Experimentally induced hyperthyroidism disrupts hippocampal long-term potentiation in adult rats

Neuroendocrinology

Volumn 94, Issue 3, 2011, Pages 218-227

  Taşkin, Eylem ^a   Artis, A Seda ^a   Bitiktas, Soner ^a   Dolu, Nazan ^a   Liman, Narin ^a   Süer, Cem ^a  

^a ERCIYES UNIVERSITY   (Turkey)

Author keywords

Hippocampal formations; Hyperthyroidism; Long term potentiation; Spatial memory task performance

Indexed keywords

LEVOTHYROXINE; TUNGSTEN; URETHAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CONTROLLED STUDY; ELECTRODE; EXCITATORY POSTSYNAPTIC POTENTIAL; GRANULE CELL; HIPPOCAMPUS POTENTIAL; HYPERTHYROIDISM; IN VIVO STUDY; LEARNING DISORDER; LEARNING TEST; LONG TERM POTENTIATION; MALE; NONHUMAN; PERFORANT NERVE TRACT; PRIORITY JOURNAL; RAT; SPATIAL MEMORY; TASK PERFORMANCE;

AGE FACTORS; ANIMALS; BEHAVIOR, ANIMAL; DISEASE MODELS, ANIMAL; ELECTROPHYSIOLOGICAL PHENOMENA; HIPPOCAMPUS; HYPERTHYROIDISM; LONG-TERM POTENTIATION; MALE; MAZE LEARNING; MEMORY DISORDERS; RATS; RATS, WISTAR; THYROID HORMONES; THYROXINE;

EID: 81355149744     PISSN: 00283835     EISSN: 14230194     Source Type: Journal    
DOI: 10.1159/000328513     Document Type: Article

References (58)

