Home LiteratureArticle Details
PMID: 24403164 Published · ppublish English Comparative Study Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Comparison of sleep spindles and theta oscillations in the hippocampus.

Sullivan D, Mizuseki K, Sorgi A, Buzsáki G

Abstract

Several network patterns allow for information exchange between the neocortex and the entorhinal-hippocampal complex, including theta oscillations and sleep spindles. How neurons are organized in these respective patterns is not well understood. We examined the cellular-synaptic generation of sleep spindles and theta oscillations in the waking rat and during rapid eye movement (REM) sleep by simultaneously recording local field and spikes in the regions and layers of the hippocampus and entorhinal cortex (EC). We show the following: (1) current source density analysis reveals that similar anatomical substrates underlie spindles and theta in the hippocampus, although the hippocampal subregions are more synchronized during spindles than theta; (2) the spiking of putative principal cells and interneurons in the CA1, CA3, and dentate gyrus subregions of the hippocampus, as well as layers 2, 3, and 5 of medial EC, are significantly phase locked to spindles detected in CA1; (3) the relationship between local field potential (LFP) phase and unit spiking differs between spindles and theta; (4) individual hippocampal principal cells generally do not fire in a rhythmic manner during spindles; (5) power in gamma (30-90 Hz) and epsilon (>90 Hz) bands of hippocampal LFP is modulated by the phase of spindle oscillations; and (6) unit firing rates during spindles were not significantly affected by whether spindles occurred during non-REM or transitions between non-REM and REM sleep. Thus, despite the similar current generator inputs and macroscopic appearance of the LFP, the organization of neuronal firing patterns during spindles bears little resemblance to that of theta oscillations.

Keywords
entorhinal cortex gamma hippocampus sleep spindle theta
MeSH Terms
Animals Hippocampus/physiology Male Rats Rats, Long-Evans Rats, Sprague-Dawley Sleep, REM/physiology Theta Rhythm/physiology
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Sullivan David
Center for Molecular and Behavioral Neuroscience, Rutgers, The State University of New Jersey, Newark, New Jersey 07102, and Neuroscience Institute, School of Medicine, New York University, New York, New York 10016.
Mizuseki Kenji
Sorgi Anthony
Buzsáki György
References (88)
88 references, click to expand
  1. Integration and segregation of activity in entorhinal-hippocampal subregions by neocortical slow oscillations.
    Neuron. 2006 Dec 7;52(5):871-82 PMID: 17145507
  2. Replay and time compression of recurring spike sequences in the hippocampus.
    J Neurosci. 1999 Nov 1;19(21):9497-507 PMID: 10531452
  3. A 4 Hz oscillation adaptively synchronizes prefrontal, VTA, and hippocampal activities.
    Neuron. 2011 Oct 6;72(1):153-65 PMID: 21982376
  4. Neuronal plasticity in thalamocortical networks during sleep and waking oscillations.
    Neuron. 2003 Feb 20;37(4):563-76 PMID: 12597855
  5. Thalamic dysfunction in schizophrenia suggested by whole-night deficits in slow and fast spindles.
    Am J Psychiatry. 2010 Nov;167(11):1339-48 PMID: 20843876
  6. Gamma oscillations in the entorhinal cortex of the freely behaving rat.
    J Neurosci. 1998 Jan 1;18(1):388-98 PMID: 9412515
  7. Laminar distribution of hippocampal rhythmic slow activity (RSA) in the behaving rat: current-source density analysis, effects of urethane and atropine.
    Brain Res. 1986 Feb 12;365(1):125-37 PMID: 3947979
  8. Nucleus reuniens thalami modulates activity in hippocampal field CA1 through excitatory and inhibitory mechanisms.
    J Neurosci. 1997 Jul 15;17(14):5640-50 PMID: 9204945
  9. Sustained increase in hippocampal sharp-wave ripple activity during slow-wave sleep after learning.
    Learn Mem. 2008 Apr 02;15(4):222-8 PMID: 18385477
  10. [Intermediate stages of sleep in the rat].
