Home LiteratureArticle Details
PMID: 24945776 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Ongoing network state controls the length of sleep spindles via inhibitory activity.

Neuron ·Vol. 82 ·No. 6 ·2014-06-18 ·Pages 1367-79

Barthó P, Slézia A, Mátyás F, Faradzs-Zade L, Ulbert I, Harris KD, Acsády L

Abstract

Sleep spindles are major transient oscillations of the mammalian brain. Spindles are generated in the thalamus; however, what determines their duration is presently unclear. Here, we measured somatic activity of excitatory thalamocortical (TC) cells together with axonal activity of reciprocally coupled inhibitory reticular thalamic cells (nRTs) and quantified cycle-by-cycle alterations in their firing in vivo. We found that spindles with different durations were paralleled by distinct nRT activity, and nRT firing sharply dropped before the termination of all spindles. Both initial nRT and TC activity was correlated with spindle length, but nRT correlation was more robust. Analysis of spindles evoked by optogenetic activation of nRT showed that spindle probability, but not spindle length, was determined by the strength of the light stimulus. Our data indicate that during natural sleep a dynamically fluctuating thalamocortical network controls the duration of sleep spindles via the major inhibitory element of the circuits, the nRT.

MeSH Terms
Animals Cerebral Cortex/physiology Electroencephalography/methods Male Mice, 129 Strain Mice, Transgenic Nerve Net/physiology Neural Inhibition/physiology Rats Rats, Wistar Sleep/physiology Thalamus/physiology Time Factors
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Barthó Péter
Laboratory of Thalamus Research, Institute of Experimental Medicine, Hungarian Academy of Sciences, 1083, Budapest, 43 Szigony utca, Hungary. Electronic address: [email protected].
Slézia Andrea
Laboratory of Thalamus Research, Institute of Experimental Medicine, Hungarian Academy of Sciences, 1083, Budapest, 43 Szigony utca, Hungary.
Mátyás Ferenc
Laboratory of Thalamus Research, Institute of Experimental Medicine, Hungarian Academy of Sciences, 1083, Budapest, 43 Szigony utca, Hungary.
Faradzs-Zade Lejla
Laboratory of Thalamus Research, Institute of Experimental Medicine, Hungarian Academy of Sciences, 1083, Budapest, 43 Szigony utca, Hungary.
Ulbert István
Institute of Cognitive Neuroscience and Psychology, Research Centre for Natural Sciences, Hungarian Academy of Sciences, 1083, Budapest, 1068, 83-85 Szondi utca, Hungary; Péter Pázmány Catholic University, Faculty of Information Technology and Bionics, 1083, Budapest, 50/A Práter utca, Hungary.
Harris Kenneth D
UCL Institute of Neurology, UCL Department of Neuroscience, Physiology, and Pharmacology, 21 University Street, London WC1E 6DE, UK.
Acsády László
Laboratory of Thalamus Research, Institute of Experimental Medicine, Hungarian Academy of Sciences, 1083, Budapest, 43 Szigony utca, Hungary. Electronic address: [email protected].
References (45)
45 references, click to expand
  1. Spindle evolution in normal and mentally retarded children: a review.
    Sleep. 1982;5(1):47-57 PMID: 7071451
  2. The stability of the sigma sleep spindle.
    Electroencephalogr Clin Neurophysiol. 1976 Jun;40(6):666-70 PMID: 57053
  3. Characteristics of spindle activity and their use in evaluation of hypnotics.
    Sleep. 1982;5(1):95-105 PMID: 7071455
  4. Prediction of general mental ability based on neural oscillation measures of sleep.
