Effects of acute microinjections of thyroid hormone to the preoptic region of euthyroid adult male rats on sleep and motor activity

Brain Research

Volumn 1516, Issue , 2013, Pages 45-54

  Martin, Joseph V ^a,b   Giannopoulos, Phillip F ^a   Moffett, Steven X ^b   James, Thomas D ^b  

^a RUTGERS UNIVERSITY   (United States)

^b USA   (United States)

Author keywords

Nongenomic; Preoptic region; REM; Sleep; Slow wave; Thyroid hormone

Indexed keywords

LIOTHYRONINE;

ANIMAL EXPERIMENT; ARTICLE; CIRCADIAN RHYTHM; CONTROLLED STUDY; CORE TEMPERATURE; DOSE RESPONSE; DRUG MECHANISM; DRUG TISSUE LEVEL; ELECTROENCEPHALOGRAM; HISTOLOGY; HORMONE SENSITIVITY; MALE; MICROINJECTION; MOTOR ACTIVITY; NEUROTRANSMISSION; NONHUMAN; PREOPTIC AREA; PRIORITY JOURNAL; RAT; REGULATORY MECHANISM; REM SLEEP; SLEEP; SLEEP TIME; SLOW WAVE SLEEP; WAKEFULNESS;

ANIMALS; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTROENCEPHALOGRAPHY; ELECTROMYOGRAPHY; HYPOTHYROIDISM; MALE; MOTOR ACTIVITY; PREOPTIC AREA; RATS; RATS, SPRAGUE-DAWLEY; SLEEP STAGES; THYROID GLAND; TIME FACTORS; TRIIODOTHYRONINE; WAKEFULNESS;

RATTUS;

EID: 84878620322     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2013.01.032     Document Type: Article

References (71)

