Amyloid-β alters ongoing neuronal activity and excitability in the frontal cortex

Neurobiology of Aging

Volumn 35, Issue 9, 2014, Pages 1982-1991

  Kellner, Vered ^a   Menkes Caspi, Noa ^a   Beker, Shlomit ^a   Stern, Edward A ^a,b  

^a BAR ILAN UNIVERSITY   (Israel)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Alzheimer's disease; APPswe PS1dE9; Background activity; Down state; Hyperexcitability; Invivo; Membrane potential; Mouse model; Up state

Indexed keywords

AMYLOID BETA PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ACTIVITY; CONTROLLED STUDY; FEMALE; FRONTAL CORTEX; IN VIVO STUDY; MALE; MOUSE; NERVE CELL; NERVE CELL EXCITABILITY; NERVE CELL MEMBRANE POTENTIAL; NERVE CELL MEMBRANE STEADY POTENTIAL; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SYNAPTIC POTENTIAL; SYNAPTIC TRANSMISSION; TRANSGENIC MOUSE; AGING; ALZHEIMER DISEASE; ANIMAL; CYTOLOGY; DISEASE COURSE; EVOKED RESPONSE; FRONTAL LOBE; MEMBRANE POTENTIAL; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY;

AGING; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; DISEASE PROGRESSION; EVOKED POTENTIALS; FRONTAL LOBE; MEMBRANE POTENTIALS; MICE, TRANSGENIC; PYRAMIDAL CELLS;

EID: 84902080993     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2014.04.001     Document Type: Article

References (47)

