Axonal tract tracing for delineating interacting brain regions: Implications for Alzheimer's disease-associated memory

Future Neurology

Volumn 9, Issue 1, 2014, Pages 89-98

  Van Groen, Thomas ^a   Miettinen, Pasi ^b   Kadish, Inga ^a  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b UNIVERSITY OF EASTERN FINLAND   (Finland)

Author keywords

entorhinal cortex; hippocampus; limbic system; perforant path; tractography

Indexed keywords

AMYLOID BETA PROTEIN;

ALZHEIMER DISEASE; BRAIN REGION; DENTATE GYRUS; DIFFUSION TENSOR IMAGING; ENTORHINAL CORTEX; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; HIPPOCAMPUS; HUMAN; MEMORY; NERVE CELL PLASTICITY; NERVE FIBER; NERVE TRACT; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; REVIEW; SUBICULUM; TRANSGENIC MOUSE; WHITE MATTER;

EID: 84890938561     PISSN: 14796708     EISSN: 17486971     Source Type: Journal    
DOI: 10.2217/fnl.13.67     Document Type: Review

References (72)

1. Witter MP, Groenewegen HJ, Lopes da Silva FH, Lohman AH. Functional organization of the extrinsic and intrinsic circuitry of the parahippocampal region. Prog. Neurobiol. 33(3), 161-253 (1989).
2. Ramon y Cajal S. [Notes on the fine anatomy of the large brain]. Z. Wissensch. Zool. 56, 615-672 (1893).
3. Van Hoesen GW, Pandya DN. Some connections of the entorhinal (area 28) and perirhinal (area 35) cortices of the rhesus monkey. III. Efferent connections. Brain Res. 95(1), 39-59 (1975).
4. Steward O, Scoville SA. Cells of origin of entorhinal cortical afferents to the hippocampus and fascia dentata of the rat. J. Comp. Neurol. 169(3), 347-370 (1976).
5. Witter MP, Groenewegen HJ. Laminar origin and septotemporal distribution of entorhinal and perirhinal projections to the hippocampus in the cat. J. Comp. Neurol. 224(3), 371-385 (1984).
6. Amaral DG, Witter MP. The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience 31(3), 571-591 (1989).
7. van Groen T, Miettinen P, Kadish I. The entorhinal cortex of the mouse: organization of the projection to the hippocampal formation. Hippocampus 13(1), 133-149 (2003).
8. Pohle W, Ott T, Muller-Welde P. Identification of neurons of origin providing the dopaminergic innervation of the hippocampus. J. Hirnforsch. 25(1), 1-10 (1984).
9. Dolorfo CL, Amaral DG. Entorhinal cortex of the rat: topographic organization of the cells of origin of the perforant path projection to the dentate gyrus. J. Comp. Neurol. 398(1), 25-48 (1998).
10. Ruth RE, Collier TJ, Routtenberg A. Topography between the entorhinal cortex and the dentate septotemporal axis in rats: I. Medial and intermediate entorhinal projecting cells. J. Comp. Neurol. 209(1), 69-78 (1982).
11. Ruth RE, Collier TJ, Routtenberg A. Topographical relationship between the entorhinal cortex and the septotemporal axis of the dentate gyrus in rats: II. Cells projecting from lateral entorhinal subdivisions. J. Comp. Neurol. 270(4), 506-516 (1988).
12. Hjorth-Simonsen A, Jeune B. Origin and termination of the hippocampal perforant path in the rat studied by silver impregnation. J. Comp. Neurol. 144(2), 215-232 (1972).
13. Deller T, Haas CA, Frotscher M. Sprouting in the hippocampus after entorhinal cortex lesion is layer-specific but not translaminar: which molecules may be involved? Restor. Neurol. Neurosci. 19(3-4), 159-167 (2001).
14. von Gunten A, Kovari E, Bussiere T et al. Cognitive impact of neuronal pathology in the entorhinal cortex and CA1 field in Alzheimer's disease. Neurobiol. Aging 27(2), 270-277 (2006).
