Attempted and successful compensation in preclinical and early manifest neurodegeneration - a review of task fMRI studies

Frontiers in Psychiatry

Volumn 5, Issue SEP, 2014, Pages

  Scheller, Elisa ^a,b   Minkova, Lora ^a,b   Leitner, Mathias ^a   Klöppel, Stefan ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Amnestic mild cognitive impairment; Compensation; Functional magnetic resonance imaging; Healthy aging; Huntington's disease

Indexed keywords

AGING; ARTICLE; BASAL GANGLION; BOLD SIGNAL; BRAIN DEPTH STIMULATION; BRAIN FUNCTION; BRAIN REGION; CINGULATE GYRUS; COGNITIVE THERAPY; CONNECTOME; DISEASE ASSOCIATION; EPISODIC MEMORY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUNTINGTON CHOREA; LATERAL PREFRONTAL CORTEX; MEDIAL PREFRONTAL CORTEX; MEMORY DISORDER; MILD COGNITIVE IMPAIRMENT; NERVE DEGENERATION; NONHUMAN; PHYSICAL ACTIVITY; PREFRONTAL CORTEX; RECOGNITION; TASK PERFORMANCE; WORKING MEMORY;

EID: 84907945925     PISSN: None     EISSN: 16640640     Source Type: Journal    
DOI: 10.3389/fpsyt.2014.00132     Document Type: Article

References (170)

1. Cabeza R, McIntosh AR, Tulving E, Nyberg L, Grady CL. Age-related differences in effective neural connectivity during encoding and recall. Neuroreport (1997) 8:3479-3483.
2. Grady CL, Maisog JM, Horwitz B, Ungerleider LG, Mentis MJ, Salerno JA, Pietrini P, Wagner E, Haxby JV. Age-related changes in cortical blood flow activation during visual processing of faces and location. J Neurosci (1994) 14:1450-1462.
3. Grady CL. Cognitive Neuroscience of Aging. Ann N Y Acad Sci (2008) 1124:127-144. doi:10.1196/annals.1440.009
4. Dennis NA, Cabeza RE. "Frontal lobes and aging: deterioration and compensation," in Principles of frontal lobe function, eds. Stuss, D. T., Knight, R. T. (New York: Oxford University Press). Available at: http://canlab.psych.psu.edu/compensationchapter_stussknightbook_cabezadennis_final. pdf [Accessed April 29, 2014]
5. Barulli D, Stern Y. Efficiency, capacity, compensation, maintenance, plasticity: emerging concepts in cognitive reserve. Trends Cogn Sci (2013) 17:502-509. doi:10.1016/j.tics.2013.08.012
6. Cabeza R. Hemispheric asymmetry reduction in older adults: The HAROLD model. Psychol Aging (2002) 17:85-100. doi:10.1037//0882-7974.17.1.85
7. Davis SW, Dennis NA, Daselaar SM, Fleck MS, Cabeza R. Qué PASA? The Posterior- Anterior Shift in Aging. Cereb Cortex (2008) 18:1201-1209. doi:10.1093/cercor/bhm155
8. Dennis NA, Cabeza RE. "Neuroimaging of healthy cognitive aging," in Handbook of aging and cognition, eds. F. I. M. Craik, T. A. Salthouse (Mahwah (NJ): Erlbaum), 1-54.
9. Reuter-Lorenz PA, Cappell KA. Neurocognitive Aging and the Compensation Hypothesis. Curr Dir Psychol Sci (2008) 17:177-182. doi:10.1111/j.1467-8721.2008.00570.x
10. Reuter-Lorenz PA, Lustig C. Brain aging: reorganizing discoveries about the aging mind. Curr Opin Neurobiol (2005) 15:245-251. doi:10.1016/j.conb.2005.03.016
11. Reuter-Lorenz PA, Mikels JA. "The Aging Mind and Brain: Implications of Enduring Plasticity for Behavioral and Cultural Change," in Lifespan Development and the Brain (Cambridge University Press). Available at: http://dx.doi.org/10.1017/CBO9780511499722.014
12. Park DC, Reuter-Lorenz PA. The Adaptive Brain: Aging and Neurocognitive Scaffolding. Annu Rev Psychol (2009) 60:173-196. doi:10.1146/annurev.psych.59.103006.093656
13. Goh JO, Park DC. Neuroplasticity and cognitive aging: The scaffolding theory of aging and cognition. Restor Neurol Neurosci (2009) 27:391-403. doi:10.3233/RNN-2009-0493
14. Stern Y. What is cognitive reserve? Theory and research application of the reserve concept. J Int Neuropsychol Soc JINS (2002) 8:448-460.
