Chronic nicotine treatment reverses hypothyroidism-induced impairment of L-LTP induction phase: Critical role of CREB

Molecular Neurobiology

Volumn 49, Issue 3, 2014, Pages 1245-1255

  Alzoubi, K H ^a   Alkadhi, K A ^b  

^a JORDAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Jordan)

^b UNIVERSITY OF HOUSTON   (United States)

Author keywords

CaMKIV; ERK1 2; Hypothyroidism; L LTP induction phase; MHFS; Nicotine; P CREB; Rat

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE IV; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; NICOTINE;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; HIPPOCAMPAL CA1 REGION; HYPOTHYROIDISM; LONG TERM POTENTIATION; NONHUMAN; RAT; WESTERN BLOTTING; ANIMAL; DRUG EFFECTS; MALE; PATHOPHYSIOLOGY; PHYSIOLOGY; TREATMENT OUTCOME; WISTAR RAT;

ANIMALS; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; HYPOTHYROIDISM; LONG-TERM POTENTIATION; MALE; NICOTINE; RATS; RATS, WISTAR; TREATMENT OUTCOME;

EID: 84902544731     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-013-8594-4     Document Type: Article

References (92)

1. Levin ED, Conners CK, Silva D, Hinton SC, Meck WH, March J, Rose JE (1998) Transdermal nicotine effects on attention. Psychopharmacology (Berl) 140(2):135-141 (Pubitemid 28538472)
2. 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(2):269-276 (Pubitemid 20249740)
3. Fujii S, Ji Z, Morita N, Sumikawa K (1999) Acute and chronic nicotine exposure differentially facilitate the induction of LTP. Brain Res 846(1):137-143 (Pubitemid 29486450)
4. Aleisa AM, Alzoubi KH, Gerges NZ, Alkadhi KA (2006) Nicotine blocks stress-induced impairment of spatial memory and long-term potentiation of the hippocampal CA1 region. Int J Neuropsychopharmacol 9:417-426 (Pubitemid 43979701)
5. Alzoubi KH, Aleisa AM, Alkadhi KA (2008) The sliding threshold of modification hypothesis: application to the effect of hypothyroidism or chronic psychosocial stress and nicotine on synaptic plasticity. Neurosci Lett 430(3):203-206. doi:10.1016/j.neulet.2007.10.043
6. Alzoubi KH, Aleisa AM, Gerges NZ, Alkadhi KA (2006) Nicotine reverses adult-onset hypothyroidism-induced impairment of learning and memory: behavioral and electrophysiological studies. J Neurosci Res 84(5):944-953. doi:10.1002/jnr.21014 (Pubitemid 44521038)
7. White HK, Levin ED (2004) Chronic transdermal nicotine patch treatment effects on cognitive performance in age-associated memory impairment. Psychopharmacology (Berl) 171(4):465-471 (Pubitemid 38200060)
8. Alzoubi KH, Khabour OF, Salah HA, Abu Rashid BE (2013) The combined effect of sleep deprivation and Western diet on spatial learning and memory: role of BDNF and oxidative stress. J Mol Neurosci 50(1):124-133. doi:10.1007/s12031-012-9881-7
9. Aleisa AM, Alzoubi KH, Alkadhi KA (2011) Post-learning REM sleep deprivation impairs long-term memory: reversal by acute nicotine treatment. Neurosci Lett 499(1):28-31. doi:10.1016/j.neulet.2011.05.025
10. Aleisa AM, Helal G, Alhaider IA, Alzoubi KH, Srivareerat M, Tran TT, Al-Rejaie SS, Alkadhi KA (2011) Acute nicotine treatment prevents REM sleep deprivation-induced learning and memory impairment in rat. Hippocampus 21(8):899-909. doi:10.1002/hipo.20806
11. Alkadhi KA, Alzoubi KH, Srivareerat M, Tran TT (2011) Chronic psychosocial stress exacerbates impairment of synaptic plasticity in beta-amyloid rat model of Alzheimer's disease: prevention by nicotine. Curr Alzheimers Res 8(7):718-731
12. Tran TT, Srivareerat M, Alkadhi KA (2010) Chronic psychosocial stress triggers cognitive impairment in a novel at-risk model of Alzheimer's disease. Neurobiol Dis 37(3):756-763. doi:10.1016/j.nbd.2009.12.016
