Sensory network dysfunction, behavioral impairments, and their reversibility in an alzheimer's β-amyloidosis mouse model

Journal of Neuroscience

Volumn 31, Issue 44, 2011, Pages 15962-15971

  Wesson, Daniel W ^a,b,c   Borkowski, Anne H ^a   Landreth, Gary E ^c   Nixon, Ralph A ^a,b   Levy, Efrat ^a,b   Wilson, Donald A ^a,b,d  

^a NATHAN S KLINE INSTITUTE FOR PSYCHIATRIC RESEARCH   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d NEW YORK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; LIVER X RECEPTOR AGONIST;

ALZHEIMER DISEASE; AMYLOIDOSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR DISORDER; CONTROLLED STUDY; HIPPOCAMPUS; HISTOLOGY; IN VIVO STUDY; MOUSE; NONHUMAN; ODOR; OLFACTORY BULB; OLFACTORY SYSTEM; PRIORITY JOURNAL; PROTEIN DEGRADATION; PYRIFORM CORTEX; SENSORY DYSFUNCTION; SMELLING; SYNAPTIC TRANSMISSION;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; AMYLOIDOSIS; ANIMALS; BEHAVIORAL SYMPTOMS; BENZOIC ACIDS; BENZYLAMINES; BRAIN WAVES; CEREBRAL CORTEX; DISEASE MODELS, ANIMAL; ELECTROENCEPHALOGRAPHY; ENZYME-LINKED IMMUNOSORBENT ASSAY; FOURIER ANALYSIS; HABITUATION, PSYCHOPHYSIOLOGIC; HUMANS; MICE; MICE, TRANSGENIC; ODORS; OLFACTORY PATHWAYS; SENSATION DISORDERS; SMELL; THIAZOLES;

EID: 80155123438     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2085-11.2011     Document Type: Article

References (55)

