Early-onset dysfunction of retrosplenial cortex precedes overt amyloid plaque formation in Tg2576 mice

Neuroscience

Volumn 174, Issue , 2011, Pages 71-83

  Poirier, G L ^a   Amin, E ^a   Good, M A ^a   Aggleton, J P ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

Alzheimer's disease; Connectivity; Diaschisis; Disconnection; Energy metabolism; Posterior cingulate cortex

Indexed keywords

AMYLOID BETA PROTEIN[1-42]; CYTOCHROME C OXIDASE; PROTEIN C FOS;

AMYLOID PLAQUE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN REGION; CELL ACTIVITY; CONTROLLED STUDY; GENOTYPE; HIPPOCAMPUS; MALE; MOUSE; MUTATION; NERVE CELL; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RETROSPLENIAL CORTEX; THALAMUS; VISUAL CORTEX;

AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; ELECTRON TRANSPORT COMPLEX IV; ENTORHINAL CORTEX; EXPLORATORY BEHAVIOR; GYRUS CINGULI; HIPPOCAMPUS; MICE; MICE, TRANSGENIC; MUTATION; PEPTIDE FRAGMENTS; PLAQUE, AMYLOID; PROTO-ONCOGENE PROTEINS C-FOS; THALAMUS; VISUAL CORTEX;

EID: 78650955183     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2010.11.025     Document Type: Article

References (114)

