Morphological alterations to neurons of the amygdala and impaired fear conditioning in a transgenic mouse model of Alzheimer's disease

Journal of Pathology

Volumn 219, Issue 1, 2009, Pages 41-51

  Knafo, Shira ^a   Venero, Cesar ^b   Merino Serrais, Paula ^a   Fernaud Espinosa, Isabel ^a   Gonzalez Soriano, Juncal ^c   Ferrer, Isidro ^d   Santpere, Gabriel ^d   DeFelipe, Javier ^a  

^a INSTITUTO CAJAL   (Spain)

^b UNIVERSIDAD NACIONAL DE EDUCACIÓN A DISTANCIA   (Spain)

^c UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^d HOSPITAL UNIVERSITARI DE BELLVITGE   (Spain)

Author keywords

Alzheimer's disease; Amyloid; APP; Cognition; Confocal microscopy; Dementia; Dendritic spines; Learning; Morphology; Plaques; PS1; Unbiased stereology

Indexed keywords

AMYLOID BETA PROTEIN;

ALZHEIMER DISEASE; AMYGDALOID NUCLEUS; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY; ARTICLE; AUDITORY STIMULATION; BRAIN NERVE CELL; CELL DENSITY; CELL STRUCTURE; CONDITIONED REFLEX; CONDITIONING; CONTROLLED STUDY; DENDRITIC SPINE; FEAR; LEARNING; MALE; MOUSE; NERVE PROJECTION; NONHUMAN; PRIORITY JOURNAL;

ALZHEIMER DISEASE; AMYGDALA; ANIMALS; CONDITIONING, CLASSICAL; DENDRITIC SPINES; FEAR; MALE; MICE; MICE, TRANSGENIC; MICROSCOPY, CONFOCAL; MODELS, ANIMAL; NEURONAL PLASTICITY; SENILE PLAQUES;

EID: 68849084411     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.2565     Document Type: Article

References (72)

