Journal of Korean Neurosurgical Society

The Korean Neurosurgical Society (대한신경외과학회)
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Isoflurane Induces Transient Anterograde Amnesia through Suppression of Brain-Derived Neurotrophic Factor in Hippocampus

  • Cho, Han-Jin (Department of Emergency Medicine, Korea University College of Medicine, Ansan Hospital) ;
  • Sung, Yun-Hee (Department of Physical Therapy, Kyungnam University) ;
  • Lee, Seung-Hwan (Department of Neurosurgery, Kyung Hee University College of Medicine, Kyung Hee University Hospital at Gangdong) ;
  • Chung, Jun-Young (Department of Anesthesiology and Pain Medicine, Kyung Hee University College of Medicine, Kyung Hee University Hospital at Gangdong) ;
  • Kang, Jong-Man (Department of Anesthesiology and Pain Medicine, Kyung Hee University College of Medicine, Kyung Hee University Hospital at Gangdong) ;
  • Yi, Jae-Woo (Department of Anesthesiology and Pain Medicine, Kyung Hee University College of Medicine, Kyung Hee University Hospital at Gangdong)
  • Received : 2012.04.12
  • Accepted : 2013.02.25
  • Published : 2013.03.28
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Abstract

Objective : Transient anterograde amnesia is occasionally observed in a number of conditions, including migraine, focal ischemia, venous flow abnormalities, and after general anesthesia. The inhalation anesthetic, isoflurane, is known to induce transient anterograde amnesia. We examined the involvement of brain-derived neurotrophic factor (BDNF) and its receptor tyrosine kinase B (TrkB) in the underlying mechanisms of the isoflurane-induced transient anterograde amnesia. Methods : Adult male Sprague-Dawley rats were divided into three groups : the control group, the 10 minutes after recovery from isoflurane anesthesia group, and the 2 hours after recovery from isoflurane anesthesia group (n=8 in each group). The rats in the isoflurane-exposed groups were anesthetized with 1.2% isoflurane in 75% nitrous oxide and 25% oxygen for 2 hours in a Plexiglas anesthetizing chamber. Short-term memory was determined using the step-down avoidance task. BDNF and TrkB expressions in the hippocampus were evaluated by immunofluorescence staining and western blot analysis. Results : Latency in the step-down avoidance task was decreased 10 minutes after recovery from isoflurane anesthesia, whereas it recovered to the control level 2 hours after isoflurane anesthesia. The expressions of BDNF and TrkB in the hippocampus were decreased immediately after isoflurane anesthesia but were increased 2 hours after isoflurane anesthesia. Conclusion : In this study, isoflurane anesthesia induced transient anterograde amnesia, and the expressions of BDNF and TrkB in the hippocampus might be involved in the underlying mechanisms of this transient anterograde amnesia.

