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Isoflurane mediated neuropathological and cognitive impairments in the triple transgenic Alzheimer’s mouse model are associated with hippocampal synaptic deficits in an age-dependent manner


Autoři: Donald J. Joseph aff001;  Chunxia Liu aff001;  Jun Peng aff001;  Ge Liang aff001;  Huafeng Wei aff001
Působiště autorů: Department of Anesthesiology and Critical Care, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, United States of America aff001;  Department of Anesthesiology, China-Japan Friendship Hospital, Beijing, China aff002;  Department of Anesthesiology, sun Yat-sen Memorial Hospital, Sun Yat-Sen University, Guangzhou, China aff003
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0223509

Souhrn

Many in vivo studies suggest that inhalational anesthetics can accelerate or prevent the progression of neuropathology and cognitive impairments in Alzheimer Disease (AD), but the synaptic mechanisms mediating these ambiguous effects are unclear. Here, we show that repeated exposures of neonatal and old triple transgenic AD (3xTg) and non-transgenic (NonTg) mice to isoflurane (Iso) distinctly increased neurodegeneration as measured by S100β levels, intracellular Aβ, Tau oligomerization, and apoptotic markers. Spatial cognition measured by reference and working memory testing in the Morris Water Maze (MWM) were altered in young NonTg and 3xTg. Field recordings in the cornu ammonis 1 (CA1) hippocampus showed that neonatal control 3xTg mice exhibited hypo-excitable synaptic transmission, reduced paired-pulse facilitation (PPF), and normal long-term potentiation (LTP) compared to NonTg controls. By contrast, the old control 3xTg mice exhibited hyper-excitable synaptic transmission, enhanced PPF, and unstable LTP compared to NonTg controls. Repeated Iso exposures reduced synaptic transmission and PPF in neonatal NonTg and old 3xTg mice. LTP was normalized in old 3xTg mice, but reduced in neonates. By contrast, LTP was reduced in old but not neonatal NonTg mice. Our results indicate that Iso-mediated neuropathologic and cognitive defects in AD mice are associated with synaptic pathologies in an age-dependent manner. Based on these findings, the extent of this association with age and, possibly, treatment paradigms warrant further study.

Klíčová slova:

Alzheimer's disease – Anesthetics – Cognitive impairment – Mice – Mouse models – Neonates – Working memory – Long term memory


Zdroje

1. Bohnen N, Warner MA, Kokmen E, Kurland LT. Early and midlife exposure to anesthesia and age of onset of Alzheimer's disease. Int J Neurosci. 1994;77(3–4):181–5. doi: 10.3109/00207459408986029 7814211.

2. Gasparini M, Vanacore N, Schiaffini C, Brusa L, Panella M, Talarico G, et al. A case-control study on Alzheimer's disease and exposure to anesthesia. Neurol Sci. 2002;23(1):11–4. doi: 10.1007/s100720200017 12111615.

3. Lee TA, Wolozin B, Weiss KB, Bednar MM. Assessment of the emergence of Alzheimer's disease following coronary artery bypass graft surgery or percutaneous transluminal coronary angioplasty. J Alzheimers Dis. 2005;7(4):319–24. 16131734.

4. Chen CW, Lin CC, Chen KB, Kuo YC, Li CY, Chung CJ. Increased risk of dementia in people with previous exposure to general anesthesia: a nationwide population-based case-control study. Alzheimers Dement. 2014;10(2):196–204. doi: 10.1016/j.jalz.2013.05.1766 23896612.

5. Zuo C, Zuo Z. Spine Surgery under general anesthesia may not increase the risk of Alzheimer's disease. Dement Geriatr Cogn Disord. 2010;29(3):233–9. doi: 10.1159/000295114 20375503; PubMed Central PMCID: PMC2865396.

6. Shapiro S, Hamby CL, Shapiro DA. Alzheimer's disease: an emerging affliction of the aging population. J Am Dent Assoc. 1985;111(2):287–92. doi: 10.14219/jada.archive.1985.0103 2931467.

7. Ehlenbach WJ, Hough CL, Crane PK, Haneuse SJ, Carson SS, Curtis JR, et al. Association between acute care and critical illness hospitalization and cognitive function in older adults. JAMA. 2010;303(8):763–70. doi: 10.1001/jama.2010.167 20179286; PubMed Central PMCID: PMC2943865.

8. Chen CC, Chiu MJ, Chen SP, Cheng CM, Huang GH. Patterns of cognitive change in elderly patients during and 6 months after hospitalisation: a prospective cohort study. Int J Nurs Stud. 2011;48(3):338–46. doi: 10.1016/j.ijnurstu.2010.03.011 20403601.