1. Copeland MP, Daly E, Hines V, Mastromauro C, Zaitchik D, Gunther J, et al. Psychiatric symptomatology and prodromal Alzheimer's disease. Alzheimer Dis Assoc Disord 2003;17:1-8.
2. Mirra SS, Hyman BT. Aging and dementia. In Greenfield's Neuropathology (7th edn), Graham DI, Lantos PI (eds). Arnold: New York, 2002; 195-272.
3. Schafe GE, Doyere V, LeDoux JE. Tracking the fear engram: the lateral amygdala is an essential locus of fear memory storage. J Neurosci 2005;25:10010-10014.
4. Vereecken TH, Vogels OJ, Nieuwenhuys R. Neuron loss and shrinkage in the amygdala in Alzheimer's disease. Neurobiol Aging 1994;15:45-54.
5. Scott SA, DeKosky ST, Scheff SW. Volumetric atrophy of the amygdala in Alzheimer's disease: quantitative serial reconstruction. Neurology 1991;41:351.
6. Mori E, Ikeda M, Hirono N, Kitagaki H, Imamura T, Shimomura T. Amygdalar volume and emotional memory in Alzheimer's disease. Am J Psychiatry 1999;156:216-222.
7. Blair HT, Schafe GE, Bauer EP, Rodrigues SM, LeDoux JE. Synaptic plasticity in the lateral amygdala: a cellular hypothesis of fear conditioning. Learn Mem 2001;8:229-242.
8. Rodrigues SM, Schafe GE, LeDoux JE. Molecular mechanisms underlying emotional learning and memory in the lateral amygdala. Neuron 2004;44:75-91.
9. McDonald AJ. Cortical pathways to the mammalian amygdala. Prog Neurobiol 1998;55:257-332.
10. McDonald AJ, Culberson JL. Neurons of the basolateral amygdala: a Golgi study in the opossum (Didelphis virginiana). Am J Anat 1981;162:327-342.
11. Borchelt DR, Ratovitski T, van Lare J, Lee MK, Gonzales V, Jenkins NA, et al. Accelerated amyloid deposition in the brains of transgenic mice coexpressing mutant presenilin 1 and amyloid precursor proteins. Neuron 1997;19:939-945.
12. Gerlai R, Fitch T, Bales KR, Gitter BD. Behavioral impairment of APP(V717F) mice in fear conditioning: is it only cognition? Behav Brain Res 2002;136:503-509.
13. Dineley KT, Xia X, Bui D, Sweatt JD, Zheng H. Accelerated plaque accumulation, associative learning deficits, and upregulation of alpha 7 nicotinic receptor protein in transgenic mice co-expressing mutant human presenilin 1 and amyloid precursor proteins. J Biol Chem 2002;277:22768-22780.
14. Trinchese F, Fa' M, Liu S, Zhang H, Hidalgo A, Schmidt SD, et al. Inhibition of calpains improves memory and synaptic transmission in a mouse model of Alzheimer disease. J Clin Invest 2008;118:2796-2807.
15. Sah S, Faber ES, Lopez De AM, POWER J. The amygdaloid complex: anatomy and physiology. Physiol Rev 2003;83:803-834.
16. Gray EG. Electron microscopy of synaptic contacts on dendrite spines of the cerebral cortex. Nature 1959;183:1592-1593.
17. Lamprecht R, LeDoux J. Structural plasticity and memory. Nat Rev Neurosci 2004;5:45-54.
18. Lang C, Barco A, Zablow L, Kandel ER, Siegelbaum SA, Zakharenko SS. Transient expansion of synaptically connected dendritic spines upon induction of hippocampal long-term potentiation. Proc Natl Acad Sci U S A 2004;101:16665-16670.
19. Majewska A, Tashiro A, Yuste R. Regulation of spine calcium dynamics by rapid spine motility. J Neurosci 2000;20:8262-8268.
20. Lacor PN, Buniel MC, Furlow PW, Sanz Clemente A, Velasco PT, Wood M, et al. A{beta} oligomer-induced aberrations in synapse composition, shape, and density provide a molecular basis for loss of connectivity in Alzheimer's disease. J Neurosci 2007;27:796-807.
21. 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;30:572-580.
22. Terry RD. Cell death or synaptic loss in Alzheimer disease. J Neuropathol Exp Neurol 2000;59:1118-1119.
23. Tsai J, Grutzendler J, Duff K, Gan WB. Fibrillar amyloid deposition leads to local synaptic abnormalities and breakage of neuronal branches. Nature Neurosci 2004;7:1181-1183.
24. Dong H, Martin MV, Chambers S, Csernansky JG. Spatial relationship between synapse loss and beta-amyloid deposition in Tg2576 mice. J Comp Neurol 2007;500:311-321.
