Cholinergic basal forebrain structure influences the reconfiguration of white matter connections to support residual memory in mild cognitive impairment

Journal of Neuroscience

Volumn 35, Issue 2, 2015, Pages 739-747

  Ray, Nicola J ^a   Metzler Baddeley, Claudia ^b   Khondoker, Mizanur R ^a   Grothe, Michel J ^d   Teipel, Stefan ^c   Wright, Paul ^a   Heinsen, Helmut ^e   Jones, Derek K ^b   Aggleton, John P ^b   O’Sullivan, Michael J ^a,b  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b CARDIFF UNIVERSITY   (United Kingdom)

^c GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^d ROSTOCK UNIVERSITY MEDICAL CENTER   (Germany)

^e UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

Cholinergic system; Diffusion; Episodic memory; Fornix; Mild cognitive impairment; White matter

Indexed keywords

ADULT; AGED; ARTICLE; CHOLINERGIC SYSTEM; CLINICAL DEMENTIA RATING; CONTROLLED STUDY; DIFFUSION WEIGHTED IMAGING; DOORS AND PEOPLE TEST; EPISODIC MEMORY; FEMALE; FOREBRAIN; HUMAN; MALE; MEMORY; MILD COGNITIVE IMPAIRMENT; MINI MENTAL STATE EXAMINATION; NEUROPSYCHOLOGICAL TEST; NORMAL HUMAN; PARAHIPPOCAMPAL CINGULUM; PRIORITY JOURNAL; RECALL; SCORING SYSTEM; TASK PERFORMANCE; TRACTOGRAPHY; VISUAL MEMORY; WHITE MATTER; BIOLOGICAL MODEL; BRAIN FORNIX; MIDDLE AGED; PATHOLOGY; PATHOPHYSIOLOGY; VERY ELDERLY;

AGED; AGED, 80 AND OVER; FEMALE; FORNIX, BRAIN; HUMANS; MALE; MEMORY, EPISODIC; MENTAL RECALL; MIDDLE AGED; MILD COGNITIVE IMPAIRMENT; MODELS, NEUROLOGICAL; PROSENCEPHALON; WHITE MATTER;

EID: 84920973745     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3617-14.2015     Document Type: Article

References (63)

