Sleep spindles in humans: Insights from intracranial EEG and unit recordings

Journal of Neuroscience

Volumn 31, Issue 49, 2011, Pages 17821-17834

  Andrillon, Thomas ^a,b   Nir, Yuval ^a   Staba, Richard J ^c   Ferrarelli, Fabio ^a   Cirelli, Chiara ^a   Tononi, Giulio ^a   Fried, Itzhak ^c,d  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b E ́cole Normale Supe ́rieure ^*  (France)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d TEL AVIV UNIVERSITY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

AMYGDALOID NUCLEUS; ANTERIOR CINGULATE; ARTICLE; CLINICAL ARTICLE; ELECTROENCEPHALOGRAM; ENTORHINAL CORTEX; EPILEPSY; FEMALE; HIPPOCAMPUS; HUMAN; MALE; NEOCORTEX; NERVE CELL MEMBRANE POTENTIAL; NONREM SLEEP; ORBITAL CORTEX; PARAHIPPOCAMPAL GYRUS; POLYSOMNOGRAPHY; POSTERIOR CINGULATE; PRIORITY JOURNAL; SLEEP SPINDLE; SUPPLEMENTARY MOTOR AREA; THALAMOCORTICAL TRACT;

ACTION POTENTIALS; ADULT; BRAIN; BRAIN MAPPING; BRAIN WAVES; ELECTROENCEPHALOGRAPHY; ELECTROMYOGRAPHY; ELECTROOCULOGRAPHY; EPILEPSY; FEMALE; HUMANS; MALE; MIDDLE AGED; NEURONS; NONLINEAR DYNAMICS; POLYSOMNOGRAPHY; SLEEP; SPECTRUM ANALYSIS; TIME FACTORS; YOUNG ADULT;

EID: 83055170040     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2604-11.2011     Document Type: Article

References (92)

1. Achermann P, Borbely AA (1998) Temporal evolution of coherence and power in the human sleep electroencephalogram. J Sleep Res 7 [Suppl 1]:36-41.
2. Akkal D, Dum RP, Strick PL (2007) Supplementary motor area and pre-supplementary motor area: targets of basal ganglia and cerebellar output. J Neurosci 27:10659-10673.
3. Anderer P, Klösch G, Gruber G, Trenker E, Pascual-Marqui RD, Zeitlhofer J, Barbanoj MJ, Rappelsberger P, Saletu B (2001) Low-resolution brain electromagnetic tomography revealed simultaneously active frontal and parietal sleep spindle sources in the human cortex. Neuroscience 103:581-592.
4. Andersen P, Andersson S (1968) Physiological basis of the alpha rhythm. New York: Meridith.
5. Bal T, von Krosigk M, McCormick DA (1995) Synaptic and membrane mechanisms underlying synchronized oscillations in the ferret lateral geniculate nucleus in vitro. J Physiol 483:641-663.
6. Bonjean M, Baker T, Lemieux M, Timofeev I, Sejnowski T, Bazhenov M (2011) Corticothalamic feedback controls sleep spindle duration in vivo. J Neurosci 31:9124-9134.
7. Caderas M, Niedermeyer E, Uematsu S, Long DM, Nastalski J (1982) Sleep spindles recorded from deep cerebral structures in man. Clin Electroen-cephalogr 13:216-225.
8. Caporale N, Dan Y (2008) Spike timing-dependent plasticity: a Hebbian learning rule. Annu Rev Neurosci 31:25-46.
9. Cappe C, Morel A, Barone P, Rouiller EM (2009) The thalamocortical projection systems in primate: an anatomical support for multisensory and sensorimotor interplay. Cereb Cortex 19:2025-2037.
10. öCash SS, Halgren E, Dehghani N, Rossetti AO, Thesen T, Wang C, Devinsky O, Kuzniecky R, Doyle W, Madsen JR, Bromfield E, Eross L, Halász P, Karmos G, Csercsa R, Wittner L, Ulbert I (2009) The human K-complex represents an isolated cortical down-state. Science 324:1084-1087.