15. Stern Y. Cognitive reserve. Neuropsychologia (2009) 47:2015-2028. doi:10.1016/j.neuropsychologia.2009.03.004
16. Satz P. Brain reserve capacity on symptom onset after brain injury: A formulation and review of evidence for threshold theory. Neuropsychology (1993) 7:273-295. doi:10.1037/0894-4105.7.3.273
17. Solé-Padullés C, Bartrés-Faz D, Junqué C, Vendrell P, Rami L, Clemente IC, Bosch B, Villar A, Bargalló N, Jurado MA, et al. Brain structure and function related to cognitive reserve variables in normal aging, mild cognitive impairment and Alzheimer's disease. Neurobiol Aging (2009) 30:1114-1124. doi:10.1016/j.neurobiolaging.2007.10.008
18. Steffener J, Stern Y. Exploring the neural basis of cognitive reserve in aging. Biochim Biophys Acta BBA - Mol Basis Dis (2012) 1822:467-473. doi:10.1016/j.bbadis.2011.09.012
19. Xu W, Yu J-T, Tan M-S, Tan L. Cognitive Reserve and Alzheimer's Disease. Mol Neurobiol (2014) doi:10.1007/s12035-014-8720-y
20. Grady CL. The cognitive neuroscience of ageing. Nat Rev Neurosci (2012) 13:491-505 doi:10.1038/nrn3256
21. Prvulovic D, Van de Ven V, Sack AT, Maurer K, Linden DEJ. Functional activation imaging in aging and dementia. Psychiatry Res Neuroimaging (2005) 140:97-113. doi:10.1016/j.pscychresns.2005.06.006
22. Spreng RN, Wojtowicz M, Grady CL. Reliable differences in brain activity between young and old adults: A quantitative meta-analysis across multiple cognitive domains. Neurosci Biobehav Rev (2010) 34:1178-1194. doi:10.1016/j.neubiorev.2010.01.009
23. Duverne S, Motamedinia S, Rugg MD. The Relationship between Aging, Performance, and the Neural Correlates of Successful Memory Encoding. Cereb Cortex (2009) 19:733-744. doi:10.1093/cercor/bhn122
24. Price CJ, Friston KJ. Scanning patients with tasks they can perform. Hum Brain Mapp (1999) 8:102-108.
25. Friston KJ, Price CJ. Degeneracy and redundancy in cognitive anatomy. Trends Cogn Sci (2003) 7:151-152. doi:10.1016/S1364-6613(03)00054-8
26. Dickerson BC, Salat DH, Greve DN, Chua EF, Rand-Giovannetti E, Rentz DM, Bertram L, Mullin K, Tanzi RE, Blacker D, et al. Increased hippocampal activation in mild cognitive impairment compared to normal aging and AD. Neurology (2005) 65:404-411. doi:10.1212/01.wnl.0000171450.97464.49
27. Whalley LJ. Brain ageing and dementia: what makes the difference? Br J Psychiatry (2002) 181:369-371. doi:10.1192/bjp.181.5.369
28. Ball MJ. Neuronal loss, neurofibrillary tangles and granulovacuolar degeneration in the hippocampus with ageing and dementia. Acta Neuropathol (Berl) (1977) 37:111-118.
29. Katzman R. Education and the prevalence of dementia and Alzheimer's disease. Neurology (1993) 43:13-20.
30. Katzman R, Aronson M, Fuld P, Kawas C, Brown T, Morgenstern H, Frishman W, Gidez L, Eder H, Ooi WL. Development of dementing illnesses in an 80-year-old volunteer cohort. Ann Neurol (1989) 25:317-324. doi:10.1002/ana.410250402
31. Kaye JA, Swihart T, Howieson D, Dame A, Moore MM, Karnos T, Camicioli R, Ball M, Oken B, Sexton G. Volume loss of the hippocampus and temporal lobe in healthy elderly persons destined to develop dementia. Neurology (1997) 48:1297-1304. doi:10.1212/WNL.48.5.1297
32. Bartzokis G, Cummings JL, Sultzer D, Henderson VW, Nuechterlein KH, Mintz J. White matter structural integrity in healthy aging adults and patients with alzheimer disease: A magnetic resonance imaging study. Arch Neurol (2003) 60:393-398. doi:10.1001/archneur.60.3.393
33. Frisoni GB, Fox NC, Jack CR, Scheltens P, Thompson PM. The clinical use of structural MRI in Alzheimer disease. Nat Rev Neurol (2010) 6:67-77. doi:10.1038/nrneurol.2009.215
34. Rajah MN, D'Esposito M. Region-specific changes in prefrontal function with age: a review of PET and fMRI studies on working and episodic memory. Brain J Neurol (2005) 128:1964-83. doi:10.1093/brain/awh608
35. Pasquini L, Tonch A, Plant C, Zherdin A, Ortner M, Kurz A, Förstl H, Zimmer C, Grimmer T, Wohlschäger A, et al. Intrinsic brain activity of cognitively normal older persons resembles more that of patients both with and at-risk for Alzheimer's disease than that of healthy younger persons. Brain Connect (2014) doi:10.1089/brain.2013.0213
36. Hampel H, Wilcock G, Andrieu S, Aisen P, Blennow K, Broich K, Carrillo M, Fox NC, Frisoni GB, Isaac M, et al. Biomarkers for Alzheimer's disease therapeutic trials. Prog Neurobiol (2011) 95:579-593. doi:10.1016/j.pneurobio.2010.11.005
37. Klöppel S, Henley SM, Hobbs NZ, Wolf RC, Kassubek J, Tabrizi SJ, Frackowiak RSJ. Magnetic resonance imaging of Huntington's disease: preparing for clinical trials. Neuroscience (2009) 164:205-219. doi:10.1016/j.neuroscience.2009.01.045
38. Weir DW, Sturrock A, Leavitt BR. Development of biomarkers for Huntington's disease. Lancet Neurol (2011) 10:573-590. doi:10.1016/S1474-4422(11)70070-9
39. The Huntington's Disease Collaborative Research Group. A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. The Huntington's Disease Collaborative Research Group. Cell (1993) 72:971-983.