1. Aggleton JP (2012) Multiple anatomical systems embedded within the primate medial temporal lobe: implications for hippocampal function. Neurosci Biobehav Rev 36:1579-1596. CrossRef Medline
2. Aggleton JP, Brown MW (2006) Interleaving brain systems for episodic and recognition memory. Trends Cogn Sci 10:455-463. CrossRef Medline
3. Aggleton JP, Friedman DP, Mishkin M (1987) A comparison between the connections of the amygdala and hippocampus with the basal forebrain in the macaque. Exp Brain Res 67:556-568. Medline
4. Aggleton JP, McMackin D, Carpenter K, Hornak J, Kapur N, Halpin S, Wiles CM, Kamel H, Brennan P, Carton S, Gaffan D (2000) Differential cognitive effects of colloid cysts in the third ventricle that spare or compromise the fornix. Brain 123:800–815. CrossRef Medline
5. Albert MS, DeKosky ST, Dickson D, Dubois B, Feldman HH, Fox NC, Gamst A, Holtzman DM, Jagust WJ, Petersen RC, Snyder PJ, Carrillo MC, Thies B, Phelps CH (2011) The diagnosis of mild cognitive impairment due to Alzheimer’s disease: recommendations from the National Institute on Aging-Alzheimer’s Association workgroups on diagnostic guidelines for Alzheimer’s disease. Alzheimers Dement 7:270-279. CrossRef Medline
6. Anderson ND, Ebert PL, Jennings JM, Grady CL, Cabeza R, Graham SJ (2008) Recollection- and familiarity-based memory in healthy aging and amnestic mild cognitive impairment. Neuropsychology 22:177–187. CrossRef Medline
7. Ashburner J (2007) A fast diffeomorphic image registration algorithm. Neuroimage 38:95–113. CrossRef Medline
8. Augustinack JC, van der Kouwe AJ, Salat DH, Benner T, Stevens AA, Annese J, Fischl B, Frosch MP, Corkin S (2014) H.M.’s contributions to neuroscience: a review and autopsy studies. Hippocampus 24:1267–1286. CrossRef Medline
9. Baddeley AD, Emslie H, Nimmo-Smith I (1994) Doors and people test. Bury St. Edmunds, UK: Thames Valley Test Company.
10. Berlot R, Metzler-Baddeley C, Jones DK, O’Sullivan MJ (2014) CSF contamination contributes to apparent microstructural alterations in mild cognitive impairment. Neuroimage 92:27–35. CrossRef Medline
11. Bozzali M, Parker GJ, Spanò B, Serra L, Giulietti G, Perri R, Magnani G, Marra C, G Vita M, Caltagirone C, Cercignani M (2013) Brain tissue modifications induced by cholinergic therapy in Alzheimer’s disease. HumBrain Mapp 34:3158-3167. CrossRef Medline
12. Browning PGF, Gaffan D, Croxson PL, Baxter MG (2010) Severe scene learning impairment, but intact recognition memory, after cholinergic depletion of inferotemporal cortex followed by fornix depletion. Cereb Cortex 20:282–293. CrossRef Medline
13. Croxson PL, Browning PGF, Gaffan D, Baxter MG (2012) Acetylcholine facilitates recovery of episodic memory after brain damage. J Neurosci 32:13787–13795. CrossRef Medline
14. Delis DC, Kaplan E, Kramer JH (2001) Delis–Kaplan Executive Function System (D-KEFS). Oxford, UK: Pearson Assessment.
15. D’Esposito M, Verfaellie M, Alexander MP, Katz DI (1995) Amnesia following traumatic bilateral fornix transection. Neurology 45:1546-1550. CrossRef Medline
16. Douaud G, Menke RAL, Gass A, Monsch AU, Rao A, Whitcher B, Zamboni G, Matthews PM, Sollberger M, Smith S (2013) Brain microstructure reveals early abnormalities more than two years prior to clinical progression from mild cognitive impairment to Alzheimer’s disease. J Neurosci 33: 2147–2155. CrossRef Medline
17. Easton A, Douchamps V, Eacott M, Lever C (2012) A specific role for septohippocampal acetylcholine in memory? Neuropsychologia 50:3156-3168. CrossRef Medline
18. Gaffan D (2002) Against memory systems. Philos Trans R Soc Lond B Biol Sci 357:1111–1121. CrossRef Medline
19. Gaffan D, Gaffan EA (1991) Amnesia in man following transection of the fornix. A review. Brain 114:2611–2618. CrossRef Medline
20. Gao FQ, Pettersen JA, Bocti C, Nestor SM, Kiss A, Black SE (2013) Is encroachment of the carotid termination into the substantia innominata associated with its atrophy and cognition in Alzheimer’s disease? Neurobiol Aging 34:1807–1814. CrossRef Medline
21. Grober E, Merling A, Heimlich T, Lipton RB (1997) Free and cued selective reminding and selective reminding in the elderly. J Clin Exp Neuropsychol 19:643-654. CrossRef Medline