25. Scheuner D, Eckman C, Jensen M, Song X, Citron M, Suzuki N, et al. Secreted amyloid beta-protein similar to that in the senile plaques of Alzheimer's disease is increased in vivo by the presenilin 1 and 2 and APP mutations linked to familial Alzheimer's disease. Nature Med 1996;2:864-870.
26. Herrero AI, Sandi C, Venero C. Individual differences in anxiety trait are related to spatial learning abilities and hippocampal expression of mineralocorticoid receptors. Neurobiol Learn Mem 2006;86:150-159.
27. Moller A, Strange P, Gundersen HJ. Efficient estimation of cell volume and number using the nucleator and the disector. J Microsc 1990;159:61-71.
28. Knafo S, Alonso-Nanclares L, Gonzalez-Soriano J, Merino-Serrais P, Fernaud-Espinosa I, Ferrer I, et al. Widespread changes in dendritic spines in a model of Alzheimer's disease. Cereb Cortex 2009;19:586-592.
29. Conover WJ. Statistics of the Kolmogorov-Smirnov type. In Practical Nonparametric Statistics. John Wiley: New York, 1999;428-456.
30. Lister RG. The use of a plus-maze to measure anxiety in the mouse. Psychopharmacology (Berlin) 1987;92:180-185.
31. Phillips RG, LeDoux JE. Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav Neurosci 1992;106:274-285.
32. Kim M, Davis M. Electrolytic lesions of the amygdala block acquisition and expression of fear-potentiated startle even with extensive training but do not prevent reacquisition. Behav Neurosci 1993;107:580-595.
33. Fanselow MS, LeDoux JE. Why we think plasticity underlying Pavlovian fear conditioning occurs in the basolateral amygdala. Neuron 1999;23:229-232.
34. Nader K, Schafe GE, Le Doux JE. Fear memories require protein synthesis in the amygdala for reconsolidation after retrieval. Nature 2000;406:722-726.
35. Marsch R, Foeller E, Rammes G, Bunck M, Kossl M, Holsboer F, et al. Reduced anxiety, conditioned fear, and hippocampal long-term potentiation in transient receptor potential vanilloid type 1 receptor-deficient mice. J Neurosci 2007;27:832-839.
36. Koo JW, Han JS, Kim JJ. Selective neurotoxic lesions of basolateral and central nuclei of the amygdala produce differential effects on fear conditioning. J Neurosci 2004;24:7654-7662.
37. Stark AK, Pelvig DP, Jorgensen AM, Andersen BB, Pakkenberg B. Measuring morphological and cellular changes in Alzheimer's dementia: a review emphasizing stereology. Curr Alzheimer Res 2005;2:449-481.
38. Kromer Vogt LJ, Hyman BT, Van Hoesen GW, Damasio AR. Pathological alterations in the amygdala in Alzheimer's disease. Neuroscience 1990;37:377-385.
39. Mullen RJ, Buck CR, Smith AM. NeuN, a neuronal specific nuclear protein in vertebrates. Development 1992;116:201-211.
40. Rogan MT, Staubli UV, LeDoux JE. Fear conditioning induces associative long-term potentiation in the amygdala. Nature 1997;390:604-607.
41. Yuste R, Denk W. Dendritic spines as basic functional units of neuronal integration. Nature 1995;375:682-684.
42. Alpar A, Ueberham U, Bruckner MK, Seeger G, Arendt T, Gartner U. Different dendrite and dendritic spine alterations in basal and apical arbors in mutant human amyloid precursor protein transgenic mice. Brain Res 2006;1099:189-198.
43. Cruz L, Urbanc B, Buldyrev SV, Christie R, Gomez-Isla T, Havlin S, et al. Aggregation and disaggregation of senile plaques in Alzheimer disease. Proc Natl Acad Sci U S A 1997;94:7612-7616.
44. Spires TL, Meyer-Luehmann M, Stern EA, McLean PJ, Skoch J, Nguyen PT, et al. Dendritic spine abnormalities in amyloid precursor protein transgenic mice demonstrated by gene transfer and intravital multiphoton microscopy. J Neurosci 2005;25:7278-7287.
45. Hamann S, Monarch ES, Goldstein FC. Impaired fear conditioning in Alzheimer's disease. Neuropsychologia 2002;40:1187-1195.
46. Hsiao K, Chapman P, Nilsen S, Eckman C, Harigaya Y, Younkin S, et al. Correlative memory deficits, abeta elevation, and amyloid plaques in transgenic mice. Science 1996;274:99-103.
47. Clarke J, Thornell A, Corbett D, Soininen H, Hiltunen M, Jolkkonen J. Overexpression of APP provides neuroprotection in the absence of functional benefit following middle cerebral artery occlusion in rats. Eur J Neurosci 2007;26:1845-1852.