40. Langbehn DR, Brinkman RR, Falush D, Paulsen JS, Hayden MR. A new model for prediction of the age of onset and penetrance for Huntington's disease based on CAG length. Clin Genet (2004) 65:267-277. doi:10.1111/j.1399-0004.2004.00241.x
41. Langbehn DR, Hayden MR, Paulsen JS. CAG repeat length and the age of onset in Huntington disease (HD): A review and validation study of statistical approaches. Am J Med Genet B Neuropsychiatr Genet (2010) 153B:397-408. doi:10.1002/ajmg.b.30992
42. Ross CA, Aylward EH, Wild EJ, Langbehn DR, Long JD, Warner JH, Scahill RI, Leavitt BR, Stout JC, Paulsen JS, et al. Huntington disease: natural history, biomarkers and prospects for therapeutics. Nat Rev Neurol (2014) 10:204-216. doi:10.1038/nrneurol.2014.24
43. Walker FO. Huntington's disease. The Lancet (2007) 369:218-228. doi:10.1016/S0140-6736(07)60111-1
44. Beglinger LJ, O'Rourke JJF, Wang C, Langbehn DR, DuffK, Paulsen JS. Earliest functional declines in Huntington disease. Psychiatry Res (2010) 178:414-418. doi:10.1016/j.psychres.2010.04.030
45. Chatterjee A, Anderson KE, Moskowitz CB, Hauser WA, Marder KS. A Comparison of Self-Report and Caregiver Assessment of Depression, Apathy, and Irritability in Huntington's Disease. J Neuropsychiatry Clin Neurosci (2005) 17:378-383. doi:10.1176/appi.neuropsych.17.3.378
46. Harrington DL, Smith MM, Zhang Y, Carlozzi NE, Paulsen JS. Cognitive domains that predict time to diagnosis in prodromal Huntington disease. J Neurol Neurosurg Psychiatry (2012) 83:612-619. doi:10.1136/jnnp-2011-301732
47. Papoutsi M, Labuschagne I, Tabrizi SJ, Stout JC. The cognitive burden in Huntington's disease: Pathology, phenotype, and mechanisms of compensation. Mov Disord (2014) 29:673-683. doi:10.1002/mds.25864
48. Stout JC, Jones R, Labuschagne I, O'Regan AM, Say MJ, Dumas EM, Queller S, Justo D, Santos RD, Coleman A, et al. Evaluation of longitudinal 12 and 24 month cognitive outcomes in premanifest and early Huntington's disease. J Neurol Neurosurg Psychiatry (2012) 83:687-694. doi:10.1136/jnnp-2011-301940
49. Tabrizi SJ, Langbehn DR, Leavitt BR, Roos RA, Durr A, Craufurd D, Kennard C, Hicks SL, Fox NC, Scahill RI, et al. Biological and clinical manifestations of Huntington's disease in the longitudinal TRACK-HD study: cross-sectional analysis of baseline data. Lancet Neurol (2009) 8:791-801. doi:10.1016/S1474-4422(09)70170-X
50. Tabrizi SJ, Scahill RI, Durr A, Roos RA, Leavitt BR, Jones R, Landwehrmeyer GB, Fox NC, Johnson H, Hicks SL, et al. Biological and clinical changes in premanifest and early stage Huntington's disease in the TRACK-HD study: the 12-month longitudinal analysis. Lancet Neurol (2011) 10:31-42. doi:10.1016/S1474-4422(10)70276-3
51. Tabrizi SJ, Scahill RI, Owen G, Durr A, Leavitt BR, Roos RA, Borowsky B, Landwehrmeyer B, Frost C, Johnson H, et al. Predictors of phenotypic progression and disease onset in premanifest and early-stage Huntington's disease in the TRACK-HD study: analysis of 36-month observational data. Lancet Neurol (2013) 12:637-649. doi:10.1016/S1474-4422(13)70088-7
52. Nithianantharajah J, Hannan AJ. Mechanisms mediating brain and cognitive reserve: Experience-dependent neuroprotection and functional compensation in animal models of neurodegenerative diseases. Prog Neuropsychopharmacol Biol Psychiatry (2011) 35:331-339. doi:10.1016/j.pnpbp.2010.10.026
53. Panza F, D'Introno A, Colacicco AM, Capurso C, Del Parigi A, Caselli RJ, Pilotto A, Argentieri G, Scapicchio PL, Scafato E. Current epidemiology of mild cognitive impairment and other predementia syndromes. Am J Geriatr Psychiatry (2005) 13:633-644.