9. Perouansky M, Hemmings HC Jr. Neurotoxicity of general anesthetics: cause for concern? Anesthesiology. 2009;111(6):1365–71. Epub 2009/11/26. doi: 10.1097/ALN.0b013e3181bf1d61 19934883; PubMed Central PMCID: PMC2784653.

10. Tang JX, Eckenhoff MF. Anesthetic effects in Alzheimer transgenic mouse models. Prog Neuropsychopharmacol Biol Psychiatry. 2013;47:167–71. doi: 10.1016/j.pnpbp.2012.06.007 22705294; PubMed Central PMCID: PMC3521854.

11. Jiang J, Jiang H. Effect of the inhaled anesthetics isoflurane, sevoflurane and desflurane on the neuropathogenesis of Alzheimer's disease (review). Mol Med Rep. 2015;12(1):3–12. doi: 10.3892/mmr.2015.3424 25738734; PubMed Central PMCID: PMC4438950.

12. Su D, Zhao Y, Xu H, Wang B, Chen X, Chen J, et al. Isoflurane exposure during mid-adulthood attenuates age-related spatial memory impairment in APP/PS1 transgenic mice. PLoS One. 2012;7(11):e50172. doi: 10.1371/journal.pone.0050172 23185565; PubMed Central PMCID: PMC3501473.

13. Shen X, Liu Y, Xu S, Zhao Q, Guo X, Shen R, et al. Early life exposure to sevoflurane impairs adulthood spatial memory in the rat. Neurotoxicology. 2013;39:45–56. Epub 2013/09/03. S0161-813X(13)00131-9 [pii] doi: 10.1016/j.neuro.2013.08.007 23994303.

14. Zhu C, Gao J, Karlsson N, Li Q, Zhang Y, Huang Z, et al. Isoflurane anesthesia induced persistent, progressive memory impairment, caused a loss of neural stem cells, and reduced neurogenesis in young, but not adult, rodents. J Cereb Blood Flow Metab. 2010;30(5):1017–30. doi: 10.1038/jcbfm.2009.274 20068576; PubMed Central PMCID: PMC2949194.

15. Valentim AM, Di Giminiani P, Ribeiro PO, Rodrigues P, Olsson IA, Antunes LM. Lower isoflurane concentration affects spatial learning and neurodegeneration in adult mice compared with higher concentrations. Anesthesiology. 2010;113(5):1099–108. doi: 10.1097/ALN.0b013e3181f79c7c 20885290.

16. Terry RD, Masliah E, Salmon DP, Butters N, DeTeresa R, Hill R, et al. Physical basis of cognitive alterations in Alzheimer's disease: synapse loss is the major correlate of cognitive impairment. Ann Neurol. 1991;30(4):572–80. Epub 1991/10/01. doi: 10.1002/ana.410300410 1789684.

17. Oddo S, Caccamo A, Shepherd JD, Murphy MP, Golde TE, Kayed R, et al. Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Abeta and synaptic dysfunction. Neuron. 2003;39(3):409–21. doi: 10.1016/s0896-6273(03)00434-3 12895417.

18. Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG. Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biol. 2010;8(6):e1000412. Epub 2010/07/09. doi: 10.1371/journal.pbio.1000412 20613859; PubMed Central PMCID: PMC2893951.

19. Orliaguet G, Vivien B, Langeron O, Bouhemad B, Coriat P, Riou B. Minimum alveolar concentration of volatile anesthetics in rats during postnatal maturation. Anesthesiology. 2001;95(3):734–9. Epub 2001/09/29. doi: 10.1097/00000542-200109000-00028 11575548.

20. Bianchi SL, Tran T, Liu C, Lin S, Li Y, Keller JM, et al. Brain and behavior changes in 12-month-old Tg2576 and nontransgenic mice exposed to anesthetics. Neurobiol Aging. 2008;29(7):1002–10. doi: 10.1016/j.neurobiolaging.2007.02.009 17346857; PubMed Central PMCID: PMC4899817.

21. Wilder RT, Flick RP, Sprung J, Katusic SK, Barbaresi WJ, Mickelson C, et al. Early exposure to anesthesia and learning disabilities in a population-based birth cohort. Anesthesiology. 2009;110(4):796–804. doi: 10.1097/01.anes.0000344728.34332.5d 19293700; PubMed Central PMCID: PMC2729550.

22. Tang JX, Mardini F, Caltagarone BM, Garrity ST, Li RQ, Bianchi SL, et al. Anesthesia in presymptomatic Alzheimer's disease: a study using the triple-transgenic mouse model. Alzheimers Dement. 2011;7(5):521–31 e1. doi: 10.1016/j.jalz.2010.10.003 21745760; PubMed Central PMCID: PMC3167023.

