Apolipoprotein E4 Causes Age-Dependent Disruption of Slow Gamma Oscillations during Hippocampal Sharp-Wave Ripples

Neuron

Volumn 90, Issue 4, 2016, Pages 740-751

  Gillespie, Anna K ^a,b   Jones, Emily A ^a,b   Lin, Yuan Hung ^a,b   Karlsson, Mattias P ^b   Kay, Kenneth ^b   Yoon, Seo Yeon ^a   Tong, Leslie M ^a,b   Nova, Philip ^a,b   Carr, Jessie S ^a,b   Frank, Loren M ^b   Huang, Yadong ^a,b  

^a GLADSTONE INSTITUTE OF NEUROLOGICAL DISEASE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN E4;

AGE; AGED; AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ELECTROPHYSIOLOGY; FEMALE; GABAERGIC SYSTEM; GAMMA RHYTHM; HIPPOCAMPUS; HISTOLOGY; INTERNEURON; LEARNING DISORDER; MEMORY DISORDER; MOUSE; NONHUMAN; OSCILLATION; PHENOTYPE; PRIORITY JOURNAL; SHARP WAVE RIPPLE; ALZHEIMER DISEASE; ANIMAL; COGNITIVE DEFECT; DISEASE MODEL; GENE TARGETING; GENETICS; MAZE TEST; METABOLISM; PHYSIOLOGY; PROCEDURES; TRANSGENIC MOUSE;

AGING; ALZHEIMER DISEASE; ANIMALS; APOLIPOPROTEIN E4; COGNITION DISORDERS; DISEASE MODELS, ANIMAL; GENE KNOCK-IN TECHNIQUES; HIPPOCAMPUS; INTERNEURONS; MAZE LEARNING; MEMORY DISORDERS; MICE, TRANSGENIC;

EID: 84964944683     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2016.04.009     Document Type: Article

References (56)