13. Srivareerat M, Tran TT, Salim S, Aleisa AM, Alkadhi KA (2011) Chronic nicotine restores normal Abeta levels and prevents short-term memory and E-LTP impairment in Abeta rat model of Alzheimer's disease. Neurobiol Aging 32(5):834-844. doi:10.1016/j.neurobiolaging.2009.04.015
14. Newhouse PA, Potter A, Kelton M, Corwin J (2001) Nicotinic treatment of Alzheimer's disease. Biol Psychiatry 49(3):268-278 (Pubitemid 32178436)
15. Levin ED, Wilson W, Rose JE, McEvoy J (1996) Nicotine-haloperidol interactions and cognitive performance in schizophrenics. Neuropsychopharmacology 15(5):429-436 (Pubitemid 26389866)
16. Levin ED, Christopher NC, Briggs SJ, Rose JE (1993) Chronic nicotine reverses working memory deficits caused by lesions of the fimbria or medial basalocortical projection. Brain Res Cogn Brain Res 1(3):137-143 (Pubitemid 23288130)
17. Newhouse PA, Potter A, Levin ED (1997) Nicotinic system involvement in Alzheimer's and Parkinson's diseases. Implications for therapeutics. Drugs Aging 11(3):206-228 (Pubitemid 27421319)
18. Alzoubi KH, Aleisa AM, Alkadhi KA (2007) Nicotine prevents disruption of the late phase LTP-related molecular cascade in adult-onset hypothyroidism. Hippocampus 17(8):654-664. doi:10.1002/hipo.20306 (Pubitemid 47292036)
19. Alzoubi KH, Alkadhi KA (2007) A critical role of CREB in the impairment of late-phase LTP by adult onset hypothyroidism. Exp Neurol 203(1):63-71. doi:10.1016/j.expneurol.2006.07.019 (Pubitemid 44821164)
20. Koromilas C, Liapi C, Schulpis KH, Kalafatakis K, Zarros A, Tsakiris S (2010) Structural and functional alterations in the hippocampus due to hypothyroidism. Metab Brain Dis 25(3):339-354. doi:10.1007/s11011-010-9208-8
21. 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(12):1177-1185 (Pubitemid 34041899)
22. He XS, Ma N, Pan ZL, Wang ZX, Li N, Zhang XC, Zhou JN, Zhu DF, Zhang DR (2011) Functional magnetic resource imaging assessment of altered brain function in hypothyroidism during working memory processing. Eur J Endocrinol 164(6):951-959. doi:10.1530/EJE-11-0046
23. Ge JF, Peng L, Hu CM, Wu TN (2012) Impaired learning and memory performance in a subclinical hypothyroidism rat model induced by hemi-thyroid electrocauterisation. J Neuroendocrinol 24(6):953-961. doi:10.1111/j.1365-2826. 2012.02297.x
24. Alzoubi KH, Gerges NZ, Aleisa AM, Alkadhi KA (2009) Levothyroxin restores hypothyroidism-induced impairment of hippocampus-dependent learning and memory: Behavioral, electrophysiological, and molecular studies. Hippocampus 19(1):66-78. doi:10.1002/hipo.20476
25. 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(1):77-84 (Pubitemid 39119968)
26. Rivas M, Naranjo JR (2007) Thyroid hormones, learning and memory. Genes Brain Behav 6(Suppl 1):40-44 (Pubitemid 46744110)
27. 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(2-3):299-303 (Pubitemid 46770810)
28. Aghili R, Khamseh ME, Malek M, Hadian A, Baradaran HR, Najafi L, Emami Z (2012) Changes of subtests of Wechsler Memory Scale and cognitive function in subjects with subclinical hypothyroidism following treatment with levothyroxine. Arch Med Sci 8(6):1096-1101. doi:10.5114/aoms.2012.32423
29. Mennemeier M, Garner RD, Heilman KM (1993) Memory, mood and measurement in hypothyroidism. J Clin Exp Neuropsychol 15(5):822-831 (Pubitemid 23328976)
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(2):193-208 (Pubitemid 20296013)
31. Leentjens AF, Kappers EJ (1995) Persistent cognitive defects after corrected hypothyroidism. Psychopathology 28(5):235-237