1. Abeles M. Quantification, smoothing, and confidence limits for single-units' histograms. J.Neurosci. Methods 1982, 5:317-325.
2. Amatniek J.C., Hauser W.A., DelCastillo-Castaneda C., Jacobs D.M., Marder K., Bell K., Albert M., Brandt J., Stern Y. Incidence and predictors of seizures in patients with Alzheimer's disease. Epilepsia 2006, 47:867-872.
3. Arieli A., Sterkin A., Grinvald A., Aertsen A. Dynamics of ongoing activity: explanation of the large variability in evoked cortical responses. Science 1996, 273:1868-1871.
4. Azouz R., Gray C.M. Cellular mechanisms contributing to response variability of cortical neurons invivo. J.Neurosci. 1999, 19:2209-2223.
5. Bernander O., Douglas R.J., Martin K.A., Koch C. Synaptic background activity influences spatiotemporal integration in single pyramidal cells. Proc. Natl. Acad. Sci. U.S.A 1991, 88:11569-11573.
6. Bero A.W., Bauer A.Q., Stewart F.R., White B.R., Cirrito J.R., Raichle M.E., Culver J.P., Holtzman D.M. Bidirectional relationship between functional connectivity and amyloid-beta deposition in mouse brain. J.Neurosci. 2012, 32:4334-4340.
7. Bero A.W., Yan P., Roh J.H., Cirrito J.R., Stewart F.R., Raichle M.E., Lee J.M., Holtzman D.M. Neuronal activity regulates the regional vulnerability to amyloid-beta deposition. Nat. Neurosci. 2011, 14:750-756.
8. Busche M.A., Eichhoff G., Adelsberger H., Abramowski D., Wiederhold K.H., Haass C., Staufenbiel M., Konnerth A., Garaschuk O. Clusters of hyperactive neurons near amyloid plaques in a mouse model of Alzheimer's disease. Science 2008, 321:1686-1689.
9. Cirrito J.R., Yamada K.A., Finn M.B., Sloviter R.S., Bales K.R., May P.C., Schoepp D.D., Paul S.M., Mennerick S., Holtzman D.M. Synaptic activity regulates interstitial fluid amyloid-beta levels invivo. Neuron 2005, 48:913-922.
10. Connors B.W., Gutnick M.J. Intrinsic firing patterns of diverse neocortical neurons. Trends Neurosci. 1990, 13:99-104.
11. Cowan R.L., Wilson C.J. Spontaneous firing patterns and axonal projections of single corticostriatal neurons in the rat medial agranular cortex. J.Neurophysiol. 1994, 71:17-32.
12. Crimins J.L., Pooler A., Polydoro M., Luebke J.I., Spires-Jones T.L. The intersection of amyloid beta and tau in glutamatergic synaptic dysfunction and collapse in Alzheimer's disease. Ageing Res. Rev. 2013, 12:757-763.
13. D'Amore J.D., Kajdasz S.T., McLellan M.E., Bacskai B.J., Stern E.A., Hyman B.T. Invivo multiphoton imaging of a transgenic mouse model of Alzheimer disease reveals marked thioflavine-S-associated alterations in neurite trajectories. J.Neuropathol. Exp. Neurol. 2003, 62:137-145.
14. Garcia-Alloza M., Robbins E.M., Zhang-Nunes S.X., Purcell S.M., Betensky R.A., Raju S., Prada C., Greenberg S.M., Bacskai B.J., Frosch M.P. Characterization of amyloid deposition in the APPswe/PS1dE9 mouse model of Alzheimer disease. Neurobiol. Dis. 2006, 24:516-524.
15. Grienberger C., Rochefort N.L., Adelsberger H., Henning H.A., Hill D.N., Reichwald J., Staufenbiel M., Konnerth A. Staged decline of neuronal function invivo in an animal model of Alzheimer's disease. Nat. Commun. 2012, 3:774.
16. Gurevicius K., Lipponen A., Tanila H. Increased cortical and thalamic excitability in freely moving APPswe/PS1dE9 mice modeling epileptic activity associated with Alzheimer's disease. Cereb. Cortex 2013, 23:1148-1158.
17. Haider B., Duque A., Hasenstaub A.R., McCormick D.A. Neocortical network activity invivo is generated through a dynamic balance of excitation and inhibition. J.Neurosci. 2006, 26:4535-4545.
18. Hardy J., Selkoe D.J. The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 2002, 297:353-356.
19. Ingelsson M., Fukumoto H., Newell K.L., Growdon J.H., Hedley-Whyte E.T., Frosch M.P., Albert M.S., Hyman B.T., Irizarry M.C. Early Abeta accumulation and progressive synaptic loss, gliosis, and tangle formation in AD brain. Neurology 2004, 62:925-931.
20. Jankowsky J.L., Slunt H.H., Ratovitski T., Jenkins N.A., Copeland N.G., Borchelt D.R. Co-expression of multiple transgenes in mouse CNS: a comparison of strategies. Biomol. Eng. 2001, 17:157-165.
21. Kamenetz F., Tomita T., Hsieh H., Seabrook G., Borchelt D., Iwatsubo T., Sisodia S., Malinow R. APP processing and synaptic function. Neuron 2003, 37:925-937.
22. Knowles R.B., Wyart C., Buldyrev S.V., Cruz L., Urbanc B., Hasselmo M.E., Stanley H.E., Hyman B.T. Plaque-induced neurite abnormalities: implications for disruption of neural networks in Alzheimer's disease. Proc. Natl. Acad. Sci. U.S.A 1999, 96:5274-5279.
23. Koffie R.M., Meyer-Luehmann M., Hashimoto T., Adams K.W., Mielke M.L., Garcia-Alloza M., Micheva K.D., Smith S.J., Kim M.L., Lee V.M., Hyman B.T., Spires-Jones T.L. Oligomeric amyloid beta associates with postsynaptic densities and correlates with excitatory synapse loss near senile plaques. Proc. Natl. Acad. Sci. U.S.A 2009, 106:4012-4017.