1. Okada T, Yamada N, Tsuzuki K, Horikawa HPM, Tanaka K, Ozawa S: Long-term potentiation in the hippocampal CA1 area and dentate gyrus plays different roles in spatial learning. Eur J Neurosci 2003; 17: 341-349. (Pubitemid 36459514)
2. Hernandez-Rabaza V, Barcia JA, Llorens-Martin M, Trejo JL, Canales JJ: Spared place and object-place learning but limited spatial working memory capacity in rats with selective lesions of the dentate gyrus. Brain Res Bull 2007; 72: 315-323. (Pubitemid 46602755)
3. Eyre MD, Richter-Levin G, Avital A, Stewart MG: Morphological changes in hippocampal dentate gyrus synapses following spatial learning in rats are transient. Eur J Neurosci 2003; 17: 1973-1980. (Pubitemid 36645347)
4. Aisa B, Elizalde N, Tordera R, Lasheras B, Del Rio J, Ramirez MJ: Effects of neonatal stress on markers of synaptic plasticity in the hippocampus: implications for spatial memory. Hippocampus 2009; 19: 1222-1231.
5. van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage FH: Functional neurogenesis in the adult hippocampus. Nature 2002; 415: 1030-1034. (Pubitemid 34193451)
6. Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH: Neurogenesis in the adult human hippocampus. Nat Med 1998; 4: 1313-1317. (Pubitemid 28512114)
7. Kempermann G, Gage FH: Neurogenesis in the adult hippocampus; in Chadwick DJ, Goode JA (eds): Neural Transplantation in Neurodegenerative Disease: Current Status and New Directions. Novartis Foundation Symp 2000; 231: 220-235.
8. Cameron HA, Woolley CS, McEwen BS, Gould E: Differentiation of newly born neurons and glia in the dentate gyrus of the adult-rat. Neuroscience 1993; 56: 337-344. (Pubitemid 23274753)
9. Seki T, Arai Y: Highly polysialylated neural cell-adhesion molecule (NCAM-H) is expressed by newly generated granule cells in the dentate gyrus of the adult-rat. J Neurosci 1993; 13: 2351-2358. (Pubitemid 23151752)
10. Zhang LQ, Blomgren K, Kuhn HG, Cooper-Kuhn CM: Effects of postnatal thyroid hormone deficiency on neurogenesis in the juvenile and adult rat. Neurobiol Dis 2009; 34: 366-374.
11. Kaplan MS, Bell DH: Mitotic neuroblasts in the 9-day-old and 11-month-old rodent hippocampus. J Neurosci 1984; 4: 1429-1441. (Pubitemid 14058662)
12. Okano HJ, Pfaff DW, Gibbs RB: Rb and cdc2 expression in brain-correlations with h-3 thymidine incorporation and neurogenesis. J Neurosci 1993; 13: 2930-2938. (Pubitemid 23199220)
13. Stanfield BB, Trice JE: Evidence that granule cells generated in the dentate gyrus of adultrats extend axonal projections. Exp Brain Res 1988; 72: 399-406.
14. Gould E, Allan MD, McEwen BS: Dendritic spine density of adult hippocampal pyramidal cells is sensitive to thyroid-hormone. Brain Res 1990; 525: 327-329. (Pubitemid 20257756)
15. Schinder AF, Gage FH: A hypothesis about the role of adult neurogenesis in hippocampal function. Physiology 2004; 19: 253-261. (Pubitemid 39472636)
16. Shors TJ, Matzel LD: Long-term potentiation: what's learning got to do with it? Behav Brain Sci 1997; 20: 597-614.
17. Madsen TM, Kristjansen PEG, Bolwig TG, Wortwein G: Arrested neuronal proliferation and impaired hippocampal function following fractionated brain irradiation in the adult rat. Neuroscience 2003; 119: 635-642. (Pubitemid 36694791)
18. Santarelli L, Saxe M, Gross C, Surget A, Battaglia F, Dulawa S, Weisstaub N, Lee J, Duman R, Arancio O, Belzung C, Hen R: Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 2003; 301: 805-809. (Pubitemid 36962615)
19. Porterfield SP, Hendry LB: Impact of PCBs on thyroid hormone directed brain development. Toxicol Indust Health 1998; 14: 103-120. (Pubitemid 28044972)
20. Anderson GW, Schoonover CM, Jones SA: Control of thyroid hormone action in the developing rat brain. Thyroid 2003; 13: 1039-1056. (Pubitemid 37464557)