54. Petersen RC, Aisen PS, Beckett LA, Donohue MC, Gamst AC, Harvey DJ, Jack CR, Jagust WJ, Shaw LM, Toga AW, et al. Alzheimer's Disease Neuroimaging Initiative (ADNI). Neurology (2010) 74:201-209. doi:10.1212/WNL.0b013e3181cb3e25
55. Albert MS, DeKosky ST, Dickson D, Dubois B, Feldman HH, Fox NC, Gamst A, Holtzman DM, Jagust WJ, Petersen RC, et al. 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 J Alzheimers Assoc (2011) 7:270-279. doi:10.1016/j.jalz.2011.03.008
56. Dubois B, Feldman HH, Jacova C, Cummings JL, DeKosky ST, Barberger-Gateau P, Delacourte A, Frisoni G, Fox NC, Galasko D, et al. Revising the definition of Alzheimer's disease: a new lexicon. Lancet Neurol (2010) 9:1118-1127. doi:10.1016/S1474-4422(10)70223-4
57. Jack CR, Albert M, Knopman DS, McKhann GM, Sperling RA, Carillo M, Thies W, Phelps CH. Introduction to Revised Criteria for the Diagnosis of Alzheimer's Disease: National Institute on Aging and the Alzheimer Association Workgroups. Alzheimers Dement J Alzheimers Assoc (2011) 7:257-262. doi:10.1016/j.jalz.2011.03.004
58. McKhann GM, Knopman DS, Chertkow H, Hyman BT, Jack CR, Kawas CH, Klunk WE, Koroshetz WJ, Manly JJ, Mayeux R, et al. The diagnosis of dementia 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 J Alzheimers Assoc (2011) 7:263-269. doi:10.1016/j.jalz.2011.03.005
59. Sperling RA, Aisen PS, Beckett LA, Bennett DA, Craft S, Fagan AM, Iwatsubo T, Jack Jr. CR, Kaye J, Montine TJ, et al. Toward defining the preclinical stages of Alzheimer's disease: Recommendations from the National Institute on Aging-Alzheimer's Association workgroups on diagnostic guidelines for Alzheimer's disease. Alzheimers Dement (2011) 7:280-292. doi:10.1016/j.jalz.2011.03.003
60. Wilson RS, Leurgans SE, Boyle PA, Bennett DA. Cognitive decline in prodromal alzheimer disease and mild cognitive impairment. Arch Neurol (2011) 68:351-356. doi:10.1001/archneurol.2011.31
61. Clément F, Belleville S. Test-retest reliability of fMRI verbal episodic memory paradigms in healthy older adults and in persons with mild cognitive impairment. Hum Brain Mapp (2009) 30:4033-4047. doi:10.1002/hbm.20827
62. Zanto TP, Pa J, Gazzaley A. Reliability measures of functional magnetic resonance imaging in a longitudinal evaluation of mild cognitive impairment. NeuroImage (2014) 84:443-452. doi:10.1016/j.neuroimage.2013.08.063
63. Paulsen JS, Zimbelman JL, Hinton SC, Langbehn DR, Leveroni CL, Benjamin ML, Reynolds NC, Rao SM. fMRI Biomarker of Early Neuronal Dysfunction in Presymptomatic Huntington's Disease. Am J Neuroradiol (2004) 25:1715-1721.
64. Feigin A, Ghilardi M-F, Huang C, Ma Y, Carbon M, Guttman M, Paulsen JS, Ghez CP, Eidelberg D. Preclinical Huntington's disease: Compensatory brain responses during learning. Ann Neurol (2006) 59:53-59. doi:10.1002/ana.20684
65. Klöppel S, Draganski B, Siebner HR, Tabrizi SJ, Weiller C, Frackowiak RSJ. Functional Compensation of Motor Function in Pre-Symptomatic Huntington's Disease. Brain (2009) 132:1624-1632. doi:10.1093/brain/awp081
66. Scheller E, Abdulkadir A, Peter J, Tabrizi SJ, Frackowiak RSJ, Klöppel S. Interregional compensatory mechanisms of motor functioning in progressing preclinical neurodegeneration. NeuroImage (2013) 75:146-154. doi:10.1016/j.neuroimage.2013.02.058
67. Wolf RC, Sambataro F, Vasic N, Schönfeldt-Lecuona C, Ecker D, Landwehrmeyer B. Altered frontostriatal coupling in pre-manifest Huntington's disease: effects of increasing cognitive load. Eur J Neurol (2008) 15:1180-1190. doi:10.1111/j.1468-1331.2008.02253.x
68. Wolf RC, Sambataro F, Vasic N, Wolf ND, Thomann PA, Landwehrmeyer GB, Orth M. Longitudinal functional magnetic resonance imaging of cognition in preclinical Huntington's disease. Exp Neurol (2011) 231:214-222. doi:10.1016/j.expneurol.2011.06.011
69. Wolf RC, Vasic N, Schönfeldt-Lecuona C, Ecker D, Landwehrmeyer GB. Cortical dysfunction in patients with Huntington's disease during working memory performance. Hum Brain Mapp (2009) 30:327-339. doi:10.1002/hbm.20502
70. Wolf RC, Sambataro F, Vasic N, Wolf ND, Thomann PA, Landwehrmeyer GB, Orth M. Longitudinal task-negative network analyses in preclinical Huntington's disease. Eur Arch Psychiatry Clin Neurosci (2013) doi:10.1007/s00406-013-0447-7
71. Callicott JH, Egan MF, Mattay VS, Bertolino A, Bone AD, Verchinksi B, Weinberger DR. Abnormal fMRI Response of the Dorsolateral Prefrontal Cortex in Cognitively Intact Siblings of Patients With Schizophrenia. Am J Psychiatry (2003) 160:709-719. doi:10.1176/appi.ajp.160.4.709