1. Abramov E, Dolev I, Fogel H, Ciccotosto GD, Ruff E, Slutsky I (2009) Amyloid-β as a positive endogenous regulator of release probability at hippocampal synapses. Nat Neurosci 12:1567-1576.
2. Adrian ED (1951) The role of air movement in olfactory stimulation. J Physiol 114:4-5.
3. A-Gonzalez N, Bensinger SJ, Hong C, Beceiro S, Bradley MN, Zelcer N, Deniz J, Ramirez C, Díaz M, Gallardo G, de Galarreta CR, Salazar J, Lopez F, Edwards P, Parks J, Andujar M, Tontonoz P, Castrillo A (2009) Apoptotic cells promote their own clearance and immune tolerance through activation of the nuclear receptor LXR. Immunity 31:245-258.
4. Arnold SE, Hyman BT, Flory J, Damasio AR, Van Hoesen GW (1991) The topographical and neuroanatomical distribution of neurofibrillary tangles and neuritic plaques in the cerebral cortex of patients with Alzheimer's disease. Cereb Cortex 1:103-116.
5. Arnold SE, Lee EB, Moberg PJ, Stutzbach L, Kazi H, Han LY, Lee VM, Trojanowski JQ (2010) Olfactory epithelium amyloid-beta and paired helical filament-tau pathology in Alzheimer disease. Ann Neurol 67:462-469.
6. Bacon AW, Bondi MW, Salmon DP, Murphy C (1998) Very early changes in olfactory functioning due to Alzheimer's disease and the role of apolipoprotein E in olfaction. Ann N Y Acad Sci 855:723-731.
7. Barnes DC, Hofacer RD, Zaman AR, Rennaker RL, Wilson DA (2008) Olfactory perceptual stability and discrimination. Nat Neurosci 11:1378-1380.
8. Bishop NA, Lu T, Yankner BA (2010) Neural mechanisms of ageing and cognitive decline. Nature 464:529-535.
9. Buckner RL, Sepulcre J, Talukdar T, Krienen FM, Liu H, Hedden T, Andrews-Hanna JR, Sperling RA, Johnson KA (2009) Cortical hubs revealed by intrinsic functional connectivity: mapping, assessment of stability, and relation to Alzheimer's disease. J Neurosci 29:1860-1873.
10. Busche MA, Eichhoff G, Adelsberger H, Abramowski D, Wiederhold KH, Haass C, Staufenbiel M, Konnerth A, Garaschuk O (2008) Clusters of hyperactive neurons near amyloid plaques in a mouse model of Alzheimer's disease. Science 321:1686-1689.
11. Buzsaki G (2006) Rhythms of the brain. New York: Oxford UP.
12. Chabaud P, Ravel N, Wilson DA, Gervais R (1999) Functional coupling in rat central olfactory pathways: a coherence analysis. Neurosci Lett 276:17-20.
13. Cirrito JR, Yamada KA, Finn MB, Sloviter RS, Bales KR, May PC, Schoepp DD, Paul SM, Mennerick S, Holtzman DM (2005) Synaptic activity regulates interstitial fluid amyloid-β levels in vivo. Neuron 48:913-922.
14. Dalton P, Wysocki CJ (1996) The nature and duration of adaptation following long-term odor exposure. Percept Psychophys 58:781-792.
15. Doucette W, Milder J, Restrepo D (2007) Adrenergic modulation of olfactory bulb circuitry affects odor discrimination. Learn Mem 14:539-547.
16. Freeman WJ (1975) Mass action in the nervous system: examination of the neurophysiological basis of adaptive behavior through the EE. New York: Academic.
17. Gilbert PE, Murphy C (2004) The effect of the ApoE e4 allele on recognition memory for olfactory and visual stimuli in patients with pathologically confirmed Alzheimer's disease, probable Alzheimer's disease, and healthy elderly controls. J Clin Exp Neuropsychol 26:779-794.
18. Hsiao K, Chapman P, Nilsen S, Eckman C, Harigaya Y, Younkin S, Yang F, Cole G (1996) Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice. Science 274:99-102.
19. Janus C, Pearson J, McLaurin J, Mathews PM, Jiang Y, Schmidt SD, Chishti MA, Horne P, Heslin D, French J, Mount HT, Nixon RA, Mercken M, Bergeron C, Fraser PE, St George-Hyslop P, Westaway D (2000) Aβ peptide immunization reduces behavioural impairment and plaques in a model of Alzheimer's disease. Nature 408:979-982.
20. Jeong J (2004) EEG dynamics in patients with Alzheimer's disease. Clin Neurophysiol 115:1490-1505.
21. Jiang Q, Lee CY, Mandrekar S, Wilkinson B, Cramer P, Zelcer N, Mann K, Lamb B, Willson TM, Collins JL, Richardson JC, Smith JD, Comery TA, Riddell D, Holtzman DM, Tontonoz P, Landreth GE (2008) ApoE promotes the proteolytic degradation of Aβ. Neuron 58:681-693.
22. Kamenetz F, Tomita T, Hsieh H, Seabrook G, Borchelt D, Iwatsubo T, Sisodia S, Malinow R (2003) APP processing and synaptic function. Neuron 37:925-937.
23. Kapogiannis D, Mattson MP (2011) Disrupted energy metabolism and neuronal circuit dysfunction in cognitive impairment and Alzheimer's disease. Lancet Neurol 10:187-198.
24. Kay LM, Beshel J (2010) A beta oscillation network in the rat olfactory system during a 2-alternative choice odor discrimination task. J Neurophysiol 104:829-839.
25. Kay LM, Beshel J, Brea J, Martin C, Rojas-Líbano D, Kopell N (2009) Olfactory oscillations: the what, how and what for. Trends Neurosci 32:207-214.
26. Koenigsknecht J, Landreth G (2004) Microglial phagocytosis of fibrillar β-amyloid through a β1 integrin-dependent mechanism. J Neurosci 24:9838-9846.
27. Kopell N, Ermentrout GB, Whittington MA, Traub RD (2000) Gamma rhythms and beta rhythms have different synchronization properties. Proc Natl Acad Sci USA 97:1867-1872.