1. Aggleton J.P. EPS Mid-Career Award 2006. Understanding anterograde amnesia: disconnections and hidden lesions. Q J Exp Psychol 2008, 61:1441-1471.
2. Aggleton J.P. Understanding retrosplenial amnesia: insights from animal studies. Neuropsychologia 2009, 48:2328-2338.
3. Albasser M.M., et al. Hippocampal lesions halve immediate-early gene protein counts in retrosplenial cortex: distal dysfunctions in a spatial memory system. Eur J Neurosci 2007, 26:1254-1266.
4. Allaman I., et al. Amyloid-{beta} aggregates cause alterations of astrocytic metabolic phenotype: impact on neuronal viability. J Neurosci 2010, 30:3326-3338.
5. Anandatheerthavarada H.K., et al. Mitochondrial targeting and a novel transmembrane arrest of Alzheimer's amyloid precursor protein impairs mitochondrial function in neuronal cells. J Cell Biol 2003, 161:41-54.
6. Arevalo-Serrano J., et al. Beta-amyloid peptide-induced modifications in alpha7 nicotinic acetylcholine receptor immunoreactivity in the hippocampus of the rat: relationship with GABAergic and calcium-binding proteins perikarya. Brain Res Bull 2008, 75:533-544.
7. Aupée A.M., et al. Voxel-based mapping of brain hypometabolism in permanent amnesia with PET. Neuroimage 2001, 13:1164-1173.
8. Bayer T.A., Wirths O. Intracellular accumulation of amyloid-beta-a predictor for synaptic dysfunction and neuron loss in Alzheimer's disease. Front Aging Neurosci 2010, 2:8.
9. Beher D., et al. Generation of C-terminally truncated amyloid-β peptides is dependent on γ-secretase activity. J Neurochem 2002, 82:563-575.
10. Borg J., Chereul E. Differential MRI patterns of brain atrophy in double or single transgenic mice for APP and/or SOD. J Neurosci Res 2008, 86:3275-3284.
11. Braak H., Braak E. Alzheimer's disease affects limbic nuclei of the thalamus. Acta Neuropathol 1991, 81:261-268.
12. Braak H., Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 1991, 82:239-259.
13. Braak H., Braak E. Alzheimer neuropathology and limbic circuits. Neurobiology of cingulate cortex and limbic thalamus: a comprehensive handbook 1993, 606-626. Birkhäuser, Boston, MA. B.A. Vogt, M. Gabriel (Eds.).
14. Buckner R.L., et al. Molecular, Structural, and Functional Characterization of Alzheimer's disease: evidence for a relationship between default activity, amyloid, and memory. J Neurosci 2005, 25:7709-7717.
15. Chapman P.F., et al. Impaired synaptic plasticity and learning in aged amyloid precursor protein transgenic mice. Nat Neurosci 1999, 2:271-276.
16. Chaudhuri A. Neural activity mapping with inducible transcription factors. Neuroreport 1997, 8:iii-viii.
17. Chételat G., et al. Dissociating atrophy and hypometabolism impact on episodic memory in mild cognitive impairment. Brain 2003, 126:1955-1967.
18. Chételat G., et al. Direct voxel-based comparison between grey matter hypometabolism and atrophy in Alzheimer's disease. Brain 2008, 131:60-71.
19. Chételat G., et al. Posterior cingulate hypometabolism in early Alzheimer's disease: what is the contribution of local atrophy versus disconnection? Brain 2009, 132:e133. author reply e134.
20. Christensen D.Z., et al. Formic acid is essential for immunohistochemical detection of aggregated intraneuronal A[beta] peptides in mouse models of Alzheimer's disease. Brain Res 2009, 1301:116-125.
21. Conejo N.M., et al. Brain c-Fos immunocytochemistry and cytochrome oxidase histochemistry after a fear conditioning task. Psicothema 2007, 19:295-301.
22. D'Andrea M.R., et al. The use of formic acid to embellish amyloid plaque detection in Alzheimer's disease tissues misguides key observations. Neurosci Lett 2003, 342:114-118.
23. Dickey C.A., et al. Selectively reduced expression of synaptic plasticity-related genes in amyloid precursor protein + presenilin-1 transgenic mice. J Neurosci 2003, 23:5219-5226.
24. Dong H., et al. Spatial relationship between synapse loss and beta-amyloid deposition in Tg2576 mice. J Comp Neurol 2007, 500:311-321.