    J Sleep Res. 2005 Sep;14(3):285-92 PMID: 16120103
  5. Motor sequence learning increases sleep spindles and fast frequencies in post-training sleep.
    Sleep. 2008 Aug;31(8):1149-56 PMID: 18714787
  6. Sleep spindle characteristics in healthy subjects of different age groups.
    Clin Neurophysiol. 2001 Mar;112(3):521-7 PMID: 11222974
  7. Selective T-type calcium channel block in thalamic neurons reveals channel redundancy and physiological impact of I(T)window.
    J Neurosci. 2010 Jan 6;30(1):99-109 PMID: 20053892
  8. Differential spike timing and phase dynamics of reticular thalamic and prefrontal cortical neuronal populations during sleep spindles.
    J Neurosci. 2013 Nov 20;33(47):18469-80 PMID: 24259570
  9. A cortical motor nucleus drives the basal ganglia-recipient thalamus in singing birds.
    Nat Neurosci. 2012 Feb 12;15(4):620-7 PMID: 22327474
  10. Mechanisms of oscillatory activity in guinea-pig nucleus reticularis thalami in vitro: a mammalian pacemaker.
    J Physiol. 1993 Aug;468:669-91 PMID: 8254530
  11. Control of spatiotemporal coherence of a thalamic oscillation by corticothalamic feedback.
    Science. 1996 Nov 1;274(5288):771-4 PMID: 8864114
  12. Selective optical drive of thalamic reticular nucleus generates thalamic bursts and cortical spindles.
    Nat Neurosci. 2011 Jul 24;14(9):1118-20 PMID: 21785436
  13. Cellular actions of urethane on rat visual cortical neurons in vitro.
    J Neurophysiol. 2006 Jun;95(6):3865-74 PMID: 16510775
  14. Massively parallel recording of unit and local field potentials with silicon-based electrodes.
    J Neurophysiol. 2003 Aug;90(2):1314-23 PMID: 12904510
  15. Reduced sleep spindle activity in schizophrenia patients.
    Am J Psychiatry. 2007 Mar;164(3):483-92 PMID: 17329474
  16. Spindle oscillations during cortical spreading depression in naturally sleeping cats.
    Neuroscience. 1997 Apr;77(4):933-6 PMID: 9130774
  17. Thalamic burst patterns in the naturally sleeping cat: a comparison between cortically projecting and reticularis neurones.
    J Physiol. 1986 Oct;379:429-49 PMID: 3560000
  18. Spike-and-wave discharges of absence seizures as a transformation of sleep spindles: the continuing development of a hypothesis.
    Clin Neurophysiol. 2000 Sep;111 Suppl 2:S27-38 PMID: 10996552
  19. Short duration waveforms recorded extracellularly from freely moving rats are representative of axonal activity.
    Front Neural Circuits. 2013 Nov 18;7:181 PMID: 24348338
  20. Periodicity of thalamic synchronized oscillations: the role of Ca2+-mediated upregulation of Ih.
    Neuron. 1998 Mar;20(3):553-63 PMID: 9539128
  21. Corticothalamic feedback controls sleep spindle duration in vivo.
    J Neurosci. 2011 Jun 22;31(25):9124-34 PMID: 21697364
  22. Dissociable learning-dependent changes in REM and non-REM sleep in declarative and procedural memory systems.
    Behav Brain Res. 2007 Jun 4;180(1):48-61 PMID: 17400305
  23. Synaptic and membrane mechanisms underlying synchronized oscillations in the ferret lateral geniculate nucleus in vitro.
    J Physiol. 1995 Mar 15;483 ( Pt 3):641-63 PMID: 7776249
  24. Thalamic synchrony and dynamic regulation of global forebrain oscillations.
    Trends Neurosci. 2007 Jul;30(7):350-6 PMID: 17544519
  25. The role of the thalamus in vigilance and epileptogenic mechanisms.
    Clin Neurophysiol. 2000 Sep;111 Suppl 2:S19-26 PMID: 10996551
