Levothyroxin restores hypothyroidism-induced impairment of hippocampus-dependent learning and memory: Behavioral, electrophysiological, and molecular studies

Hippocampus

Volumn 19, Issue 1, 2009, Pages 66-78

  Alzoubi, Karem H ^a   Gerges, Nashaat Z ^b   Aleisa, Abdulaziz M ^c   Alkadhi, Karim A ^b  

^a JORDAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Jordan)

^b UNIVERSITY OF HOUSTON   (United States)

^c KING SAUD UNIVERSITY   (Saudi Arabia)

Author keywords

CA1; CaMKIV; CERB; ERK; L LTP; MAPK; Maze; n NOS; Rat

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; LEVOTHYROXINE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR; COGNITION; COGNITIVE DEFECT; CONTROL GROUP; CONTROLLED STUDY; ELECTROPHYSIOLOGY; HIPPOCAMPUS; HYPOTHYROIDISM; IMMUNOBLOTTING; LEARNING; LONG TERM MEMORY; LONG TERM POTENTIATION; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; SHORT TERM MEMORY; TASK PERFORMANCE; THYROIDECTOMY; WESTERN BLOTTING;

ANIMALS; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; HIPPOCAMPUS; HYPOTHYROIDISM; LEARNING; LONG-TERM POTENTIATION; MALE; MAP KINASE SIGNALING SYSTEM; MAZE LEARNING; MEMORY; MEMORY DISORDERS; RATS; RATS, WISTAR; THYROXINE; TREATMENT OUTCOME;

EID: 58149469365     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.20476     Document Type: Article

References (72)