25. Fellgiebel A., et al. Functional relevant loss of long association fibre tracts integrity in early Alzheimer's disease. Neuropsychologia 2008, 46:1698-1706.
26. Fennema-Notestine C., et al. Structural MRI biomarkers for preclinical and mild Alzheimer's disease. Hum Brain Mapp 2009, 30:3238-3253.
27. Ferrer I. Altered mitochondria, energy metabolism, voltage-dependent anion channel, and lipid rafts converge to exhaust neurons in Alzheimer's disease. J Bioenerg Biomembr 2009, 41:425-431.
28. Fleischmann A., et al. Impaired long-term memory and NR2A-Type NMDA receptor-dependent synaptic plasticity in mice lacking c-Fos in the CNS. J Neurosci 2003, 23:9116-9122.
29. Fox N.C., et al. Imaging of onset and progression of Alzheimer's disease with voxel-compression mapping of serial magnetic resonance images. Lancet 2001, 358:201-205.
30. Gabriel M., et al. Anterior thalamic lesions and neuronal activity in the cingulate and retrosplenial cortices during discriminative avoidance behavior in rabbits. Behav Neurosci 1983, 97:675-696.
31. Garden D.L., et al. Anterior thalamic lesions stop synaptic plasticity in retrosplenial cortex slices: expanding the pathology of diencephalic amnesia. Brain 2009, 132:1847-1857.
32. Garrido G.E.J., et al. Relation between medial temporal atrophy and functional brain activity during memory processing in Alzheimer's disease: a combined MRI and SPECT study. J Neurol Neurosurg Psychiatry 2002, 73:508-516.
33. González I., et al. Effects of beta-amyloid peptide on the density of M2 muscarinic acetylcholine receptor protein in the hippocampus of the rat: relationship with GABA-, calcium-binding protein and somatostatin-containing cells. Neuropathol Appl Neurobiol 2008, 34:506-522.
34. González I., et al. Effects of β-amyloid protein on M1 and M2 subtypes of muscarinic acetylcholine receptors in the medial septum-diagonal band complex of the rat: relationship with cholinergic, GABAergic, and calcium-binding protein perikarya. Acta Neuropathol 2007, 113:637-651.
35. Gonzalo-Ruiz A. Changes in neurotransmission systems after the injection of beta-amyloid protein beta (12-28) in the hypothalamus and anterior thalamus of the rat. Rev Neurol 1999, 28:931-941.
36. Gonzalo-Ruiz A., Arévalo-Serrano J. Interaction between β-amyloid protein and the α7 nicotinic acetylcholine receptor in cholinergic, GABAergic and calcium-binding proteins-containing neurons in the septum-diagonal band complex of the rat. Eur J Anat 2006, 10:127-142.
37. Gonzalo-Ruiz A., Sanz J.M. Alteration of cholinergic, excitatory amino acid and neuropeptide markers in the septum-diagonal band complex following injections of fibrilliar β-amyloid protein into the retrosplenial cortex of the rat. Eur J Anat 2002, 6:58-71.
38. Gonzalo-Ruiz A., et al. Glutamate and aspartate immunoreactivity in the reciprocal projections between the anterior thalamic nuclei and the retrosplenial granular cortex in the rat. Brain Res Bull 1997, 42:309-321.
39. Greenberg M.E., et al. Stimulation of neuronal acetylcholine receptors induces rapid gene transcription. Science 1986, 234:80-83.
40. Hale G., Good M. Impaired visuospatial recognition memory but normal object novelty detection and relative familiarity judgments in adult mice expressing the APPswe Alzheimer's disease mutation. Behav Neurosci 2005, 119:884-891.
41. 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.
42. Herdegen T., Leah J.D. Inducible and constitutive transcription factors in the mammalian nervous system: control of gene expression by Jun, Fos and Krox, and CREB/ATF proteins. Brain Res Brain Res Rev 1998, 28:370-490.
43. Herrera D.G., Robertson H.A. Activation of c-fos in the brain. Prog Neurobiol 1996, 50:83-107.
44. Hirao K., et al. Functional interactions between entorhinal cortex and posterior cingulate cortex at the very early stage of Alzheimer's disease using brain perfusion single-photon emission computed tomography. Nucl Med Commun 2006, 27:151-156.