72. Georgiou-Karistianis N, Poudel GR, Domínguez D JF, Langmaid R, Gray MA, Churchyard A, Chua P, Borowsky B, Egan GF, Stout JC. Functional and connectivity changes during working memory in Huntington's disease: 18 month longitudinal data from the IMAGE-HD study. Brain Cogn (2013) 83:80-91. doi:10.1016/j.bandc.2013.07.004
73. Georgiou-Karistianis N, Stout JC, Domínguez D. JF, Carron SP, Ando A, Churchyard A, Chua P, Bohanna I, Dymowski AR, Poudel G, et al. Functional magnetic resonance imaging of working memory in Huntington's disease: Cross-sectional data from the IMAGE-HD study. Hum Brain Mapp (2014) 35:1847-1864. doi:10.1002/hbm.22296
74. Poudel GR, Stout JC, D JFD, Gray MA, Salmon L, Churchyard A, Chua P, Borowsky B, Egan GF, Georgiou-Karistianis N. Functional changes during working memory in Huntington's disease: 30-month longitudinal data from the IMAGE-HD study. Brain Struct Funct (2013)1-12. doi:10.1007/s00429-013-0670-z
75. Gray MA, Egan GF, Ando A, Churchyard A, Chua P, Stout JC, Georgiou-Karistianis N. Prefrontal activity in Huntington's disease reflects cognitive and neuropsychiatric disturbances: The IMAGE-HD study. Exp Neurol (2013) 239:218-228. doi:10.1016/j.expneurol.2012.10.020
76. Wolf RC, Grön G, Sambataro F, Vasic N, Wolf ND, Thomann PA, Saft C, Landwehrmeyer GB, Orth M. Brain activation and functional connectivity in premanifest Huntington's disease during states of intrinsic and phasic alertness. Hum Brain Mapp (2012) 33:2161-2173. doi:10.1002/hbm.21348
77. Wolf RC, Sambataro F, Vasic N, Wolf ND, Thomann PA, Saft C, Landwehrmeyer GB, Orth M. Default-mode network changes in preclinical Huntington's disease. Exp Neurol (2012) 237:191-198. doi:10.1016/j.expneurol.2012.06.014
78. Buckner RL, Andrews-Hanna JR, Schacter DL. The Brain's Default Network. Ann N Y Acad Sci (2008) 1124:1-38. doi:10.1196/annals.1440.011
79. Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, Shulman GL. A default mode of brain function. Proc Natl Acad Sci (2001) 98:676-682. doi:10.1073/pnas.98.2.676
80. Novak MJU, Warren JD, Henley SMD, Draganski B, Frackowiak RS, Tabrizi SJ. Altered brain mechanisms of emotion processing in pre-manifest Huntington's disease. Brain (2012) 135:1165-1179. doi:10.1093/brain/aws024
81. Welsh K, Butters N, Hughes J, Mohs R, Heyman A. Detection of abnormal memory decline in mild cases of alzheimer's disease using cerad neuropsychological measures. Arch Neurol (1991) 48:278-281. doi:10.1001/archneur.1991.00530150046016
82. Braak H, Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol (Berl) (1991) 82:239-259.
83. Rombouts SARB, Barkhof F, Veltman DJ, Machielsen WCM, Witter MP, Bierlaagh MA, Lazeron RHC, Valk J, Scheltens P. Functional MR Imaging in Alzheimer's Disease during Memory Encoding. Am J Neuroradiol (2000) 21:1869-1875.
84. Sperling R, Bates J, Chua E, Cocchiarella A, Rentz D, Rosen B, Schacter D, Albert M. fMRI studies of associative encoding in young and elderly controls and mild Alzheimer's disease. J Neurol Neurosurg Psychiatry (2003) 74:44-50. doi:10.1136/jnnp.74.1.44
85. Dickerson BC, Sperling RA. 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. doi:10.1016/j.neuropsychologia.2007.11.030
86. Sperling RA, Dickerson BC, Pihlajamaki M, Vannini P, LaViolette PS, Vitolo OV, Hedden T, Becker JA, Rentz DM, Selkoe DJ, et al. Functional Alterations in Memory Networks in Early Alzheimer's Disease. NeuroMolecular Med (2010) 12:27-43. doi:10.1007/s12017-009-8109-7
87. Belleville S, Sylvain-Roy S, de Boysson C, Ménard M-C. "Characterizing the memory changes in persons with mild cognitive impairment," in Progress in Brain Research Essence of Memory., ed. J.-C. L., Vincent F. Castellucci and Sylvie Belleville Wayne S. Sossin (Elsevier), 365-375. Available at: http://www.sciencedirect.com/science/article/pii/S0079612307000234 [Accessed May 12, 2014]
88. Celone KA, Calhoun VD, Dickerson BC, Atri A, Chua EF, Miller SL, DePeau K, Rentz DM, Selkoe DJ, Blacker D, et al. Alterations in Memory Networks in Mild Cognitive Impairment and Alzheimer's Disease: An Independent Component Analysis. J Neurosci (2006) 26:10222-10231. doi:10.1523/JNEUROSCI.2250-06.2006
89. Kircher TT, Weis S, Freymann K, Erb M, Jessen F, Grodd W, Heun R, Leube DT. Hippocampal activation in patients with mild cognitive impairment is necessary for successful memory encoding. J Neurol Neurosurg Psychiatry (2007) 78:812-818. doi:10.1136/jnnp.2006.104877