11. Clemens Z, Mölle M, Eross L, Barsi P, Halász P, Born J (2007) Temporal coupling of parahippocampal ripples, sleep spindles and slow oscillations in humans. Brain 130:2868-2878.
12. Clemens Z, Mölle M, Eross L, Jakus R, Rásonyi G, Halász P, Born J (2011) Fine-tuned coupling between human parahippocampal ripples and sleep spindles. Eur J Neurosci 33:511-520.
13. Contreras D, Steriade M (1996) Spindle oscillation in cats: the role of corticothalamic feedback in a thalamically generated rhythm. J Physiol 490:159-179.
14. Contreras D, Destexhe A, Sejnowski TJ, Steriade M (1996) Control of spa-tiotemporal coherence of a thalamic oscillation by corticothalamic feedback. Science 274:771-774.
15. Contreras D, Destexhe A, Steriade M (1997a) Intracellular and computational characterization of the intracortical inhibitory control of synchronized thalamic inputs in vivo. J Neurophysiol 78:335-350.
16. Contreras D, Destexhe A, Steriade M (1997b) Spindle oscillations during cortical spreading depression in naturally sleeping cats. Neuroscience 77:933-936.
17. Contreras D, Destexhe A, Sejnowski TJ, Steriade M (1997c) Spatiotemporal patterns of spindle oscillations in cortex and thalamus. J Neurosci 17:1179-1196.
18. de Curtis M, Avanzini G (2001) Interictal spikes in focal epileptogenesis. Prog Neurobiol 63:541-567.
19. De Gennaro L, Ferrara M (2003) Sleep spindles: an overview. Sleep Med Rev 7:423-440.
20. Dehghani N, Cash SS, Chen CC, Hagler DJ, Huang M, Dale AM, Halgren E (2010a) Divergent cortical generators of MEG and EEG during human sleep spindles suggested by distributed source modeling. PLoS One 5:e11454.
21. Dehghani N, Peyrache A, Destexhe A (2010b) Dynamics of excitation and inhibition, and local interactions, during slow wave sleep oscillations in rat prefrontal cortex. Soc Neurosci Abstr 36:44.5.
22. Dehghani N, Cash SS, Halgren E (2011) Topographical frequency dynamics within EEG and MEG sleep spindles. Clin Neurophysiol 122:229-235.
23. Destexhe A, Sejnowski TJ (2001) Thalamocortical assemblies: how ion channels, single neurons and large-scale networks organize sleep oscillations. Oxford: Oxford UP.
24. Destexhe A, Sejnowski TJ (2002) The initiation of bursts in thalamic neurons and the cortical control of thalamic sensitivity. Philos Trans R Soc Lond B Biol Sci 357:1649-1657.
25. Destexhe A, Contreras D, Steriade M (1998) Mechanisms underlying the synchronizing action of corticothalamic feedback through inhibition of thalamic relay cells. J Neurophysiol 79:999-1016.
26. Diekelmann S, Born J (2010) The memory function of sleep. Nat Rev Neu-rosci 11:114-126.
27. Dinner DS, Lüders HO, eds (2001) Epilepsy and sleep: physiological and clinical relationships. San Diego: Academic.
28. Esser SK, Huber R, Massimini M, Peterson MJ, Ferrarelli F, Tononi G (2006) A direct demonstration ofcortical LTPin humans:acombined TMS/EEG study. Brain Res Bull 69:86-94.
29. Evarts EV (1964) Temporal patterns of discharge of pyramidal tract neurons during sleep and waking in the monkey. J Neurophysiol 27:152-171.
30. Ferrarelli F, Huber R, Peterson MJ, Massimini M, Murphy M, Riedner BA, Watson A, Bria P, Tononi G (2007) Reduced sleep spindle activity in schizophrenia patients. Am J Psychiatry 164:483-492.
31. Ferrarelli F, Peterson MJ, Sarasso S, Riedner BA, Murphy MJ, Benca RM, Bria P, Kalin NH, Tononi G (2010) Thalamic dysfunction in schizophrenia suggested by whole-night deficits in slow and fast spindles. Am J Psychiatry 167:1339-1348.