    Rev Electroencephalogr Neurophysiol Clin. 1973 Jan-Mar;3(1):65-8 PMID: 4807416
  11. Differential responses of hippocampal subfields to cortical up-down states.
    Proc Natl Acad Sci U S A. 2007 Mar 20;104(12):5169-74 PMID: 17360347
  12. Replay of rule-learning related neural patterns in the prefrontal cortex during sleep.
    Nat Neurosci. 2009 Jul;12(7):919-26 PMID: 19483687
  13. Regional slow waves and spindles in human sleep.
    Neuron. 2011 Apr 14;70(1):153-69 PMID: 21482364
  14. Early motor activity drives spindle bursts in the developing somatosensory cortex.
    Nature. 2004 Dec 9;432(7018):758-61 PMID: 15592414
  15. REM sleep reorganizes hippocampal excitability.
    Neuron. 2012 Sep 20;75(6):1001-7 PMID: 22998869
  16. Gamma oscillations dynamically couple hippocampal CA3 and CA1 regions during memory task performance.
    Proc Natl Acad Sci U S A. 2007 Sep 4;104(36):14495-500 PMID: 17726109
  17. The memory function of sleep.
    Nat Rev Neurosci. 2010 Feb;11(2):114-26 PMID: 20046194
  18. Sleep function and synaptic homeostasis.
    Sleep Med Rev. 2006 Feb;10(1):49-62 PMID: 16376591
  19. Selective optical drive of thalamic reticular nucleus generates thalamic bursts and cortical spindles.
    Nat Neurosci. 2011 Jul 24;14(9):1118-20 PMID: 21785436
  20. 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 Aug;13(8):3284-99 PMID: 8340808
  21. Mechanisms of gamma oscillations in the hippocampus of the behaving rat.
    Neuron. 2003 Jan 23;37(2):311-22 PMID: 12546825
  22. Definitions of state variables and state space for brain-computer interface : Part 1. Multiple hierarchical levels of brain function.
    Cogn Neurodyn. 2007 Mar;1(1):3-14 PMID: 19003492
  23. Dentate EEG spikes and associated interneuronal population bursts in the hippocampal hilar region of the rat.
    J Neurophysiol. 1995 Apr;73(4):1691-705 PMID: 7643175
  24. Corticothalamic resonance, states of vigilance and mentation.
    Neuroscience. 2000;101(2):243-76 PMID: 11074149
  25. Sleep-dependent directional coupling between human neocortex and hippocampus.
    Cortex. 2010 Feb;46(2):256-63 PMID: 19552899
  26. Reduced sleep spindle activity in schizophrenia patients.
    Am J Psychiatry. 2007 Mar;164(3):483-92 PMID: 17329474
  27. Coordinated interactions between hippocampal ripples and cortical spindles during slow-wave sleep.
    Neuron. 1998 Nov;21(5):1123-8 PMID: 9856467
  28. Sleep in schizophrenia: time for closer attention.
    Br J Psychiatry. 2012 Apr;200(4):273-4 PMID: 22474232
  29. Organization of hippocampal cell assemblies based on theta phase precession.
    Hippocampus. 2006;16(9):785-94 PMID: 16921501
  30. Elevated sleep spindle density after learning or after retrieval in rats.
    J Neurosci. 2006 Dec 13;26(50):12914-20 PMID: 17167082
  31. Hippocampal-cortical interaction during periods of subcortical silence.
    Nature. 2012 Nov 22;491(7425):547-53 PMID: 23172213
  32. Reciprocal interaction of sleep and synaptic plasticity.
    Mol Interv. 2003 Oct;3(7):404-17 PMID: 14993461
  33. Cellular bases of hippocampal EEG in the behaving rat.
    Brain Res. 1983 Oct;287(2):139-71 PMID: 6357356
  34. Analysis of dynamic brain imaging data.
    Biophys J. 1999 Feb;76(2):691-708 PMID: 9929474
  35. Cross-frequency phase-phase coupling between θ and γ oscillations in the hippocampus.
    J Neurosci. 2012 Jan 11;32(2):423-35 PMID: 22238079
  36. Projection from the nucleus reuniens thalami to the hippocampal region: light and electron microscopic tracing study in the rat with the anterograde tracer Phaseolus vulgaris-leucoagglutinin.
    J Comp Neurol. 1990 Jun 8;296(2):179-203 PMID: 2358531
  37. Inhibition recruitment in prefrontal cortex during sleep spindles and gating of hippocampal inputs.
    Proc Natl Acad Sci U S A. 2011 Oct 11;108(41):17207-12 PMID: 21949372
  38. Theta and gamma coordination of hippocampal networks during waking and rapid eye movement sleep.
    J Neurosci. 2008 Jun 25;28(26):6731-41 PMID: 18579747
  39. Ensemble patterns of hippocampal CA3-CA1 neurons during sharp wave-associated population events.
    Neuron. 2000 Nov;28(2):585-94 PMID: 11144366
  40. The function of the sleep spindle: a physiological index of intelligence and a mechanism for sleep-dependent memory consolidation.
