Thalamic reticular nucleus induces fast and local modulation of arousal state

eLife

Volumn 4, Issue OCTOBER2015, 2015, Pages

  Lewis, Laura D ^a,b,c   Voigts, Jakob ^c   Flores, Francisco J ^b,c,d   Ian Schmitt, L ^e   Wilson, Matthew A ^c   Halassa, Michael M ^e   Brown, Emery N ^b,c,d,f  

^a HARVARD UNIVERSITY   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

^e NEW YORK UNIVERSITY   (United States)

^f Massachusetts Institute of Technology Cambridge   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AROUSAL; BEHAVIOR CHANGE; ELECTROPHYSIOLOGY; MODULATION; OPTOGENETICS; THALAMUS RETICULAR NUCLEUS; ANIMAL; BRAIN CORTEX; MOUSE; PHYSIOLOGY; PROCEDURES; SLEEP; THALAMUS NUCLEUS;

ANIMALS; AROUSAL; CEREBRAL CORTEX; ELECTROPHYSIOLOGY; MICE; OPTOGENETICS; SLEEP; THALAMIC NUCLEI;

EID: 84949895540     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.08760     Document Type: Article

References (75)

1. Adamantidis AR, Zhang F, Aravanis AM, Deisseroth K, de Lecea L. 2007. Neural substrates of awakening probed with optogenetic control of hypocretin neurons. Nature 450:420-424. doi: 10.1038/nature06310
2. Alkire MT, Haier RJ, Fallon JH. 2000. Toward a unified theory of narcosis: brain imaging evidence for a thalamocortical switch as the neurophysiologic basis of anesthetic-induced unconsciousness. Consciousness and Cognition 9:370-386. doi: 10.1006/ccog.1999.0423
3. Amzica F, Steriade M. 1998. Electrophysiological correlates of sleep delta waves. Electroencephalography and Clinical Neurophysiology 107:69-83. doi: 10.1016/S0013-4694(98)00051-0
4. Anaclet C, Ferrari L, Arrigoni E, Bass CE, Saper CB, Lu J, Fuller PM. 2014. The GABAergic parafacial zone is a medullary slow wave sleep-promoting center. Nature Neuroscience 17:1217-1224. doi: 10.1038/nn.3789
5. Barrionuevo G, Benoit O, Tempier P. 1981. Evidence for two types of firing pattern during the sleep-waking cycle in the reticular thalamic nucleus of the cat. Experimental Neurology 72:486-501. doi: 10.1016/0014-4886(81)90238-7
6. Barthó P, Slézia A, Mátyás F, Faradzs-Zade L, Ulbert I, Harris KD, Acsády L. 2014. Ongoing network state controls the length of sleep spindles via inhibitory activity. Neuron 82:1367-1379. doi: 10.1016/j.neuron.2014.04.046
7. Bazhenov M, Timofeev I, Steriade M, Sejnowski T. 2000. Spiking-bursting activity in the thalamic reticular nucleus initiates sequences of spindle oscillations in thalamic networks. Journal of Neurophysiology 84:1076-1087.
8. Beltramo R, D’Urso G, dal Maschio M, Farisello P, Bovetti S, Clovis Y, Lassi G, Tucci V, de Pietri Tonelli D, Fellin T. 2013. Layer-specific excitatory circuits differentially control recurrent network dynamics in the neocortex. Nature Neuroscience 16:227-234. doi: 10.1038/nn.3306
9. Berens P. 2009. CircStat : a MATLAB toolbox for circular statistics. Journal of Statistical Software 31:1-21. doi: 10.18637/jss.v031.i10
10. Brown EN, Purdon PL, van Dort CJ. 2011. General anesthesia and altered states of arousal: a systems neuroscience analysis. Annual Review of Neuroscience 34:601-628. doi: 10.1146/annurev-neuro-060909-153200