1. Abel T, Nguyen PV, Barad M, Deuel TA, Kandel ER, Bourtchouladze R. 1997. Genetic demonstration of a role for PKA in the late phase of LTP and in hippocampus-based long-term memory. Cell 88:615-626,
2. Adams JP, Roberson ED, English JD, Selcher JC, Sweatt JD. 2000. MAPK regulation of gene expression in the central nervous system. Acta Neurobiol Exp (Wars) 60:377-394.
3. Alzoubi KH, Alkadhi KA. 2007. A critical role of CREB in the impairment of late-phase LTP by adult onset hypothyroidism. Exp Neurol 203:63-71.
4. Alzoubi KH, Bedawi AS, Aleisa AM, Alkadhi KA. 2004. Hypothyroidism impairs long-term potentiation in sympathetic ganglia: Electrophysiologic and molecular studies. J Neurosci Res 78:393-402.
5. Alzoubi KH, Gerges NZ, Alkadhi KA. 2005. Levothyroxin restores hypothyroidism-induced impairment of LTP of hippocampal CA1: electrophysiological and molecular studies. Exp Neurol 195:330-341.
6. Alzoubi KH, Aleisa AM, Alkadhi KA. 2006a. Molecular studies on the protective effect of nicotine in adult-onset hypothyroidisminduced impairment of long-term potentiation. Hippocampus 16:861-874,
7. Alzoubi KH, Aleisa AM, Gerges NZ, Alkadhi KA. 2006b. Nicotine reverses adult-onset hypothyroidism-induced impairment of learning and memory: Behavioral and electrophysiological studies. J Neurosci Res 84:944-953.
8. Alzoubi KH, Aleisa AM, Alkadhi KA. 2007. Nicotine prevents disruption of the late5r phase LTP-related molecular cascade in adultonset hypothyroidism. Hippocampus 17:654-664.
9. Astur RS, Taylor LB, Mamelak AN, Philpott L, Sutherland RJ. 2002. Humans with hippocampus damage display severe spatial memory impairments in a virtual Morris water task. Behav Brain Res 132: 77-84.
10. Baldini IM, Vita A, Mauri MC, Amodei V, Carrisi M, Bravin S, Cantalamessa L. 1997. Psychopathological and cognitive features in subclinical hypothyroidism. Prog Neuropsychopharmacol Biol Psychiatry 21:925-935.
11. Barco A, Alarcon JM, Kandel ER, 2002. Expression of constitutively active CREB protein facilitates the late phase of long-term potentiation by enhancing synaptic capture. Cell 108:689-703.
12. Bito H, Deisseroth K, Tsien RW. 1996. CREB phosphorylation and dephosphorylation: A Ca(2+)- and stimulus duration-dependent switch for hippocampal gene expression. Cell 87:1203-1214.
13. Bliss TV, Collingridge GL. 1993. A synaptic model of memory: Longterm potentiation in the hippocampus. Nature 361:31-39.
14. Bourtchuladze R, Frenguelli B, Blendy J, Cioffi D, Schutz G, Silva AJ. 1994. Deficient long-term memory in mice with a targeted mutation of the cAMP-responsive element-binding protein. Cell 79: 59-68.
15. Bozon B, Davis S, Laroche S. 2003. A requirement for the immediate early gene zif268 in reconsolidation of recognition memory after retrieval. Neuron 40:695-701.
16. Brent GA. 1999. Thyroid hormone action: Down novel paths. Focus on "thyroid hormone induces activation of mitogen-activated protein kinase in cultured cells". Am J Physiol 276:C1012-C1013.
17. Buresova O, Bures J, Oitzl MS, Zahalka A. 1985. Radial maze in the water tank: An aversively motivated spatial working memory task. Physiol Behav 34:1003-1005.
18. Burgess N, Maguire EA, O'Keefe J. 2002. The human hippocampus and spatial and episodic memory. Neuron 35:625-641.
19. Burmeister LA, Ganguli M, Dodge HH, Toczek T, DeKosky ST, Nebes RD. 2001. Hypothyroidism and cognition: preliminary evidence for a specific defect in memory. Thyroid 11:1177-1185.
20. Capet C, Jego A, Denis P, Noel D, Clerc I, Cornier AC, Lefebvre H, Levesque H, Chassagne P, Bercoff E, Doucet J. 2000, Is cognitive change related to hypothyroidism reversible with replacement therapy? Rev Med Interne 21:672-678.
21. Diamond DM, Fleshner M, Ingersoll N, Rose GM. 1996. Psychological stress impairs spatial working memory: Relevance to electrophysiological studies of hippocampal function. Behav Neurosci 110:661-672,
22. Diamond DM, Park CR, Heman KL, Rose GM. 1999. Exposing rats to a predator impairs spatial working memory in the radial arm water maze. Hippocampus 9:542-552.
23. Frey U, Huang YY, Kandel ER, 1993a. Effects of cAMP simulate a late stage of LTP in hippocampal CA1 neurons. Science 260:1661-1664.