45. Hsiao K., et al. Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice. Science 1996, 274:99-102.
46. Hughes P.E., et al. Activity and injury-dependent expression of inducible transcription factors, growth factors and apoptosis-related genes within the central nervous system. Prog Neurobiol 1999, 57:421-450.
47. Iaria G., et al. Retrosplenial and hippocampal brain regions in human navigation: complementary functional contributions to the formation and use of cognitive maps. Eur J Neurosci 2007, 25:890-899.
48. Ida N., et al. Analysis of heterogeneous βa4 peptides in human cerebrospinal fluid and blood by a newly developed sensitive western blot assay. J Biol Chem 1996, 271:22908-22914.
49. Jacobsen J.S., et al. Early-onset behavioral and synaptic deficits in a mouse model of Alzheimer's disease. Proc Natl Acad Sci U S A 2006, 103:5161-5166.
50. Jenkins T.A., et al. Anterior thalamic lesions stop immediate early gene activation in selective laminae of the retrosplenial cortex: evidence of covert pathology in rats? Eur J Neurosci 2004, 19:3291-3304.
51. Jinno S., et al. Neuronal diversity in GABAergic long-range projections from the hippocampus. J Neurosci 2007, 27:8790-8804.
52. Kasahara J., et al. Activation of calcium/calmodulin-dependent protein kinase IV in long term potentiation in the rat hippocampal CA1 region. J Biol Chem 2001, 276:24044-24050.
53. Kawarabayashi T., et al. Age-dependent changes in brain, CSF, and plasma amyloid (beta) protein in the Tg2576 transgenic mouse model of Alzheimer's disease. J Neurosci 2001, 21:372-381.
54. Lanz T.A., et al. Dendritic spine loss in the hippocampus of young PDAPP and Tg2576 mice and its prevention by the ApoE2 genotype. Neurobiol Dis 2003, 13:246-253.
55. Liang W.S., et al. Altered neuronal gene expression in brain regions differentially affected by Alzheimer's disease: a reference data set. Physiol Genomics 2008, 33:240-256.
56. Liang W.S., et al. Alzheimer's disease is associated with reduced expression of energy metabolism genes in posterior cingulate neurons. Proc Natl Acad Sci U S A 2008, 105:4441-4446.
57. Maguire E. The retrosplenial contribution to human navigation: a review of lesion and neuroimaging findings. Scand J Psychol 2001, 42:225-238.
58. Manczak M., et al. Time-course of mitochondrial gene expressions in mice brains: implications for mitochondrial dysfunction, oxidative damage, and cytochrome c in aging. J Neurochem 2005, 92:494-504.
59. Matsuda H. Cerebral blood flow and metabolic abnormalities in Alzheimer's disease. Ann Nucl Med 2001, 15:85-92.
60. Matsuda H., et al. Longitudinal evaluation of both morphologic and functional changes in the same individuals with Alzheimer's disease. J Nucl Med 2002, 43:304-311.
61. Meguro K., et al. Neocortical and hippocampal glucose hypometabolism following neurotoxic lesions of the entorhinal and perirhinal cortices in the non-human primate as shown by PET: implications for Alzheimer's disease. Brain 1999, 122:1519-1531.
62. Meyer M., et al. H2O2 and antioxidants have opposite effects on activation of NF-kappaB and AP-1 in intact cells: AP-1 as secondary antioxidant-responsive factor. EMBO J 1993, 12:2005-2015.
63. Minoshima S., et al. Metabolic reduction in the posterior cingulate cortex in very early Alzheimer's disease. Ann Neurol 1997, 42:85-94.
64. Miyashita T., Rockland K.S. GABAergic projections from the hippocampus to the retrosplenial cortex in the rat. Eur J Neurosci 2007, 26:1193-1204.
65. Morgan J.I., Curran T. Stimulus-transcription coupling in the nervous system: involvement of the inducible proto-oncogenes fos and jun. Annu Rev Neurosci 1991, 14:421-451.
66. Munter L.M., et al. GxxxG motifs within the amyloid precursor protein transmembrane sequence are critical for the etiology of A[beta]42. EMBO J 2007, 26:1702-1712.
67. Nestor P.J., et al. Retrosplenial cortex (BA 29/30) hypometabolism in mild cognitive impairment (prodromal Alzheimer's disease). Eur J Neurosci 2003, 18:2663-2667.