11. Buzsaki G, Bickford RG, Ponomareff G, Thal LJ, Mandel R, Gage FH. 1988. Nucleus basalis and thalamic control of neocortical activity in the freely moving rat. Journal of Neuroscience 8:4007-4026.
12. Constantinople CM, Bruno RM. 2011. Effects and mechanisms of wakefulness on local cortical networks. Neuron 69:1061-1068. doi: 10.1016/j.neuron.2011.02.040
13. Crandall SR, Cruikshank SJ, Connors BW. 2015. A corticothalamic switch: controlling the thalamus with dynamic synapses. Neuron 86:768-782. doi: 10.1016/j.neuron.2015.03.040
14. Crick F. 1984. Function of the thalamic reticular complex: The searchlight hypothesis. Proceedings of the National Academy of Sciences of the United States of America 81:4586-4590. doi: 10.1073/pnas.81.14.4586
15. Crunelli V, Hughes SW. 2010. The slow (<1 hz) rhythm of non-REM sleep: a dialogue between three cardinal oscillators. Nature Neuroscience 13:9-17. doi: 10.1038/nn.2445
16. Cueni L, Canepari M, Luján R, Emmenegger Y, Watanabe M, Bond CT, Franken P, Adelman JP, Lüthi A. 2008. T-type Ca2+ channels, SK2 channels and SERCAs gate sleep-related oscillations in thalamic dendrites. Nature Neuroscience 11:683-692. doi: 10.1038/nn.2124
17. David F, Schmiedt JT, Taylor HL, Orban G, di Giovanni G, Uebele VN, Renger JJ, Lambert RC, Leresche N, Crunelli V. 2013. Essential thalamic contribution to slow waves of natural sleep. Journal of Neuroscience 33: 19599-19610. doi: 10.1523/JNEUROSCI.3169-13.2013
18. Deleuze C, Huguenard JR. 2006. Distinct electrical and chemical connectivity maps in the thalamic reticular nucleus: potential roles in synchronization and sensation. Journal of Neuroscience 26:8633-8645. doi: 10.1523/JNEUROSCI.2333-06.2006
19. Destexhe A, Contreras D. 2011. The Fine Structure of Slow-Wave Sleep Oscillations: from Single Neurons to Large Networks. In: Hutt A Sleep and anesthesia. New York, NY: Springer New York; 69-105.
20. Dossi RC, Nuñez A, Steriade M. 1992. Electrophysiology of a slow (0.5-4 hz) intrinsic oscillation of cat thalamocortical neurones in vivo. The Journal of Physiology 447:215-234. doi: 10.1113/jphysiol.1992.sp018999
21. Espinosa F, Torres-Vega MA, Marks GA, Joho RH. 2008. Ablation of Kv3.1 and Kv3.3 potassium channels disrupts thalamocortical oscillations in vitro and in vivo. Journal of Neuroscience 28:5570-5581. doi: 10.1523/JNEUROSCI.0747-08.2008
22. Franks NP. 2008. General anaesthesia: from molecular targets to neuronal pathways of sleep and arousal. Nature Reviews. Neuroscience 9:370-386. doi: 10.1038/nrn2372
23. Giber K, Diana MA, Plattner VM, Dugué GP, Bokor H, Rousseau CV, Maglóczky Z, Havas L, Hangya B, Wildner H, Zeilhofer HU, Dieudonné S, Acsády L. 2015. A subcortical inhibitory signal for behavioral arrest in the thalamus. Nature Neuroscience 18:562-568. doi: 10.1038/nn.3951
24. Guillery RW, Harting JK. 2003. Structure and connections of the thalamic reticular nucleus: advancing views over half a century. The Journal of Comparative Neurology 463:360-371. doi: 10.1002/cne.10738
25. Halassa MM, Chen Z, Wimmer RD, Brunetti PM, Zhao S, Zikopoulos B, Wang F, Brown EN, Wilson MA. 2014. State-dependent architecture of thalamic reticular subnetworks. Cell 158:808-821. doi: 10.1016/j.cell.2014.06.025