24. Frey U, Schibler A, Kraemer R. 1993b. The interrupter technique-a renaissance of a non-invasive approach for lung function testing in infants and children. Agents Actions Suppl 40:64-72.
25. Gerges NZ, Alkadhi KA. 2004. Hypothyroidism impairs late LTP in CA1 region but not in dentate gyrus of the intact rat hippocampus: MAPK involvement. Hippocampus 14:40-45.
26. Gerges NZ, Stringer JL, Alkadhi KA. 2001. Combination of hypothyroidism and stress abolishes early LTP in the CA1 but not dentate gyrus of hippocampus of adult rats. Brain Res 922:250-260.
27. Gerges NZ, Alzoubi KH, Park CR, Diamond DM, Alkadhi KA. 2004. Adverse effect of the combination of hypothyroidism and chronic psychosocial stress on hippocampus-dependent memory in rats. Behav Brain Res 155:77-84.
28. Gerges NZ, Alzoubi KH, Alkadhi KA. 2005. Role of phosphorylated CaMKII and calcineurin in the differential effect of hypothyroidism on LTP of CA1 and dentate gyrus. Hippocampus 15:480-490.
29. Ghosh M, Gharami K, Paul S, Das S. 2005. Thyroid hormoneinduced morphological differentiation and maturation of astrocytes involves activation of protein kinase A, ERK signalling pathway. Eur J Neurosci 22:1609-1617.
30. Haggerty JJ Jr, Garbutt JC, Evans DL, Golden RN, Pedersen C, Simon JS, Nemeroff CB. 1990. Subclinical hypothyroidism: A review of neuropsychiatric aspects. Int J Psychiatry Med 20:193-208.
31. He J, Yamada K, Zou LB, Nabeshima T. 2001. Spatial memory deficit and neurodegeneration induced by the direct injection of okadaic acid into the hippocampus in rats. J Neural Transm 108:1435-1443.
32. 2+/calmodulin-dependent protein kinase type IV/Gr-deficient mice. J Neurosci 20:6459-6472.
33. Hodges H. 1996. Maze procedures: The radial-arm and water maze compared. Brain Res Cogn Brain Res 3:167-181.
34. Huang YY, Li XC, Kandel ER. 1994. cAMP contributes to mossy fiber LTP by initiating both a covalently mediated early phase and macromolecular synthesis-dependent late phase. Cell 79:69-79.
35. Hyde LA, Hoplight BJ, Denenberg VH, 1998. Water version of the radial-arm maze: Learning in three inbred strains of mice. Brain Res 785:236-244.
36. 2+ stimulation of CREB-dependent transcription and ERK nuclear translocation. Neuron 21:869-883.
37. Jaeschke R, Guyatt G, Gerstein H, Patterson C, Molloy W, Cook D, Harper S, Griffith L, Carbotte R. 1996. Does treatment with L-thyroxine influence health status in middle-aged and older adults with subclinical hypothyroidism? J Gen Intern Med 11:744-749.
38. Jensovsky J, Ruzicka E, Spackova N, Hejdukova B. 2002. Changes of event related potential and cognitive processes in patients with subclinical hypothyroidism after thyroxine treatment. Endocr Regul 36:115-122.
39. Kandel ER. 2001. The molecular biology of memory storage: a dialogue between genes and synapses. Science 294:1030-1038.
40. Kudrjavcev T. 1978. Neurologic complications of thyroid dysfunction. Adv Neurol 19:619-636.
41. Lai CL, Lin RT, Tai CT, Liu CK, Howng SL. 2000. The recovery potential of central conduction disorder in hypothyroid rats. J Neurol Sci 173:113-119.
42. Lansing RW, Trunnell JB. 1963. Electroencephalographic changes accompanying thyroid deficiency in man. J Clin Endocrinol Metab 23:470-480.
43. Larson EB, Reifler BV, Sumi SM, Canfield CG, Chinn NM. 1985. Diagnostic evaluation of 200 elderly outpatients with suspected dementia. J Gerontol 40:536-543.
44. Leentjens AF, Kappers EJ. 1995. Persistent cognitive defects after corrected hypothyroidism. Psychopathology 28:235-237.
45. Lin HY, Davis FB, Gordinier JK, Martino LJ, Davis PJ. 1999. Thyroid hormone induces activation of mitogen-activated protein kinase in cultured cells. Am J Physiol 276:C1014-C1024.
46. Lopes da Silva FH, Gorter JA, Wadman WJ. 1986. Kindling of the hippocampus induces spatial memory deficits in the rat. Neurosci Lett 63:115-120.
47. Malenka RC, Kauer JA, Perkel DJ, Mauk MD, Kelly PT, Nicoll RA, Waxham MN. 1989. An essential role for postsynaptic calmodulin and protein kinase activity in long-term potentiation. Nature 340: 554-557.
48. Mennemeier M, Garner RD, Heilman KM. 1993. Memory, mood and measurement in hypothyroidism. J Clin Exp Neuropsychol 15: 822-831.