90. Miller SL, Fenstermacher E, Bates J, Blacker D, Sperling RA, Dickerson BC. Hippocampal activation in adults with mild cognitive impairment predicts subsequent cognitive decline. J Neurol Neurosurg Psychiatry (2008) 79:630-635. doi:10.1136/jnnp.2007.124149
91. De Rover M, Pironti VA, McCabe JA, Acosta-Cabronero J, Arana FS, Morein-Zamir S, Hodges JR, Robbins TW, Fletcher PC, Nestor PJ, et al. Hippocampal dysfunction in patients with mild cognitive impairment: A functional neuroimaging study of a visuospatial paired associates learning task. Neuropsychologia (2011) 49:2060-2070. doi:10.1016/j.neuropsychologia.2011.03.037
92. Heun R, Freymann K, Erb M, Leube DT, Jessen F, Kircher TT, Grodd W. Mild cognitive impairment (MCI) and actual retrieval performance affect cerebral activation in the elderly. Neurobiol Aging (2007) 28:404-413. doi:10.1016/j.neurobiolaging.2006.01.012
93. Morbelli S, Perneczky R, Drzezga A, Frisoni GB, Caroli A, Berckel BNM van, Ossenkoppele R, Guedj E, Didic M, Brugnolo A, et al. Metabolic Networks Underlying Cognitive Reserve in Prodromal Alzheimer Disease: A European Alzheimer Disease Consortium Project. J Nucl Med (2013) 54:894-902. doi:10.2967/jnumed.112.113928
94. Yassa MA, Stark SM, Bakker A, Albert MS, Gallagher M, Stark CEL. High-resolution structural and functional MRI of hippocampal CA3 and dentate gyrus in patients with amnestic mild cognitive impairment. NeuroImage (2010) 51:1242-1252. doi:10.1016/j.neuroimage.2010.03.040
95. Bakker A, Krauss GL, Albert MS, Speck CL, Jones LR, Stark CE, Yassa MA, Bassett SS, Shelton AL, Gallagher M. Reduction of Hippocampal Hyperactivity Improves Cognition in Amnestic Mild Cognitive Impairment. Neuron (2012) 74:467-474. doi:10.1016/j.neuron.2012.03.023
96. Mandzia JL, McAndrews MP, Grady CL, Graham SJ, Black SE. Neural correlates of incidental memory in mild cognitive impairment: An fMRI study. Neurobiol Aging (2009) 30:717-730. doi:10.1016/j.neurobiolaging.2007.08.024
97. Protzner AB, Mandzia JL, Black SE, McAndrews MP. Network interactions explain effective encoding in the context of medial temporal damage in MCI. Hum Brain Mapp (2011) 32:1277-1289. doi:10.1002/hbm.21107
98. Clément F, Belleville S, Mellah S. Functional neuroanatomy of the encoding and retrieval processes of verbal episodic memory in MCI. Cortex (2010) 46:1005-1015. doi:10.1016/j.cortex.2009.07.003
99. Dannhauser TM, Shergill SS, Stevens T, Lee L, Seal M, Walker RWH, Walker Z. An fMRI study of verbal episodic memory encoding in amnestic mild cognitive impairment. Cortex (2008) 44:869-880. doi:10.1016/j.cortex.2007.04.005
100. Parra MA, Pattan V, Wong D, Beaglehole A, Lonie J, Wan HI, Honey G, Hall J, Whalley HC, Lawrie SM. Medial temporal lobe function during emotional memory in early Alzheimer's disease, mild cognitive impairment and healthy ageing: an fMRI study. BMC Psychiatry (2013) 13:76.
101. EickhoffSB, Laird AR, Grefkes C, Wang LE, Zilles K, Fox PT. Coordinate-based activation likelihood estimation meta-analysis of neuroimaging data: A random-effects approach based on empirical estimates of spatial uncertainty. Hum Brain Mapp (2009) 30:2907-2926. doi:10.1002/hbm.20718
102. Clément F, Belleville S. Compensation and Disease Severity on the Memory-Related Activations in Mild Cognitive Impairment. Biol Psychiatry (2010) 68:894-902. doi:10.1016/j.biopsych.2010.02.004
103. Clément F, Belleville S. Effect of Disease Severity on Neural Compensation of Item and Associative Recognition in Mild Cognitive Impairment. J Alzheimers Dis (2012) 29:109-123. doi:10.3233/JAD-2012-110426
104. Nellessen N, Rottschy C, EickhoffSB, Ketteler ST, Kuhn H, Shah NJ, Schulz JB, Reske M, Reetz K. Specific and disease stage-dependent episodic memory-related brain activation patterns in Alzheimer's disease: a coordinate-based meta-analysis. Brain Struct Funct (2014)1-17. doi:10.1007/s00429-014-0744-6
105. Woodard JL, Seidenberg M, Nielson KA, Antuono P, Guidotti L, Durgerian S, Zhang Q, Lancaster M, Hantke N, Butts A, et al. Semantic memory activation in amnestic mild cognitive impairment. Brain (2009) 132:2068-2078. doi:10.1093/brain/awp157
106. O'Brien JL, O'Keefe KM, LaViolette PS, DeLuca AN, Blacker D, Dickerson BC, Sperling RA. Longitudinal fMRI in elderly reveals loss of hippocampal activation with clinical decline. Neurology (2010) 74:1969-1976. doi:10.1212/WNL.0b013e3181e3966e
107. Brandt J, Aretouli E, Neijstrom E, Samek J, Manning K, Albert MS, Bandeen-Roche K. Selectivity of executive function deficits in mild cognitive impairment. Neuropsychology (2009) 23:607-618. doi:10.1037/a0015851