68. Nestor P.J., et al. Limbic hypometabolism in Alzheimer's disease and mild cognitive impairment. Ann Neurol 2003, 54:343-351.
69. Nikolaev E., et al. c-fos protooncogene expression in rat hippocampus and entorhinal cortex following tetanic stimulation of the perforant path. Brain Res 1991, 560:346-349.
70. Ogita K., et al. Transcription factor activator protein-1 expressed by kainate treatment can bind to the non-coding region of mitochondrial genome in murine hippocampus. J Neurosci Res 2003, 73:794-802.
71. Ogita K., et al. Localization of activator protein-1 complex with DNA binding activity in mitochondria of murine brain after in vivo treatment with kainate. J Neurosci 2002, 22:2561-2570.
72. Ohyagi Y., et al. Intraneuronal amyloid [beta]42 enhanced by heating but counteracted by formic acid. J Neurosci Methods 2007, 159:134-138.
73. Palop J.J., et al. Vulnerability of dentate granule cells to disruption of arc expression in human amyloid precursor protein transgenic mice. J Neurosci 2005, 25:9686-9693.
74. Palop J.J., et al. Neuronal depletion of calcium-dependent proteins in the dentate gyrus is tightly linked to Alzheimer's disease-related cognitive deficits. Proc Natl Acad Sci U S A 2003, 100:9572-9577.
75. Paxinos G., Franklin K.B.J. The mouse brain in stereotaxic coordinates 2001, Elsevier, New York, NY.
76. Pengas G., et al. Focal posterior cingulate atrophy in incipient Alzheimer's disease. Neurobiol Aging 2010, 31:25-33.
77. Perez J.L., et al. Soluble oligomeric forms of beta-amyloid (Abeta) peptide stimulate Abeta production via astrogliosis in the rat brain. Exp Neurol 2010, 223:410-421.
78. Petersen R.B., et al. Signal transduction cascades associated with oxidative stress in Alzheimer's disease. J Alzheimers Dis 2007, 11:143-152.
79. Poirier G.L., et al. Anterior thalamic lesions produce chronic and profuse transcriptional deregulation in retrosplenial cortex: a model of retrosplenial hypoactivity and covert pathology. Thalamus Relat Syst 2008, 4:59-77. doi: 10.1017/S1472928808000368.
80. Reddy P.H., et al. Gene expression profiles of transcripts in amyloid precursor protein transgenic mice: up-regulation of mitochondrial metabolism and apoptotic genes is an early cellular change in Alzheimer's disease. Hum Mol Genet 2004, 13:1225-1240.
81. Reiman E.M., et al. Tracking Alzheimer's disease in transgenic mice using fluorodeoxyglucose autoradiography. Neuroreport 2000, 11:987-991.
82. Rémy F., et al. Verbal episodic memory impairment in Alzheimer's disease: a combined structural and functional MRI study. Neuroimage 2005, 25:253-266.
83. Ribé E.M., et al. Accelerated amyloid deposition, neurofibrillary degeneration and neuronal loss in double mutant APP/tau transgenic mice. Neurobiol Dis 2005, 20:814-822.
84. Robertson R.T., et al. Amyloid-beta expression in retrosplenial cortex of triple transgenic mice: relationship to cholinergic axonal afferents from medial septum. Neuroscience 2009, 164:1334-1346.
85. Rutten B.P.F., et al. No alterations of hippocampal neuronal number and synaptic bouton number in a transgenic mouse model expressing the [beta]-cleaved C-terminal APP fragment. Neurobiol Dis 2003, 12:110-120.
86. Salin P., et al. High-frequency stimulation of the subthalamic nucleus selectively reverses dopamine denervation-induced cellular defects in the output structures of the basal ganglia in the rat. J Neurosci 2002, 22:5137-5148.
87. Schmidt C., et al. Amyloid precursor protein and amyloid beta-peptide bind to ATP synthase and regulate its activity at the surface of neural cells. Mol Psychiatry 2008, 13:953-969.
88. Sheng J.G., et al. Disruption of corticocortical connections ameliorates amyloid burden in terminal fields in a transgenic model of Abeta amyloidosis. J Neurosci 2002, 22:9794-9799.
89. Sheng M., Greenberg M.E. The regulation and function of c-fos and other immediate early genes in the nervous system. Neuron 1990, 4:477-485.