21. Rami A, Patel AJ, Rabie A: Thyroid-hormone and development of the rat hippocampus-morphological alterations in granule and pyramidal cells. Neuroscience 1986; 19: 1217-1226. (Pubitemid 17217016)
22. Rami A, Rabie A, Patel AJ: Thyroid-hormone and development of the rat hippocampus-cell acquisition in the dentate gyrus. Neuroscience 1986; 19: 1207-1216. (Pubitemid 17217015)
23. Madeira MD, Cadeteleite A, Andrade JP, Paulabarbosa MM: Effects of hypothyroidism upon the granular layer of the dentate gyrus in male and female-adult rats-a morphometric study. J Comp Neurol 1991; 314: 171-186.
24. Madeira MD, Sousa N, Limaandrade MT, Calheiros F, Cadeteleite A, Paulabarbosa MM: Selective vulnerability of the hippocampal pyramidal neurons to hypothyroidism in male and female rats. J Comp Neurol 1992; 322: 501-518.
25. Alva-Sanchez C, Ortiz-Butron R, Pacheco-Rosado J: Kainic acid does not affect ca3 hippocampal region pyramidal cells in hypothyroid rats. Brain Res Bull 2004; 63: 167-171. (Pubitemid 38591400)
26. Montero-Pedrazuela A, Venero C, Lavado-Autric R, Fernandez-Lamo I, Garcia-Verdugo JM, Bernal J, Guadano-Ferraz A: Modulation of adult hippocampal neurogenesis by thyroid hormones: implications in depressive-like behavior. Mol Psychiatry 2006; 11: 361-371.
27. Desouza LA, Ladiwala U, Daniel SM, Agashe S, Vaidya RA, Vaidya VA: Thyroid hormone regulates hippocampal neurogenesis in the adult rat brain. Mol Cell Neurosci 2005; 29: 414-426. (Pubitemid 40799214)
28. Lauder JM, Mugnaini E: Infrapyramidal mossy fibers in the hippocampus of the hyper-thyroid rat-a light and electron-microscopic study. Dev Neurosci 1980; 3: 248-265. (Pubitemid 11243192)
29. Lipp HP, Schwegler H, Crusio WE, Wolfer DP, Leisingertrigona MC, Heimrich B, Driscoll P: Using genetically-defined rodent strains for the identification of hippocampal traits relevant for 2-way avoidance-behavior-a non-invasive approach. Experientia 1989; 45: 845-859. (Pubitemid 19230427)
30. Schwegler H, Crusio WE, Lipp HP, Brust I, Mueller GG: Early postnatal hyperthyroidism alters hippocampal circuitry and improves radial-maze learning in adult mice. J Neurosci 1991; 11: 2102-2106.
31. Sala-Roca J, Estebanez-Perpina E, Balada F, Garau A, Marti-Carbonell MA: Effects of adult dysthyroidism on the morphology of hippocampal neurons. Behav Brain Res 2008; 188: 348-354.
32. Anthony A, Adams PM, Stein SA: The effects of congenital hypothyroidism using the hyt/hyt mouse on locomotor-activity and learned behavior. Horm Behav 1993; 27: 418-433. (Pubitemid 23281961)
33. Adams PM, Stein SA, Palnitkar M, Anthony A, Gerrity L, Shanklin DR: Evaluation and characterization of the hypothyroid hyt/hyt mouse. 1. Somatic and behavioral studies. Neuroendocrinology 1989; 49: 138-143. (Pubitemid 19083000)
34. Akaike M, Kato N, Ohno H, Kobayashi T: Hyperactivity and spatial maze-learning impairment of adult-rats with temporary neonatal-hypothyroidism. Neurotoxicol Teratol 1991; 13: 317-322.
35. MacNabb C, O'Hare E, Cleary J, Georgopoulos AP: Congenital hypothyroidism impairs response alternation discrimination behavior. Brain Res 1999; 847: 231-239.
36. Pavlides C, Westlind-Danielsson AI, Nyborg H, McEwen BS: Neonatal hyperthyroidism disrupts hippocampal LTP and spatiallearning. Exp Brain Res 1991; 85: 559-564.
37. Oguro K, Ito M, Tsuda H, Mutoh K, Shiraishi H, Shirasaka Y, Mikawa H: Interactions of thyroid-hormones with L-( 3 H)glutamate binding-sites, with special reference to Nmethyl-D-aspartate receptors. Res Commun Chem Pathol Pharmacol 1989; 65: 181-196. (Pubitemid 19214449)
38. Lee PR, Brady D, Koenig JI: Thyroid hormone regulation of N-methyl-D-aspartic acid receptor subunit mRNA expression in adult brain. J Neuroendocrinol 2003; 15: 87-92. (Pubitemid 36149918)
39. Losi G, Garzon G, Puja G: Nongenomic regulation of glutamatergic neurotransmission in hippocampus by thyroid hormones. Neuroscience 2008; 151: 155-163.
