learning: Current Approaches and Missing Biological Elements (2021, neutral): “…ripples (100–200 Hz) in the hippocampus (Buzsáki, Horvath, Urioste, Hetke, & Wise, 1992), spindles (7–14 Hz) (Morison & Dempsey, 1941) and slow ( < 1 Hz) oscillations (Steriade, Timofeev, & Grenier, 2001; Steriade, Nunez, & Amzica, 1993) in the thalamocortical network (Bazhenov & Timofeev, 2006).”
Resting‐state networks show dynamic functional connectivity in awake humans and anesthetized macaques (2013, methodology): “Studies typically cite their role in coordinating other sleep rhythms [Achermann and Borbély, 1997; Contreras et al., 1996; Steriade et al., 1993c] and memory consolidation [Lee and Wilson, 2002; Mölle et al., 2004].”
Psychedelics (2016, background): “The neocortex is constantly active in vivo, as cortical and subcortical networks generate rhythmic patterns of activity at a variety of frequencies (Steriade et al., 1993).”
Sleep oscillations in the thalamocortical system induce long-term neuronal plasticity (2012, unknown): “The cortical slow oscillation has a frequency of about 1 Hz (Steriade et al., 1993).”
An oscillatory hierarchy controlling neuronal excitability and stimulus processing in the auditory cortex. (2005, background): “Intracellular recordings in carnivores provided a striking demonstration of neuronal membrane potentials undergoing slow rhythmic shifts between depolarized and hyperpolarized states during slow wave sleep (Sanchez-Vives and McCormick 2000; Steriade et al. 1993).”
Thalamocortical oscillations (2006, background): “The following observations point to an intracortical origin for this rhythm: It survives extensive thalamic lesions in vivo (Steriade et al., 1993b) and exists in cortical in vitro preparations (Sanchez-Vives and McCormick, 2000).”
Sleeping on the motor engram: The multifaceted nature of sleep‐related motor memory consolidation (2017, unknown): “Each slow oscillation consists of a hyperpolarized “down-state” that is characterized by neuronal silence, and a depolarized “up-state” associated with high rates of cortical activity [for reviews, see (Riedner et al., 2011; Steriade et al., 1993)].”
Neurophysiological and Computational Principles of Cortical Rhythms in Cognition (2010, background): “A qualitatively similar scenario underlies the generation of slow ( 1 Hz) oscillations observed in quiet sleep (190, 195, 553, 610, 679, 776, 779, 839, 905, 912, 915, 916).”
Functional neuroimaging of normal human sleep by positron emission tomography (2000, background): “In the thalamus, active inhibition by GABA, as well as intrinsic membrane properties of thalamic neurones, plays an important role in the maintenance and modulation of sleep rhythms (Steriade et al. 1993a).”