Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
Review
. 2010 Jan;13(1):9-17.
doi: 10.1038/nn.2445. Epub 2009 Dec 6.

The slow (<1 Hz) rhythm of non-REM sleep: a dialogue between three cardinal oscillators

Affiliations
Review

The slow (<1 Hz) rhythm of non-REM sleep: a dialogue between three cardinal oscillators

Vincenzo Crunelli et al. Nat Neurosci. 2010 Jan.

Abstract

The slow (<1 Hz) rhythm, the most important electroencephalogram (EEG) signature of non-rapid eye movement (NREM) sleep, is generally viewed as originating exclusively from neocortical networks. Here we argue that the full manifestation of this fundamental sleep oscillation in a corticothalamic module requires the dynamic interaction of three cardinal oscillators: one predominantly synaptically based cortical oscillator and two intrinsic, conditional thalamic oscillators. The functional implications of this hypothesis are discussed in relation to other EEG features of NREM sleep, with respect to coordinating activities in local and distant neuronal assemblies and in the context of facilitating cellular and network plasticity during slow-wave sleep.

PubMed Disclaimer

Figures

Figure 1
Figure 1. The EEG slow (<1 Hz) rhythm and its cellular counterpart in cortical and thalamic neurons
(a) Schematic diagram of a cortico-thalamo-cortical module with its most relevant cellular components and synaptic connections (thalamic interneurons and neocortical neurons other than those in layer 4 and 5/6 have been omitted for clarity). (+) and (−) indicate excitatory and inhibitory synapses, respectively. (b) The slow (<1 Hz) rhythm in the EEG (top trace), and its cellular counterpart, the slow (<1 Hz) oscillation, recorded in cortical and thalamic neurons of anaesthetized cats. TC: thalamocortical; NRT: nucleus reticular thalami. Traces in b are reproduced with permission from refs. ,,, (from top to bottom).
Figure 2
Figure 2. The slow (<1 Hz) oscillation in cortical and thalamic neurons in vivo and its reproduction in vitro
(a) Comparison of the slow oscillation recorded in cat area 5, rat entorhinal and mouse auditory cortex in vivo during anaesthesia (top traces, from left to right, respectively) with that recorded in vitro in slices of ferret prefrontal, rat entorhinal and mouse auditory cortex (bottom traces from left to right, respectively). In vitro recordings were obtained in the presence of a modified medium containing either a reduced Ca2+ concentration (left and middle) or the cholinergic agonist carbachol (right). (b) Comparison of the slow oscillation recorded in vivo in three TC neurons of anaesthetized cats (top traces) and with that observed in slices of the cat dorsal lateral geniculate nucleus (LGN) in vitro in the presence of an mGluR agonist (bottom traces). Arrows mark inflection points in the membrane potential at the transition from the UP to the DOWN state. (c) Comparison of the slow oscillation recorded in vivo in two nucleus reticularis thalami (NRT) neurons of anaesthetized cats (top traces) with that observed in NRT neurons from cat LGN-perigeniculate nucleus slices in vitro in the presence of an mGluR agonist (bottom traces). Note the presence of sleep spindle activity in the top two traces on the right (surface and depth EEG records). Traces in a are reproduced with permission from refs. ,,, (from top left to bottom right). Traces in b are reproduced with permission from refs. ,,, (from top left to bottom right). Traces in c are reproduced with permission from refs. ,, (from top left to bottom right).
Figure 3
Figure 3. The frequency of the EEG slow rhythm at different depths of sleep and anesthesia matches the voltage-dependence of the slow oscillation frequency in TC neurons
(a) EEG recordings during light and deep natural sleep in freely moving cats are compared to those during light and deep anaesthesia in the same species. The frequency of the slow oscillation increases with the deepening of natural sleep and anaesthesia. Note the presence of sleep spindles occurring in combination with some of the individual K complexes/slow waves that are enlarged on the right. (b) Voltage-dependence of the slow oscillation in TC neurons of sensory, motor and intralaminar thalamic nuclei of the cat in vitro. For each nucleus, three traces recorded from the same TC neuron in the presence of an mGluR agonist are shown at increasingly negative values of steady current injection (from top to bottom). Note how the increase in frequency with increasingly negative steady current is due to the shortening of the UP state duration, whereas the length of the DOWN state remains constant. (LGN: dorsal lateral geniculate nucleus; MGB: medial geniculate body; VL: ventrolateral nucleus; CL: central lateral nucleus). a and b are reproduced with permission from refs. and , respectively. CL traces in b are unpublished observations (Watson J. & Crunelli, V.).