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References

  1. Alonso M, Vianna MR, Depino AM, Mello e Souza T, Pereira P, Szapiro G, et al. : BDNF-triggered events in the rat hippocampus are required for both short- and long-term memory formation. Hippocampus 12 : 551-560, 2002 https://doi.org/10.1002/hipo.10035
  2. Arancio O, Chao MV : Neurotrophins, synaptic plasticity and dementia. Curr Opin Neurobiol 17 : 325-330, 2007 https://doi.org/10.1016/j.conb.2007.03.013
  3. Bartsch T, Schonfeld R, Müller FJ, Alfke K, Leplow B, Aldenhoff J, et al. : Focal lesions of human hippocampal CA1 neurons in transient global amnesia impair place memory. Science 328 : 1412-1415, 2010 https://doi.org/10.1126/science.1188160
  4. Bliss TV, Collingridge GL : A synaptic model of memory : long-term potentiation in the hippocampus. Nature 361 : 31-39, 1993 https://doi.org/10.1038/361031a0
  5. Bortolon RJ, Weglinski MR, Sprung J : Transient global amnesia after general anesthesia. Anesth Analg 101 : 916-919, 2005 https://doi.org/10.1213/01.ANE.0000175208.76574.54
  6. Cunha C, Brambilla R, Thomas KL : A simple role for BDNF in learning and memory? Front Mol Neurosci 3 : 1, 2010
  7. Dutton RC, Maurer AJ, Sonner JM, Fanselow MS, Laster MJ, Eger EI 2nd : Isoflurane causes anterograde but not retrograde amnesia for pavlovian fear conditioning. Anesthesiology 96 : 1223-1229, 2002 https://doi.org/10.1097/00000542-200205000-00027
  8. Jia F, Pignataro L, Harrison NL : GABAA receptors in the thalamus : alpha4 subunit expression and alcohol sensitivity. Alcohol 41 : 177-185, 2007 https://doi.org/10.1016/j.alcohol.2007.03.010
  9. Kesner RP, Goodrich-Hunsaker NJ : Developing an animal model of human amnesia : the role of the hippocampus. Neuropsychologia 48 : 2290-2302, 2010 https://doi.org/10.1016/j.neuropsychologia.2009.10.027
  10. Kim H, Lee SH, Kim SS, Yoo JH, Kim CJ : The influence of maternal treadmill running during pregnancy on short-term memory and hippocampal cell survival in rat pups. Int J Dev Neurosci 25 : 243-249, 2007 https://doi.org/10.1016/j.ijdevneu.2007.03.003
  11. Kim SE, Ko IG, Kim BK, Shin MS, Cho S, Kim CJ, et al. : Treadmill exercise prevents aging-induced failure of memory through an increase in neurogenesis and suppression of apoptosis in rat hippocampus. Exp Gerontol 45 : 357-365, 2010 https://doi.org/10.1016/j.exger.2010.02.005
  12. Kohara K, Kitamura A, Morishima M, Tsumoto T : Activity-dependent transfer of brain-derived neurotrophic factor to postsynaptic neurons. Science 291 : 2419-2423, 2001 https://doi.org/10.1126/science.1057415
  13. Koponen E, Voikar V, Riekki R, Saarelainen T, Rauramaa T, Rauvala H, et al. : Transgenic mice overexpressing the full-length neurotrophin receptor trkB exhibit increased activation of the trkB-PLCgamma pathway, reduced anxiety, and facilitated learning. Mol Cell Neurosci 26 : 166-181, 2004 https://doi.org/10.1016/j.mcn.2004.01.006
  14. Lee E, Son H : Adult hippocampal neurogenesis and related neurotrophic factors. BMB Rep 42 : 239-244, 2009 https://doi.org/10.5483/BMBRep.2009.42.5.239
  15. Lu LX, Yon JH, Carter LB, Jevtovic-Todorovic V : General anesthesia activates BDNF-dependent neuroapoptosis in the developing rat brain. Apoptosis 11 : 1603-1615, 2006 https://doi.org/10.1007/s10495-006-8762-3
  16. Lu Y, Christian K, Lu B : BDNF : a key regulator for protein synthesis-dependent LTP and long-term memory? Neurobiol Learn Mem 89 : 312-323, 2008 https://doi.org/10.1016/j.nlm.2007.08.018
  17. Ma YL, Wang HL, Wu HC, Wei CL, Lee EH : Brain-derived neurotrophic factor antisense oligonucleotide impairs memory retention and inhibits long-term potentiation in rats. Neuroscience 82 : 957-967, 1998
  18. Martin SJ, Grimwood PD, Morris RG : Synaptic plasticity and memory : an evaluation of the hypothesis. Annu Rev Neurosci 23 : 649-711, 2000 https://doi.org/10.1146/annurev.neuro.23.1.649