32. Samuels MH, Schuff KG, Carlson NE, Carello P, Janowsky JS (2007) Health status, mood, and cognition in experimentally induced subclinical hypothyroidism. J Clin Endocrinol Metab 92(7):2545-2551 (Pubitemid 47037356)
33. 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(4):325-335
34. Yin JJ, Liao LM, Luo DX, Xu K, Ma SH, Wang ZX, Le HB, Huang RR, Cai ZL, Zhang J (2013) Spatial working memory impairment in subclinical hypothyroidism: an FMRI study. Neuroendocrinology 97(3):260-270. doi:10.1159/000343201
35. Tong H, Chen GH, Liu RY, Zhou JN (2007) Age-related learning and memory impairments in adult-onset hypothyroidism in Kunming mice. Physiol Behav 91(2-3):290-298. doi:10.1016/j.physbeh.2007.03.008
36. Alzoubi KH, Gerges NZ, Alkadhi KA (2005) Levothyroxin restores hypothyroidism-induced impairment of LTP of hippocampal CA1: electrophysiological and molecular studies. Exp Neurol 195(2):330-341 (Pubitemid 41297786)
37. 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(1):40-45 (Pubitemid 38351170)
38. Bliss TV, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361(6407):31-39 (Pubitemid 23020772)
39. Barnes CA (1995) Involvement of LTP inmemory: arewe "searching under the street light"? Neuron 15(4):751-754
40. Frey U, Huang YY, Kandel ER (1993) Effects of cAMP simulate a late stage of LTP in hippocampal CA1 neurons. Science 260(5114):1661-1664 (Pubitemid 23247151)
41. 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(1):69-79
42. 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(6234):554-557 (Pubitemid 19201695)
43. Thomas KL, Laroche S, Errington ML, Bliss TV, Hunt SP (1994) Spatial and temporal changes in signal transduction pathways during LTP. Neuron 13(3):737-745 (Pubitemid 24300177)
44. Roberts LA, Large CH, Higgins MJ, Stone TW, O'Shaughnessy CT, Morris BJ (1998) Increased expression of dendritic mRNA following the induction of long-term potentiation. Brain Res Mol Brain Res 56(1-2):38-44 (Pubitemid 28271659)
45. Pettit DL, Perlman S, Malinow R (1994) Potentiated transmission and prevention of further LTP by increased CaMKII activity in postsynaptic hippocampal slice neurons. Science 266(5192):1881-1885
46. Giese KP, Fedorov NB, Filipkowski RK, Silva AJ (1998) Autophosphorylation at Thr286 of the alpha calcium-calmodulin kinase II in LTP and learning. Science 279(5352):870-873 (Pubitemid 28106282)
47. Lledo PM, Hjelmstad GO, Mukherji S, Soderling TR, Malenka RC, Nicoll RA (1995) Calcium/calmodulin-dependent kinase II and long-term potentiation enhance synaptic transmission by the same mechanism. Proc Natl Acad Sci U S A 92(24):11175-11179
48. 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(5):615-626 (Pubitemid 27152404)
49. Huang YY, Martin KC, Kandel ER (2000) Both protein kinase A and mitogen-activated protein kinase are required in the amygdala for the macromolecular synthesis-dependent late phase of long-term potentiation. J Neurosci 20(17):6317-6325
50. English JD, Sweatt JD (1997) A requirement for the mitogen-activated protein kinase cascade in hippocampal long term potentiation. J Biol Chem 272(31):19103-19106 (Pubitemid 27337694)
51. 2+ stimulation of CREB-dependent transcription and ERK nuclear translocation. Neuron 21(4):869-883
52. Kang H, Sun LD, Atkins CM, Soderling TR, Wilson MA, Tonegawa S (2001) An important role of neural activity-dependent CaMKIV signaling in the consolidation of long-term memory. Cell 106(6):771-783 (Pubitemid 32900667)
53. 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(7):1203-1214 (Pubitemid 27010104)