Figure 4
Figure 4. The start of the TC neuron UP state firing precedes that of the cortical UP states
(a) Simultaneous EEG and intracellular recordings from a cortical and a TC neuron from an anaesthetized cat show that the LTCP-mediated burst of action potentials that is present at the start of the TC neuron UP state precedes the firing of the cortical neuron and the depth-negative peak of the EEG wave. The seven events superimposed on each panel are aligned with respect to the peak-negativity of the EEG wave. The dashed red bar marks the earliest LTCP-burst of the illustrated TC neuron records. One LTCP burst is enlarged. (b) Simultaneous cortical local field potential (FP) and multi-unit activity (MUA), together with a thalamic single unit recording obtained in a slice with functionally viable thalamocortical and corticothalamic connections show the TC neuron firing to precede the cortical population firing. The dashed red bars mark the start of the thalamic unit firing. a and b are reproduced with permission from refs. and , respectively.
Figure 5
Figure 5. Synchronized thalamic slow oscillation during natural sleep and in a brain slice
(a) Slow (<1 Hz) oscillation recorded in the local field potential from the dorsal lateral geniculate nucleus of a naturally sleeping cat and (b) in a slice of the same thalamic nucleus in the presence of an mGluR agonist, with the respective power spectra illustrated at the top right. (c and d) Four consecutive slow waves (top traces) recorded under the same experimental conditions as in a and b, respectively, and the corresponding single unit activity (bottom left traces). In both cases, during the large positive wave the neuron is silent, whereas at the end of the wave it generates a characteristic LTCP-mediated high-frequency burst of action potentials with interspike intervals that increase as the burst progresses (enlarged in the bottom right traces). All traces are reproduced with permission from ref. .
Figure 6
Figure 6. Schematic flow diagram of the dialogue between cortical and thalamic oscillators that underlies the slow (<1 Hz) rhythm within a thalamocortical module
The prolonged UP states of the slow oscillation in layer 5/6 cortical neurons lead to long-lasting corticothalamic EPSPs in TC and NRT neurons. These slow EPSPs represent an mGluR-induced reduction in ILeak which is the necessary ‘condition’ that must be met in order for thalamic neurons to exhibit the slow oscillation. The LTCP-mediated high-frequency burst that is invariably present at the start of each UP state of the TC neuron slow oscillation leads to highly effective bursts of thalamocortical EPSPs that initiate a new UP state in NRT and layer 4 neurons. The overall UP and DOWN state dynamics of a cortical region, however, are maintained by synaptically-generated barrages of excitation and inhibition from other cortical neurons as well as being potentially fine tuned by additional intracortical inputs from intrinsically oscillating neurons in layer 2/3 and 5. Across different thalamocortical modules (including both primary and association cortices), additional synchronizing inputs are provided by short- and long-distance intracortical connections and by intralaminar thalamic afferents which are not restricted to layer 4 (not shown).

References

    1. Metherate R, Cox CL, Ashe JH. Cellular bases of neocortical activation: modulation of neural oscillations by the nucleus basalis and endogenous acetylcholine. J. Neurosci. 1992;12:4701–4711. - PMC - PubMed
    1. Steriade M, Nuñez A, Amzica F. A novel slow (< 1 Hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components. J. Neurosci. 1993;13:3253–3265. - PMC - PubMed
    1. Steriade M, Nuñez A, Amzica F. Intracellular analysis between slow (< 1 Hz) neocortical oscillation and other sleep rhythms of the electroencephalogram. J. Neurosci. 1993;13:3266–3283. - PMC - PubMed
    1. Steriade M, Contreras D, Dossi R. Curró, 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. 1993;13:3284–3299. - PMC - PubMed
    1. Achermann P, Borbély A. Low-frequency (<1 Hz) oscillations in the human sleep EEG. Neuroscience. 1997;81:213–222. - PubMed

Publication types