Partial loss in septo-hippocampal cholinergic neurons alters memory-dependent measures of brain connectivity without overt memory deficits

Neurobiology of Disease

Volumn 54, Issue , 2013, Pages 372-381

  Brayda Bruno, Laurent ^a,b   Mons, Nicole ^b   Yee, Benjamin K ^c   Micheau, Jacques ^b   Abrous, Djoher Nora ^a,b   Nogues, Xavier ^a,b   Marighetto, Aline ^a,b  

^a INSTITUT FRANÇOIS MAGENDIE   (France)

^b UNIVERSITÉ DE BORDEAUX   (France)

^c LEGACY RESEARCH   (United States)

Author keywords

Aging; Declarative memory; Fos immunohistochemistry; Functional connectivity; Mouse; P75 saporin immunotoxin; Radial arm maze; Spatial memory

Indexed keywords

PROTEIN FOS; SAPORIN;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; CORPUS STRIATUM; DECLARATIVE MEMORY; EMOTIONAL MEMORY; HIPPOCAMPAL CA3 REGION; HIPPOCAMPUS; MALE; MAZE TEST; MEMORY; MEMORY DISORDER; MOUSE; NERVE CELL NETWORK; NERVE DEGENERATION; NONHUMAN; PRIORITY JOURNAL; PROCEDURAL MEMORY; RECALL; SEPTUM PELLUCIDUM;

AGING; ALZHEIMER DISEASE; ANIMALS; BRAIN; CHOLINERGIC NEURONS; IMMUNOHISTOCHEMISTRY; MALE; MAZE LEARNING; MEMORY; MICE; MICE, INBRED C57BL; NERVE DEGENERATION; NEURAL PATHWAYS;

EID: 84876337577     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2013.01.010     Document Type: Article

References (60)