23. Xie Z, Culley DJ, Dong Y, Zhang G, Zhang B, Moir RD, et al. The common inhalation anesthetic isoflurane induces caspase activation and increases amyloid beta-protein level in vivo. Ann Neurol. 2008;64(6):618–27. doi: 10.1002/ana.21548 19006075; PubMed Central PMCID: PMC2612087.

24. Thelin EP, Zeiler FA, Ercole A, Mondello S, Buki A, Bellander BM, et al. Serial Sampling of Serum Protein Biomarkers for Monitoring Human Traumatic Brain Injury Dynamics: A Systematic Review. Front Neurol. 2017;8:300. Epub 2017/07/19. doi: 10.3389/fneur.2017.00300 28717351; PubMed Central PMCID: PMC5494601.

25. Morris R. Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods. 1984;11(1):47–60. doi: 10.1016/0165-0270(84)90007-4 6471907.

26. Vorhees CV, Williams MT. Morris water maze: procedures for assessing spatial and related forms of learning and memory. Nat Protoc. 2006;1(2):848–58. doi: 10.1038/nprot.2006.116 17406317; PubMed Central PMCID: PMC2895266.

27. Barnhart CD, Yang D, Lein PJ. Using the Morris water maze to assess spatial learning and memory in weanling mice. PLoS One. 2015;10(4):e0124521. Epub 2015/04/18. doi: 10.1371/journal.pone.0124521 PONE-D-15-03461 [pii]. 25886563; PubMed Central PMCID: PMC4401674.

28. Rudy JW, Stadler-Morris S, Albert P. Ontogeny of spatial navigation behaviors in the rat: dissociation of "proximal"- and "distal"-cue-based behaviors. Behav Neurosci. 1987;101(1):62–73. Epub 1987/02/01. doi: 10.1037//0735-7044.101.1.62 3828056.

29. Drew LJ, Stark KL, Fenelon K, Karayiorgou M, Macdermott AB, Gogos JA. Evidence for altered hippocampal function in a mouse model of the human 22q11.2 microdeletion. Mol Cell Neurosci. 2011;47(4):293–305. doi: 10.1016/j.mcn.2011.05.008 21635953; PubMed Central PMCID: PMC3539311.

30. Stratmann G. Review article: Neurotoxicity of anesthetic drugs in the developing brain. Anesth Analg. 2011;113(5):1170–9. doi: 10.1213/ANE.0b013e318232066c 21965351.

31. Jevtovic-Todorovic V, Absalom AR, Blomgren K, Brambrink A, Crosby G, Culley DJ, et al. Anaesthetic neurotoxicity and neuroplasticity: an expert group report and statement based on the BJA Salzburg Seminar. Br J Anaesth. 2013;111(2):143–51. Epub 2013/06/01. S0007-0912(17)32438-8 [pii] doi: 10.1093/bja/aet177 23722106; PubMed Central PMCID: PMC3711392.

32. Mohan S, Abdelwahab SI, Kamalidehghan B, Syam S, May KS, Harmal NS, et al. Involvement of NF-kappaB and Bcl2/Bax signaling pathways in the apoptosis of MCF7 cells induced by a xanthone compound Pyranocycloartobiloxanthone A. Phytomedicine. 2012;19(11):1007–15. Epub 2012/06/29. S0944-7113(12)00190-0 [pii] doi: 10.1016/j.phymed.2012.05.012 22739412.

33. Yip KW, Reed JC. Bcl-2 family proteins and cancer. Oncogene. 2008;27(50):6398–406. Epub 2008/10/29. onc2008307 [pii] doi: 10.1038/onc.2008.307 18955968.

34. Stratmann G, Sall JW, Bell JS, Alvi RS, May L, Ku B, et al. Isoflurane does not affect brain cell death, hippocampal neurogenesis, or long-term neurocognitive outcome in aged rats. Anesthesiology. 2010;112(2):305–15. Epub 2010/01/26. doi: 10.1097/ALN.0b013e3181ca33a1 00000542-201002000-00014 [pii]. 20098132; PubMed Central PMCID: PMC5214622.

35. Gallagher M, Burwell R, Burchinal M. Severity of spatial learning impairment in aging: Development of a learning index for performance in the Morris water maze. Behav Neurosci. 2015;129(4):540–8. Epub 2015/07/28. 2015-33468-009 [pii] doi: 10.1037/bne0000080 26214219; PubMed Central PMCID: PMC5640430.

36. Dobrunz LE, Stevens CF. Heterogeneity of release probability, facilitation, and depletion at central synapses. Neuron. 1997;18(6):995–1008. Epub 1997/06/01. S0896-6273(00)80338-4 [pii]. doi: 10.1016/s0896-6273(00)80338-4 9208866.