28. Kounnas MZ, Danks AM, Cheng S, Tyree C, Ackerman E, Zhang X, Ahn K, Nguyen P, Comer D, Mao L, Yu C, Pleynet D, Digregorio PJ, Velicelebi G, Stauderman KA, Comer WT, Mobley WC, Li YM, Sisodia SS, Tanzi RE, Wagner SL (2010) Modulation of gamma-secretase reduces betaamyloid deposition in a transgenic mouse model of Alzheimer's disease. Neuron 67:769-780.
29. Lazarov O, Lee M, Peterson DA, Sisodia SS (2002) Evidence that synaptically released β-amyloid accumulates as extracellular deposits in the hippocampus of transgenic mice. J Neurosci 22:9785-9793.
30. Li W, Howard JD, Gottfried JA (2010) Disruption of odour quality coding in piriform cortex mediates olfactory deficits in Alzheimer's disease. Brain 133:2714-2726.
31. Mesholam RI, Moberg PJ, Mahr RN, Doty RL (1998) Olfaction in neurodegenerative disease: a meta-analysis of olfactory functioning in Alzheimer's and Parkinson's diseases. Arch Neurol 55:84-90.
32. Mi W, Pawlik M, Sastre M, Jung SS, Radvinsky DS, Klein AM, Sommer J, Schmidt SD, Nixon RA, Mathews PM, Levy E (2007) Cystatin C inhibits amyloid-β deposition in Alzheimer's disease mouse models. Nat Genet 39:1440-1442.
33. Murphy C (1999) Loss of olfactory function in dementing disease. Physiol Behav 66:177-182.
34. Neville KR, Haberly LB (2003) Beta and gamma oscillations in the olfactory system of the urethane-anesthetized rat. J Neurophysiol 90:3921-3930.
35. Nusser Z, Kay LM, Laurent G, Homanics GE, Mody I (2001) Disruption of GABAA receptors on GABAergic interneurons leads to increased oscillatory power in the olfactory bulb network. J Neurophysiol 86:2823-2833.
36. Palop JJ, Mucke L (2010) Amyloid-β-induced neuronal dysfunction in Alzheimer's disease: from synapses toward neural networks. Nat Neurosci 13:812-818.
37. Palop JJ, Chin J, Roberson ED, Wang J, Thwin MT, Bien-Ly N, Yoo J, Ho KO, Yu GQ, Kreitzer A, Finkbeiner S, Noebels JL, Mucke L (2007) Aberrant excitatory neuronal activity and compensatory remodeling of inhibitory hippocampal circuits in mouse models of Alzheimer's disease. Neuron 55:697-711.
38. Paxinos G, Franklin K (2000) The mouse brain in stereotaxic coordinates, Ed 2. San Diego: Academic.
39. Price JL, Davis PB, Morris JC, White DL (1991) The distribution of tangles, plaques and related immunohistochemical markers in healthy aging and Alzheimer's disease. Neurobiol Aging 12:295-312.
40. Puzzo D, Privitera L, Leznik E, Fà M, Staniszewski A, Palmeri A, Arancio O (2008) Picomolar amyloid-β positively modulates synaptic plasticity and memory in hippocampus. J Neurosci 28:14537-14545.
41. Rall W, Shepherd GM (1968) Theoretical reconstruction of field potentials and dendrodendritic synaptic interactions in olfactory bulb. J Neurophysiol 31:884-915.
42. Santos SF, Pierrot N, Octave JN (2010) Network excitability dysfunction in Alzheimer's disease: insights from in vitro and in vivo models. Rev Neurosci 21:153-171.
43. Schmidt SD, Nixon RA, Mathews PM (2005) ELISA method for measurement of amyloid-β levels. Methods Mol Biol 299:279-297.
44. Seeley WW, Crawford RK, Zhou J, Miller BL, Greicius MD (2009) Neurodegenerative diseases target large-scale human brain networks. Neuron 62:42-52.
45. Selkoe DJ (2008) Soluble oligomers of the amyloid β-protein impair synaptic plasticity and behavior. Behav Brain Res 192:106-113.
46. Sperling RA, Laviolette PS, O'Keefe K, O'Brien J, Rentz DM, Pihlajamaki M, Marshall G, Hyman BT, Selkoe DJ, Hedden T, Buckner RL, Becker JA, Johnson KA (2009) Amyloid deposition is associated with impaired default network function in older persons without dementia. Neuron 63:178-188.
47. Spires TL, Meyer-Luehmann M, Stern EA, McLean PJ, Skoch J, Nguyen PT, Bacskai BJ, Hyman BT (2005) Dendritic spine abnormalities in amyloid precursor protein transgenic mice demonstrated by gene transfer and intravital multiphoton microscopy. J Neurosci 25:7278-7287.
48. Uhlhaas PJ, Singer W (2006) Neural synchrony in brain disorders: relevance for cognitive dysfunctions and pathophysiology. Neuron 52:155-168.
49. Varela F, Lachaux JP, Rodriguez E, Martinerie J (2001) The brainweb: phase synchronization and large-scale integration. Nat Rev Neurosci 2:229-239.
50. Wesson DW, Levy E, Nixon RA, Wilson DA (2010) Olfactory dysfunction correlates withβ-amyloid plaque burden in an Alzheimer's disease mouse model. J Neurosci 30:505-514.
51. Wilson DA (2001) Scopolamine enhances generalization between odor representations in rat olfactory cortex. Learn Mem 8:279-285.
52. Wilson DA, Linster C (2008) Neurobiology of a simple memory. J Neurophysiol 100:2-7.
53. Wilson DA, Yan X (2010) Sleep-like states modulate functional connectivity in the rat olfactory system. J Neurophysiol 104:3231-3239.
54. Wilson DA, Kadohisa M, Fletcher ML (2006) Cortical contributions to olfaction: plasticity and perception. Semin Cell Dev Biol 17:462-470.
55. Zelcer N, Khanlou N, Clare R, Jiang Q, Reed-Geaghan EG, Landreth GE, Vinters HV, Tontonoz P (2007) Attenuation of neuroinflammation and Alzheimer's disease pathology by liver x receptors. Proc Natl Acad Sci USA 104:10601-10606.