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Orexin-Immunopositive Structures in the Thalamic Reticular Nucleus

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Abstract

Orexin-A and orexin-B were immunolocalized in laboratory rodents (adult Wistar and Sprague–Dawley rats, C57Bl/6J mice) in neurons of different areas of the thalamic reticular nucleus, where the level of their immunoreactivity was significantly lower than in neurons of the hypothalamic perifornical area. In Wistar rats, orexin-immunopositive neurons in these brain structures exhibited opposite reactions after 6-h sleep deprivation and 3-h supine immobilization. During the ontogeny of Wistar rats, the thalamic orexin-immunopositive structures emerged already on E18, were still poorly developed on P14, and became definitive on P30, which coincides with the period of ultimate formation of the sleep-wake cycle in rats. These data suggest that orexins of the thalamic reticular nucleus are involved in the regulation of the sleep-wake cycle.

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REFERENCES

  1. de Lecea L, Kilduff TS, Peyron C, Gao X-B, Foye PE, Danielson PE, Fukuhara C, Battenberg ELF, Gautvik V, Bartlett FS, Frankel WN, Van Den Pol AN, Bloom FE, Gautvik KM, Sutcliffe JG (1998) The hypocretins: Hypothalamus-specific peptides with neuroexcitatory activity. Proc Natl Acad Sci USA; Neurobiology 95 (1): 322–327. https://doi.org/10.1073/pnas.95.1.322

    Article  Google Scholar 

  2. Sakurai T, Amemiya A, Ishii M, Matsuzaki I, Chemelli RM, Tanaka H, Williams SC, Richardson JA, Kozlowski GP, Wilson S, Arch JR, Buckingham RE, Haynes AC, Carr SA, Annan RS, McNulty DE, Liu WS, Terrett JA, Elshourbagy NA, Bergsma DJ, Yanagisawa M (1998) Orexins and orexin receptors: a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior. Cell 92 (4): 573-585. https://doi.org/10.1016/s0092-8674(00)80949-6

    Article  CAS  PubMed  Google Scholar 

  3. Nakamura T, Uramura K, Nambu T, Yada T, Goto K, Yanagisawa M, Sakurai T (2000) Orexin-induced hyperlocomotion and stereotypy are mediated by the dopaminergic system. Brain Res 873 (1): 181–187. https://doi.org/10.1016/s0006-8993(00)02555-5

    Article  CAS  PubMed  Google Scholar 

  4. Sakuraia Т (2005) Roles of orexin/hypocretin in regulation of sleep/wakefulness and energy homeostasis. Sleep Medicine Reviews 9(4): 231–241. https://doi.org/10.1016/j.smrv.2004.07.007

    Article  Google Scholar 

  5. Sargin D (2018) The role of the orexin system in stress response. Neuropharmacology 154: 68–78. https://doi.org/10.1016/j.neuropharm.2018.09.034

    Article  CAS  PubMed  Google Scholar 

  6. Waleh NS, Apte-Deshpande A, Terao A, Ding J, Kilduff TS (2001) Modulation of the promoter region of prepro-hypocretin by alpha-interferon. Gene 262 (1–2): 123–128. https://doi.org/10.1016/s0378-1119(00)00544-8

    Article  CAS  PubMed  Google Scholar 

  7. Hara J, Yanagisawa M, Sakurai T (2005) Difference in obesity phenotype between orexin-knockout mice and orexin neuron-deficient mice with same genetic background and environmental conditions. Neurosci Lett 380(3): 239–242. https://doi.org/10.1016/j.neulet.2005.01.046

    Article  CAS  PubMed  Google Scholar 

  8. Morina IYu, Stankova EP, Romanova IV (2020) Effects of prenatal stress on the formation of the orexinergic system of the hypothalamus in rats. Neurosci Behav Physiol 50: 607–617. https://doi.org/10.1007/s11055-020-00942-x

    Article  CAS  Google Scholar 

  9. Lin L, Faraco J, Li R, Kadotani H, Rogers W, Lin X, Qiu X, de Jong PJ, Nishino S, Mignot ES (1999) The sleep disorder canine narcolepsy is caused by a mutation in the hypocretin (orexin) receptor 2 gene. Cell 98 (3): 365–376. https://doi.org/10.1016/s0092-8674(00)81965-0

    Article  CAS  PubMed  Google Scholar 

  10. Chemelli RM, Willie JT, Sinton CM, Elmquist JK, Scammell T, Lee C, Richardson JA, Williams SC, Xiong Y, Kisanuki Y, Fitch TE, Nakazato M, Hammer RE, Saper CB, Yanagisawa M (1999) Narcolepsy in orexin knockout mice: molecular genetics of sleep regulation. Cell 98(4): 437–451. https://doi.org/10.1016/s0092-8674(00)81973-x