1. D. Belelli, and J.J. Lambert Neurosteroids: endogenous regulators of the GABA(A) receptor Nat. Rev. Neurosci. 6 2005 565 575
2. T.B. Browning, R.W. Atkins, and H. Weiner Cerebral metabolic disturbances in hypothyroidism; clinical and electroencephalographic studies of the psychosis of myxedema and hypothyroidism AMA Arch. Intern. Med. 93 1954 938 950
3. A. Campos-Barros, A. Musa, A. Flechner, C. Hessenius, U. Gaio, H. Meinhold, and A. Baumgartner Evidence for circadian variations of thyroid hormone concentrations and type II 5′-iodothyronine deiodinase activity in the rat central nervous system J. Neurochem. 68 1997 795 803
4. M.A. Caria, M.B. Dratman, L.M. Kow, O. Mameli, and C. Pavlides Thyroid hormone action: nongenomic modulation of neuronal excitability in the hippocampus J. Neuroendocrinol. 21 2009 98 107
5. A.C. Carpenter, and P.S. Timiras Sleep organization in hypo- and hyperthyroid rats Neuroendocrinology 34 1982 438 443
6. R. Chapell, J. Martin, T.K. Machu, and N.J. Leidenheimer Direct channel-gating and modulatory effects of triiodothyronine on recombinant GABA(A) receptors Eur. J. Pharmacol. 349 1998 115 121
7. T.C. Chou, A.A. Bjorkum, S.E. Gaus, J. Lu, T.E. Scammell, and C.B. Saper Afferents to the ventrolateral preoptic nucleus J. Neurosci. 22 2002 977 990
8. V. Cody, P.J. Davis, and F.B. Davis Molecular modeling of the thyroid hormone interactions with alpha v beta 3 integrin Steroids 72 2007 165 170
9. Davis, P.J.; Davis, F.B.; Mousa, S.A.; Luidens, M.K.; Lin, H.Y.; 2011a. Membrane receptor for thyroid hormone: physiologic and pharmacologic implications. Annual Review of Pharmacology and Toxicology, vol 51, 2011. Annual Reviews, Palo Alto, pp. 99-115.
10. P.J. Davis, H.-Y. Lin, S.a. Mousa, M.K. Luidens, A.a. Hercbergs, M. Wehling, and F.B. Davis Overlapping nongenomic and genomic actions of thyroid hormone and steroids Steroids 2011 1 5
11. M.M. Demet, B. Ozmen, A. Deveci, S. Boyvada, H. Adiguzel, and O. Aydemir Depression and anxiety in hyperthyroidism Arch. Med. Res. 33 2002 552 556
12. M.B. Dratman On the mechanism of action of thyroxine, an amino acid analog of tyrosine J. Theor. Biol. 46 1974 225 270
13. M.B. Dratman, F.L. Crutchfield, J. Axelrod, R.W. Colburn, and N. Thoa Localization of triiodothyronine in nerve ending fractions of rat brain Proc. Nat. Acad. Sci. U.S.A. 73 1976 941 944
14. M.B. Dratman, and F.L. Crutchfield Synaptosomal [125 I]triiodothyronine after intravenous [125 I]thyroxine Am. J. Physiol. 235 1978 E638 E647
15. M.B. Dratman, Y. Futaesaku, F.L. Crutchfield, N. Berman, B. Payne, W.E. Stumpf, and M. Sar Iodine125-labeled triiodothyronine in rat brain: evidence for localization in discrete neural systems Science 215 1982 309 312
16. M.B. Dratman, F.L. Crutchfield, J.T. Gordon, and A.S. Jennings Iodothyronine homeostasis in rat brain during hypo- and hyperthyroidism Am. J. Physiol. 245 1983 E189 E193
17. M.B. Dratman, and F.L. Crutchfield Thyroxine, triiodothyronine, and reverse triiodothyronine processing in the cerebellum; Autoradiographic studies in adult rats Endocrinology 125 1989 1723 1733
18. M.B. Dratman, and J.T. Gordon Thyroid hormones as neurotransmitters Thyroid 6 1996 639 647
19. D.L. Dunleavy, I. Oswald, P. Brown, and J.A. Strong Hyperthyroidism, sleep and growth hormone Electroencephalogr. Clin. Neurophysiol. 36 1974 259 263
20. C.I. Eastman, and A. Rechtschaffen Effect of thyroxine on sleep in the rat Sleep 2 1979 215 232
21. C.H. Emerson, C. Liberman, and L.E. Braverman Hypothyroidism W.L. Green, The thyroid 1987 Elsevier New York 219 270 vol.
22. W. Emlen, D.S. Segal, and A.J. Mandell Thyroid state: effects on pre- and postsynaptic central noradrenergic mechanisms Science 175 1972 79 82
23. A. Galeeva, E. Treuter, P. Tuohimaa, and M. Pelto-Huikko Comparative distribution of the mammalian mediator subunit thyroid hormone receptor-associated protein (TRAP220) mRNA in developing and adult rodent brain Eur. J. Neurosci. 16 2002 671 683
24. B. Gereben, A.M. Zavacki, S. Ribich, B.W. Kim, S.A. Huang, W.S. Simonides, A. Zeold, and A.C. Bianco Cellular and molecular basis of deiodinase-regulated thyroid hormone signaling Endocr. Rev. 29 2008 898 938
25. H. Gong, R. Szymusiak, J. King, T. Steininger, and D. McGinty Sleep-related c-Fos protein expression in the preoptic hypothalamus: effects of ambient warming Am. J. Physiol.-Regul. Integrative Comp. Physiol. 279 2000 R2079 R2088