22. Grothe M, Heinsen H, Teipel SJ (2012) Atrophy of the cholinergic Basal forebrain over the adult age range and in early stages of Alzheimer’s disease. Biol Psychiatry 71:805-813. CrossRef Medline
23. Grothe M, Heinsen H, Teipel S (2013) Longitudinal measures of cholinergic forebrain atrophy in the transition from healthy aging to Alzheimer’s disease. Neurobiol Aging 34:1210-1220. CrossRef Medline
24. Haense C, Kalbe E, Herholz K, Hohmann C, Neumaier B, Krais R, Heiss WD (2012) Cholinergic system function and cognition in mild cognitive impairment. Neurobiol Aging 33:867-877. CrossRef Medline
25. Horel JA (1978) The neuroanatomy of amnesia.Acritique of the hippocampal memory hypothesis. Brain 101:403-445. CrossRef Medline
26. Jeurissen B, Leemans A, Jones DK, Tournier JD, Sijbers J (2011) Probabilistic fiber tracking using the residual bootstrap with constrained spherical deconvolution. Hum Brain Mapp 32:461-479. CrossRef Medline
27. Jones DK, Horsfield MA, Simmons A (1999) Optimal strategies for measuring diffusion in anisotropic systems by magnetic resonance imaging. Magn Reson Med 42:515–525. CrossRef Medline
28. Kilimann I, Grothe M, Heinsen H, Alho EJL, Grinberg L, Amaro E Jr, Dos Santos GAB, da Silva RE, Mitchell AJ, Frisoni GB, Bokde ALW, Fellgiebel A, Filippi M, Hampel H, Klöppel S, Teipel SJ (2014) Subregional basal forebrain atrophy in Alzheimer’s disease: a multicenter study. J Alzheimers Dis 40:687–700. CrossRef Medline
29. Kitt CA, Mitchell SJ, DeLong MR, Wainer BH, Price DL (1987) Fiber pathways of basal forebrain cholinergic neurons in monkeys. Brain Res 406: 192–206. CrossRef Medline
30. Koliatsos VE, Martin LJ, Walker LC, Richardson RT, DeLong MR, Price DL (1988) Topographic, non-collateralized basal forebrain projections to the amygdala, hippocampus, and anterior cingulate cortex in the rhesus monkey. Brain Res 463:133–139. CrossRef Medline
31. Leemans A, Jones DK (2009) The B-matrix must be rotated when correcting for subject motion in DTI data. Magn Reson Med 61:1336-1349. CrossRef Medline
32. McMackin D, Cockburn J, Anslow P, Gaffan D (1995) Correlation of fornix damage with memory impairment in six cases of colloid cyst removal. Acta Neurochir 135:12–18. CrossRef Medline
33. McMahan RW, Sobel TJ, Baxter MG (1997) Selective immunolesions of hippocampal cholinergic input fail to impair spatial working memory. Hippocampus 7:130-136. CrossRef Medline
34. Mesulam MM (1995) Cholinergic pathways and the ascending reticular activating system of the human brain. Ann NY Acad Sci 757:169-179. CrossRef Medline
35. Mesulam MM, Mufson EJ, Levey AI, Wainer BH (1983) Cholinergic innervation of cortex by the basal forebrain: cytochemistry and cortical connections of the septal area, diagonal band nuclei, nucleus basalis (substantia innominata), and hypothalamus in the rhesus monkey. J Comp Neurol 214:170-197. CrossRef Medline
36. Metzler-Baddeley C, Jones DK, Belaroussi B, Aggleton JP, O’Sullivan MJ (2011) Frontotemporal connections in episodic memory and aging: a diffusion MRI tractography study. J Neurosci 31:13236-13245. CrossRef Medline
37. Metzler-Baddeley C, Hunt S, Jones DK, Leemans A, Aggleton JP, O’Sullivan MJ (2012a) Temporal association tracts and the breakdown of episodic memory in mild cognitive impairment. Neurology 79:2233–2240. CrossRef Medline
38. Metzler-Baddeley C, O’Sullivan MJ, Bells S, Pasternak O, Jones DK (2012b) How and how not to correct for CSF-contamination in diffusion MRI. Neuroimage 59:1394-1403. CrossRef Medline
39. Mioshi E, Dawson K, Mitchell J, Arnold R, Hodges JR (2006) The Addenbrooke’s Cognitive Examination Revised (ACE-R): a brief cognitive test battery for dementia screening. Int J Geriatr Psychiatry 21:1078-1085. CrossRef Medline
40. Morris JC (1993) The Clinical Dementia Rating (CDR): current version and scoring rules. Neurology 43:2412–2414. CrossRef Medline
41. Muir JL, Page KJ, Sirinathsinghji DJ, Robbins TW, Everitt BJ (1993) Excitotoxic lesions of basal forebrain cholinergic neurons: effects on learning, memory and attention. Behav Brain Res 57:123–131. CrossRef Medline
42. Nelson HE, Willison J (1991) National Adult Reading Test (NART) test manual (2nd ed). Windsor, UK: NFER-Nelson.