1. Bartus R.T., Dean R.L., Pontecorvo M.J., Flicker C. The cholinergic hypothesis: a historical overview, current perspective, and future directions. Ann. N. Y. Acad. Sci. 1985, 444:332-358.
2. Bassett S.S., Yousem D.M., Cristinzio C., Kusevic I., Yassa M.A., Caffo B.S., Zeger S.L. Familial risk for Alzheimer's disease alters fMRI activation patterns. Brain 2006, 129:1229-1239.
3. Boucard A., Mons N., Micheau J., Nogues X. Activating a memory system focuses connectivity toward its central structure. Behav. Brain Res. 2009, 204:226-234.
4. Burke S.N., Barnes C.A. Neural plasticity in the ageing brain. Nat. Rev. Neurosci. 2006, 7:30-40.
5. Buzsaki G. Two-stage model of memory trace formation: a role for "noisy" brain states. Neuroscience 1989, 31:551-570.
6. Calandreau L., Trifilieff P., Mons N., Costes L., Marien M., Marighetto A., Micheau J., Jaffard R., Desmedt A. Extracellular hippocampal acetylcholine level controls amygdala function and promotes adaptive conditioned emotional response. J. Neurosci. 2006, 26:13556-13566.
7. Chang Q., Gold P.E. Switching memory systems during learning: changes in patterns of brain acetylcholine release in the hippocampus and striatum in rats. J. Neurosci. 2003, 23:3001-3005.
8. Dennis N.A., Cabeza R. Age-related dedifferentiation of learning systems: an fMRI study of implicit and explicit learning. Neurobiol. Aging 2011, 32(2318):e2317-e2330.
9. Devan B.D., White N.M. Parallel information processing in the dorsal striatum: relation to hippocampal function. J. Neurosci. 1999, 19:2789-2798.
10. Dickerson B.C., Sperling R.A. Functional abnormalities of the medial temporal lobe memory system in mild cognitive impairment and Alzheimer's disease: insights from functional MRI studies. Neuropsychologia 2008, 46:1624-1635.
11. Eaton J. Manual Network Theory: GNU Octave 2002, (Chapter Chapter).
12. Efron B., Tibshirani R. Statistical data analysis in the computer age. Science 1991, 253:390-395.
13. Etchamendy N., Desmedt A., Cortes-Torrea C., Marighetto A., Jaffard R. Hippocampal lesions and discrimination performance of mice in the radial maze: sparing or impairment depending on the representational demands of the task. Hippocampus 2003, 13:197-211.
14. Farovik A., Place R.J., Miller D.R., Eichenbaum H. Amygdala lesions selectively impair familiarity in recognition memory. Nat. Neurosci. 2011, 14:1416-1417.
15. Gallagher M., Rapp P.R. The use of animal models to study the effects of aging on cognition. Annu. Rev. Psychol. 1997, 48:339-370.
16. Gallagher M., Bakker A., Yassa M.A., Stark C.E. Bridging neurocognitive aging and disease modification: targeting functional mechanisms of memory impairment. Curr. Alzheimer Res. 2010, 7:197-199.
17. Gold P.E. Coordination of multiple memory systems. Neurobiol. Learn. Mem. 2004, 82:230-242.
18. Grady C.L. Cognitive neuroscience of aging. Ann. N. Y. Acad. Sci. 2008, 1124:127-144.
19. Hasselmo M.E. The role of acetylcholine in learning and memory. Curr. Opin. Neurobiol. 2006, 16:710-715.
20. Hasselmo M.E., Bower J.M. Acetylcholine and memory. Trends Neurosci. 1993, 16:218-222.
21. Hedden T., Gabrieli J.D. Healthy and pathological processes in adult development: new evidence from neuroimaging of the aging brain. Curr. Opin. Neurol. 2005, 18:740-747.
22. Ho N.F., Han S.P., Dawe G.S. Effect of voluntary running on adult hippocampal neurogenesis in cholinergic lesioned mice. BMC Neurosci. 2009, 10:57.
23. Horwitz B., Grady C.L., Schlageter N.L., Duara R., Rapoport S.I. Intercorrelations of regional cerebral glucose metabolic rates in Alzheimer's disease. Brain Res. 1987, 407:294-306.
24. Ikonen S., McMahan R., Gallagher M., Eichenbaum H., Tanila H. Cholinergic system regulation of spatial representation by the hippocampus. Hippocampus 2002, 12:386-397.
25. McIntyre C.K., Pal S.N., Marriott L.K., Gold P.E. Competition between memory systems: acetylcholine release in the hippocampus correlates negatively with good performance on an amygdala-dependent task. J. Neurosci. 2002, 22:1171-1176.
26. McIntyre C.K., Marriott L.K., Gold P.E. Cooperation between memory systems: acetylcholine release in the amygdala correlates positively with performance on a hippocampus-dependent task. Behav. Neurosci. 2003, 117:320-326.
27. Mesulam M.M., Mufson E.J., Wainer B.H., Levey A.I. Central cholinergic pathways in the rat: an overview based on an alternative nomenclature (Ch1-Ch6). Neuroscience 1983, 10:1185-1201.
28. Micheau J., Marighetto A. Acetylcholine and memory: a long, complex and chaotic but still living relationship. Behav. Brain Res. 2011, 221:424-429.
29. Minati L., Grisoli M., Bruzzone M.G. MR spectroscopy, functional MRI, and diffusion-tensor imaging in the aging brain: a conceptual review. J. Geriatr. Psychiatry Neurol. 2007, 20:3-21.
30. Mingaud F., Le Moine C., Etchamendy N., Mormede C., Jaffard R., Marighetto A. The hippocampus plays a critical role at encoding discontiguous events for subsequent declarative memory expression in mice. Hippocampus 2007, 17:264-270.
31. Mingaud F., Mormede C., Etchamendy N., Mons N., Niedergang B., Wietrzych M., Pallet V., Jaffard R., Krezel W., Higueret P., Marighetto A. Retinoid hyposignaling contributes to aging-related decline in hippocampal function in short-term/working memory organization and long-term declarative memory encoding in mice. J. Neurosci. 2008, 28:279-291.