    Article  CAS  PubMed  Google Scholar 

  11. Peyron C, Faraco J, Rogers W, Ripley B, Overeem S, Charnay Y, Nevsimalova S, Aldrich M, Reynolds D, Albin R, Li R, Hungs M, Pedrazzoli M, Padigaru M, Kucherlapati M, Fan J, Maki R, Lammers GJ, Bouras C, Kucherlapati R, Nishino S, Mignot E (2000) A mutation in a case of early onset narcolepsy and a generalized absence of hypocretin peptides in human narcoleptic brains. Nature Med 6(9): 991–997. https://doi.org/10.1038/79690

    Article  CAS  PubMed  Google Scholar 

  12. Abrahamson EE, Leak RK, Moore RYT (2001) The suprachiasmatic nucleus projects to posterior hypothalamic arousal systems. Neuroreport 12 (2): 435-440. https://doi.org/10.1097/00001756-200102120-00048

    Article  CAS  PubMed  Google Scholar 

  13. Herrera CG, Cadavieco MC, Jego S, Ponomarenko A, Korotkova T, Adamantidis A (2016) Hypothalamic feedforward inhibition of thalamocortical network controls arousal and consciousness. Nat Neurosci 19: 290–298. https://doi.org/10.1038/nn.4209

    Article  CAS  PubMed  Google Scholar 

  14. Steriade M, Domich L, Oakson G, Deschenes M (1987) The deafferented reticular thalamic nucleus generates spindle rhythmicity. Neurophysiol 57 (1): 260–273. https://doi.org/10.1152/jn.1987.57.1.260

    Article  CAS  Google Scholar 

  15. Guillery RW, Harting JK (2003) Structure and connections of the thalamic reticular nucleus: advancing views over half a century. Comp Neurol 463 (3): 360–371. https://doi.org/10.1002/cne.10738

    Article  CAS  Google Scholar 

  16. Pinault D (2004) The thalamic reticular nucleus: structure, function and concept. Brain Res Rev 46 (1): 1–31. https://doi.org/10.1016/j.brainresrev.2004.04.008

    Article  PubMed  Google Scholar 

  17. Spreafico R, de Curtis M, Frassoni C, Avanzini G (1988) Electrophysiological characteristics of morphologically identified reticular thalamic neurons from rat slices. Neuroscience 27: 629–638. https://doi.org/10.1016/0306-4522(88)90294-1

    Article  CAS  PubMed  Google Scholar 

  18. Houser CR, Vaughn JE, Barber R.P, Roberts E (1980) GABA neurons are the major cell type of the nucleus reticularis thalami. Brain Res 200(2): 341–354. https://doi.org/10.1016/0006-8993(80)90925-7

    Article  CAS  PubMed  Google Scholar 

  19. Lizier C, Spreafico R, Battaglia G (1997) Calretinin in the thalamic reticular nucleus of the rat: distribution and relationship with ipsilateral and contralateral efferents. Comp Neurol 377(2): 217–233. https://doi.org/10.1002/(sici)1096-9861(19970113)377:2<217::aid-cne5>3.0.co;2-6

    Article  CAS  Google Scholar 

  20. Bartho P, Payne JA, Freund TF, Acsady L (2004) Differential distribution of the KCl cotransporter KCC2 in thalamic relay and reticular nuclei. Eur J Neurosci 20(4): 965–975. https://doi.org/10.1111/j.1460-9568.2004.03562.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Contreras-Rodriguez J, Gonzalez-Soriano J, Martinez-Sainz P, Marin-Garcia P, Rodriguez-Veiga E (2003) Neurochemical heterogeneity of the thalamic reticular and perireticular nuclei in developing rabbits: patterns of calbindin expression. Brain Res Dev Brain Res 144(2): 211–221. https://doi.org/10.1016/s0165-3806(03)00194-9

    Article  CAS  PubMed  Google Scholar 

  22. Segerson TP, Hoefler H, Childers H, Wolfe HJ, Wu P, Jackson IM, Lechan RM (1987) Localization of thyrotropin-releasing hormone prohormone messenger ribonucleic acid in rat brain in situ hybridization. Endocrinology 121(1): 98–107. https://doi.org/10.1210/endo-121-1-98

    Article  CAS  PubMed  Google Scholar 

  23. Burgunder JM, Heyberger B, Lauterburg T (1999) Thalamic reticular nucleus parcellation delineated by VIP and TRH gene expression in the rat. Chem Neuroanat 17(3): 147–152. https://doi.org/10.1016/s0891-0618(99)00033-2

    Article  CAS  Google Scholar 

  24. Roland BL, Sutton SW, Wilson SJ, Luo L, Pyati J, Huvar R, Erlander MG, Lovenberg TW (1999) Anatomical distribution of prolactin-releasing peptide and its receptor suggests reticular nucleus regulation of local sleep additional functions in the central nervous system and periphery. Endocrinology 140(12): 5736–5745. https://doi.org/10.1210/en.140.12.5736

    Article  CAS  PubMed  Google Scholar 

  25. Crabtree JW (1996) Organization in the somatosensory sector of the cat’s thalamic reticular nucleus. Comp Neurol 366 (2): 207–222. https://doi.org/10.1002/(SICI)1096-9861(19960304)366:2<207::AID-CNE2>3.0.CO;2-9.26.