15. Kadish I, Van Groen T. Low levels of estrogen significantly diminish axonal sprouting after entorhinal cortex lesions in the mouse. J. Neurosci. 22(10), 4095-4102 (2002).
16. Deller T, Haas CA, Frotscher M. Reorganization of the rat fascia dentata after a unilateral entorhinal cortex lesion. Role of the extracellular matrix. Ann. NY Acad. Sci. 911, 207-220 (2000).
17. van Groen T. Entorhinal cortex of the mouse: cytoarchitectonical organization. Hippocampus 11(4), 397-407 (2001).
18. Lorente De Nó R. Studies on the structure of the cerebral cortex. II. Continuation of the study of the ammonic system. J. Psychol. Neurol. 46, 113-177 (1934).
19. Blackstad TW. Commissural connections of the hippocampal region in the rat, with special reference to their mode of termination. J. Comp. Neurol. 105(3), 417-537 (1956).
20. West MJ, Andersen AH. An allometric study of the area dentata in the rat and mouse. Brain Res. 2(3), 317-348 (1980).
21. van Groen T, Kadish I, Wyss JM. Species differences in the projections from the entorhinal cortex to the hippocampus. Brain Res. Bull. 57(3-4), 553-556 (2002).
22. Suzuki WA, Amaral DG. Topographic organization of the reciprocal connections between the monkey entorhinal cortex and the perirhinal and parahippocampal cortices. J. Neurosci. 14(3 Pt 2), 1856-1877 (1994).
23. Witter MP, Amaral DG. Entorhinal cortex of the monkey: V. Projections to the dentate gyrus, hippocampus, and subicular complex. J. Comp. Neurol. 307(3), 437-459 (1991).
24. van Groen T, van Haren FJ, Witter MP, Groenewegen HJ. The organization of the reciprocal connections between the subiculum and the entorhinal cortex in the cat: I. A neuroanatomical tracing study. J. Comp. Neurol. 250(4), 485-497 (1986).
25. Phinney AL, Deller T, Stalder M et al. Cerebral amyloid induces aberrant axonal sprouting and ectopic terminal formation in amyloid precursor protein transgenic mice. J. Neurosci. 19(19), 8552-8559 (1999).
26. Amaral DG, Insausti R, Cowan WM. The commissural connections of the monkey hippocampal formation. J. Comp. Neurol. 224(3), 307-336 (1984).
27. Kondo H, Lavenex P, Amaral DG. Intrinsic connections of the macaque monkey hippocampal formation: II. CA3 connections. J. Comp. Neurol. 515(3), 349-377 (2009).
28. Swanson LW, Sawchenko PE, Cowan WM. Evidence for collateral projections by neurons in Ammon's horn, the dentate gyrus, and the subiculum: a multiple retrograde labeling study in the rat. J. Neurosci. 1(5), 548-559 (1981).
29. Laurberg S. Commissural and intrinsic connections of the rat hippocampus. J. Comp. Neurol. 184(4), 685-708 (1979).
30. Witter MP, Van Hoesen GW, Amaral DG. Topographical organization of the entorhinal projection to the dentate gyrus of the monkey. J. Neurosci. 9(1), 216-228 (1989).
31. Kadish I, van Groen T. Lesion-induced hippocampal plasticity in transgenic Alzheimer's disease mouse models: influences of age, genotype, and estrogen. J. Alzheimers Dis. 18(2), 429-445 (2009).
32. de la Monte SM. Quantitation of cerebral atrophy in preclinical and end-stage Alzheimer's disease. Ann. Neurol. 25(5), 450-459 (1989).
33. Laakso MP, Vaurio O, Savolainen L et al. A volumetric MRI study of the hippocampus in type 1 and 2 alcoholism. Behav. Brain Res. 109(2), 177-186 (2000).
34. Laakso MP, Frisoni GB, Kononen M et al. Hippocampus and entorhinal cortex in frontotemporal dementia and Alzheimer's disease: a morphometric MRI study. Biol. Psychiatry 47(12), 1056-1063 (2000).