54. Ho N, Liauw JA, Blaeser F, Wei F, Hanissian S, Muglia LM, Wozniak DF, Nardi A, Arvin KL, Holtzman DM, Linden DJ, Zhuo M, Muglia LJ, Chatila TA (2000) Impaired synaptic plasticity and cAMP response element-binding protein activation in Ca2+/calmodulin-dependent protein kinase type IV/Gr-deficient mice. J Neurosci 20(17):6459-6472
55. Ferguson GD, Storm DR (2004) Why calcium-stimulated adenylyl cyclases? Physiology (Bethesda) 19:271-276 (Pubitemid 39472638)
56. Bach ME, Barad M, Son H, Zhuo M, Lu YF, Shih R, Mansuy I, Hawkins RD, Kandel ER (1999) Age-related defects in spatial memory are correlated with defects in the late phase of hippocampal long-term potentiation in vitro and are attenuated by drugs that enhance the cAMP signaling pathway. Proc Natl Acad Sci U S A 96(9):5280-5285 (Pubitemid 29214574)
57. 2+-stimulated adenylyl cyclases in LTP and memory formation. Int J Dev Neurosci 19(4):387-394
58. 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(4):787-798 (Pubitemid 29411567)
59. Rosenblum K, Futter M, Voss K, Erent M, Skehel PA, French P, Obosi L, Jones MW, Bliss TV (2002) The role of extracellular regulated kinases I/II in late-phase long-term potentiation. J Neurosci 22(13):5432-5441 (Pubitemid 35386465)
60. Barco A, Pittenger C, Kandel ER (2003) CREB, memory enhancement and the treatment of memory disorders: promises, pitfalls and prospects. Expert Opin Ther Targets 7(1):101-114 (Pubitemid 36204592)
61. Alarcon JM, Malleret G, Touzani K, Vronskaya S, Ishii S, Kandel ER, Barco A (2004) Chromatin acetylation, memory, and LTP are impaired in CBP+/- mice: a model for the cognitive deficit in Rubinstein-Taybi syndrome and its amelioration. Neuron 42(6):947-959 (Pubitemid 38798233)
62. 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(5):689-703 (Pubitemid 34245387)
63. Kandel ER (2001) The molecular biology of memory storage: a dialogue between genes and synapses. Science 294(5544):1030-1038
64. Kasahara J, Fukunaga K, Miyamoto E (2001) Activation of calcium/calmodulin-dependent protein kinase IV in long term potentiation in the rat hippocampal CA1 region. J Biol Chem 276(26):24044-24050
65. Tokuda M, Ahmed BY, Lu YF, Matsui H, Miyamoto O, Yamaguchi F, Konishi R, Hatase O (1997) Involvement of calmodulin-dependent protein kinases-I and -IVin long-term potentiation. Brain Res 755(1):162-166 (Pubitemid 27192012)
66. 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 (Pubitemid 40916295)
67. 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(2):250-260 (Pubitemid 34017487)
68. Gerges NZ, Aleisa AM, Schwarz LA, Alkadhi KA (2004) Reduced basal CaMKII levels in hippocampal CA1 region: possible cause of stress-induced impairment of LTP in chronically stressed rats. Hippocampus 14(3):402-410 (Pubitemid 38594413)
69. 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(4):480-490. doi:10.1002/hipo.20073 (Pubitemid 40916295)
70. Tamamaki N, Abe K, Nojyo Y (1988) Three-dimensional analysis of the whole axonal arbors originating from single CA2 pyramidal neurons in the rat hippocampus with the aid of a computer graphic technique. Brain Res 452(1-2):255-272
71. Ishizuka N, Weber J, Amaral DG (1990) Organization of intrahippocampal projections originating from CA3 pyramidal cells in the rat. J Comp Neurol 295(4):580-623 (Pubitemid 20183185)
72. Laurberg S (1979) Commissural and intrinsic connections of the rat hippocampus. J Comp Neurol 184(4):685-708