37. Pensalfini A, Albay R 3rd, Rasool S, Wu JW, Hatami A, Arai H, et al. Intracellular amyloid and the neuronal origin of Alzheimer neuritic plaques. Neurobiol Dis. 2014;71:53–61. Epub 2014/08/06. S0969-9961(14)00212-5 [pii] doi: 10.1016/j.nbd.2014.07.011 25092575; PubMed Central PMCID: PMC4179983.

38. Oddo S, Caccamo A, Tran L, Lambert MP, Glabe CG, Klein WL, et al. Temporal profile of amyloid-beta (Abeta) oligomerization in an in vivo model of Alzheimer disease. A link between Abeta and tau pathology. J Biol Chem. 2006;281(3):1599–604. Epub 2005/11/12. M507892200 [pii] doi: 10.1074/jbc.M507892200 16282321.

39. Kayed R, Head E, Thompson JL, McIntire TM, Milton SC, Cotman CW, et al. Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science. 2003;300(5618):486–9. Epub 2003/04/19. doi: 10.1126/science.1079469 300/5618/486 [pii]. 12702875.

40. Kayed R, Head E, Sarsoza F, Saing T, Cotman CW, Necula M, et al. Fibril specific, conformation dependent antibodies recognize a generic epitope common to amyloid fibrils and fibrillar oligomers that is absent in prefibrillar oligomers. Mol Neurodegener. 2007;2:18. Epub 2007/09/28. 1750-1326-2-18 [pii] doi: 10.1186/1750-1326-2-18 17897471; PubMed Central PMCID: PMC2100048.

41. Kayed R, Pensalfini A, Margol L, Sokolov Y, Sarsoza F, Head E, et al. Annular protofibrils are a structurally and functionally distinct type of amyloid oligomer. J Biol Chem. 2009;284(7):4230–7. Epub 2008/12/23. M808591200 [pii] doi: 10.1074/jbc.M808591200 19098006; PubMed Central PMCID: PMC2640961.

42. Glabe CG. Structural classification of toxic amyloid oligomers. J Biol Chem. 2008;283(44):29639–43. Epub 2008/08/30. R800016200 [pii] doi: 10.1074/jbc.R800016200 18723507; PubMed Central PMCID: PMC2573087.

43. Necula M, Breydo L, Milton S, Kayed R, van der Veer WE, Tone P, et al. Methylene blue inhibits amyloid Abeta oligomerization by promoting fibrillization. Biochemistry. 2007;46(30):8850–60. Epub 2007/06/28. doi: 10.1021/bi700411k 17595112.

44. Cummings BJ, Mason AJ, Kim RC, Sheu PC, Anderson AJ. Optimization of techniques for the maximal detection and quantification of Alzheimer's-related neuropathology with digital imaging. Neurobiol Aging. 2002;23(2):161–70. Epub 2002/01/24. S0197458001003165 [pii]. doi: 10.1016/s0197-4580(01)00316-5 11804699.

45. Gouras GK, Tsai J, Naslund J, Vincent B, Edgar M, Checler F, et al. Intraneuronal Abeta42 accumulation in human brain. Am J Pathol. 2000;156(1):15–20. Epub 2000/01/07. S0002-9440(10)64700-1 [pii]. doi: 10.1016/s0002-9440(10)64700-1 10623648; PubMed Central PMCID: PMC1868613.

46. Hunter S, Brayne C. Do anti-amyloid beta protein antibody cross reactivities confound Alzheimer disease research? J Negat Results Biomed. 2017;16(1):1. Epub 2017/01/28. doi: 10.1186/s12952-017-0066-3 [pii]. 28126004; PubMed Central PMCID: PMC5270220.

47. Hofling C, Morawski M, Zeitschel U, Zanier ER, Moschke K, Serdaroglu A, et al. Differential transgene expression patterns in Alzheimer mouse models revealed by novel human amyloid precursor protein-specific antibodies. Aging Cell. 2016;15(5):953–63. Epub 2016/07/30. doi: 10.1111/acel.12508 27470171; PubMed Central PMCID: PMC5013031.

48. Wang S, Peretich K, Zhao Y, Liang G, Meng Q, Wei H. Anesthesia-induced neurodegeneration in fetal rat brains. Pediatr Res. 2009;66(4):435–40. doi: 10.1203/PDR.0b013e3181b3381b 20016413; PubMed Central PMCID: PMC3069715.

49. Butterfield NN, Graf P, Ries CR, MacLeod BA. The effect of repeated isoflurane anesthesia on spatial and psychomotor performance in young and aged mice. Anesth Analg. 2004;98(5):1305–11, table of contents. doi: 10.1213/01.ane.0000108484.91089.13 15105206.