    Article  CAS  Google Scholar 

  26. Shosaku A, Sumitomo I (1983) Auditory neurons in the rat thalamic reticular nucleus. Exp Brain Res 49 (3): 432–442. https://doi.org/10.1007/BF00238784

    Article  CAS  PubMed  Google Scholar 

  27. Hayama T, Hashimoto K, Ogawa H (1994) Anatomical location of a taste-related region in the thalamic reticular nucleus in rats. Neurosci Res 18 (4): 291–299. https://doi.org/10.1016/0168-0102(94)90165-1

    Article  CAS  PubMed  Google Scholar 

  28. Stehberg J, Acuna-Goycolea C, Ceric F, Torrealba F (2001) The visceral sector of the thalamic reticular nucleus in the rat. Neuroscience 106 (4): 745–755. https://doi.org/10.1016/s0306-4522(01)00316-5

    Article  CAS  PubMed  Google Scholar 

  29. Vantomme G, Osorio-Forero A, Lüthi A, Fernandez LMJ (2019) Regulation of local sleep by the thalamic reticular nucleus. Front Neurosci 13: 576. https://doi.org/10.3389/fnins.2019.00576

    Article  PubMed  PubMed Central  Google Scholar 

  30. Gonzalo-Ruiz A, Lieberman AR (1995) GABAergic projections from the thalamic reticular nucleus to the anteroventral and anterodorsal thalamic nuclei of the rat. Chem Neuroanat 9 (3): 165–174. https://doi.org/10.1016/0891-0618(95)00078-x

    Article  CAS  Google Scholar 

  31. Zikopoulos B, Barbas H (2007) Circuits for multisensory integration and attentional modulation through the prefrontal cortex and the thalamic reticular nucleus in primates. Rev Neurosci 18 (6):417–438. https://doi.org/10.1515/revneuro.2007.18.6.417

    Article  PubMed  PubMed Central  Google Scholar 

  32. MacDonald EE, Volkoff H (2010) Molecular cloning and characterization of preproorexin in winter skate (Leucoraja ocellata). General and Comparative Endocrinology 169(3): 192–196. https://doi.org/10.1016/j.ygcen.2010.09.014

    Article  CAS  PubMed  Google Scholar 

  33. Romanova IV, Mikhrina AL (2013) Participation of Agouti related peptide in machanisms of wakefulness-sleep cycle regulation. Human Physiology 39(6): 584-589. PMID: 25509169

    Article  Google Scholar 

  34. Morina IYu, Mikhailova EV, Romanova IV (2021) Studies of the effects of monoamines on orexinergic neurons in the hypothalamus of rat embryos. Neurosci Behav Physi 51: 350–356. https://doi.org/10.1007/s11055-021-01078-2

    Article  CAS  Google Scholar 

  35. Paxinos GT, Watson Ch (1998) The rat brain in stereotaxic coordinates. (Fourth Edition). Academic Press. San Diego, California, USA. Int. Standard Book Number: 0-12-547617-5.- CD-ROM. http://www.apnet.com

    Google Scholar 

  36. Paxinos G, Franklin KBJ (2001) The mouse brain in stereotaxic coordinates. Academic press001. Int. Standard Book Number: 0-12-547636-1. – CD-ROM.- http://www.academicpress.com

    Google Scholar 

  37. Coggeshall RE (1964) A Study of diencephalic development in the albino rat. J Comp Neurol 122 (2): 241–299. https://doi.org/10.1002/cne.901220208

    Article  CAS  PubMed  Google Scholar 

  38. Steininger TL, Kilduff TS, Behan M, Benca RM, Landry CF (2004) Comparison of hypocretin/orexin and melanin-concentrating hormone neurons and axonal projections in the embryonic and postnatal rat brain. J Chem Neuroana 27(3): 165–181. https://doi.org/10.1016/j.jchemneu.2004.02.007

    Article  CAS  Google Scholar 

  39. Aristakesian EA (1997) Comparative neurophysiological analysis of the waking-sleeping cycle during the early postnatal ontogeny in rats and guinea pigs. J Evol Biochem Physiol 33(6): 545–550.

    Google Scholar 

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Funding

This work was state budget funded (theme reg. no. ААА-А18-118012290427-7).

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Conceptualization and experimental design (I.V.R.); conducting experiments and data collection (I.Yu.M., I.V.R.); data processing (I.Yu.M.); writing and editing the manuscript (I.V.R.).

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Correspondence to I. V. Romanova.

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Translated by A. Polyanovsky

Russian Text © The Author(s), 2022, published in Rossiiskii Fiziologicheskii Zhurnal imeni I.M. Sechenova, 2022, Vol. 108, No. 7, pp. 836–849https://doi.org/10.31857/S0869813922070056.

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Morina, I.Y., Romanova, I.V. Orexin-Immunopositive Structures in the Thalamic Reticular Nucleus. J Evol Biochem Phys 58, 1099–1109 (2022). https://doi.org/10.1134/S0022093022040135

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