Nicotine reverses adult-onset hypothyroidism-induced impairment of learning and memory: Behavioral and electrophysiological studies

Journal of Neuroscience Research

Volumn 84, Issue 5, 2006, Pages 944-953

  Alzoubi, K H ^a   Aleisa, A M ^b   Gerges, N Z ^a,c   Alkadhi, K A ^a  

^a UNIVERSITY OF HOUSTON   (United States)

^b KING SAUD UNIVERSITY   (Saudi Arabia)

^c MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

Hypothyroidism; Learning and memory; Nicotine

Indexed keywords

NICOTINE; THYROTROPIN; THYROXINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BEHAVIORAL SCIENCE; BRAIN ELECTROPHYSIOLOGY; CONTROLLED STUDY; DRUG EFFECT; EXTRACELLULAR SPACE; HIPPOCAMPUS; HYPOTHYROIDISM; LEARNING DISORDER; LONG TERM CARE; LONG TERM MEMORY; LONG TERM POTENTIATION; MALE; MAZE TEST; MEMORY CONSOLIDATION; MEMORY DISORDER; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; RAT; SHORT TERM MEMORY; SYNAPTIC TRANSMISSION; THYROIDECTOMY; THYROTROPIN BLOOD LEVEL;

ACTION POTENTIALS; ANIMALS; BEHAVIOR, ANIMAL; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, RADIATION; ELECTRIC STIMULATION; EXCITATORY POSTSYNAPTIC POTENTIALS; HIPPOCAMPUS; HYPOTHYROIDISM; LEARNING DISORDERS; MALE; MAZE LEARNING; MEMORY DISORDERS; NICOTINE; NICOTINIC AGONISTS; RATS; RATS, WISTAR; SPATIAL BEHAVIOR; THYROIDECTOMY; TIME FACTORS;

EID: 33749487621     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.21014     Document Type: Article

References (71)