49. Miller KJ, Parsons TD, Whybrow PC, van Herle K, Rasgon N, van Herle A, Martinez D, Silverman DH, Bauer M. 2006. Memory improvement with treatment of hypothyroidism. Int J Neurosci 116: 895-906.
50. Mons N, Guillou JL, Decorte L, Jaffard R. 2003. Spatial learning induces differential changes in calcium/calmodulin-stimulated (ACI) and calcium-insensitive (ACII) adenylyl cyclases in the mouse hippocampus. Neurobiol Learn Mem 79:226-235.
51. Monzani F, Del Guerra P, Caraccio N, Pruned CA, Pucci E, Luisi M, Baschieri L. 1993. Subclinical hypothyroidism: Neurobehavioral features and beneficial effect of L-thyroxine treatment, Clin Investig 71:367-371.
52. Morris RG, Garrud P, Rawlins JN, O'Keefe J. 1982. Place navigation impaired in rats with hippocampal lesions. Nature 297:681-683.
53. Nishitani H, Kooi KA. 1968. Cerebral evoked responses in hypothyroidism. Electroencephalogr Clin Neurophysiol 24:554-560.
54. Osterweil D, Syndulko K, Cohen SN, Pettler-Jennings PD, Hershman JM, Cummings JL, Tourtellotte WW, Solomon DH. 1992. Cognitive function in non-demented older adults with hypothyroidism. J Am Geriatr Soc 40:325-335.
55. Park CR, Campbell AM, Diamond DM. 2001. Chronic psychosocial stress impairs learning and memory and increases sensitivity to yohimbine in adult rats. Biol Psychiatry 50:994-1004.
56. 2+-stimulated adenylyl cyclases in LTP, memory formation. Int J Dey Neurosci 19:387-394.
57. Prinz PN, Scanlan JM, Vitaliano PR Moe KE, Borson S, Toiyola B, Merriam GR, Larsen LH, Reed HL. 1999. Thyroid hormones: Positive relationships with cognition in healthy, euthyroid older men. J Gerontol A Biol Sci Med Sci 54:M111-M116.
58. Reid RE, Kim EM, Page D, O'Mara SM, O'Hare E. 2007. Thyroxine replacement in an animal model of congenital hypothyroidism. Physiol Behav 91:299-303.
59. Rivas M, Naranjo JR. 2007. Thyroid hormones, learning and memory. Genes Brain Behav 6(Suppl 1):40-44.
60. Samuels MH, Schuff KG, Carlson NE, Carello P, Janowsky JS. 2007a. Health status, mood, and cognition in experimentally induced subclinical hypothyroidism. J Clin Endocrinol Metab 92:2545-2551.
61. Samuels MH, Schuff KG, Carlson NE, Carello P, Janowsky JS. 2007b. Health status, psychological symptoms, mood, and cognition in L-thyroxine-treated hypothyroid subjects. Thyroid 17:249-258.
62. Sherry DF, Jacobs LF, Gaulin SJ. 1992. Spatial memory and adaptive specialization of the hippocampus. Trends Neurosci 15:298-303.
63. Shukitt-Hale B, McEwen JJ, Szprengiel A, Joseph JA. 2004. Effect of age on the radial arm water maze-a test of spatial learning and memory. Neurobiol Aging 25:223-229.
64. Smith JW, Evans AT, Costall B, Smythe JW. 2002. Thyroid hormones, brain function and cognition: a brief review, Neurosci Biobehav Rev 26:45-60.
65. Squire LR. 1993. The hippocampus and spatial memory. Trends Neurosci 16:56-57.
66. Sui L, Anderson WL, Gilbert ME. 2005. Impairment in short-term but enhanced long-term synaptic potentiation and ERK activation in adult hippocampal area CA1 following developmental thyroid hormone insufficiency. Toxicol Sci 85:647-656.
67. Sui L, Wang F, Liu F, Wang J, Li BM. 2006. Dorsal hippocampal administration of triiodothyronine enhances long-term memory for trace cued and delay contextual fear conditioning in rats. J Neuroendocrinol 18:811-819.
68. Tang YP, Ma YL, Chen SK, Lee EH. 2001. mRNA differential display identification of thyroid hormone-responsive protein (THRP) gene in association with early phase of long-term potentiation. Hippocampus 11:637-646.
69. Treadway CR, Prange AJ Jr, Doehne EF, Edens CJ, Whybrow PC. 1967. Myxedema psychosis: clinical and biochemical changes during recovery. J Psychiatr Res 5:289-296.
70. Tremont G, Stern RA. 1997. Use of thyroid hormone to diminish the cognitive side effects of psychiatric treatment. Psychopharmacol Bull 33:273-280.
71. Wekking EM, Appelhof BC, Fliers E, Schene AH, Huyser J, Tijssen JG, Wiersinga WM. 2005. Cognitive functioning and well-being in euthyroid patients on thyroxine replacement therapy for primary hypothyroidism. Eur J Endocrinol 153:747-753.
72. Wong ST, Athos J, Figueroa XA, Pineda VV, Schaefer ML, Chavkin CC, Muglia LJ, Storm DR. 1999. Calcium-stimulated adenylyl cyclase activity is critical for hippocampus-dependent long-term memory and late phase LTP. Neuron 23:787-798.