90. Spires-Jones T.L., et al. Impaired spine stability underlies plaque-related spine loss in an Alzheimer's disease mouse model. Am J Pathol 2007, 171:1304-1311.
91. Stack E., et al. P1-011: neurogenesis is increased in retrosplenial cortex of six month-old Tg2576 mice. Alzheimers Dement 2006, 2:S97.
92. Stern E.A., et al. Cortical synaptic integration in vivo is disrupted by amyloid-beta plaques. J Neurosci 2004, 24:4535-4540.
93. Strazielle C., et al. Regional brain cytochrome oxidase activity in beta-amyloid precursor protein transgenic mice with the Swedish mutation. Neuroscience 2003, 118:1151-1163.
94. Takahashi R.H., et al. Intraneuronal Alzheimer aβ42 accumulates in multivesicular bodies and is associated with synaptic pathology. Am J Pathol 2002, 161:1869-1879.
95. Thal D.R., et al. Phases of A beta-deposition in the human brain and its relevance for the development of AD. Neurology 2002, 58:1791-1800.
96. Tischmeyer W., Grimm R. Activation of immediate early genes and memory formation. Cell Mol Life Sci 1999, 55:564-574.
97. Valla J., et al. Energy hypometabolism in posterior cingulate cortex of Alzheimer's patients: superficial laminar cytochrome oxidase associated with disease duration. J Neurosci 2001, 21:4923-4930.
98. Valla J., et al. Age- and transgene-related changes in regional cerebral metabolism in PSAPP mice. Brain Res 2006, 1116:194-200.
99. van Groen T., et al. Deposition of mouse amyloid beta in human APP/PS1 double and single AD model transgenic mice. Neurobiol Dis 2006, 23:653-662.
100. van Groen T., et al. Diffuse amyloid deposition, but not plaque number, is reduced in amyloid precursor protein/presenilin 1 double-transgenic mice by pathway lesions. Neuroscience 2003, 119:1185-1197.
101. van Groen T., et al. Interconnections between the thalamus and retrosplenial cortex in the rodent brain. Neurobiology of cingulate cortex and limbic thalamus: a comprehensive handbook 1993, 123-150. Birkhäuser, Boston, MA. B.A. Vogt, M. Gabriel (Eds.).
102. van Hoesen G.W., et al. Entorhinal cortex pathology in Alzheimer's disease. Hippocampus 1991, 1:1-8.
103. Vann S.D., et al. What does the retrosplenial cortex do? Nat Rev Neurosci 2009, 10:792-802.
104. Villain N., et al. Relationships between hippocampal atrophy, white matter disruption, and gray matter hypometabolism in Alzheimer's disease. J Neurosci 2008, 28:6174-6181.
105. Villain N., et al. Sequential relationships between grey matter and white matter atrophy and brain metabolic abnormalities in early Alzheimer's disease. Brain 2010, 133:3301-3314.
106. Vogt B.A. Structural organization of cingulate cortex: areas, neurons, and somatodendritic transmitter receptors. Neurobiology of cingulate cortex and limbic thalamus: a comprehensive handbook 1993, 19-70. Birkhäuser, Boston, MA. B.A. Vogt, M. Gabriel (Eds.).
107. Vogt B.A., et al. Cingulate cortex of the rhesus monkey: I. Cytoarchitecture and thalamic afferents. J Comp Neurol 1987, 262:256-270.
108. Walsh D.M., Selkoe D.J. Deciphering the molecular basis of memory failure in Alzheimer's disease. Neuron 2004, 44:181-193.
109. Wang B., et al. Glutamatergic components of the retrosplenial granular cortex in the rat. J Neurocytol 2001, 30:427-441.
110. Wong-Riley M.T. Cytochrome oxidase: an endogenous metabolic marker for neuronal activity. Trends Neurosci 1989, 12:94-101.
111. Wyss J.M., van Groen T. Connections between the retrosplenial cortex and the hippocampal formation in the rat: a review. Hippocampus 1992, 2:1-11.
112. Xie S., et al. Voxel-based detection of white matter abnormalities in mild Alzheimer disease. Neurology 2006, 66:1845-1849.
113. Zhang Y., et al. Diffusion tensor imaging of cingulum fibers in mild cognitive impairment and Alzheimer disease. Neurology 2007, 68:13-19.
114. Zhou Y., et al. Abnormal connectivity in the posterior cingulate and hippocampus in early Alzheimer's disease and mild cognitive impairment. Alzheimers Dement 2008, 4:265-270.