48. Balogh SA, Wehner JM. Inbred mouse strain differences in the establishment of long-term fear memory. Behav Brain Res 2003;140:97-106.
49. Kaplan PS, Hearst E. Bridging temporal gaps between CS and US in autoshaping: insertion of other stimuli before, during, and after CS. J Exp Psychol Anim Behav Process 1982;8:187-203.
50. Rescorla RA. 'Configural' conditioning in discrete-trial bar pressing. J Comp Physiol Psychol 1972;79:307-317.
51. Herzog AG, Kemper TL. Amygdaloid changes in aging and dementia. Arch Neurol 1980;37:625-629.
52. Selkoe DJ. Alzheimer's disease is a synaptic failure. Science 2002;298:789-791.
53. Poirazi P, Mel BW. Impact of active dendrites and structural plasticity on the memory capacity of neural tissue. Neuron 2001;29:779-796.
54. Masliah E, Crews L, Hansen L. Synaptic remodeling during aging and in Alzheimer's disease. J Alzheimer's Dis 2006;9:91-99.
55. Harris KM, Stevens JK. Dendritic spines of CA 1 pyramidal cells in the rat hippocampus: serial electron microscopy with reference to their biophysical characteristics. J Neurosci 1989;9:2982-2997.
56. Schikorski T, Stevens CF. Quantitative ultrastructural analysis of hippocampal excitatory synapses. J Neurosci 1997;17:5858-5867.
57. Arellano JI, Espinosa A, Fairen A, Yuste R, Defelipe J. Non-synaptic dendritic spines in neocortex. Neuroscience 2007;145:464-469.
58. Nusser Z, Lujan R, Laube G, Roberts JD, Molnar E, Somogyi P. Cell type and pathway dependence of synaptic AMPA receptor number and variability in the hippocampus. Neuron 1998;21:545-559.
59. Dobrunz LE, Stevens CF. Heterogeneity of release probability, facilitation, and depletion at central synapses. Neuron 1997;18:995-1008.
60. Humeau Y, Herry C, Kemp N, Shaban H, Fourcaudot E, Bissiere S, et al. Dendritic spine heterogeneity determines afferent-specific Hebbian plasticity in the amygdala. Neuron 2005;45:119-131.
61. Kasai H, Matsuzaki M, Noguchi J, Yasumatsu N, Nakahara H. Structure-stability-function relationships of dendritic spines. Trends Neurosci 2003;26:360-368.
62. Bourne J, Harris KM. Do thin spines learn to be mushroom spines that remember? Curr Opin Neurobiol 2007;17:381-386.
63. Trachtenberg JT, Chen BE, Knott GW, Feng G, Sanes JR, Welker E, et al. Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex. Nature 2002;420:788-794.
64. Grutzendler J, Kasthuri N, Gan WB. Long-term dendritic spine stability in the adult cortex. Nature 2002;420:812-816.
65. Matsuo N, Reijmers L, Mayford M. Spine-type-specific recruitment of newly synthesized AMPA receptors with learning. Science 2008;319:1104- 1107.
66. Matsuzaki M, Ellis-Davies GC, Nemoto T, Miyashita Y, Iino M, Kasai H. Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons. Nature Neurosci 2001;4:1086-1092.
67. Ashby MC, Maier SR, Nishimune A, Henley JM. Lateral diffusion drives constitutive exchange of AMPA receptors at dendritic spines and is regulated by spine morphology. J Neurosci 2006;26:7046-7055.
68. Nimchinsky EA, Yasuda R, Oertner TG, Svoboda K. The number of glutamate receptors opened by synaptic stimulation in single hippocampal spines. J Neurosci 2004;24:2054-2064.
69. Lee HK, Takamiya K, Han JS, Man H, Kim CH, Rumbaugh G, et al. Phosphorylation of the AMPA receptor GluR1 subunit is required for synaptic plasticity and retention of spatial memory. Cell 2003;112:631-643.
70. Moechars D, Lorent K, de SB, Dewachter I, Van LF. Expression in brain of amyloid precursor protein mutated in the alpha-secretase site causes disturbed behavior, neuronal degeneration and premature death in transgenic mice. EMBO J 1996;15:1265-1274.
71. Westerman MA, Cooper-Blacketer D, Mariash A, Kotilinek L, Kawarabayashi T, Younkin LH, et al. The relationship between Abeta and memory in the Tg2576 mouse model of Alzheimer's disease. J Neurosci 2002;22:1858-1867.
72. Haass C, Selkoe DJ. Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid beta-peptide. Nature Rev Mol Cell Biol 2007;8:101-112.