26. H. Gong, D. McGinty, R. Guzman-Marin, K.T. Chew, D. Stewart, and R. Szymusiak Activation of c-fos in GABAergic neurones in the preoptic area during sleep and in response to sleep deprivation J. Physiol.-London 556 2004 935 946
27. J.T. Gordon, D.M. Kaminski, C.B. Rozanov, and M.B. Dratman Evidence that 3,3 ',5-triiodothyronine is concentrated in and delivered from the locus coeruleus to its noradrenergic targets via anterograde axonal transport Neuroscience 93 1999 943 954
28. M.J. Haas, A. Mreyoud, M. Fishman, and A.D. Mooradian Microarray analysis of thyroid hormone-induced changes in mRNA expression in the adult rat brain Neurosci. Lett. 365 2004 14 18
29. U. Hemmeter, B. Rothe, J. Guldner, F. Holsboer, and A. Steiger Effects of thyrotropin-releasing hormone on the sleep EEG and nocturnal hormone secretion in male volunteers Neuropsychobiology 38 1998 25 31
30. H.T. Hermann, and G.C. Quarton Changes in alpha frequency with change in thyroid hormone level Electroencephalogr. Clin. Neurophysiol. 16 1964 515
31. A. Kales, G. Heuser, A. Jacobson, J.D. Kales, J. Hanley, J.R. Zweizig, and M.J. Paulson All night sleep studies in hypothyroid patients, before and after treatment J. Clin. Endocrinol. Metab. 27 1967 1593 1599
32. J. Kohrle, G. Brabant, and R.D. Hesch Metabolism of the thyroid hormones Horm. Res. 26 1987 58 78
33. L. Kruger, S. Saporta, and L.W. Swanson Photographic Atlas of the Rat Brain: The Cell and Fiber Architecture Illustrated in Three Planes with Stereotaxic Coordinates 1995 Cambridge University Press New York
34. S. Kundu, M. Pramanik, S. Roy, J. De, A. Biswas, and A.K. Ray Maintenance of brain thyroid hormone level during peripheral hypothyroid condition in adult rat Life Sci. 79 2006 1450 1455
35. M. Lancel, T.A. Cronlein, P. Muller-Preuss, and F. Holsboer Pregnenolone enhances EEG delta activity during non-rapid eye movement sleep in the rat, in contrast to midazolam Brain Res. 646 1994 85 94
36. R.J. Lohman, L.G. Liu, M. Morris, and T.J. O'Brien Validation of a method for localised microinjection of drugs into thalamic subregions in rats for epilepsy pharmacological studies J. Neurosci. Methods 146 2005 191 197
37. G. Losi, G. Garzon, and G. Puja Nongenomic regulation of glutamatergic neurotransmission in hippocampus by thyroid hormones Neuroscience 151 2008 155 163
38. J.V. Martin, J.M. Cook, T.J. Hagen, and W.B. Mendelson Inhibition of sleep and benzodiazepine receptor binding by a beta-carboline derivative Pharmacol. Biochem. Behav. 34 1989 37 42
39. J.V. Martin, and W.B. Mendelson Benzodiazepines and sleep induction: a possible role of potential-dependent calcium flux in neurons Excerpta Med. Int. Congr. Ser. 839 1990 231 242
40. J.V. Martin, D.B. Williams, R.M. Fitzgerald, H.K. Im, and P.F. Vonvoigtlander Thyroid hormonal modulation of the binding and activity of the GABA(A) receptor complex of brain Neuroscience 73 1996 705 713
41. J.V. Martin, J.M. Padron, M.A. Newman, R. Chapell, N.J. Leidenheimer, and L.A. Burke Inhibition of the activity of the native gamma-aminobutyric acid(A) receptor by metabolites of thyroid hormones: correlations with molecular modeling studies Brain Res. 1004 2004 98 107
42. D. McGinty, and R. Szymusiak Keeping cool: A hypothesis about the mechanisms and functions of slow-wave sleep Trends Neurosci. 13 1990 480 487
43. D. McGinty, M.N. Alam, R. Szymusiak, M. Nakao, and M. Yamamoto Hypothalamic sleep-promoting mechanisms: Coupling to thermoregulation Arch. Ital. Biol. 139 2001 63 75
44. D. McGinty, and R. Szymusiak Brain structures and mechanisms involved in the generation of NREM sleep: focus on the preoptic hypothalamus Sleep Med. Rev. 5 2001 323 342
45. D. McGinty, and R. Szymusiak Hypothalamic regulation of sleep and arousal Front. Biosci. 8 2003 S1074 S1083
46. W.B. Mendelson, R.D. Guthrie, G. Frederick, and R.J. Wyatt The flower pot technique of rapid eye movement (REM) sleep deprivation Pharmacol. Biochem. Behav. 2 1974 553 556
47. W.B. Mendelson, J.V. Martin, M. Perlis, and R. Wagner Enhancement of sleep by microinjection of triazolam into the medial preoptic area Neuropsychopharmacology 2 1989 61 66
