Thalamic Reticular Control of Local Sleep in Mouse Sensory Cortex

Overview

Journal Elife

Specialty Biology

Date 2018 Dec 26

PMID 30583750

Citations 42

Authors

Laura Mj Fernandez

Gil Vantomme

Alejandro Osorio-Forero

Romain Cardis

Elidie Beard

Anita Luthi

Affiliations

Soon will be listed here.

Abstract

Sleep affects brain activity globally, but many cortical sleep waves are spatially confined. Local rhythms serve cortical area-specific sleep needs and functions; however, mechanisms controlling locality are unclear. We identify the thalamic reticular nucleus (TRN) as a source for local, sensory-cortex-specific non-rapid-eye-movement sleep (NREMS) in mouse. Neurons in optogenetically identified sensory TRN sectors showed stronger repetitive burst discharge compared to non-sensory TRN cells due to higher activity of the low-threshold Ca channel Ca3.3. Major NREMS rhythms in sensory but not non-sensory cortical areas were regulated in a Ca3.3-dependent manner. In particular, NREMS in somatosensory cortex was enriched in fast spindles, but switched to delta wave-dominated sleep when Ca3.3 channels were genetically eliminated or somatosensory TRN cells chemogenetically hyperpolarized. Our data indicate a previously unrecognized heterogeneity in a powerful forebrain oscillator that contributes to sensory-cortex-specific and dually regulated NREMS, enabling local sleep regulation according to use- and experience-dependence.

Citing Articles

Mechanistic insights into the interaction between epilepsy and sleep.

Sheybani L, Frauscher B, Bernard C, Walker M Nat Rev Neurol. 2025; .

PMID: 40065066 DOI: 10.1038/s41582-025-01064-z.

Anesthetic spindles serve as EEG markers of the depth variations in anesthesia induced by multifarious general anesthetics in mouse experiments.

You Y, Liu H, Yang Z, Chen Y, Yang F, Yu T Front Pharmacol. 2024; 15:1474923.

PMID: 39734402 PMC: 11671261. DOI: 10.3389/fphar.2024.1474923.

Infraslow noradrenergic locus coeruleus activity fluctuations are gatekeepers of the NREM-REM sleep cycle.

Osorio-Forero A, Foustoukos G, Cardis R, Cherrad N, Devenoges C, Fernandez L Nat Neurosci. 2024; 28(1):84-96.

PMID: 39587312 DOI: 10.1038/s41593-024-01822-0.

Oscillatory-Quality of sleep spindles links brain state with sleep regulation and function.

Blanco-Duque C, Bond S, Krone L, Dufour J, Gillen E, Purple R Sci Adv. 2024; 10(36):eadn6247.

PMID: 39241075 PMC: 11378912. DOI: 10.1126/sciadv.adn6247.

GABAergic neurons of anterior thalamic reticular nucleus regulate states of consciousness in propofol- and isoflurane-mediated general anesthesia.

Yi R, Cheng S, Zhong F, Luo D, You Y, Yu T CNS Neurosci Ther. 2024; 30(6):e14782.

PMID: 38828651 PMC: 11145368. DOI: 10.1111/cns.14782.

References

Kattler , Dijk , Borbely . Effect of unilateral somatosensory stimulation prior to sleep on the sleep EEG in humans. J Sleep Res. 1994; 3(3):159-164. DOI: 10.1111/j.1365-2869.1994.tb00123.x. View

Huber R, Deboer T, Tobler I . Topography of EEG dynamics after sleep deprivation in mice. J Neurophysiol. 2000; 84(4):1888-93. DOI: 10.1152/jn.2000.84.4.1888. View

Vyazovskiy V, Borbely A, Tobler I . Unilateral vibrissae stimulation during waking induces interhemispheric EEG asymmetry during subsequent sleep in the rat. J Sleep Res. 2000; 9(4):367-71. DOI: 10.1046/j.1365-2869.2000.00230.x. View

Crabtree J . Intrathalamic sensory connections mediated by the thalamic reticular nucleus. Cell Mol Life Sci. 2001; 56(7-8):683-700. PMC: 11146980. DOI: 10.1007/s000180050462. View