1. Andrews-Zwilling Y., Bien-Ly N., Xu Q., Li G., Bernardo A., Yoon S.Y., Zwilling D., Yan T.X., Chen L., Huang Y. Apolipoprotein E4 causes age- and Tau-dependent impairment of GABAergic interneurons, leading to learning and memory deficits in mice. J. Neurosci. 2010, 30:13707-13717.
2. Andrews-Zwilling Y., Gillespie A.K., Kravitz A.V., Nelson A.B., Devidze N., Lo I., Yoon S.Y., Bien-Ly N., Ring K., Zwilling D., et al. Hilar GABAergic interneuron activity controls spatial learning and memory retrieval. PLoS ONE 2012, 7:e40555.
3. Beydoun M.A., Boueiz A., Abougergi M.S., Kitner-Triolo M.H., Beydoun H.A., Resnick S.M., O'Brien R., Zonderman A.B. Sex differences in the association of the apolipoprotein E epsilon 4 allele with incidence of dementia, cognitive impairment, and decline. Neurobiol. Aging 2012, 33:720-731.e4, e724.
4. Bien-Ly N., Gillespie A.K., Walker D., Yoon S.Y., Huang Y. Reducing human apolipoprotein E levels attenuates age-dependent Aβ accumulation in mutant human amyloid precursor protein transgenic mice. J. Neurosci. 2012, 32:4803-4811.
5. Bragin A., Jandó G., Nádasdy Z., Hetke J., Wise K., Buzsáki G. Gamma (40-100 Hz) oscillation in the hippocampus of the behaving rat. J. Neurosci. 1995, 15:47-60.
6. Bragin A., Jandó G., Nádasdy Z., van Landeghem M., Buzsáki G. Dentate EEG spikes and associated interneuronal population bursts in the hippocampal hilar region of the rat. J. Neurophysiol. 1995, 73:1691-1705.
7. Buzsáki G. Hippocampal sharp waves: their origin and significance. Brain Res. 1986, 398:242-252.
8. Buzsáki G. Two-stage model of memory trace formation: a role for "noisy" brain states. Neuroscience 1989, 31:551-570.
9. Buzsáki G. The hippocampo-neocortical dialogue. Cereb. Cortex 1996, 6:81-92.
10. Buzsáki G. Hippocampal sharp wave-ripple: A cognitive biomarker for episodic memory and planning. Hippocampus 2015, 25:1073-1188.
11. Buzsáki G., Horváth Z., Urioste R., Hetke J., Wise K. High-frequency network oscillation in the hippocampus. Science 1992, 256:1025-1027.
12. Buzsáki G., Buhl D.L., Harris K.D., Csicsvari J., Czéh B., Morozov A. Hippocampal network patterns of activity in the mouse. Neuroscience 2003, 116:201-211.
13. Carr M.F., Karlsson M.P., Frank L.M. Transient slow gamma synchrony underlies hippocampal memory replay. Neuron 2012, 75:700-713.
14. Cheng S., Frank L.M. New experiences enhance coordinated neural activity in the hippocampus. Neuron 2008, 57:303-313.
15. Ciupek S.M., Cheng J., Ali Y.O., Lu H.C., Ji D. Progressive functional impairments of hippocampal neurons in a tauopathy mouse model. J. Neurosci. 2015, 35:8118-8131.
16. Clemens Z., Mölle M., Eross L., Barsi P., Halász P., Born J. Temporal coupling of parahippocampal ripples, sleep spindles and slow oscillations in humans. Brain 2007, 130:2868-2878.
17. Colgin L.L. Slow gamma takes the reins in replay. Neuron 2012, 75:549-550.
18. Colgin L.L., Denninger T., Fyhn M., Hafting T., Bonnevie T., Jensen O., Moser M.B., Moser E.I. Frequency of gamma oscillations routes flow of information in the hippocampus. Nature 2009, 462:353-357.
19. Corder E.H., Saunders A.M., Strittmatter W.J., Schmechel D.E., Gaskell P.C., Small G.W., Roses A.D., Haines J.L., Pericak-Vance M.A. Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families. Science 1993, 261:921-923.
20. Csicsvari J., Hirase H., Mamiya A., Buzsáki G. Ensemble patterns of hippocampal CA3-CA1 neurons during sharp wave-associated population events. Neuron 2000, 28:585-594.
21. Csicsvari J., Jamieson B., Wise K.D., Buzsáki G. Mechanisms of gamma oscillations in the hippocampus of the behaving rat. Neuron 2003, 37:311-322.
22. Ego-Stengel V., Wilson M.A. Disruption of ripple-associated hippocampal activity during rest impairs spatial learning in the rat. Hippocampus 2010, 20:1-10.
23. Farrer L.A., Cupples L.A., Haines J.L., Hyman B., Kukull W.A., Mayeux R., Myers R.H., Pericak-Vance M.A., Risch N., van Duijn C.M. Effects of age, sex, and ethnicity on the association between apolipoprotein E genotype and Alzheimer disease. A meta-analysis. JAMA 1997, 278:1349-1356. APOE and Alzheimer Disease Meta Analysis Consortium.
24. Girardeau G., Benchenane K., Wiener S.I., Buzsáki G., Zugaro M.B. Selective suppression of hippocampal ripples impairs spatial memory. Nat. Neurosci. 2009, 12:1222-1223.
25. Huang Y., Mucke L. Alzheimer mechanisms and therapeutic strategies. Cell 2012, 148:1204-1222.
26. Jadhav S.P., Kemere C., German P.W., Frank L.M. Awake hippocampal sharp-wave ripples support spatial memory. Science 2012, 336:1454-1458.
27. Karlsson M.P., Frank L.M. Network dynamics underlying the formation of sparse, informative representations in the hippocampus. J. Neurosci. 2008, 28:14271-14281.
28. Knoferle J., Yoon S.Y., Walker D., Leung L., Gillespie A.K., Tong L.M., Bien-Ly N., Huang Y. Apolipoprotein E4 produced in GABAergic interneurons causes learning and memory deficits in mice. J. Neurosci. 2014, 34:14069-14078.
29. Kudrimoti H.S., Barnes C.A., McNaughton B.L. Reactivation of hippocampal cell assemblies: effects of behavioral state, experience, and EEG dynamics. J. Neurosci. 1999, 19:4090-4101.
30. Larkin M.C., Lykken C., Tye L.D., Wickelgren J.G., Frank L.M. Hippocampal output area CA1 broadcasts a generalized novelty signal during an object-place recognition task. Hippocampus 2014, 24:773-783.