108. Saunders NLJ, Summers MJ. Longitudinal deficits to attention, executive, and working memory in subtypes of mild cognitive impairment. Neuropsychology (2011) 25:237-doi:10.1037/a0021134
109. Gagnon LG, Belleville S. Working memory in mild cognitive impairment and Alzheimer's disease: Contribution of forgetting and predictive value of complex span tasks. Neuropsychology (2011) 25:226-236. doi:10.1037/a0020919
110. Yetkin FZ, Rosenberg RN, Weiner MF, Purdy PD, Cullum CM. FMRI of working memory in patients with mild cognitive impairment and probable Alzheimer's disease. Eur Radiol (2006) 16:193-206. doi:10.1007/s00330-005-2794-x
111. Döhnel K, Sommer M, Ibach B, Rothmayr C, Meinhardt J, Hajak G. Neural correlates of emotional working memory in patients with mild cognitive impairment. Neuropsychologia (2008) 46:37-48. doi:10.1016/j.neuropsychologia.2007.08.012
112. Kochan NA, Breakspear M, Slavin MJ, Valenzuela M, McCraw S, Brodaty H, Sachdev PS. Functional Alterations in Brain Activation and Deactivation in Mild Cognitive Impairment in Response to a Graded Working Memory Challenge. Dement Geriatr Cogn Disord (2010) 30:553-568. doi:10.1159/000322112
113. Kochan NA, Breakspear M, Valenzuela M, Slavin MJ, Brodaty H, Wen W, Trollor JN, Turner A, Crawford JD, Sachdev PS. Cortical Responses to a Graded Working Memory Challenge Predict Functional Decline in Mild Cognitive Impairment. Biol Psychiatry (2011) 70:123-130. doi:10.1016/j.biopsych.2011.03.006
114. Migo EM, Mitterschiffthaler M, O'Daly O, Dawson GR, Dourish CT, Craig KJ, Simmons A, Wilcock GK, McCulloch E, Jackson SHD, et al. Alterations in working memory networks in amnestic mild cognitive impairment. Aging Neuropsychol Cogn (2014)1-22. doi:10.1080/13825585.2014.894958
115. Bokde ALW, Karmann M, Born C, Teipel SJ, Omerovic M, Ewers M, Frodl T, Meisenzahl E, Reiser M, Möller H-J, et al. Altered Brain Activation During a Verbal Working Memory Task in Subjects with Amnestic Mild Cognitive Impairment. J Alzheimers Dis (2010) 21:103-118. doi:10.3233/JAD-2010-091054
116. Axmacher N, Mormann F, Fernández G, Cohen MX, Elger CE, Fell J. Sustained Neural Activity Patterns during Working Memory in the Human Medial Temporal Lobe. J Neurosci (2007) 27:7807-7816. doi:10.1523/JNEUROSCI.0962-07.2007
117. Axmacher N, Henseler MM, Jensen O, Weinreich I, Elger CE, Fell J. Cross-frequency coupling supports multi-item working memory in the human hippocampus. Proc Natl Acad Sci (2010) 107:3228-3233. doi:10.1073/pnas.0911531107
118. Leszczynski M. How does hippocampus contribute to working memory processing? Front Hum Neurosci (2011)168. doi:10.3389/fnhum.2011.00168
119. Faraco CC, Puente AN, Brown C, Terry DP, Stephen Miller L. Lateral temporal hyperactivation as a novel biomarker of mild cognitive impairment. Neuropsychologia (2013) 51:2281-2293. doi:10.1016/j.neuropsychologia.2013.07.023
120. Haller S, Montandon M-L, Rodriguez C, Moser D, Toma S, Hofmeister J, Sinanaj I, Lovblad K-O, Giannakopoulos P. Acute Caffeine Administration Effect on Brain Activation Patterns in Mild Cognitive Impairment. J Alzheimers Dis (2014) doi:10.3233/JAD-132360
121. Owen AM, McMillan KM, Laird AR, Bullmore E. N-back working memory paradigm: A meta-analysis of normative functional neuroimaging studies. Hum Brain Mapp (2005) 25:46-59. doi:10.1002/hbm.20131
122. Rottschy C, Langner R, Dogan I, Reetz K, Laird AR, Schulz JB, Fox PT, EickhoffSB. Modelling neural correlates of working memory: A coordinate-based meta-analysis. NeuroImage (2012) 60:830-846. doi:10.1016/j.neuroimage.2011.11.050
123. Saur R, Milian M, Erb M, Eschweiler GW, Grodd W, Leyhe T. Cortical Activation during Clock Reading as a Quadratic Function of Dementia State. J Alzheimers Dis (2010) 22:267-284. doi:10.3233/JAD-2010-091390
124. Lenzi D, Serra L, Perri R, Pantano P, Lenzi GL, Paulesu E, Caltagirone C, Bozzali M, Macaluso E. Single domain amnestic MCI: A multiple cognitive domains fMRI investigation. Neurobiol Aging (2011) 32:1542-1557. doi:10.1016/j.neurobiolaging.2009.09.006
125. Jacobs HIL, Boxtel MPJV, Heinecke A, Gronenschild EHBM, Backes WH, Ramakers IHGB, Jolles J, Verhey FRJ. Functional integration of parietal lobe activity in early Alzheimer disease. Neurology (2012) 78:352-360. doi:10.1212/WNL.0b013e318245287d
126. Clément F, Gauthier S, Belleville S. Executive functions in mild cognitive impairment: Emergence and breakdown of neural plasticity. Cortex (2013) 49:1268-1279. doi:10.1016/j.cortex.2012.06.004