  26. Intracerebral recordings of nocturnal hyperkinetic seizures: demonstration of a longer duration of the pre-seizure sleep spindle.
    Clin Neurophysiol. 2007 Apr;118(4):928-39 PMID: 17317299
  27. What stops synchronized thalamocortical oscillations?
    Neuron. 1996 Aug;17(2):297-308 PMID: 8780653
  28. Cellular mechanisms of a synchronized oscillation in the thalamus.
    Science. 1993 Jul 16;261(5119):361-4 PMID: 8392750
  29. Periodicity of thalamic spindle waves is abolished by ZD7288,a blocker of Ih.
    J Neurophysiol. 1998 Jun;79(6):3284-9 PMID: 9636128
  30. Action potential fidelity during normal and epileptiform activity in paired soma-axon recordings from rat hippocampus.
    J Physiol. 2005 Jul 15;566(Pt 2):425-41 PMID: 15890699
  31. Spindle density in sleep of normal subjects.
    Sleep. 1981;4(4):385-91 PMID: 7313391
  32. The thalamus as a neuronal oscillator.
    Brain Res. 1984 Nov;320(1):1-63 PMID: 6440659
  33. GABAergic neurons are present in the dorsal column nuclei but not in the ventroposterior complex of rats.
    Brain Res. 1986 Sep 24;382(2):305-26 PMID: 2428443
  34. Coherent oscillations and short-term plasticity in corticothalamic networks.
    Trends Neurosci. 1999 Aug;22(8):337-45 PMID: 10407416
  35. Functional and ionic properties of a slow afterhyperpolarization in ferret perigeniculate neurons in vitro.
    J Neurophysiol. 1998 Sep;80(3):1222-35 PMID: 9744934
  36. POTENTIAL RHYTHMS OF THE CEREBRAL CORTEX DURING SLEEP.
    Science. 1935 Jun 14;81(2111):597-8 PMID: 17739875
  37. Abolition of spindle oscillations in thalamic neurons disconnected from nucleus reticularis thalami.
    J Neurophysiol. 1985 Dec;54(6):1473-97 PMID: 4087044
  38. Role of the ferret perigeniculate nucleus in the generation of synchronized oscillations in vitro.
    J Physiol. 1995 Mar 15;483 ( Pt 3):665-85 PMID: 7776250
  39. T-type Ca2+ channels, SK2 channels and SERCAs gate sleep-related oscillations in thalamic dendrites.
    Nat Neurosci. 2008 Jun;11(6):683-92 PMID: 18488023
  40. Extreme spindles: correlation of electroencephalographic sleep pattern with mental retardation.
    Science. 1962 Dec 7;138(3545):1106-7 PMID: 13947675
  41. Axonal propagation of simple and complex spikes in cerebellar Purkinje neurons.
    J Neurosci. 2005 Jan 12;25(2):454-63 PMID: 15647489
  42. Quantitative measures of cluster quality for use in extracellular recordings.
    Neuroscience. 2005;131(1):1-11 PMID: 15680687
  43. Substrate for cross-talk inhibition between thalamic barreloids.
    J Neurosci. 2002 May 1;22(9):RC218 PMID: 11978859
  44. Projection and innervation patterns of individual thalamic reticular axons in the thalamus of the adult rat: a three-dimensional, graphic, and morphometric analysis.
    J Comp Neurol. 1998 Feb 9;391(2):180-203 PMID: 9518268
  45. Characterization of neocortical principal cells and interneurons by network interactions and extracellular features.
    J Neurophysiol. 2004 Jul;92(1):600-8 PMID: 15056678
Article Info
Journal
Neuron
Abbr.
Neuron
ISSN
1097-4199
DOI
10.1016/j.neuron.2014.04.046
Email
[email protected]
[email protected]
Published
2014-06-18
Pages
1367-79
Language
English
Region
United States
NLM ID
8809320
PMCID
PMC4064116
Subset
IM
Grants
Wellcome Trust · 094513 · United Kingdom
Wellcome Trust · 095668 · United Kingdom
External Links
PubMed source DOI: 10.1016/j.neuron.2014.04.046 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2