50. Callaway JK, Jones NC, Royse AG, Royse CF. Sevoflurane anesthesia does not impair acquisition learning or memory in the Morris water maze in young adult and aged rats. Anesthesiology. 2012;117(5):1091–101. doi: 10.1097/ALN.0b013e31826cb228 22929734.

51. Culley DJ, Baxter M, Yukhananov R, Crosby G. The memory effects of general anesthesia persist for weeks in young and aged rats. Anesth Analg. 2003;96(4):1004–9, table of contents. doi: 10.1213/01.ane.0000052712.67573.12 12651650.

52. Crosby C, Culley DJ, Baxter MG, Yukhananov R, Crosby G. Spatial memory performance 2 weeks after general anesthesia in adult rats. Anesth Analg. 2005;101(5):1389–92. doi: 10.1213/01.ANE.0000180835.72669.AD 16243999.

53. Eckel B, Ohl F, Starker L, Rammes G, Bogdanski R, Kochs E, et al. Effects of isoflurane-induced anaesthesia on cognitive performance in a mouse model of Alzheimer's disease: A randomised trial in transgenic APP23 mice. Eur J Anaesthesiol. 2013;30(10):605–11. doi: 10.1097/EJA.0b013e32835b824b 23274617.

54. Rammes G, Starker LK, Haseneder R, Berkmann J, Plack A, Zieglgansberger W, et al. Isoflurane anaesthesia reversibly improves cognitive function and long-term potentiation (LTP) via an up-regulation in NMDA receptor 2B subunit expression. Neuropharmacology. 2009;56(3):626–36. doi: 10.1016/j.neuropharm.2008.11.002 19059421.

55. Zheng H, Dong Y, Xu Z, Crosby G, Culley DJ, Zhang Y, et al. Sevoflurane anesthesia in pregnant mice induces neurotoxicity in fetal and offspring mice. Anesthesiology. 2013;118(3):516–26. doi: 10.1097/ALN.0b013e3182834d5d 23314109; PubMed Central PMCID: PMC3580035.

56. Murman DL. The Impact of Age on Cognition. Semin Hear. 2015;36(3):111–21. Epub 2016/08/16. doi: 10.1055/s-0035-1555115 [pii]. 27516712; PubMed Central PMCID: PMC4906299.

57. Matzel LD, Grossman H, Light K, Townsend D, Kolata S. Age-related declines in general cognitive abilities of Balb/C mice are associated with disparities in working memory, body weight, and general activity. Learn Mem. 2008;15(10):733–46. Epub 2008/10/04. 15/10/733 [pii] doi: 10.1101/lm.954808 18832560; PubMed Central PMCID: PMC2632791.

58. Weber M, Wu T, Hanson JE, Alam NM, Solanoy H, Ngu H, et al. Cognitive Deficits, Changes in Synaptic Function, and Brain Pathology in a Mouse Model of Normal Aging(1,2,3). eNeuro. 2015;2(5). Epub 2015/10/17. doi: 10.1523/ENEURO.0047-15.2015 eN-NWR-0047-15 [pii]. 26473169; PubMed Central PMCID: PMC4606159.

59. Cabeza R, Anderson ND, Locantore JK, McIntosh AR. Aging gracefully: compensatory brain activity in high-performing older adults. Neuroimage. 2002;17(3):1394–402. Epub 2002/11/05. S1053811902912802 [pii]. 12414279.

60. Davis HP, Small SA, Stern Y, Mayeux R, Feldstein SN, Keller FR. Acquisition, recall, and forgetting of verbal information in long-term memory by young, middle-aged, and elderly individuals. Cortex. 2003;39(4–5):1063–91. Epub 2003/10/31. S0010-9452(08)70878-5 [pii]. doi: 10.1016/s0010-9452(08)70878-5 14584567.

61. Daffner KR, Ryan KK, Williams DM, Budson AE, Rentz DM, Wolk DA, et al. Age-related differences in attention to novelty among cognitively high performing adults. Biol Psychol. 2006;72(1):67–77. Epub 2005/10/04. S0301-0511(05)00121-3 [pii] doi: 10.1016/j.biopsycho.2005.07.006 16198046.

62. Boric K, Munoz P, Gallagher M, Kirkwood A. Potential adaptive function for altered long-term potentiation mechanisms in aging hippocampus. J Neurosci. 2008;28(32):8034–9. Epub 2008/08/08. 28/32/8034 [pii] doi: 10.1523/JNEUROSCI.2036-08.2008 18685028; PubMed Central PMCID: PMC2615232.