Varga C, Lavallee P, Deschenes M . Substrate for cross-talk inhibition between thalamic barreloids. J Neurosci. 2002; 22(9):RC218. PMC: 6758391. DOI: 20026338. View

McCormick D, Von Krosigk M . Corticothalamic activation modulates thalamic firing through glutamate "metabotropic" receptors. Proc Natl Acad Sci U S A. 1992; 89(7):2774-8. PMC: 48745. DOI: 10.1073/pnas.89.7.2774. View

Contreras D, Curro Dossi R, Steriade M . Bursting and tonic discharges in two classes of reticular thalamic neurons. J Neurophysiol. 1992; 68(3):973-7. DOI: 10.1152/jn.1992.68.3.973. View

Miyamoto H, Hensch T . Reciprocal interaction of sleep and synaptic plasticity. Mol Interv. 2004; 3(7):404-17. DOI: 10.1124/mi.3.7.404. View

Huber R, Ghilardi M, Massimini M, Tononi G . Local sleep and learning. Nature. 2004; 430(6995):78-81. DOI: 10.1038/nature02663. View

10.

Massimini M, Huber R, Ferrarelli F, Hill S, Tononi G . The sleep slow oscillation as a traveling wave. J Neurosci. 2004; 24(31):6862-70. PMC: 6729597. DOI: 10.1523/JNEUROSCI.1318-04.2004. View

11.

Pinault D . The thalamic reticular nucleus: structure, function and concept. Brain Res Brain Res Rev. 2004; 46(1):1-31. DOI: 10.1016/j.brainresrev.2004.04.008. View

12.

Fuentealba P, Steriade M . The reticular nucleus revisited: intrinsic and network properties of a thalamic pacemaker. Prog Neurobiol. 2005; 75(2):125-41. DOI: 10.1016/j.pneurobio.2005.01.002. View

13.

Nunez A, Curro Dossi R, Contreras D, Steriade M . Intracellular evidence for incompatibility between spindle and delta oscillations in thalamocortical neurons of cat. Neuroscience. 1992; 48(1):75-85. DOI: 10.1016/0306-4522(92)90339-4. View

14.

Rector D, Topchiy I, Carter K, Rojas M . Local functional state differences between rat cortical columns. Brain Res. 2005; 1047(1):45-55. DOI: 10.1016/j.brainres.2005.04.002. View

15.

Terrier G, Gottesmann C . Study of cortical spindles during sleep in the rat. Brain Res Bull. 1978; 3(6):701-6. DOI: 10.1016/0361-9230(78)90021-7. View

16.

Huber R, Ghilardi M, Massimini M, Ferrarelli F, Riedner B, Peterson M . Arm immobilization causes cortical plastic changes and locally decreases sleep slow wave activity. Nat Neurosci. 2006; 9(9):1169-76. DOI: 10.1038/nn1758. View

17.

Lee S, Govindaiah G, Cox C . Heterogeneity of firing properties among rat thalamic reticular nucleus neurons. J Physiol. 2007; 582(Pt 1):195-208. PMC: 2075282. DOI: 10.1113/jphysiol.2007.134254. View

18.

Schabus M, Dang-Vu T, Albouy G, Balteau E, Boly M, Carrier J . Hemodynamic cerebral correlates of sleep spindles during human non-rapid eye movement sleep. Proc Natl Acad Sci U S A. 2007; 104(32):13164-9. PMC: 1941810. DOI: 10.1073/pnas.0703084104. View

19.

Cueni L, Canepari M, Lujan R, Emmenegger Y, Watanabe M, Bond C . T-type Ca2+ channels, SK2 channels and SERCAs gate sleep-related oscillations in thalamic dendrites. Nat Neurosci. 2008; 11(6):683-92. DOI: 10.1038/nn.2124. View

20.

Molle M, Eschenko O, Gais S, Sara S, Born J . The influence of learning on sleep slow oscillations and associated spindles and ripples in humans and rats. Eur J Neurosci. 2009; 29(5):1071-81. DOI: 10.1111/j.1460-9568.2009.06654.x. View