35. Stranahan AM, Mattson MP. Selective vulnerability of neurons in layer II of the entorhinal cortex during aging and Alzheimer's disease. Neural Plast. 2010, 108190 (2010).
36. Kordower JH, Chu Y, Stebbins GT et al. Loss and atrophy of layer II entorhinal cortex neurons in elderly people with mild cognitive impairment. Ann. Neurol. 49(2), 202-213 (2001).
37. Gomez-Isla T, Price JL, Mckeel DW Jr, Morris JC, Growdon JH, Hyman BT. Profound loss of layer II entorhinal cortex neurons occurs in very mild Alzheimer's disease. J. Neurosci. 16(14), 4491-4500 (1996).
38. Hyman BT, Van Hoesen GW, Damasio AR. Alzheimer's disease: glutamate depletion in the hippocampal perforant pathway zone. Ann. Neurol. 22(1), 37-40 (1987).
39. Cabalka LM, Hyman BT, Goodlett CR, Ritchie TC, Van Hoesen GW. Alteration in the pattern of nerve terminal protein immunoreactivity in the perforant pathway in Alzheimer's disease and in rats after entorhinal lesions. Neurobiol. Aging 13(2), 283-291 (1992).
40. Mielke MM, Okonkwo OC, Oishi K et al. Fornix integrity and hippocampal volume predict memory decline and progression to Alzheimer's disease. Alzheimer's Dement. 8(2), 105-113 (2012).
41. Oishi K, Mielke MM, Albert M, Lyketsos CG, Mori S. The fornix sign: a potential sign for Alzheimer's disease based on diffusion tensor imaging. J. Neuroimaging 22(4), 365-374 (2012).
42. Schmued LC, Raymick J, Paule MG, Dumas M, Sarkar S. Characterization of myelin pathology in the hippocampal complex of a transgenic mouse model of Alzheimer's disease. Curr. Alzheimers Res. 10(1), 30-37 (2013).
43. Yassa MA, Muftuler LT, Stark CE. Ultrahigh-resolution microstructural diffusion tensor imaging reveals perforant path degradation in aged humans in vivo. Proc. Natl Acad. Sci. USA 107(28), 12687-12691 (2010).
44. Hyman BT, Kromer LJ, Van Hoesen GW. Reinnervation of the hippocampal perforant pathway zone in Alzheimer's disease. Ann. Neurol. 21(3), 259-267 (1987).
45. Cotman CW, Anderson KJ. Synaptic plasticity and functional stabilization in the hippocampal formation: possible role in Alzheimer's disease. Adv. Neurol. 47, 313-335 (1988).
46. Hyman BT, Van Hoesen GW, Kromer LJ, Damasio AR. Perforant pathway changes and the memory impairment of Alzheimer's disease. Ann. Neurol. 20(4), 472-481 (1986).
47. Deller T, Del Turco D, Rappert A, Bechmann I. Structural reorganization of the dentate gyrus following entorhinal denervation: species differences between rat and mouse. Prog. Brain Res. 163, 501-528 (2007).
48. Van Groen T, Liu L, Ikonen S, Kadish I. Diffuse amyloid deposition, but not plaque number, is reduced in amyloid precursor protein/presenilin 1 double-transgenic mice by pathway lesions. Neuroscience 119(4), 1185-1197 (2003).
49. Arendt T. Disturbance of neuronal plasticity is a critical pathogenetic event in Alzheimer's disease. Int. J. Dev. Neurosci. 19(3), 231-245 (2001).
50. Arendt T. Synaptic degeneration in Alzheimer's disease. Acta Neuropathol. 118(1), 167-179 (2009).
51. Spires-Jones TL, Meyer-Luehmann M, Osetek JD et al. Impaired spine stability underlies plaque-related spine loss in an Alzheimer's disease mouse model. Am. J. Pathol. 171(4), 1304-1311 (2007).
52. Shankar GM, Li S, Mehta TH et al. Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat. Med. 14(8), 837-842 (2008).