32. Fried I, Wilson CL, Maidment NT, Engel J, Behnke E, Fields TA, MacDon-ald KA, Morrow JW, Ackerson L (1999) Cerebral microdialysis combined with single-neuron and electroencephalographic recording in neurosurgical patients. Technical note. J Neurosurg 91:697-705.
33. Gibbs FA, Gibbs EL (1950) Atlas of electroencephalography. Boston: Addison-Wesley.
34. Golshani P, Liu XB, Jones EG (2001) Differences in quantal amplitude reflect GluR4-subunit number at corticothalamic synapses on two populations of thalamic neurons. Proc Natl Acad Sci U S A 98:4172-4177.
35. Guillery RW, Harting JK (2003) Structure and connections of the thalamic reticular nucleus: advancing views over half a century. J Comp Neurol 463:360-371.
36. Halassa MM, Siegle JH, Ritt JT, Ting JT, Feng G, Moore CI (2011) Selective optical drive of thalamic reticular nucleus generates thalamic bursts and cortical spindles. Nat Neurosci 14:1118-1120.
37. Himanen SL, Virkkala J, Huhtala H, Hasan J (2002) Spindle frequencies in sleep EEG show U-shape within first four NREM sleep episodes. J Sleep Res 11:35-42.
38. Huber R, Ghilardi MF, Massimini M, Tononi G (2004) Local sleep and learning. Nature 430:78-81.
39. Huber R, Ghilardi MF, Massimini M, Ferrarelli F, Riedner BA, Peterson MJ, Tononi G (2006) Arm immobilization causes cortical plastic changes and locally decreases sleep slow wave activity. Nat Neurosci 9:1169-1176.
40. Iber C, Ancoli-Israel S, Chesson AL, Quan SF (2007) AASM manual for the scoring of sleep and associate events. Rules, terminology and technical specifications. Westchester, IL: American Association of Sleep Medicine.
41. Jankel WR, Niedermeyer E (1985) Sleep spindles. J Clin Neurophysiol 2:1-35.
42. Jobert M, Poiseau E, Jahnig P, Schulz H, Kubicki S (1992) Topographical analysis of sleep spindle activity. Neuropsychobiology 26:210-217.
43. Jones EG (2002) Thalamic circuitry and thalamocortical synchrony. Philos Trans RSoc Lond B Biol Sci 357:1659-1673.
44. Jones EG (2007) The thalamus, Ed 2. Cambridge, UK: Cambridge UP.
45. Jones EG (2009) Synchrony in the interconnected circuitry of the thalamus and cerebral cortex. AnnN Y Acad Sci 1157:10-23.
46. Khazipov R, Sirota A, Leinekugel X, Holmes GL, Ben-Ari Y, Buzsaki G (2004) Early motor activity drives spindle bursts in the developing somatosensory cortex. Nature 432:758-761.
47. Kim U, Bal T, McCormick DA (1995) Spindle waves are propagating synchronized oscillations in the ferret LGNd in vitro. J Neurophysiol 74:1301-1323.
48. Krueger JM, Rector DM, Roy S, Van Dongen HP, Belenky G, Panksepp J (2008) Sleep as a fundamental property of neuronal assemblies. Nat Rev Neurosci 9:910-919.
49. Lam YW, Sherman SM (2011) Functional organization of the thalamic input to the thalamic reticular nucleus. J Neurosci 31:6791-6799.
50. Loomis AL, Harvey EN, Hobart G (1935) Potential rhythms of the cerebral cortex during sleep. Science 81:597-598.
51. Lüthi A, McCormick DA (1998) Periodicity of thalamic synchronized oscillations: the role of Ca +-mediated upregulation of Ih. Neuron 20:553-563.
52. Malow BA, Carney PR, Kushwaha R, Bowes RJ (1999) Hippocampal sleep spindles revisited: physiologic or epileptic activity? Clin Neurophysiol 110:687-693.
53. Marini G, Macchi G, Mancia M (1992) Potentiation of electroencephalo-graphic spindles by ibotenate microinjections into nucleus reticularis thalami of cats. Neuroscience 51:759-762.