    Neurosci Biobehav Rev. 2011 Apr;35(5):1154-65 PMID: 21167865
  41. Gamma (40-100 Hz) oscillation in the hippocampus of the behaving rat.
    J Neurosci. 1995 Jan;15(1 Pt 1):47-60 PMID: 7823151
  42. Effects of skilled training on sleep slow wave activity and cortical gene expression in the rat.
    Sleep. 2009 Jun;32(6):719-29 PMID: 19544747
  43. Daytime naps, motor memory consolidation and regionally specific sleep spindles.
    PLoS One. 2007 Apr 04;2(4):e341 PMID: 17406665
  44. Hippocampal network dynamics constrain the time lag between pyramidal cells across modified environments.
    J Neurosci. 2008 Dec 10;28(50):13448-56 PMID: 19074018
  45. Sleep spindles: an overview.
    Sleep Med Rev. 2003 Oct;7(5):423-40 PMID: 14573378
  46. Reduced sleep spindles and spindle coherence in schizophrenia: mechanisms of impaired memory consolidation?
    Biol Psychiatry. 2012 Jan 15;71(2):154-61 PMID: 21967958
  47. Decoupling of sleep-dependent cortical and hippocampal interactions in a neurodevelopmental model of schizophrenia.
    Neuron. 2012 Nov 8;76(3):526-33 PMID: 23141065
  48. Power and coherence of sleep spindle frequency activity following hemispheric stroke.
    Brain. 2002 Feb;125(Pt 2):373-83 PMID: 11844737
  49. Communication between neocortex and hippocampus during sleep in rodents.
    Proc Natl Acad Sci U S A. 2003 Feb 18;100(4):2065-9 PMID: 12576550
  50. Sleep abnormalities in schizophrenia may suggest impaired trans-thalamic cortico-cortical communication: towards a dynamic model of the illness.
    Eur J Neurosci. 2011 Oct;34(7):1031-9 PMID: 21895800
  51. Hippocampus-independent phase precession in entorhinal grid cells.
    Nature. 2008 Jun 26;453(7199):1248-52 PMID: 18480753
  52. The connections of the nucleus reuniens thalami: evidence for a direct thalamo-hippocampal pathway in the rat.
    J Comp Neurol. 1978 Feb 15;177(4):589-610 PMID: 624792
  53. Stored-trace reactivation in rat prefrontal cortex is correlated with down-to-up state fluctuation density.
    J Neurosci. 2010 Feb 17;30(7):2650-61 PMID: 20164349
  54. Novel object presentation affects sleep-wake behavior in rats.
    Neurosci Lett. 2002 Aug 2;328(1):41-4 PMID: 12123855
  55. Current source density analysis of the hippocampal theta rhythm: associated sustained potentials and candidate synaptic generators.
    Brain Res. 1993 Jul 2;615(2):310-27 PMID: 8364740
  56. Reactivation of hippocampal ensemble memories during sleep.
    Science. 1994 Jul 29;265(5172):676-9 PMID: 8036517
  57. Phase relationship between hippocampal place units and the EEG theta rhythm.
    Hippocampus. 1993 Jul;3(3):317-30 PMID: 8353611
  58. Klusters, NeuroScope, NDManager: a free software suite for neurophysiological data processing and visualization.
    J Neurosci Methods. 2006 Sep 15;155(2):207-16 PMID: 16580733
  59. Thalamocortical oscillations in the sleeping and aroused brain.
    Science. 1993 Oct 29;262(5134):679-85 PMID: 8235588
  60. Temporal coupling of parahippocampal ripples, sleep spindles and slow oscillations in humans.
    Brain. 2007 Nov;130(Pt 11):2868-78 PMID: 17615093
  61. Theta oscillations in somata and dendrites of hippocampal pyramidal cells in vivo: activity-dependent phase-precession of action potentials.
    Hippocampus. 1998;8(3):244-61 PMID: 9662139
  62. The Ca(V)3.3 calcium channel is the major sleep spindle pacemaker in thalamus.
    Proc Natl Acad Sci U S A. 2011 Aug 16;108(33):13823-8 PMID: 21808016
  63. Topographic and sex-related differences in sleep spindles in major depressive disorder: a high-density EEG investigation.