63. Lee HK, Min SS, Gallagher M, Kirkwood A. NMDA receptor-independent long-term depression correlates with successful aging in rats. Nat Neurosci. 2005;8(12):1657–9. Epub 2005/11/16. nn1586 [pii] doi: 10.1038/nn1586 16286930.

64. Billings LM, Oddo S, Green KN, McGaugh JL, LaFerla FM. Intraneuronal Abeta causes the onset of early Alzheimer's disease-related cognitive deficits in transgenic mice. Neuron. 2005;45(5):675–88. Epub 2005/03/08. S0896-6273(05)00078-4 [pii] doi: 10.1016/j.neuron.2005.01.040 15748844.

65. Oh KJ, Perez SE, Lagalwar S, Vana L, Binder L, Mufson EJ. Staging of Alzheimer's pathology in triple transgenic mice: a light and electron microscopic analysis. Int J Alzheimers Dis. 2010;2010. Epub 2010/08/28. doi: 10.4061/2010/780102 20798886; PubMed Central PMCID: PMC2925282.

66. Webster SJ, Bachstetter AD, Nelson PT, Schmitt FA, Van Eldik LJ. Using mice to model Alzheimer's dementia: an overview of the clinical disease and the preclinical behavioral changes in 10 mouse models. Front Genet. 2014;5:88. Epub 2014/05/06. doi: 10.3389/fgene.2014.00088 24795750; PubMed Central PMCID: PMC4005958.

67. Webster SJ, Bachstetter AD, Van Eldik LJ. Comprehensive behavioral characterization of an APP/PS-1 double knock-in mouse model of Alzheimer's disease. Alzheimers Res Ther. 2013;5(3):28. Epub 2013/05/28. doi: 10.1186/alzrt182 alzrt182 [pii]. 23705774; PubMed Central PMCID: PMC3706792.

68. Choi J, Jeong Y. Elevated emotional contagion in a mouse model of Alzheimer's disease is associated with increased synchronization in the insula and amygdala. Sci Rep. 2017;7:46262. Epub 2017/04/08. srep46262 [pii] doi: 10.1038/srep46262 28387348; PubMed Central PMCID: PMC5384199.

69. Canete T, Blazquez G, Tobena A, Gimenez-Llort L, Fernandez-Teruel A. Cognitive and emotional alterations in young Alzheimer's disease (3xTgAD) mice: effects of neonatal handling stimulation and sexual dimorphism. Behav Brain Res. 2015;281:156–71. Epub 2014/12/03. S0166-4328(14)00733-5 [pii] doi: 10.1016/j.bbr.2014.11.004 25446741.

70. Stover KR, Campbell MA, Van Winssen CM, Brown RE. Early detection of cognitive deficits in the 3xTg-AD mouse model of Alzheimer's disease. Behav Brain Res. 2015;289:29–38. Epub 2015/04/22. S0166-4328(15)00254-5 [pii] doi: 10.1016/j.bbr.2015.04.012 25896362.

71. Davis KE, Fox S, Gigg J. Increased hippocampal excitability in the 3xTgAD mouse model for Alzheimer's disease in vivo. PLoS One. 2014;9(3):e91203. doi: 10.1371/journal.pone.0091203 24621690; PubMed Central PMCID: PMC3951322.

72. Torres-Lista V, De la Fuente M, Giménez-Llort L. Survival Curves and Behavioral Profiles of Female 3xTg-AD Mice Surviving to 18-Months of Age as Compared to Mice with Normal Aging. Journal of Alzheimer's Disease Reports. 2017;vol. 1 (no. 1): 47–57. Epub 5 June doi: 10.3233/ADR-170011 30480229

73. Vutskits L, Xie Z. Lasting impact of general anaesthesia on the brain: mechanisms and relevance. Nat Rev Neurosci. 2016;17(11):705–17. doi: 10.1038/nrn.2016.128 27752068.

74. Hazra A, Gu F, Aulakh A, Berridge C, Eriksen JL, Ziburkus J. Inhibitory neuron and hippocampal circuit dysfunction in an aged mouse model of Alzheimer's disease. PLoS One. 2013;8(5):e64318. doi: 10.1371/journal.pone.0064318 23691195; PubMed Central PMCID: PMC3656838.

75. Palop JJ, Mucke L. Epilepsy and cognitive impairments in Alzheimer disease. Arch Neurol. 2009;66(4):435–40. doi: 10.1001/archneurol.2009.15 19204149; PubMed Central PMCID: PMC2812914.

76. Palop JJ, Mucke L. Synaptic depression and aberrant excitatory network activity in Alzheimer's disease: two faces of the same coin? Neuromolecular Med. 2010;12(1):48–55. doi: 10.1007/s12017-009-8097-7 19838821; PubMed Central PMCID: PMC3319077.