54. Massimini M, Huber R, Ferrarelli F, Hill S, Tononi G (2004) The sleep slow oscillation as a traveling wave. J Neurosci 24:6862-6870.
55. McCormick DA, Bal T (1997) Sleep and arousal: thalamocortical mechanisms. Annu Rev Neurosci 20:185-215.
56. Molle M, Marshall L, Gais S, Born J (2002) Grouping of spindle activity during slow oscillations in human non-rapid eye movement sleep. J Neurosci 22:10941-10947.
57. Morison RS, Bassett DI (1945) Electrical activity of the thalamus and basal ganglia in decorticated cats. J Neurophysiol 8:309-314.
58. Nakabayashi T, Uchida S, Maehara T, Hirai N, Nakamura M, Arakaki H, Shimisu H, Okubo Y (2001) Absence of sleep spindles in human medial and basal temporal lobes. Psychiatry Clin Neurosci 55:57-65.
59. Nakamura M, Uchida S, Maehara T, Kawai K, Hirai N, Nakabayashi T, Arakaki H, Okubo Y, Nishikawa T, Shimizu H (2003) Sleep spindles in human prefrontal cortex: an electrocorticographic study. Neurosci Res 45:419 - 427.
60. Nir Y, Mukamel R, Dinstein I, Privman E, Harel M, Fisch L, Gelbard-Sagiv H, Kipervasser S, Andelman F, Neufeld MY, Kramer U, Arieli A, Fried I, Malach R (2008) Interhemispheric correlations of slow spontaneous neuronal fluctuations revealed in human sensory cortex. Nat Neurosci 11:1100-1108.
61. Nir Y, Staba RJ, Andrillon T, Vyazovskiy VV, Cirelli C, Fried I, Tononi G (2011) Regional slow waves and spindles in human sleep. Neuron 70:153-169.
62. Nishida M, Walker MP (2007) Daytime naps, motor memory consolidation and regionally specific sleep spindles. PLoS One 2:e341.
63. Nunez A, Curro Dossi R, Contreras D, Steriade M (1992) Intracellular evidence for incompatibility between spindle and delta oscillations in thalamocortical neurons of cat. Neuroscience 48:75-85.
64. Pare D, Steriade M, Deschenes M, Oakson G (1987) Physiological characteristics of anterior thalamic nuclei, a group devoid of inputs from reticular thalamic nucleus. J Neurophysiol 57:1669-1685.
65. Pare D, Collins DR, Pelletier JG (2002) Amygdala oscillations and the consolidation of emotional memories. Trends Cogn Sci 6:306-314.
66. Quiroga RQ, Nadasdy Z, Ben-Shaul Y (2004) Unsupervised spike detection and sorting with wavelets and superparamagnetic clustering. Neural Comput 16:1661-1687.
67. Riedner BA, Vyazovskiy VV, Huber R, Massimini M, Esser S, Murphy M, Tononi G (2007) Sleep homeostasis and cortical synchronization: III. A high-density EEG study of sleep slow waves in humans. Sleep 30:1643-1657.
68. Rubio-Garrido P, Pérez-de-Manzo F, Porrero C, Galazo MJ, Clascá F (2009) Thalamic input to distal apical dendrites in neocortical layer 1 is massive and highly convergent. Cereb Cortex 19:2380-2395.
69. Schabus M, Gruber G, Parapatics S, Sauter C, Klösch G, Anderer P, Klimesch W, Saletu B, Zeitlhofer J (2004) Sleep spindles and their significance for declarative memory consolidation. Sleep 27:1479-1485.
70. Schabus M, Dang-Vu TT, Albouy G, Balteau E, Boly M, Carrier J, Darsaud A, Degueldre C, Desseilles M, Gais S, Phillips C, Rauchs G, Schnakers C, Sterpenich V, Vandewalle G, Luxen A, Maquet P (2007) Hemodynamic cerebral correlates of sleep spindles during human non-rapid eye movement sleep. Proc Natl Acad Sci U S A 104:13164-13169.
71. Siapas AG, Lubenov EV, Wilson MA (2005) Prefrontal phase locking to hippocampal theta oscillations. Neuron 46:141-151.