26. 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. Nature Neuroscience 14:1118-1120. doi: 10.1038/nn.2880
27. Hartings JA, Temereanca S, Simons DJ. 2003. State-dependent processing of sensory stimuli by thalamic reticular neurons. Journal of Neuroscience 23:5264-5271.
28. Horn BKP, Schunck BG. 1981. Determining optical flow. Artificial Intelligence 17:185-203. doi: 10.1016/0004-3702(81)90024-2
29. Huber R, Deboer T, Tobler I. 2000. Topography of EEG dynamics after sleep deprivation in mice. Journal of Neurophysiology 84:1888-1893.
30. Huber R, Ghilardi MF, Massimini M, Tononi G. 2004. Local sleep and learning. Nature 430:78-81. doi: 10.1038/nature02663
31. Kim A, Latchoumane C, Lee S, Kim GB, Cheong E, Augustine GJ, Shin H-S. 2012. Optogenetically induced sleep spindle rhythms alter sleep architectures in mice. Proceedings of the National Academy of Sciences 109: 20673-20678. doi: 10.1073/pnas.1217897109
32. Krueger JM, Rector DM, Roy S, van Dongen HPA, Belenky G, Panksepp J. 2008. Sleep as a fundamental property of neuronal assemblies. Nature Reviews. Neuroscience 9:910-919. doi: 10.1038/nrn2521
33. Lachaux JP, Rodriguez E, Martinerie J, Varela FJ. 1999. Measuring phase synchrony in brain signals. Human Brain Mapping 8:194-208.
34. Lee S-C, Patrick SL, Richardson KA, Connors BW. 2014. Two functionally distinct networks of gap junction-coupled inhibitory neurons in the thalamic reticular nucleus. Journal of Neuroscience 34:13170-13182. doi: 10.1523/JNEUROSCI.0562-14.2014
35. Lemieux M, Chen J-Y, Lonjers P, Bazhenov M, Timofeev I. 2014. The impact of cortical deafferentation on the neocortical slow oscillation. Journal of Neuroscience 34:5689-5703. doi: 10.1523/JNEUROSCI.1156-13.2014
36. Lewis LD, Weiner VS, Mukamel EA, Donoghue JA, Eskandar EN, Madsen JR, Anderson WS, Hochberg LR, Cash SS, Brown EN, Purdon PL. 2012. Rapid fragmentation of neuronal networks at the onset of propofol-induced unconsciousness. Proceedings of the National Academy of Sciences 109:E3377-E3386. doi: 10.1073/pnas.1210907109
37. Lutkenhoff ES, McArthur DL, Hua X, Thompson PM, Vespa PM, Monti MM. 2013. Thalamic atrophy in antero-medial and dorsal nuclei correlates with six-month outcome after severe brain injury. NeuroImage. Clinical 3: 396-404. doi: 10.1016/j.nicl.2013.09.010
38. Lydic R, Baghdoyan HA. 2005. Sleep, anesthesiology, and the neurobiology of arousal state control. Anesthesiology 103:1268-1295. doi: 10.1097/00000542-200512000-00024
39. Marks GA, Roffwarg HP. 1993. Spontaneous activity in the thalamic reticular nucleus during the sleep/wake cycle of the freely-moving rat. Brain Research 623:241-248. doi: 10.1016/0006-8993(93)91434-T
40. Massimini M, Tononi G, Huber R. 2009. Slow waves, synaptic plasticity and information processing: insights from transcranial magnetic stimulation and high-density EEG experiments. The European Journal of Neuroscience 29:1761-1770. doi: 10.1111/j.1460-9568.2009.06720.x
41. McAlonan K, Cavanaugh J, Wurtz RH. 2008. Guarding the gateway to cortex with attention in visual thalamus. Nature 456:391-394. doi: 10.1038/nature07382