1. Aleisa AM, Alzoubi KH, Alkadhi KA. 2006a. Nicotine prevents stress-induced enhancement of long-term depression in hippocampal area CA1: electrophysiological and molecular studies. J Neurosci Res 83:309-317.
2. Aleisa AM, Alzoubi KH, Gerges NZ, Alkadhi KA. 2006b. Chronic psychosocial stress-induced impairment of LTP: possible role of BDNF. Neurobiol Dis 22:453-462.
3. Aleisa AM, Alzoubi KH, Gerges NZ, Alkadhi KA. 2006c. Nicotine blocks stress-induced impairment of spatial memory and long-term potentiation of the hippocampal CA1 region. Int J Neuropsychopharmacol 9:417-426.
4. Alkondon M, Braga MF, Pereira EF, Maelicke A, Albuquerque EX. 2000. Alpha7 nicotinic acetylcholine receptors and modulation of gabaergic synaptic transmission in the hippocampus. Eur J Pharmacol 393:59-67.
5. Alonso M, Vianna MR, Depino AM, Mello e Souza T, Pereira P, Szapiro G, Viola H, Pitossi F, Izquierdo I, Medina JH. 2002. BDNF-triggered events in the rat hippocampus are required for both short- and long-term memory formation. Hippocampus 12:551-560.
6. Alzoubi KH, Alkadhi KA. 2006. The critical role of CREB in the impairment of late phase LTP by adult onset hypothyroidism. Exp Neurol (in press).
7. 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.
8. 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.
9. Bancroft A, Levin ED. 2000. Ventral hippocampal alpha4beta2 nicotinic receptors and chronic nicotine effects on memory. Neuropharmacology 39:2770-2778.
10. Benowitz NL. 1986. Clinical pharmacology of nicotine. Annu Rev Med 37:21-32.
11. Benowitz NL, Jacob P 3rd, Denaro C, Jenkins R. 1991. Stable isotope studies of nicotine kinetics and bioavailability. Clin Pharmacol Ther 49:270-277.
12. Bettany JH, Levin ED. 2001. Ventral hippocampal alpha 7 nicotinic receptor blockade and chronic nicotine effects on memory performance in the radial-arm maze. Pharmacol Biochem Behav 70:467-474.
13. Bliss TV, Collingridge GL. 1993. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31-39.
14. Cao J, Chen N, Xu T, Xu L. 2004. Stress-facilitated LTD induces out-put plasticity through synchronized-spikes and spontaneous unitary discharges in the CA1 region of the hippocampus. Neurosci Res 49:229-239.
15. 2+ dependent mechanism. Neuropharmacology 39:2799-2807.
16. 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.
17. Dunne MP, Macdonald D, Hartley LR. 1986. The effects of nicotine upon memory and problem solving performance. Physiol Behav 37:849-854.
18. Enderlin V, Alfos S, Pallet V, Garcin H, Azais-Braesco V, Jaffard R, Higueret P. 1997. Aging decreases the abundance of retinoic acid (RAR) and triiodothyronine (TR) nuclear receptor mRNA in rat brain: effect of the administration of retinoids. FEBS Lett 412:629-632.
19. Fujii S, Ji Z, Morita N, Sumikawa K. 1999. Acute and chronic nicotine exposure differentially facilitate the induction of LTP. Brain Res 846:137-143.
20. 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.
21. 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.
22. Gerges NZ, Aleisa AM, Schwarz LA, Alkadhi KA. 2003. Chronic psychosocial stress decreases calcineurin in the dentate gyrus: a possible mechanism for preservation of early ltp. Neuroscience 117:869-874.
23. Gerges NZ, Aleisa AM, Schwarz LA, Alkadhi KA. 2004a. Reduced basal CaMKII levels in hippocampal CA1 region: possible cause of stress-induced impairment of LTP in chronically stressed rats. Hippocampus 14:402-410.
24. Gerges NZ, Alzoubi KH, Park CR, Diamond DM, Alkadhi KA. 2004b. Adverse effect of the combination of hypothyroidism and chronic psychosocial stress on hippocampus-dependent memory in rats. Behav Brain Res 155:77-84.
25. 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.
26. Grant SG, O'Dell TJ, Karl KA, Stein PL, Soriano P, Kandel ER. 1992. Impaired long-term potentiation, spatial learning, and hippocampal development in fyn mutant mice. Science 258:1903-1910.
27. Gray R, Rajan AS, Radcliffe KA, Yakehiro M, Dani JA. 1996. Hippocampal synaptic transmission enhanced by low concentrations of nicotine. Nature 383:713-716.
28. Hinds HL, Tonegawa S, Malinow R. 1998. CA1 long-term potentiation is diminished but present in hippocampal slices from alpha-CaMKII mutant mice. Learn Mem 5:344-354.
29. Jacob P 3rd, Benowitz NL, Shulgin AT. 1988. Recent studies of nicotine metabolism in humans. Pharmacol Biochem Behav 30:249-253.
30. Ji D, Lape R, Dani JA. 2001. Timing and location of nicotinic activity enhances or depresses hippocampal synaptic plasticity. Neuron 31:131-141.
31. Kandel ER, Schwartz JH. 2001. Principles of neural science. Amsterdam: Elsevier/North-Holland.
32. Kenny PJ, File SE, Rattray M. 2000. Acute nicotine decreases, and chronic nicotine increases the expression of brain-derived neurotrophic factor mRNA in rat hippocampus. Brain Res Mol Brain Res 85:234-238.
33. Kiprianova I, Sandkuhler J, Schwab S, Hoyer S, Spranger M. 1999. Brain-derived neurotrophic factor improves long-term potentiation and cognitive functions after transient forebrain ischemia in the rat. Exp Neurol 159:511-519.
34. Klann E, Thiels E. 1999. Modulation of protein kinases and protein phosphatases by reactive oxygen species: implications for hippocampal synaptic plasticity. Prog Neuropsychopharmacol Biol Psychiatry 23:359-376.
35. Le Houezec J, Jacob P 3rd, Benowitz NL. 1993. A clinical pharmacological study of subcutaneous nicotine. Eur J Clin Pharmacol 44:225-230.
36. Levin ED, Castonguay M, Ellison GD. 1987. Effects of the nicotinic receptor blocker mecamylamine on radial-arm maze performance in rats. Behav Neural Biol 48:206-212.
37. Levin ED, Lee C, Rose JE, Reyes A, Ellison G, Jarvik M, Gritz E. 1990. Chronic nicotine and withdrawal effects on radial-arm maze performance in rats. Behav Neural Biol 53:269-276.