72. Sirota A, Csicsvari J, Buhl D, Buzsáki G (2003) Communication between neocortex and hippocampus during sleep in rodents. Proc Natl Acad Sci U S A 100:2065-2069.
73. Steriade M (2000) Corticothalamic resonance, states of vigilance and mentation. Neuroscience 101:243-276.
74. Steriade M (2003) Neuronal substrates of sleep and epilepsy, Ed 1. Cambridge, UK: Cambridge UP.
75. Steriade M (2005) Sleep, epilepsy and thalamic reticular inhibitory neurons. Trends Neurosci 28:317-324.
76. Steriade M, Amzica F (1998) Coalescence of sleep rhythms and their chronology in corticothalamic networks. Sleep Res Online 1:1-10.
77. Steriade M, Timofeev I (2003) Neuronal plasticity in thalamocortical networks during sleep and waking oscillations. Neuron 37:563-576.
78. Steriade M, DESCHEÊNES M, Oakson G (1974) Inhibitory processes and in-terneuronal apparatus in motor cortex during sleep and waking. I. Background firing and responsiveness of pyramidal tract neurons and interneurons. J Neurophysiol 37:1065-1092.
79. Steriade M, Parent A, Hada J (1984) Thalamic projections of nucleus reticu-laris thalami of cat: a study using retrograde transport of horseradish peroxidase and fluorescent tracers. J Comp Neurol 229:531-547.
80. Steriade M, Deschenes M, Domich L, Mulle C (1985) Abolition of spindle oscillations in thalamic neurons disconnected from nucleus reticularis thalami. J Neurophysiol 54:1473-1497.
81. Steriade M, Domich L, Oakson G, Deschenes M (1987) The deafferented reticular thalamic nucleus generates spindle rhythmicity. J Neurophysiol 57:260-273.
82. Steriade M, Nunez A, Amzica F (1993a) Intracellular analysis of relations between the slow (< 1 Hz) neocortical oscillation and other sleep rhythms of the electroencephalogram. J Neurosci 13:3266-3283.
83. Steriade M, Contreras D, Curro Dossi R, Nunez A (1993b) The slow (<1 Hz) oscillation in reticular thalamic and thalamocortical neurons: scenario of sleep rhythm generation in interacting thalamic and neocortical networks. J Neurosci 13:3284-3299.
84. Timofeev I, Grenier F, Steriade M (2001) Disfacilitation and active inhibition in the neocortex during the natural sleep-wake cycle: an intracellular study. Proc Natl Acad Sci USA 98:1924-1929.
85. von Krosigk M, Bal T, McCormick DA (1993) Cellular mechanisms of a synchronized oscillation in the thalamus. Science 261:361-364.
86. Vyazovskiy V, Borbely AA, Tobler I (2000) Unilateral vibrissae stimulation during waking induces interhemispheric EEG asymmetry during subsequent sleep in the rat. J Sleep Res 9:367-371.
87. Wei HG, Riel E, Czeisler CA, Dijk DJ (1999) Attenuated amplitude of circadian and sleep-dependent modulation of electroencephalo-graphic sleep spindle characteristics in elderly human subjects. Neurosci Lett 260:29-32.
88. Werth E, Achermann P, Borbely AA (1997) Fronto-occipital EEG power gradients in human sleep. J Sleep Res 6:102-112.
89. Zepelin H, Siegel JM, Tobler I (1994) Mammalian sleep. In: Principles and practice of sleep medicine (Kryger MH, Roth T, Dement WC, eds), pp 91-100. London: Saunders.
90. Zhang D, Snyder AZ, Shimony JS, Fox MD, Raichle ME (2010) Noninvasive functional and structural connectivity mapping of the human thalamocortical system. Cereb Cortex 20:1187-1194.
91. Zikopoulos B, Barbas H (2007) Parallel driving and modulatory pathways link the prefrontal cortex and thalamus. PLoS One 2:e848.
92. Zygierewicz J, Blinowska KJ, Durka PJ, Szelenberger W, Niemcewicz S, An-drosiuk W (1999) High resolution study of sleep spindles. Clin Neurophysiol 110:2136-2147.