42. McCormick DA, Bal T. 1997. Sleep and arousal: thalamocortical mechanisms. Annual Review of Neuroscience 20: 185-215. doi: 10.1146/annurev.neuro.20.1.185
43. McCormick DA, Pape HC. 1990. Properties of a hyperpolarization-activated cation current and its role in rhythmic oscillation in thalamic relay neurones. The Journal of Physiology 431:291-318. doi: 10.1113/jphysiol.1990.sp018331
44. McNaughton BL, O’Keefe J, Barnes CA. 1983. The stereotrode: a new technique for simultaneous isolation of several single units in the central nervous system from multiple unit records. Journal of Neuroscience Methods 8:391-397. doi: 10.1016/0165-0270(83)90097-3
45. Murphy M, Bruno MA, Riedner BA, Boveroux P, Noirhomme Q, Landsness EC, Brichant JF, Phillips C, Massimini M, Laureys S, Tononi G, Boly M. 2011. Propofol anesthesia and sleep: a high-density EEG study. Sleep 34:283
46. 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. doi: 10.1016/j.neuron.2011.02.043
47. O’Shea SM, Wong LC, Harrison NL. 2000. Propofol increases agonist efficacy at the GABA(A) receptor. Brain Research 852:344-348.
48. Pace-Schott EF, Hobson JA. 2002. The neurobiology of sleep: Genetics, cellular physiology and subcortical networks. Nature Reviews. Neuroscience 3:591-605. doi: 10.1038/nrn895
49. Pinault D. 2004. The thalamic reticular nucleus: Structure, function and concept. Brain Research Reviews 46:1-31. doi: 10.1016/j.brainresrev.2004.04.008
50. Poulet JFA, Fernandez LMJ, Crochet S, Petersen CCH. 2012. Thalamic control of cortical states. Nature Neuroscience 15:370-372. doi: 10.1038/nn.3035
51. Ray S, Maunsell JHR. 2011. Different origins of gamma rhythm and high-gamma activity in macaque visual cortex. PLoS Biology 9:e1000610 doi: 10.1371/journal.pbio.1000610
52. Saper CB, Fuller PM, Pedersen NP, Lu J, Scammell TE. 2010. Sleep state switching. Neuron 68:1023-1042. doi: 10.1016/j.neuron.2010.11.032
53. Saper CB, Scammell TE, Lu J. 2005. Hypothalamic regulation of sleep and circadian rhythms. Nature 437:1257-1263. doi: 10.1038/nature04284
54. Schiff ND. 2008. Central thalamic contributions to arousal regulation and neurological disorders of consciousness. Annals of the New York Academy of Sciences 1129:105-118. doi: 10.1196/annals.1417.029
55. Steriade M, Domich L, Oakson G, Deschênes M. 1987. The deafferented reticular thalamic nucleus generates spindle rhythmicity. Journal of Neurophysiology 57:260-273.
56. Steriade M, Domich L, Oakson G. 1986. Reticularis thalami neurons revisited: activity changes during shifts in states of vigilance. Journal of Neuroscience 6:68-81.
57. Steriade M, Dossi RC, Nuñez A. 1991. Network modulation of a slow intrinsic oscillation of cat thalamocortical neurons implicated in sleep delta waves: cortically induced synchronization and brainstem cholinergic suppression. Journal of Neuroscience 11:3200-3217.
58. Steriade M, Nunez A, Amzica F. 1993. Intracellular analysis of relations between the slow (<1 hz) neocortical oscillation and other sleep rhythms of the electroencephalogram. The Journal of Neuroscience 13.
59. Steriade M, Nuñez A, Amzica F. 1993. A novel slow (< 1 hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components. Journal of Neuroscience 13:3252-3265.