43. Nichols T, Hayasaka S (2003) Controlling the familywise error rate in functional neuroimaging: a comparative review. Stat Methods Med Res 12: 419–446. CrossRef Medline
44. Nowrangi MA, Lyketsos CG, Leoutsakos JMS, Oishi K, Albert M, Mori S, Mielke MM (2013) Longitudinal, region-specific course of diffusion tensor imaging measures in mild cognitive impairment and Alzheimer’s disease. Alzheimers Dement 9:519-528. CrossRef Medline
45. Parent MB, Baxter MG (2004) Septohippocampal acetylcholine: involved in but not necessary for learning and memory? Learn Mem 11:9-20. CrossRef Medline
46. Parkin AJ, Bindschaedler C, Harsent L, Metzler C (1996) Pathological false alarm rates following damage to the left frontal cortex. Brain Cogn 32:14–27. CrossRef Medline
47. Pasternak O, Sochen N, Gur Y, Intrator N, Assaf Y (2009) Free water elimination and mapping from diffusion MRI. Magn Reson Med 62:717–730. CrossRef Medline
48. Poletti CE, Creswell G (1977) Fornix system efferent projections in the squirrel monkey: an experimental degeneration study. J Comp Neurol 175:101–128. CrossRef Medline
49. Randolph C, Tierney MC, Mohr E, Chase TN (1998) The Repeatable Battery for the Assessment of Neuropsychological Status (RBANS): preliminary clinical validity. J Clin Exp Neuropsychol 20:310-319. CrossRef Medline
50. Rudebeck SR, Scholz J, Millington R, Rohenkohl G, Johansen-Berg H, Lee ACH (2009) Fornix microstructure correlates with recollection but not familiarity memory. J Neurosci 29:14987–14992. CrossRef Medline
51. Sarter M, Bruno JP (2002) The neglected constituent of the basal forebrain corticopetal projection system: GABAergic projections. Eur J Neurosci 15:1867–1873. CrossRef Medline
52. Saunders RC, Aggleton JP (2007) Origin and topography of fibers contrib-uting to the fornix in macaque monkeys. Hippocampus 17:396–411. CrossRef Medline
53. Sexton CE, Mackay CE, Lonie JA, Bastin ME, Terrière E, O’Carroll RE, Ebmeier KP (2010) MRI correlates of episodic memory in Alzheimer’s disease, mild cognitive impairment, and healthy aging. Psychiatry Res 184:57-62. CrossRef Medline
54. Tang Y, Mishkin M, Aigner TG (1997) Effects of muscarinic blockade in perirhinal cortex during visual recognition. Proc Natl Acad Sci U S A 94:12667–12669. CrossRef Medline
55. Teipel SJ, Flatz WH, Heinsen H, Bokde AL, Schoenberg SO, Stöckel S, Dietrich O, Reiser MF, Möller HJ, Hampel H (2005) Measurement of basal forebrain atrophy in Alzheimer’s disease using MRI. Brain 128:2626-2644. CrossRef Medline
56. Tournier JD, Calamante F, Connelly A (2007) Robust determination of the fibre orientation distribution in diffusion MRI: non-negativity constrained super-resolved spherical deconvolution. Neuroimage 35:1459-1472. CrossRef Medline
57. Tournier JD, Yeh CH, Calamante F, Cho KH, Connelly A, Lin CP (2008) Resolving crossing fibres using constrained spherical deconvolution: validation using diffusion-weighted imaging phantom data. Neuroimage 42:617-625. CrossRef Medline
58. Trenerry MR, Crosson B, DeBoe J, Leber WR (1989) Stroop Neuropsychological Screening Test. Odessa, FL: Psychological Assessment Resources.
59. Tsivilis D, Vann SD, Denby C, Roberts N, Mayes AR, Montaldi D, Aggleton JP (2008) A disproportionate role for the fornix and mammillary bodies in recall versus recognition memory. Nat Neurosci 11:834–842. CrossRef Medline
60. Vann SD, Tsivilis D, Denby CE Quamme JR, Yonelinas AP, Aggleton JP, Montaldi D, Mayes AR (2009) Impaired recollection but spared familiarity in patients with extended hippocampal system damage: convergence across three methods. Proc Natl Acad Sci U S A 106:5442–5447. CrossRef Medline
61. Wechsler D (1999) Wechsler Adult Intelligence Scale–3rd UK Edition (WAISIII UK). Oxford, UK: Psychological Corporation and Pearson Assessment.
62. Westerberg CE, Paller KA, Weintraub S, Mesulam MM, Holdstock JS, Mayes AR, Reber PJ (2006) When memory does not fail: familiarity-based recognition in mild cognitive impairment and Alzheimer’s disease. Neuropsychology 20:193–205. CrossRef Medline
63. Zatorre RJ, Fields RD, Johansen-Berg H (2012) Plasticity in gray and white: neuroimaging changes in brain structure during learning. Nat Neurosci 15:528-536. CrossRef Medline