24. Kuchibhotla K.V., Goldman S.T., Lattarulo C.R., Wu H.Y., Hyman B.T., Bacskai B.J. Abeta plaques lead to aberrant regulation of calcium homeostasis invivo resulting in structural and functional disruption of neuronal networks. Neuron 2008, 59:214-225.
25. Leger J.F., Stern E.A., Aertsen A., Heck D. Synaptic integration in rat frontal cortex shaped by network activity. J.Neurophysiol. 2005, 93:281-293.
26. Lesne S., Koh M.T., Kotilinek L., Kayed R., Glabe C.G., Yang A., Gallagher M., Ashe K.H. Aspecific amyloid-beta protein assembly in the brain impairs memory. Nature 2006, 440:352-357.
27. Lesne S., Kotilinek L., Ashe K.H. Plaque-bearing mice with reduced levels of oligomeric amyloid-beta assemblies have intact memory function. Neuroscience 2008, 151:745-749.
28. Liu Q., Xie X., Lukas R.J., St John P.A., Wu J. Anovel nicotinic mechanism underlies beta-amyloid-induced neuronal hyperexcitation. J.Neurosci. 2013, 33:7253-7263.
29. Lombardo J.A., Stern E.A., McLellan M.E., Kajdasz S.T., Hickey G.A., Bacskai B.J., Hyman B.T. Amyloid-beta antibody treatment leads to rapid normalization of plaque-induced neuritic alterations. J.Neurosci. 2003, 23:10879-10883.
30. Minkeviciene R., Rheims S., Dobszay M.B., Zilberter M., Hartikainen J., Fulop L., Penke B., Zilberter Y., Harkany T., Pitkanen A., Tanila H. Amyloid beta-induced neuronal hyperexcitability triggers progressive epilepsy. J.Neurosci. 2009, 29:3453-3462.
31. Palop J.J., Chin J., Roberson E.D., Wang J., Thwin M.T., Bien-Ly N., Yoo J., Ho K.O., Yu G.Q., Kreitzer A., Finkbeiner S., Noebels J.L., Mucke L. Aberrant excitatory neuronal activity and compensatory remodeling of inhibitory hippocampal circuits in mouse models of Alzheimer's disease. Neuron 2007, 55:697-711.
32. Palop J.J., Mucke L. Amyloid-beta-induced neuronal dysfunction in Alzheimer's disease: from synapses toward neural networks. Nat. Neurosci. 2010, 13:812-818.
33. Rocher A.B., Kinson M.S., Luebke J.I. Significant structural but not physiological changes in cortical neurons of 12-month-old Tg2576 mice. Neurobiol. Dis. 2008, 32:309-318.
34. Roder S., Danober L., Pozza M.F., Lingenhoehl K., Wiederhold K.H., Olpe H.R. Electrophysiological studies on the hippocampus and prefrontal cortex assessing the effects of amyloidosis in amyloid precursor protein 23 transgenic mice. Neuroscience 2003, 120:705-720.
35. Rothman S.M. Synaptic activity mediates death of hypoxic neurons. Science 1983, 220:536-537.
36. Ruan L., Kang Z., Pei G., Le Y. Amyloid deposition and inflammation in APPswe/PS1dE9 mouse model of Alzheimer's disease. Curr. Alzheimer Res. 2009, 6:531-540.
37. Sachdev R.N., Ebner F.F., Wilson C.J. Effect of subthreshold up and downstates on the whisker-evoked response in somatosensory cortex. J.Neurophysiol. 2004, 92:3511-3521.
38. Sanchez-Vives M.V., Mattia M., Compte A., Perez-Zabalza M., Winograd M., Descalzo V.F., Reig R. Inhibitory modulation of cortical up states. J.Neurophysiol. 2010, 104:1314-1324.
39. Shemer I., Holmgren C., Min R., Fulop L., Zilberter M., Sousa K.M., Farkas T., Hartig W., Penke B., Burnashev N., Tanila H., Zilberter Y., Harkany T. Non-fibrillar beta-amyloid abates spike-timing-dependent synaptic potentiation at excitatory synapses in layer 2/3 of the neocortex by targeting postsynaptic AMPA receptors. Eur. J. Neurosci. 2006, 23:2035-2047.
40. Spain W.J., Schwindt P.C., Crill W.E. Anomalous rectification in neurons from cat sensorimotor cortex invitro. J.Neurophysiol. 1987, 57:1555-1576.
41. Spires T.L., Meyer-Luehmann M., Stern E.A., McLean P.J., Skoch J., Nguyen P.T., Bacskai B.J., Hyman B.T. Dendritic spine abnormalities in amyloid precursor protein transgenic mice demonstrated by gene transfer and intravital multiphoton microscopy. J.Neurosci. 2005, 25:7278-7287.
42. Steriade M., Nunez A., Amzica F. Anovel slow (< 1 Hz) oscillation of neocortical neurons invivo: depolarizing and hyperpolarizing components. J.Neurosci. 1993, 13:3252-3265.
43. Stern E.A. Functional changes in neocortical activity in Huntington'sdisease model mice: an invivo intracellular study. Front. Syst. Neurosci. 2011, 5:47.
44. Stern E.A., Bacskai B.J., Hickey G.A., Attenello F.J., Lombardo J.A., Hyman B.T. Cortical synaptic integration invivo is disrupted by amyloid-beta plaques. J.Neurosci. 2004, 24:4535-4540.
45. Stern E.A., Kincaid A.E., Wilson C.J. Spontaneous subthreshold membrane potential fluctuations and action potential variability of rat corticostriatal and striatal neurons invivo. J.Neurophysiol. 1997, 77:1697-1715.
46. Tsodyks M., Kenet T., Grinvald A., Arieli A. Linking spontaneous activity of single cortical neurons and the underlying functional architecture. Science 1999, 286:1943-1946.
47. Zoghbi H.Y., Gage F.H., Choi D.W. Neurobiology of disease. Curr. Opin. Neurobiol. 2000, 10:655-660.