60. Steriade M, Timofeev I, Grenier F. 2001. Natural waking and sleep states: a view from inside neocortical neurons. Journal of Neurophysiology 85:1969-1985.
61. Steriade M. 2000. Corticothalamic resonance, states of vigilance and mentation. Neuroscience 101:243-276. doi: 10.1016/S0306-4522(00)00353-5
62. Todorovic SM, Lingle CJ. 1998. Pharmacological properties of t-type Ca2+ current in adult rat sensory neurons: effects of anticonvulsant and anesthetic agents. Journal of Neurophysiology 79:240-252.
63. Tort ABL, Komorowski R, Eichenbaum H, Kopell N. 2010. Measuring phase-amplitude coupling between neuronal oscillations of different frequencies. Journal of Neurophysiology 104:1195-1210. doi: 10.1152/jn.00106.2010
64. Truccolo W, Eden UT, Fellow M, Donoghue JD, Brown EN. 2005. A point process framework for relating neural spiking activity to spiking history, neural ensemble, and extrinsic covariate effects. Journal of Neurophysiology 93:1074-1089. doi: 10.1152/jn.00697.2004
65. Tsunematsu T, Kilduff TS, Boyden ES, Takahashi S, Tominaga M, Yamanaka A. 2011. Acute optogenetic silencing of orexin/hypocretin neurons induces slow-wave sleep in mice. Journal of Neuroscience 31:10529-10539. doi: 10.1523/JNEUROSCI.0784-11.2011
66. Vyazovskiy VV, Olcese U, Hanlon EC, Nir Y, Cirelli C, Tononi G. 2011. Local sleep in awake rats. Nature 472: 443-447. doi: 10.1038/nature10009
67. Vyazovskiy VV, Olcese U, Lazimy YM, Faraguna U, Esser SK, Williams JC, Cirelli C, Tononi G. 2009. Cortical firing and sleep homeostasis. Neuron 63:865-878. doi: 10.1016/j.neuron.2009.08.024
68. Wang Q, Webber RM, Stanley GB. 2010. Thalamic synchrony and the adaptive gating of information flow to cortex. Nature Neuroscience 13:1534-1541. doi: 10.1038/nn.2670
69. Wang X-J. 1994. Multiple dynamical modes of thalamic relay neurons: rhythmic bursting and intermittent phase-locking. Neuroscience 59:21-31. doi: 10.1016/0306-4522(94)90095-7
70. Wimmer RD, Schmitt LI, Davidson TJ, Nakajima M, Deisseroth K, Halassa MM. 2015. Thalamic control of sensory selection in divided attention. Nature 526:705-709. doi: 10.1038/nature15398
71. Yizhar O, Fenno LE, Davidson TJ, Mogri M, Deisseroth K. 2011. Optogenetics in neural systems. Neuron 71:9-34. doi: 10.1016/j.neuron.2011.06.004
72. Zagha E, Casale AE, Sachdev RNS, McGinley MJ, McCormick DA. 2013. Motor cortex feedback influences sensory processing by modulating network state. Neuron 79:567-578. doi: 10.1016/j.neuron.2013.06.008
73. Zhang Y, Llinas RR, Lisman JE. 2009. Inhibition of NMDARs in the nucleus reticularis of the thalamus produces delta frequency bursting. Frontiers in Neural Circuits 3 doi: 10.3389/neuro.04.020.2009
74. Zhang Y, Yoshida T, Katz DB, Lisman JE. 2012. NMDAR antagonist action in thalamus imposes d oscillations on the hippocampus. Journal of Neurophysiology 107:3181-3189. doi: 10.1152/jn.00072.2012
75. Zhao S, Ting JT, Atallah HE, Qiu L, Tan J, Gloss B, Augustine GJ, Deisseroth K, Luo M, Graybiel AM, Feng G. 2011. Cell type-specific channelrhodopsin-2 transgenic mice for optogenetic dissection of neural circuitry function. Nature Methods 8:745-752. doi: 10.1038/nmeth.1668