40. Bliss TVP, Collingridge GL: A synaptic model of memory-long-term potentiation in the hippocampus. Nature 1993; 361: 31-39. (Pubitemid 23020772)
41. Gerges NZ, Alkadhi KA: Hypothyroidism impairs late LTP in CA1 region but not in dentate gyrus of the intact rat hippocampus: Mapk involvement. Hippocampus 2004; 14: 40-45. (Pubitemid 38351170)
42. Fernandez-Lamo I, Montero-Pedrazuela A, Delgado-Garcia JM, Guadano-Ferraz A, Gruart A: Effects of thyroid hormone replacement on associative learning and hippocampal synaptic plasticity in adult hypothyroid rats. Eur J Neurosci 2009; 30: 679-692.
43. Gilbert ME, Paczkowski C: Propylthiouracil (PTU)-induced hypothyroidism in the developing rat impairs synaptic transmission and plasticity in the dentate gyrus of the adult hippocampus. Dev Brain Res 2003; 145: 19-29. (Pubitemid 38368638)
44. Gilbert ME, Sui L: Dose-dependent reductions in spatial learning and synaptic function in the dentate gyrus of adult rats following developmental thyroid hormone insufficiency. Brain Res 2006; 1069: 10-22. (Pubitemid 43145893)
45. Vara H, Martinez B, Santos A, Colino A: Thyroid hormone regulates neurotransmitter release in neonatal rat hippocampus. Neuroscience 2002; 110: 19-28. (Pubitemid 34214756)
46. Conrad CD, Galea LAM, Kuroda Y, McEwen BS: Chronic stress impairs rat spatial memory on the Y maze, and this effect is blocked by tianeptine pretreatment. Behav Neurosci 1996; 110: 1321-1334. (Pubitemid 27009196)
47. Conrad CD, Grote KA, Hobbs RJ, Ferayorni A: Sex differences in spatial and non-spatial Y-maze performance after chronic stress. Neurobiol Learn Memory 2003; 79: 32-40. (Pubitemid 36071188)
48. Wright RL, Conrad CD: Enriched environment prevents chronic stress-induced spatial learning and memory deficits. Behav Brain Res 2008; 187: 41-47. (Pubitemid 350216189)
49. Mamiya T, Ukai M: [gly(14)]-humanin improved the learning and memory impairment induced by scopolamine in vivo. Br J Pharmacol 2001; 134: 1597-1599. (Pubitemid 34038091)
50. Colicos MA, Dash PK: Apoptotic morphology of dentate gyrus granule cells following experimental cortical impact injury in rats: possible role in spatial memory deficits. Brain Res 1996; 739: 120-131. (Pubitemid 26387370)
51. Caria MA, Dratman MB, Kow LM, Mameli O, Pavlides C: Thyroid hormone action: Nongenomic modulation of neuronal excitability in the hippocampus. J Neuroendocrinol 2009; 21: 98-107.
52. MacDonald JF, Jackson MF, Beazely MA: G protein-coupled receptors control nmdars and metaplasticity in the hippocampus. Biochim Biophys Acta-Biomembranes 2007; 1768: 941-951. (Pubitemid 46452551)
53. Tang YP, Ma YL, Chen SK, Lee EH: mRNA differential display identification of thyroid hormone-responsive protein (THRP) gene in association with early phase of long-term potentiation. Hippocampus 2001; 11: 637-646. (Pubitemid 34065492)
54. Rami A, Rabie A: Effect of thyroid-deficiency on the development of glia in the hippocampal-formation of the rat-an immunocytochemical study. Glia 1988; 1: 337-345.
55. Smith JW, Evans AT, Costall B, Smythe JW: Thyroid hormones, brain function and cognition: a brief review. Neurosci Biobehav Rev 2002; 26: 45-60. (Pubitemid 34130533)
56. Hökfelt T, Tsuruo Y, Ulfhake B, Cullheim S, Arvidsson U, Foster GA, Schultzberg M, Schalling M, Arborelius L, Freedman J, Post C, Visser T: Distribution of TRH-like immunoreactivity with special reference to coexistence with other neuroactive compounds. Ann NY Acad Sci 1989; 553: 76-105. (Pubitemid 19259383)
57. Ishihara K, Katsuki H, Sugimura M, Satoh M: Ym-14673, a new thyrotropin-releasinghormone analog, augments long-term potentiation in the mossy fiber-ca3 system of guinea-pig hippocampal slices. J Pharmacobio-Dynam 1992; 15: 75-78.
58. Atzori M, Nistri A: Effects of thyrotropinreleasing hormone on gabaergic synaptic transmission of the rat hippocampus. Eur J Neurosci 1996; 8: 1299-1305. (Pubitemid 26174655)