48. W.B. Mendelson, and J.V. Martin Characterization of the hypnotic effects of triazolam microinjections into the medial preoptic area Life Sci. 50 1992 1117 1128
49. H. Motulsky Comparing dose-response or kinetic curves with graphpad prism Software Solutions 1998 1 14
50. G. Pinna, O. Brodel, T. Visser, A. Jeitner, H. Grau, M. Eravci, H. Meinhold, and A. Baumgartner Concentrations of seven iodothyronine metabolites in brain regions and the liver of the adult rat Endocrinology 143 2002 1789 1800
51. A.J. Prange Jr.; J.L. Meek, and M.A. Lipton Catecholamines: diminished rate of synth- esis in rat brain and heart after thyroxine pretreatment Life Sci. I 9 1970 901 907
52. G. Puia, and G. Losi Thyroid hormones modulate GABA(A) receptor-mediated currents in hippocampal neurons Neuropharmacology 60 2011 1254 1261
53. C.B. Rozanov, and M.B. Dratman Immunohistochemical mapping of brain triiodothyronine reveals prominent localization in central noradrenergic systems Neuroscience 74 1996 897 915
54. R.J. Salin-Pascual, M. Franco, R. Garcia-Ferrero, J. Vazquez, J. Suarez, L. Sanchez, and A. Jimenez-Anguiano Differences in sleep variables, blood adenosine, and body temperature between hypothyroid and euthyroid rats before and after REM sleep deprivation Sleep 20 1997 957 962
55. C.B. Saper, T.C. Chou, and T.E. Scammell The sleep switch: hypothalamic control of sleep and wakefulness Trends Neurosci. 24 2001 726 731
56. +-ATPase activity in adult rat cerebral cortex Horm. Metab. Res. 25 1993 1 3
57. P.K. Sarkar, and A.K. Ray Synaptosomal T 3 content in cerebral cortex of adult rat in different thyroidal states Neuropsychopharmacology 11 1994 151 155
58. P.K. Sarkar, and A.K. Ray Specific binding of l-triiodothyronine modulates Na+-K+-ATPase activity in adult rat cerebrocortical synaptosomes Neuroreport 9 1998 1149 1152
59. P.K. Sarkar, N.D. Durga, J.J. Morris, and J.V. Martin In vitro thyroid hormone rapidly modulates protein phosphorylation in cerebrocortical synaptosomes from adult rat brain Neuroscience 137 2006 125 132
60. P.K. Sarkar, J.J. Morris, and J.V. Martin Non-genomic effect of l-triiodothyronine on calmodulin-dependent synaptosomal protein phosphorylation in adult rat cerebral cortex Indian J. Exp. Biol. 49 2011 169 176
61. J.E. Silva Thyroid hormone control of thermogenesis and energy balance Thyroid 5 1995 481 492
62. A. Steiger, L. Trachsel, J. Guldner, U. Hemmeter, B. Rothe, R. Rupprecht, H. Vedder, and F. Holsboer Neurosteroid pregnenolone induces sleep-EEG changes in man compatible with inverse agonistic GABAA-receptor modulation Brain Res. 615 1993 267 274
63. N. Suntsova, R. Szymusiak, M.N. Alam, R. Guzman-Marin, and D. McGinty Sleep-waking discharge patterns of median preoptic nucleus neurons in rats J. Physiol.-London 543 2002 665 677
64. R. Szymusiak, and E. Satinoff Ambient temperature-dependence of sleep disturbances produced by basal forebrain damage in rats Brain Res. Bull. 12 1984 295 305
65. A. Uschakov, H. Gong, D. McGinty, and R. Szymusiak Sleep-active neurons in the preoptic area project to the hypothalamic paraventricular nucleus and perifornical lateral hypothalamus Eur. J. Neurosci. 23 2006 3284 3296
66. A. Uschakov, H. Gong, D. McGinty, and R. Szymusiak Efferent projections from the median preoptic nucleus to sleep- and arousal-regulatory nuclei in the rat brain Neuroscience 150 2007 104 120
67. A. Ushigome, M. Nomura, and J. Tanaka Modulation of noradrenaline release in the median preoptic area by GABAergic inputs from the organum vasculosum of the lamina terminalis in the rat Neurochem. Int. 44 2004 139 144
68. T. Watt, M. Groenvold, A.K. Rasmussen, S.J. Bonnema, L. Hegedus, J.B. Bjorner, and U. Feldt-Rasmussen Quality of life in patients with benign thyroid disorders. A review Eur. J. Endocrinol. 154 2006 501 510
69. P.C. Whybrow, and M. Bauer Behavioral and psychiatric aspects of thyrotoxicosis L.E. Braverman, R.D. Utiger, The Thyroid: A Fundamental and Clinical Text 2005 Lippincott Williams and Wilkins Philadephia 644 650
70. K. Yoshida, S. McCormack, R.A. Espana, A. Crocker, and T.E. Scammell Afferents to the orexin neurons of the rat brain J. Comp. Neurol. 494 2006 845 861
71. A.M. Zardetto-Smith, and A.K. Johnson Chemical topography of efferent projections from the median preoptic nucleus to pontine monoaminergic cell groups in the rat Neurosci. Lett. 199 1995 215 219