77. Sperling RA, Laviolette PS, O'Keefe K, O'Brien J, Rentz DM, Pihlajamaki M, et al. Amyloid deposition is associated with impaired default network function in older persons without dementia. Neuron. 2009;63(2):178–88. doi: 10.1016/j.neuron.2009.07.003 19640477; PubMed Central PMCID: PMC2738994.

78. Busche MA, Eichhoff G, Adelsberger H, Abramowski D, Wiederhold KH, Haass C, et al. Clusters of hyperactive neurons near amyloid plaques in a mouse model of Alzheimer's disease. Science. 2008;321(5896):1686–9. doi: 10.1126/science.1162844 18802001.

79. Richards CD. Anaesthetic modulation of synaptic transmission in the mammalian CNS. Br J Anaesth. 2002;89(1):79–90. doi: 10.1093/bja/aef162 12173243.

80. Fitzjohn SM, Morton RA, Kuenzi F, Rosahl TW, Shearman M, Lewis H, et al. Age-related impairment of synaptic transmission but normal long-term potentiation in transgenic mice that overexpress the human APP695SWE mutant form of amyloid precursor protein. J Neurosci. 2001;21(13):4691–8. 11425896.

81. Maclver MB, Mikulec AA, Amagasu SM, Monroe FA. Volatile anesthetics depress glutamate transmission via presynaptic actions. Anesthesiology. 1996;85(4):823–34. doi: 10.1097/00000542-199610000-00018 8873553.

82. Verret L, Mann EO, Hang GB, Barth AM, Cobos I, Ho K, et al. Inhibitory interneuron deficit links altered network activity and cognitive dysfunction in Alzheimer model. Cell. 2012;149(3):708–21. doi: 10.1016/j.cell.2012.02.046 22541439; PubMed Central PMCID: PMC3375906.

83. Klyachko VA, Stevens CF. Excitatory and feed-forward inhibitory hippocampal synapses work synergistically as an adaptive filter of natural spike trains. PLoS Biol. 2006;4(7):e207. doi: 10.1371/journal.pbio.0040207 16774451; PubMed Central PMCID: PMC1479695.

84. Walsh DM, Klyubin I, Fadeeva JV, Cullen WK, Anwyl R, Wolfe MS, et al. Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature. 2002;416(6880):535–9. doi: 10.1038/416535a 11932745.

85. Palop JJ, Mucke L. Network abnormalities and interneuron dysfunction in Alzheimer disease. Nat Rev Neurosci. 2016;17(12):777–92. doi: 10.1038/nrn.2016.141 27829687.

86. Shankar GM, Li S, Mehta TH, Garcia-Munoz A, Shepardson NE, Smith I, et al. Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat Med. 2008;14(8):837–42. doi: 10.1038/nm1782 18568035; PubMed Central PMCID: PMC2772133.

87. Lei M, Xu H, Li Z, Wang Z, O'Malley TT, Zhang D, et al. Soluble Abeta oligomers impair hippocampal LTP by disrupting glutamatergic/GABAergic balance. Neurobiol Dis. 2016;85:111–21. doi: 10.1016/j.nbd.2015.10.019 26525100; PubMed Central PMCID: PMC4778388.

88. Gengler S, Hamilton A, Holscher C. Synaptic plasticity in the hippocampus of a APP/PS1 mouse model of Alzheimer's disease is impaired in old but not young mice. PLoS One. 2010;5(3):e9764. doi: 10.1371/journal.pone.0009764 20339537; PubMed Central PMCID: PMC2842299.

89. Ye L, Qi JS, Qiao JT. Long-term potentiation in hippocampus of rats is enhanced by endogenous acetylcholine in a way that is independent of N-methyl-D-aspartate receptors. Neurosci Lett. 2001;300(3):145–8. doi: 10.1016/s0304-3940(01)01573-7 11226632.

90. Piao MH, Liu Y, Wang YS, Qiu JP, Feng CS. Volatile anesthetic isoflurane inhibits LTP induction of hippocampal CA1 neurons through alpha4beta2 nAChR subtype-mediated mechanisms. Ann Fr Anesth Reanim. 2013;32(10):e135–41. doi: 10.1016/j.annfar.2013.05.012 24011619.

91. Kim IH, Wang H, Soderling SH, Yasuda R. Loss of Cdc42 leads to defects in synaptic plasticity and remote memory recall. Elife. 2014;3. Epub 2014/07/10. doi: 10.7554/eLife.02839 25006034; PubMed Central PMCID: PMC4115656.