32. Mitchell J.A., Hall G. Caudate-putamen lesions in the rat may impair or potentiate maze learning depending upon availability of stimulus cues and relevance of response cues. Q. J. Exp. Psychol. B 1988, 40:243-258.
33. Mondadori C.R., Buchmann A., Mustovic H., Schmidt C.F., Boesiger P., Nitsch R.M., Hock C., Streffer J., Henke K. Enhanced brain activity may precede the diagnosis of Alzheimer's disease by 30years. Brain 2006, 129:2908-2922.
34. Moreau P.H., Cosquer B., Jeltsch H., Cassel J.C., Mathis C. Neuroanatomical and behavioral effects of a novel version of the cholinergic immunotoxin mu p75-saporin in mice. Hippocampus 2008, 18:610-622.
35. Murty V.P., Sambataro F., Das S., Tan H.Y., Callicott J.H., Goldberg T.E., Meyer-Lindenberg A., Weinberger D.R., Mattay V.S. Age-related alterations in simple declarative memory and the effect of negative stimulus valence. J. Cogn. Neurosci. 2009, 21:1920-1933.
36. Parent M.B., Baxter M.G. Septohippocampal acetylcholine: involved in but not necessary for learning and memory?. Learn. Mem. 2004, 11:9-20.
37. Paxinos G., Franklin K.B.J. The Mouse Brain in Stereotaxic Coordinates 2001, Academic Press, USA, (Chapter Chapter).
38. Pennanen C., Kivipelto M., Tuomainen S., Hartikainen P., Hanninen T., Laakso M.P., Hallikainen M., Vanhanen M., Nissinen A., Helkala E.L., Vainio P., Vanninen R., Partanen K., Soininen H. Hippocampus and entorhinal cortex in mild cognitive impairment and early AD. Neurobiol. Aging 2004, 25:303-310.
39. Pepeu G., Giovannini M.G. Cholinesterase inhibitors and beyond. Curr. Alzheimer Res. 2009, 6:86-96.
40. Pihlajamaki M., Jauhiainen A.M., Soininen H. Structural and functional MRI in mild cognitive impairment. Curr. Alzheimer Res. 2009, 6:179-185.
41. Poldrack R.A., Packard M.G. Competition among multiple memory systems: converging evidence from animal and human brain studies. Neuropsychologia 2003, 41:245-251.
42. Poldrack R.A., Clark J., Pare-Blagoev E.J., Shohamy D., Creso Moyano J., Myers C., Gluck M.A. Interactive memory systems in the human brain. Nature 2001, 414:546-550.
43. Pych J.C., Chang Q., Colon-Rivera C., Gold P.E. Acetylcholine release in hippocampus and striatum during testing on a rewarded spontaneous alternation task. Neurobiol. Learn. Mem. 2005, 84:93-101.
44. Quiroz Y.T., Budson A.E., Celone K., Ruiz A., Newmark R., Castrillon G., Lopera F., Stern C.E. Hippocampal hyperactivation in presymptomatic familial Alzheimer's disease. Ann. Neurol. 2010, 68:865-875.
45. Rolls E.T., Kesner R.P. A computational theory of hippocampal function, and empirical tests of the theory. Prog. Neurobiol. 2006, 79:1-48.
46. Rutishauser U., Schuman E.M., Mamelak A.N. Activity of human hippocampal and amygdala neurons during retrieval of declarative memories. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:329-334.
47. Sperling R. Functional MRI studies of associative encoding in normal aging, mild cognitive impairment, and Alzheimer's disease. Ann. N. Y. Acad. Sci. 2007, 1097:146-155.
48. Sperling R.A., Dickerson B.C., Pihlajamaki M., Vannini P., LaViolette P.S., Vitolo O.V., Hedden T., Becker J.A., Rentz D.M., Selkoe D.J., Johnson K.A. Functional alterations in memory networks in early Alzheimer's disease. Neuromolecular Med. 2010, 12:27-43.
49. St Jacques P.L., Dolcos F., Cabeza R. Effects of aging on functional connectivity of the amygdala for subsequent memory of negative pictures: a network analysis of functional magnetic resonance imaging data. Psychol. Sci. 2009, 20:74-84.
50. St Jacques P., Dolcos F., Cabeza R. Effects of aging on functional connectivity of the amygdala during negative evaluation: a network analysis of fMRI data. Neurobiol. Aging 2010, 31:315-327.
51. Stark S.M., Yassa M.A., Stark C.E. Individual differences in spatial pattern separation performance associated with healthy aging in humans. Learn. Mem. 2010, 17:284-288.
52. Toner C.K., Pirogovsky E., Kirwan C.B., Gilbert P.E. Visual object pattern separation deficits in nondemented older adults. Learn. Mem. 2009, 16:338-342.
53. Touzani K., Marighetto A., Jaffard R. Fos imaging reveals ageing-related changes in hippocampal response to radial maze discrimination testing in mice. Eur. J. Neurosci. 2003, 17:628-640.
54. Traissard N., Herbeaux K., Cosquer B., Jeltsch H., Ferry B., Galani R., Pernon A., Majchrzak M., Cassel J.C. Combined damage to entorhinal cortex and cholinergic basal forebrain neurons, two early neurodegenerative features accompanying Alzheimer's disease: effects on locomotor activity and memory functions in rats. Neuropsychopharmacology 2007, 32:851-871.
55. White N.M., McDonald R.J. Multiple parallel memory systems in the brain of the rat. Neurobiol. Learn. Mem. 2002, 77:125-184.
56. Wilson I.A., Ikonen S., Gallagher M., Eichenbaum H., Tanila H. Age-associated alterations of hippocampal place cells are subregion specific. J. Neurosci. 2005, 25:6877-6886.
57. Yassa M.A., Stark C.E. Pattern separation in the hippocampus. Trends Neurosci. 2011, 34:515-525.
58. Yassa M.A., Lacy J.W., Stark S.M., Albert M.S., Gallagher M., Stark C.E. Pattern separation deficits associated with increased hippocampal CA3 and dentate gyrus activity in nondemented older adults. Hippocampus 2010, 21:968-979.
59. Yassa M.A., Mattfeld A.T., Stark S.M., Stark C.E. Age-related memory deficits linked to circuit-specific disruptions in the hippocampus. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:8873-8878.
60. Zar J. Biostatistical Analysis 1999, Prentice Hall, Upper Saddle River, New Jersey, (Chapter Chapter).