38. Levin ED, Briggs SJ, Christopher NC, Rose JE. 1993a. Chronic nicotinic stimulation and blockade effects on working memory. Behav Pharmacol 4:179-182.
39. Levin ED, Christopher NC, Briggs SJ, Rose JE. 1993b. Chronic nicotine reverses working memory deficits caused by lesions of the fimbria or medial basalocortical projection. Brain Res Cogn Brain Res 1:137-143.
40. Levin ED, Kim P, Meray R. 1996a. Chronic nicotine working and reference memory effects in the 16-arm radial maze: interactions with D1 agonist and antagonist drugs. Psychopharmacology 127:25-30.
41. Levin ED, Wilson W, Rose JE, McEvoy J. 1996b. Nicotine-haloperidol interactions and cognitive performance in schizophrenics. Neuropsychopharmacology 15:429-436.
42. Levin ED, Christopher NC, Briggs SJ. 1997. Chronic nicotinic agonist and antagonist effects on T-maze alternation. Physiol Behav 61:863-866.
43. Levin ED, Conners CK, Silva D, Hinton SC, Meek WH, March J, Rose JE. 1998. Transdermal nicotine effects on attention. Psychopharmacology 140: 135-141.
44. Levin ED, Conners CK, Silva D, Canu W, March J. 2001. Effects of chronic nicotine and methylphenidate in adults with attention deficit/hyperactivity disorder. Exp Clin Psychopharmacol 9:83-90.
45. 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.
46. Lynch MA. 2004. Long-term potentiation and memory. Physiol Rev 84:87-136.
47. Maggio R, Riva M, Vaglini F, Fornai F, Molteni R, Armogida M, Racagni G, Corsini GU. 1998. Nicotine prevents experimental parkinsonism in rodents and induces striatal increase of neurotrophic factors. J Neurochem 71:2439-2446.
48. Mansvelder HD, McGehee DS. 2000. Long-term potentiation of excitatory inputs to brain reward areas by nicotine. Neuron 27:349-357.
49. Matsuyama S, Matsumoto A, Enomoto T, Nishizaki T. 2000. Activation of nicotinic acetylcholine receptors induces long-term potentiation in vivo in the intact mouse dentate gyrus. Eur J Neurosci 12:3741-3747.
50. 2+ concentration, and neurotoxicity and increase antioxidant enzyme activities in hippocampal neurons. J Neurochem 65:1740-1751.
51. Mons N, Enderlin V, Jaffard R, Higueret P. 2001. Selective age-related changes in the PKC-sensitive, calmodulin-binding protein, neurogranin, in the mouse brain. J Neurochem 79:859-867.
52. Morris RG, Garrud P, Rawlins JN, O'Keefe J. 1982. Place navigation impaired in rats with hippocampal lesions. Nature 297:681-683.
53. Newhouse PA, Potter A, Levin ED. 1997. Nicotinic system involvement in Alzheimer's and Parkinson's diseases. Implications for therapeutics. Drugs Aging 11:206-228.
54. Newhouse PA, Potter A, Kelton M, Corwin J. 2001. Nicotinic treatment of Alzheimer's disease. Biol Psychiatry 49:268-278.
55. Norris CM, Halpain S, Foster TC. 1998. Alterations in the balance of protein kinase/phosphatase activities parallel reduced synaptic strength during aging. J Neurophysiol 80:1567-1570.
56. Park S, Knopick C, McGurk S, Meltzer HY. 2000. Nicotine impairs spatial working memory while leaving spatial attention intact. Neuropsychopharmacology 22:200-209.
57. Parrott AC, Winder G. 1989. Nicotine chewing gum (2 mg, 4 mg) and cigarette smoking: comparative effects upon vigilance and heart rate. Psychopharmacology 97:257-261.
58. Prendergast MA, Harris BR, Mayer S, Holley RC, Pauly JR, Littleton JM. 2001. Nicotine exposure reduces N-methyl-D-aspartate toxicity in the hippocampus: relation to distribution of the alpha? nicotinic acetylcholine receptor subunit. Med Sci Monit 7:1153-1160.
59. Reisner E, Heyman A, Weinberg T, Dawson D, Ciftan E. 1983. Lack of association between Alzheimer's disease and histocompatibility antigens. Tissue Antigens 21:31-34.
60. Sawin CT, Chopra D, Azizi F, Mannix JE, Bacharach P. 1979. The aging thyroid. Increased prevalence of elevated serum thyrotropin levels in the elderly. JAMA 242:247-250.
61. Silva AJ, Stevens CF, Tonegawa S, Wang Y. 1992. Deficient hippocampal long-term potentiation in alpha-calcium-calmodulin kinase II mutant mice. Science 257:201-206.
62. Sorenson CA, Raskin LA, Suh Y. 1991. The effects of prenatal nicotine on radial-arm maze performance in rats. Pharmacol Biochem Behav 40:991-993.
63. Squire LR. 1993. The hippocampus and spatial memory. Trends Neurosci 16:56-57.
64. Sutherland MK, Wong L, Somerville MJ, Handley P, Yoong L, Bergeron C, McLachlan DR. 1992. Reduction of thyroid hormone receptor c-ERB A alpha mRNA levels in the hippocampus of Alzheimer compared with Huntington brain. Neurobiol Aging 13:301-312.
65. Vara H, Munoz-Cuevas J, Colino A. 2003. Age-dependent alterations of long-term synaptic plasticity in thyroid-deficient rats. Hippocampus 13:816-825.
66. 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.
67. Wesnes K, Warburton DM. 1984. Effects of scopolamine and nicotine on human rapid information processing performance. Psychopharmacology 82:147-150.
68. White HK, Levin ED. 1999. Four-week nicotine skin patch treatment effects on cognitive performance in Alzheimer's disease. Psychopharmacology 143:158-165.
69. White HK, Levin ED. 2004. Chronic transdermal nicotine patch treatment effects on cognitive performance in age-associated memory impairment. Psychopharmacology 171:465-471.
70. Yamagata T, Satoh T, Ishikawa Y, Nakatani A, Yamada M, Ikeuchi T, Hatanaka H. 1999. Brain-derived neurotropic factor prevents superoxide anion-induced death of PC12h cells stably expressing TrkB receptor via modulation of reactive oxygen species. Neurosci Res 35:9-17.
71. Yang CH, Huang CC, Hsu KS. 2004. Behavioral stress modifies hippocampal synaptic plasticity through corticosterone-induced sustained extracellular signal-regulated kinase/mitogen-activated protein kinase activation. J Neurosci 24:11029-11034.