92. Haseneder R, Kratzer S, von Meyer L, Eder M, Kochs E, Rammes G. Isoflurane and sevoflurane dose-dependently impair hippocampal long-term potentiation. Eur J Pharmacol. 2009;623(1–3):47–51. doi: 10.1016/j.ejphar.2009.09.022 19765574.

93. Gerlai R. Hippocampal LTP and memory in mouse strains: is there evidence for a causal relationship? Hippocampus. 2002;12(5):657–66. Epub 2002/11/21. doi: 10.1002/hipo.10101 12440580.

94. Meng J, Meng Y, Hanna A, Janus C, Jia Z. Abnormal long-lasting synaptic plasticity and cognition in mice lacking the mental retardation gene Pak3. J Neurosci. 2005;25(28):6641–50. Epub 2005/07/15. 25/28/6641 [pii] doi: 10.1523/JNEUROSCI.0028-05.2005 16014725.

95. Kumar A. Long-Term Potentiation at CA3-CA1 Hippocampal Synapses with Special Emphasis on Aging, Disease, and Stress. Front Aging Neurosci. 2011;3:7. Epub 2011/06/08. doi: 10.3389/fnagi.2011.00007 21647396; PubMed Central PMCID: PMC3102214.

96. Peng J, Drobish JK, Liang G, Wu Z, Liu C, Joseph DJ, et al. Anesthetic preconditioning inhibits isoflurane-mediated apoptosis in the developing rat brain. Anesth Analg. 2014;119(4):939–46. doi: 10.1213/ANE.0000000000000380 25099925; PubMed Central PMCID: PMC4169313.

97. Jevtovic-Todorovic V, Hartman RE, Izumi Y, Benshoff ND, Dikranian K, Zorumski CF, et al. Early exposure to common anesthetic agents causes widespread neurodegeneration in the developing rat brain and persistent learning deficits. J Neurosci. 2003;23(3):876–82. doi: 10.1523/JNEUROSCI.23-03-00876.2003 12574416.

98. Feng C, Liu Y, Yuan Y, Cui W, Zheng F, Ma Y, et al. Isoflurane anesthesia exacerbates learning and memory impairment in zinc-deficient APP/PS1 transgenic mice. Neuropharmacology. 2016;111:119–29. doi: 10.1016/j.neuropharm.2016.08.035 27586008.

99. Zou X, Liu F, Zhang X, Patterson TA, Callicott R, Liu S, et al. Inhalation anesthetic-induced neuronal damage in the developing rhesus monkey. Neurotoxicol Teratol. 2011;33(5):592–7. doi: 10.1016/j.ntt.2011.06.003 21708249.

100. Rizzi S, Carter LB, Ori C, Jevtovic-Todorovic V. Clinical anesthesia causes permanent damage to the fetal guinea pig brain. Brain Pathol. 2008;18(2):198–210. doi: 10.1111/j.1750-3639.2007.00116.x 18241241; PubMed Central PMCID: PMC3886120.

101. Peng J, Liang G, Inan S, Wu Z, Joseph DJ, Meng Q, et al. Dantrolene ameliorates cognitive decline and neuropathology in Alzheimer triple transgenic mice. Neurosci Lett. 2012;516(2):274–9. doi: 10.1016/j.neulet.2012.04.008 22516463; PubMed Central PMCID: PMC3351794.

102. Maloney SE, Yuede CM, Creeley CE, Williams SL, Huffman JN, Taylor GT, et al. Repeated neonatal isoflurane exposures in the mouse induce apoptotic degenerative changes in the brain and relatively mild long-term behavioral deficits. Sci Rep. 2019;9(1):2779. doi: 10.1038/s41598-019-39174-6 30808927; PubMed Central PMCID: PMC6391407.

103. Istaphanous GK, Howard J, Nan X, Hughes EA, McCann JC, McAuliffe JJ, et al. Comparison of the neuroapoptotic properties of equipotent anesthetic concentrations of desflurane, isoflurane, or sevoflurane in neonatal mice. Anesthesiology. 2011;114(3):578–87. doi: 10.1097/ALN.0b013e3182084a70 21293251.

104. Liang G, Ward C, Peng J, Zhao Y, Huang B, Wei H. Isoflurane causes greater neurodegeneration than an equivalent exposure of sevoflurane in the developing brain of neonatal mice. Anesthesiology. 2010;112(6):1325–34. doi: 10.1097/ALN.0b013e3181d94da5 20460994; PubMed Central PMCID: PMC2877765.

105. Johnson SC, Pan A, Sun GX, Freed A, Stokes JC, Bornstein R, et al. Relevance of experimental paradigms of anesthesia induced neurotoxicity in the mouse. PLoS One. 2019;14(3):e0213543. doi: 10.1371/journal.pone.0213543 30897103; PubMed Central PMCID: PMC6428290.


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