    J Affect Disord. 2013 Mar 20;146(1):120-5 PMID: 22974470
  64. Mechanisms of gamma oscillations.
    Annu Rev Neurosci. 2012;35:203-25 PMID: 22443509
  65. Sleep spindles and their significance for declarative memory consolidation.
    Sleep. 2004 Dec 15;27(8):1479-85 PMID: 15683137
  66. POTENTIAL RHYTHMS OF THE CEREBRAL CORTEX DURING SLEEP.
    Science. 1935 Jun 14;81(2111):597-8 PMID: 17739875
  67. Hippocampal slow oscillation: a novel EEG state and its coordination with ongoing neocortical activity.
    J Neurosci. 2006 Jun 7;26(23):6213-29 PMID: 16763029
  68. Grouping of MEG gamma oscillations by EEG sleep spindles.
    Neuroimage. 2012 Jan 16;59(2):1491-500 PMID: 21893206
  69. Spike train dynamics predicts theta-related phase precession in hippocampal pyramidal cells.
    Nature. 2002 Jun 13;417(6890):738-41 PMID: 12066184
  70. Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep.
    Neuron. 2001 Jan;29(1):145-56 PMID: 11182087
  71. Coordinated memory replay in the visual cortex and hippocampus during sleep.
    Nat Neurosci. 2007 Jan;10(1):100-7 PMID: 17173043
  72. Hippocampal place cell assemblies are speed-controlled oscillators.
    Proc Natl Acad Sci U S A. 2007 May 8;104(19):8149-54 PMID: 17470808
  73. Hippocampal sharp wave-ripples linked to slow oscillations in rat slow-wave sleep.
    J Neurophysiol. 2006 Jul;96(1):62-70 PMID: 16611848
  74. High gamma power is phase-locked to theta oscillations in human neocortex.
    Science. 2006 Sep 15;313(5793):1626-8 PMID: 16973878
  75. Grid cells and theta as oscillatory interference: electrophysiological data from freely moving rats.
    Hippocampus. 2008;18(12):1175-85 PMID: 19021251
  76. Forward and reverse hippocampal place-cell sequences during ripples.
    Nat Neurosci. 2007 Oct;10(10):1241-2 PMID: 17828259
  77. Frequency of gamma oscillations routes flow of information in the hippocampus.
    Nature. 2009 Nov 19;462(7271):353-7 PMID: 19924214
  78. Fine-tuned coupling between human parahippocampal ripples and sleep spindles.
    Eur J Neurosci. 2011 Feb;33(3):511-20 PMID: 21138489
  79. Why do we sleep?
    Brain Res. 2000 Dec 15;886(1-2):208-223 PMID: 11119697
  80. Subthreshold Na+-dependent theta-like rhythmicity in stellate cells of entorhinal cortex layer II.
    Nature. 1989 Nov 9;342(6246):175-7 PMID: 2812013
  81. Temporal encoding of place sequences by hippocampal cell assemblies.
    Neuron. 2006 Apr 6;50(1):145-57 PMID: 16600862
  82. Control of spatiotemporal coherence of a thalamic oscillation by corticothalamic feedback.
    Science. 1996 Nov 1;274(5288):771-4 PMID: 8864114
  83. Learning-dependent increases in sleep spindle density.
    J Neurosci. 2002 Aug 1;22(15):6830-4 PMID: 12151563
  84. Theta oscillations provide temporal windows for local circuit computation in the entorhinal-hippocampal loop.
    Neuron. 2009 Oct 29;64(2):267-80 PMID: 19874793
  85. Current source-density method and application in cat cerebral cortex: investigation of evoked potentials and EEG phenomena.
    Physiol Rev. 1985 Jan;65(1):37-100 PMID: 3880898
  86. Behavior-dependent coordination of multiple theta dipoles in the hippocampus.
    J Neurosci. 2009 Feb 4;29(5):1381-94 PMID: 19193885
  87. Relationships between hippocampal sharp waves, ripples, and fast gamma oscillation: influence of dentate and entorhinal cortical activity.
    J Neurosci. 2011 Jun 8;31(23):8605-16 PMID: 21653864
  88. High-frequency network oscillation in the hippocampus.
    Science. 1992 May 15;256(5059):1025-7 PMID: 1589772
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2014-01-08
Pages
662-74
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC3870943
Subset
IM
Grants
NIMH NIH HHS · R01 MH054671 · United States
NINDS NIH HHS · R01 NS034994 · United States
NIMH NIH HHS · MH54671 · United States
NINDS NIH HHS · NS034994 · United States
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]