53. Arendt T. Alzheimer's disease as a disorder of mechanisms underlying structural brain self-organization. Neuroscience 102(4), 723-765 (2001).
54. Holtmaat A, Svoboda K. Experience-dependent structural synaptic plasticity in the mammalian brain. Nat. Rev. Neurosci. 10(9), 647-658 (2009).
55. Swaab DF. Brain aging and Alzheimer's disease, 'wear and tear' versus 'use it or lose it'. Neurobiol. Aging 12(4), 317-324 (1991).
56. Braak H, Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol. 82(4), 239-259 (1991).
57. Braak H, Braak E. Staging of Alzheimer's disease-related neurofibrillary changes. Neurobiol. Aging 16(3), 271-278; discussion 278-284 (1995).
58. Arendt T, Bruckner MK, Gertz HJ, Marcova L. Cortical distribution of neurofibrillary tangles in Alzheimer's disease matches the pattern of neurons that retain their capacity of plastic remodelling in the adult brain. Neuroscience 83(4), 991-1002 (1998).
59. Small SA, Schobel SA, Buxton RB, Witter MP, Barnes CA. A pathophysiological framework of hippocampal dysfunction in ageing and disease. Nat. Rev. Neurosci. 12(10), 585-601 (2011).
60. Hardy J, Revesz T. The spread of neurodegenerative disease. N. Engl. J. Med. 366(22), 2126-2128 (2012).
61. Walker LC, Diamond MI, Duff KE, Hyman BT. Mechanisms of protein seeding in neurodegenerative diseases. JAMA Neurol. 70(3), 304-310 (2013).
62. Wu JW, Herman M, Liu L et al. Small misfolded tau species are internalized via bulk endocytosis and anterogradely and retrogradely transported in neurons. J. Biol. Chem. 288(3), 1856-1870 (2013).
63. Van Hoesen GW, Hyman BT. Hippocampal formation: anatomy and the patterns of pathology in Alzheimer's disease. Prog. Brain Res. 83, 445-457 (1990).
64. Matthews PM, Filippini N, Douaud G. Brain structural and functional connectivity and the progression of neuropathology in Alzheimer's disease. J. Alzheimers Dis. 33(Suppl. 1), S163-S172 (2013).
65. Agosta F, Pievani M, Geroldi C, Copetti M, Frisoni GB, Filippi M. Resting state fMRI in Alzheimer's disease: beyond the default mode network. Neurobiol. Aging 33(8), 1564-1578 (2012).
66. Filippi M, Agosta F. Structural and functional network connectivity breakdown in Alzheimer's disease studied with magnetic resonance imaging techniques. J. Alzheimers Dis. 24(3), 455-474 (2011).
67. Huang H, Fan X, Weiner M et al. Distinctive disruption patterns of white matter tracts in Alzheimer's disease with full diffusion tensor characterization. Neurobiol. Aging 33(9), 2029-2045 (2012).
68. Fieremans E, Benitez A, Jensen JH et al. Novel white matter tract integrity metrics sensitive to Alzheimer disease progression. AJNR Am. J. Neuroradiol. 34(11), 2105-2112 (2013).
69. Zerbi V, Kleinnijenhuis M, Fang X et al. Gray and white matter degeneration revealed by diffusion in an Alzheimer mouse model. Neurobiol. Aging 34(5), 1440-1450 (2013).
70. Johnson DK, Barrow W, Anderson R et al. Diagnostic utility of cerebral white matter integrity in early Alzheimer's disease. Int. J. Neurosci. 120(8), 544-550 (2010).
71. Chao LL, Decarli C, Kriger S et al. Associations between white matter hyperintensities and beta amyloid on integrity of projection, association, and limbic fiber tracts measured with diffusion tensor MRI. PLoS ONE 8(6), e65175 (2013).
72. Clerx L, Visser PJ, Verhey F, Aalten P. New MRI markers for Alzheimer's disease: a meta-analysis of diffusion tensor imaging and a comparison with medial temporal lobe measurements. J. Alzheimers Dis. 29(2), 405-429 (2012).