  19. Minichiello L, Korte M, Wolfer D, Kühn R, Unsicker K, Cestari V, et al. : Essential role for TrkB receptors in hippocampus-mediated learning. Neuron 24 : 401-414, 1999 https://doi.org/10.1016/S0896-6273(00)80853-3
  20. Mizuno M, Yamada K, Olariu A, Nawa H, Nabeshima T : Involvement of brain-derived neurotrophic factor in spatial memory formation and maintenance in a radial arm maze test in rats. J Neurosci 20 : 7116-7121, 2000
  21. Mu JS, Li WP, Yao ZB, Zhou XF : Deprivation of endogenous brain-derived neurotrophic factor results in impairment of spatial learning and memory in adult rats. Brain Res 835 : 259-265, 1999 https://doi.org/10.1016/S0006-8993(99)01592-9
  22. Munte S, Schmidt M, Meyer M, Nager W, Lüllwitz E, Münte TF, et al. : Implicit memory for words played during isoflurane- or propofol-based anesthesia : the lexical decision task. Anesthesiology 96 : 588-594, 2002 https://doi.org/10.1097/00000542-200203000-00013
  23. Murer MG, Yan Q, Raisman-Vozari R : Brain-derived neurotrophic factor in the control human brain, and in Alzheimer's disease and Parkinson's disease. Prog Neurobiol 63 : 71-124, 2001 https://doi.org/10.1016/S0301-0082(00)00014-9
  24. Perouansky M, Rau V, Ford T, Oh SI, Perkins M, Eger EI 2nd, et al. : Slowing of the hippocampal ${\theta}$ rhythm correlates with anesthetic-induced amnesia. Anesthesiology 113 : 1299-1309, 2010 https://doi.org/10.1097/ALN.0b013e3181f90ccc
  25. Pietropaolo S, Paterna JC, Bueler H, Feldon J, Yee BK : Bidirectional changes in water-maze learning following recombinant adenovirus-associated viral vector (rAAV)-mediated brain-derived neurotrophic factor expression in the rat hippocampus. Behav Pharmacol 18 : 533-547, 2007 https://doi.org/10.1097/FBP.0b013e3282da0bf6
  26. Rau V, Iyer SV, Oh I, Chandra D, Harrison N, Eger EI 2nd, et al. : Gamma-aminobutyric acid type A receptor alpha 4 subunit knockout mice are resistant to the amnestic effect of isoflurane. Anesth Analg 109 : 1816-1822, 2009 https://doi.org/10.1213/ANE.0b013e3181bf6ae6
  27. Saarelainen T, Pussinen R, Koponen E, Alhonen L, Wong G, Sirviö J, et al. : Transgenic mice overexpressing truncated trkB neurotrophin receptors in neurons have impaired long-term spatial memory but normal hippocampal LTP. Synapse 38 : 102-104, 2000 https://doi.org/10.1002/1098-2396(200010)38:1<102::AID-SYN11>3.0.CO;2-K
  28. Schinder AF, Poo M : The neurotrophin hypothesis for synaptic plasticity. Trends Neurosci 23 : 639-645, 2000 https://doi.org/10.1016/S0166-2236(00)01672-6
  29. Shekhar R : Transient global amnesia--a review. Int J Clin Pract 62 : 939-942, 2008 https://doi.org/10.1111/j.1742-1241.2007.01564.x
  30. Sung YH, Shin MS, Cho S, Baik HH, Jin BK, Chang HK, et al. : Depression-like state in maternal rats induced by repeated separation of pups is accompanied by a decrease of cell proliferation and an increase of apoptosis in the hippocampus. Neurosci Lett 470 : 86-90, 2010 https://doi.org/10.1016/j.neulet.2009.12.063
  31. Twersky RS, Hartung J, Berger BJ, McClain J, Beaton C : Midazolam enhances anterograde but not retrograde amnesia in pediatric patients. Anesthesiology 78 : 51-55, 1993 https://doi.org/10.1097/00000542-199301000-00009
  32. Wade JG, Stevens WC : Isoflurane: an anesthetic for the eighties? Anesth Analg 60 : 666-682, 1981
  33. Waterhouse EG, Xu B : New insights into the role of brain-derived neurotrophic factor in synaptic plasticity. Mol Cell Neurosci 42 : 81-89, 2009 https://doi.org/10.1016/j.mcn.2009.06.009
  34. Werner DF, Swihart A, Rau V, Jia F, Borghese CM, McCracken ML, et al. : Inhaled anesthetic responses of recombinant receptors and knockin mice harboring ${\alpha}2$(S270H/L277A) GABA(A) receptor subunits that are resistant to isoflurane. J Pharmacol Exp Ther 336 : 134-144, 2011 https://doi.org/10.1124/jpet.110.170431
  35. Yu Q, Wang H, Chen J, Gao Y, Liang W : Neuroprotections and mechanisms of inhalational anesthetics against brain ischemia. Front Biosci (Elite Ed) 2 : 1275-1298, 2010

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