31. Le Van Quyen M., Bragin A., Staba R., Crépon B., Wilson C.L., Engel J. Cell type-specific firing during ripple oscillations in the hippocampal formation of humans. J. Neurosci. 2008, 28:6104-6110.
32. Lee A.K., Wilson M.A. Memory of sequential experience in the hippocampus during slow wave sleep. Neuron 2002, 36:1183-1194.
33. Lega B., Burke J., Jacobs J., Kahana M.J. Slow-Theta-to-Gamma Phase-Amplitude Coupling in Human Hippocampus Supports the Formation of New Episodic Memories. Cereb. Cortex 2016, 26:268-278.
34. Leung L., Andrews-Zwilling Y., Yoon S.Y., Jain S., Ring K., Dai J., Wang M.M., Tong L., Walker D., Huang Y. Apolipoprotein E4 causes age- and sex-dependent impairments of hilar GABAergic interneurons and learning and memory deficits in mice. PLoS ONE 2012, 7:e53569.
35. Mann E.O., Paulsen O. Mechanisms underlying gamma ('40 Hz') network oscillations in the hippocampus--a mini-review. Prog. Biophys. Mol. Biol. 2005, 87:67-76.
36. Montgomery S.M., Buzsáki G. Gamma oscillations dynamically couple hippocampal CA3 and CA1 regions during memory task performance. Proc. Natl. Acad. Sci. USA 2007, 104:14495-14500.
37. Myers C.E., Scharfman H.E. Pattern separation in the dentate gyrus: a role for the CA3 backprojection. Hippocampus 2011, 21:1190-1215.
38. Nakashiba T., Buhl D.L., McHugh T.J., Tonegawa S. Hippocampal CA3 output is crucial for ripple-associated reactivation and consolidation of memory. Neuron 2009, 62:781-787.
39. O'Neill J., Senior T.J., Allen K., Huxter J.R., Csicsvari J. Reactivation of experience-dependent cell assembly patterns in the hippocampus. Nat. Neurosci. 2008, 11:209-215.
40. Penttonen M., Kamondi A., Sik A., Acsády L., Buzsáki G. Feed-forward and feed-back activation of the dentate gyrus in vivo during dentate spikes and sharp wave bursts. Hippocampus 1997, 7:437-450.
41. Pfeiffer B.E., Foster D.J. Hippocampal place-cell sequences depict future paths to remembered goals. Nature 2013, 497:74-79.
42. Pfeiffer B.E., Foster D.J. PLACE CELLS. Autoassociative dynamics in the generation of sequences of hippocampal place cells. Science 2015, 349:180-183.
43. Potter G.B., Petryniak M.A., Shevchenko E., McKinsey G.L., Ekker M., Rubenstein J.L. Generation of Cre-transgenic mice using Dlx1/Dlx2 enhancers and their characterization in GABAergic interneurons. Mol. Cell. Neurosci. 2009, 40:167-186.
44. Ramaswamy G., Xu Q., Huang Y., Weisgraber K.H. Effect of domain interaction on apolipoprotein E levels in mouse brain. J. Neurosci. 2005, 25:10658-10663.
45. Ramsden M., Kotilinek L., Forster C., Paulson J., McGowan E., SantaCruz K., Guimaraes A., Yue M., Lewis J., Carlson G., et al. Age-dependent neurofibrillary tangle formation, neuron loss, and memory impairment in a mouse model of human tauopathy (P301L). J. Neurosci. 2005, 25:10637-10647.
46. Santacruz K., Lewis J., Spires T., Paulson J., Kotilinek L., Ingelsson M., Guimaraes A., DeTure M., Ramsden M., McGowan E., et al. Tau suppression in a neurodegenerative mouse model improves memory function. Science 2005, 309:476-481.
47. Saunders A.M., Strittmatter W.J., Schmechel D., George-Hyslop P.H., Pericak-Vance M.A., Joo S.H., Rosi B.L., Gusella J.F., Crapper-MacLachlan D.R., Alberts M.J., et al. Association of apolipoprotein E allele epsilon 4 with late-onset familial and sporadic Alzheimer's disease. Neurology 1993, 43:1467-1472.
48. Scharfman H.E. The CA3 "backprojection" to the dentate gyrus. Prog. Brain Res. 2007, 163:627-637.
49. Sederberg P.B., Schulze-Bonhage A., Madsen J.R., Bromfield E.B., Litt B., Brandt A., Kahana M.J. Gamma oscillations distinguish true from false memories. Psychol. Sci. 2007, 18:927-932.
50. Skaggs W.E., McNaughton B.L. Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience. Science 1996, 271:1870-1873.
51. Strittmatter W.J., Saunders A.M., Schmechel D., Pericak-Vance M., Enghild J., Salvesen G.S., Roses A.D. Apolipoprotein E: high-avidity binding to beta-amyloid and increased frequency of type 4 allele in late-onset familial Alzheimer disease. Proc. Natl. Acad. Sci. USA 1993, 90:1977-1981.
52. Sullivan P.M., Mace B.E., Maeda N., Schmechel D.E. Marked regional differences of brain human apolipoprotein E expression in targeted replacement mice. Neuroscience 2004, 124:725-733.
53. Sullivan D., Csicsvari J., Mizuseki K., Montgomery S., Diba K., Buzsáki G. Relationships between hippocampal sharp waves, ripples, and fast gamma oscillation: influence of dentate and entorhinal cortical activity. J. Neurosci. 2011, 31:8605-8616.
54. Tong L.M., Djukic B., Arnold C., Gillespie A.K., Yoon S.Y., Wang M.M., Zhang O., Knoferle J., Rubenstein J.L.R., Alvarez-Buylla A., Huang Y. Inhibitory interneuron progenitor transplantation restores normal learning and memory in ApoE4 knock-in mice without or with Aβ accumulation. J. Neurosci. 2014, 34:9506-9515.
55. Witton J., Staniaszek L.E., Bartsch U., Randall A.D., Jones M.W., Brown J.T. Disrupted hippocampal sharp-wave ripple-associated spike dynamics in a transgenic mouse model of dementia. J. Physiol. 2014, Published online December 5, 2014. 10.1113/jphysiol.2014.282889.
56. Ylinen A., Bragin A., Nádasdy Z., Jandó G., Szabó I., Sik A., Buzsáki G. Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms. J. Neurosci. 1995, 15:30-46.