73. Alzoubi KH, Aleisa AM, Alkadhi KA (2008) Effect of chronic stress or nicotine on hypothyroidism-induced enhancement of LTD: electrophysiological and molecular studies. Neurobiol Dis 32(1):81-87. doi:10.1016/j.nbd.2008.06.008
74. Alzoubi KH, Aleisa AM, Alkadhi KA (2006) Molecular studies on the protective effect of nicotine in adult-onset hypothyroidism-induced impairment of long-term potentiation. Hippocampus 16(10):861-874. doi:10.1002/hipo.20217 (Pubitemid 44650903)
75. Aleisa AM, Alzoubi KH, Gerges NZ, Alkadhi KA (2006) Chronic psychosocial stress-induced impairment of hippocampal LTP: possible role of BDNF. Neurobiol Dis 22(3):453-462 (Pubitemid 43832119)
76. 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(3):393-402 (Pubitemid 39488263)
77. Frey U, Schibler A, Kraemer R (1993) The interrupter technique - a renaissance of a non-invasive approach for lung function testing in infants and children. Agents Actions Suppl 40:64-72 (Pubitemid 23089893)
78. 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(1):59-68
79. 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(5 Pt 1):C1012-C1013
80. 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(5 Pt 1):C1014-C1024 (Pubitemid 29244654)
81. 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(2):511-519 (Pubitemid 29485237)
82. Akaneya Y, Tsumoto T, Kinoshita S, Hatanaka H (1997) Brain-derived neurotrophic factor enhances long-term potentiation in rat visual cortex. J Neurosci 17(17):6707-6716 (Pubitemid 27366623)
83. Minichiello L, Calella AM, Medina DL, Bonhoeffer T, Klein R, Korte M (2002) Mechanism of TrkB-mediated hippocampal long-term potentiation. Neuron 36(1):121-137
84. Korte M, Kang H, Bonhoeffer T, Schuman E (1998) A role for BDNF in the late-phase of hippocampal long-term potentiation. Neuropharmacology 37(4-5):553-559 (Pubitemid 28306944)
85. Mowla SJ, Pareek S, Farhadi HF, Petrecca K, Fawcett JP, Seidah NG, Morris SJ, Sossin WS, Murphy RA (1999) Differential sorting of nerve growth factor and brain-derived neurotrophic factor in hippocampal neurons. J Neurosci 19(6):2069-2080 (Pubitemid 29133385)
86. Balkowiec A, Katz DM (2000) Activity-dependent release of endogenous brain-derived neurotrophic factor from primary sensory neurons detected by ELISA in situ. J Neurosci 20(19):7417-7423
87. Castren E, Pitkanen M, Sirvio J, Parsadanian A, Lindholm D, Thoenen H, Riekkinen PJ (1993) The induction of LTP increases BDNF and NGF mRNA but decreases NT-3 mRNA in the dentate gyrus. Neuroreport 4(7):895-898 (Pubitemid 23202243)
88. Dragunow M, Beilharz E, Mason B, Lawlor P, Abraham W, Gluckman P (1993) Brain-derived neurotrophic factor expression after long-term potentiation. Neurosci Lett 160(2):232-236 (Pubitemid 23294747)
89. Morimoto K, Sato K, Sato S, Yamada N, Hayabara T (1998) Time-dependent changes in neurotrophic factor mRNA expression after kindling and long-term potentiation in rats. Brain Res Bull 45(6):599-605 (Pubitemid 28259031)
90. Patterson SL, Grover LM, Schwartzkroin PA, Bothwell M (1992) Neurotrophin expression in rat hippocampal slices: a stimulus paradigm inducing LTP in CA1 evokes increases in BDNF and NT-3 mRNAs. Neuron 9(6):1081-1088 (Pubitemid 23007179)
91. Springer JE, Gwag BJ, Sessler FM (1994) Neurotrophic factor mRNA expression in dentate gyrus is increased following in vivo stimulation of the angular bundle. Brain Res Mol Brain Res 23(1-2):135-143 (Pubitemid 24090990)
92. Marmigere F, Givalois L, Rage F, Arancibia S, Tapia-Arancibia L (2003) Rapid induction of BDNF expression in the hippocampus during immobilization stress challenge in adult rats. Hippocampus 13(5):646-655. doi:10.1002/hipo. 10109 (Pubitemid 36958287)