127. Utevsky AV, Smith DV, Huettel SA. Precuneus Is a Functional Core of the Default-Mode Network. J Neurosci (2014) 34:932-940. doi:10.1523/JNEUROSCI.4227-13.2014
128. Petersen RC, Smith GE, Waring SC, Ivnik RJ, Tangalos EG, Kokmen E. Mild cognitive impairment: Clinical characterization and outcome. Arch Neurol (1999) 56:303-308. doi:10.1001/archneur.56.3.303
129. Paulsen JS, Zhao H, Stout JC, Brinkman RR, Guttman M, Ross CA, Como P, Manning C, Hayden MR, Shoulson I. Clinical markers of early disease in persons near onset of Huntington's disease. Neurology (2001) 57:658-662. doi:10.1212/WNL.57.4.658
130. Shapira-Lichter I, Oren N, Jacob Y, Gruberger M, Hendler T. Portraying the unique contribution of the default mode network to internally driven mnemonic processes. Proc Natl Acad Sci (2013) 110:4950-4955. doi:10.1073/pnas.1209888110
131. Persson J, Pudas S, Nilsson L-G, Nyberg L. Longitudinal assessment of default-mode brain function in aging. Neurobiol Aging (2014) doi:10.1016/j.neurobiolaging.2014.03.012
132. Lustig C, Snyder AZ, Bhakta M, O'Brien KC, McAvoy M, Raichle ME, Morris JC, Buckner RL. Functional deactivations: Change with age and dementia of the Alzheimer type. Proc Natl Acad Sci (2003) 100:14504-14509. doi:10.1073/pnas.2235925100
133. Hansen NL, Lauritzen M, Mortensen EL, Osler M, Avlund K, Fagerlund B, Rostrup E. Subclinical cognitive decline in middle-age is associated with reduced task-induced deactivation of the brain's default mode network. Hum Brain Mapp (2014)n/a-n/a. doi:10.1002/hbm.22489
134. Ingre M. Why small low-powered studies are worse than large high-powered studies and how to protect against "trivial" findings in research: Comment on Friston (2012). NeuroImage (2013) 81:496-498. doi:10.1016/j.neuroimage.2013.03.030
135. Lindquist MA, Caffo B, Crainiceanu C. Ironing out the statistical wrinkles in "ten ironic rules." NeuroImage (2013) 81:499-502. doi:10.1016/j.neuroimage.2013.02.056
136. Friston K. Sample size and the fallacies of classical inference. NeuroImage (2013) 81:503-504. doi:10.1016/j.neuroimage.2013.02.057
137. Jones RN, Manly J, Glymour MM, Rentz DM, Jefferson AL, Stern Y. Conceptual and Measurement Challenges in Research on Cognitive Reserve. J Int Neuropsychol Soc (2011) 17:593-601. doi:10.1017/S1355617710001748
138. Kaller CP, Heinze K, Mader I, Unterrainer JM, Rahm B, Weiller C, Köstering L. Linking planning performance and gray matter density in mid-dorsolateral prefrontal cortex: Moderating effects of age and sex. NeuroImage (2012) 63:1454-1463. doi:10.1016/j.neuroimage.2012.08.032
139. Steffener J, Reuben A, Rakitin B, Stern Y. Supporting performance in the face of agerelated neural changes: testing mechanistic roles of cognitive reserve. Brain Imaging Behav (2011) 5:212-221. doi:10.1007/s11682-011-9125-4
140. Friston KJ, Harrison L, Penny W. Dynamic causal modelling. NeuroImage (2003) 19:1273-1302. doi:10.1016/S1053-8119(03)00202-7
141. Goebel R, Roebroeck A, Kim D-S, Formisano E. Investigating directed cortical interactions in time-resolved fMRI data using vector autoregressive modeling and Granger causality mapping. Magn Reson Imaging (2003) 21:1251-1261. doi:10.1016/j.mri.2003.08.026
142. Rowe JB. Connectivity analysis is essential to understand neurological disorders. Front Syst Neurosci (2010) 4:144. doi:10.3389/fnsys.2010.00144
143. Grefkes C, Fink GR. Connectivity-based approaches in stroke and recovery of function. Lancet Neurol (2014) 13:206-216. doi:10.1016/S1474-4422(13)70264-3
144. D'Esposito M, Deouell LY, Gazzaley A. Alterations in the BOLD fMRI signal with ageing and disease: a challenge for neuroimaging. Nat Rev Neurosci (2003) 4:863-872. doi:10.1038/nrn1246
145. Buckner RL, Snyder AZ, Sanders AL, Raichle ME, Morris JC. Functional Brain Imaging of Young, Nondemented, and Demented Older Adults. J Cogn Neurosci (2000) 12:24-34. doi:10.1162/089892900564046
146. Hillary FG, Biswal B. The Influence of Neuropathology on the fMRI Signal: A Measurement of Brain or Vein? Clin Neuropsychol (2007) 21:58-72. doi:10.1080/13854040601064542
147. Kannurpatti SS, Motes MA, Rypma B, Biswal BB. Neural and vascular variability and the fMRI-BOLD response in normal aging. Magn Reson Imaging (2010) 28:466-476. doi:10.1016/j.mri.2009.12.007
148. Ross CA, Tabrizi SJ. Huntington's disease: from molecular pathogenesis to clinical treatment. Lancet Neurol (2011) 10:83-98. doi:10.1016/S1474-4422(10)70245-3
149. Reis J, Robertson EM, Krakauer JW, Rothwell J, Marshall L, GerloffC, Wassermann EM, Pascual-Leone A, Hummel F, Celnik PA, et al. Consensus: Can transcranial direct current stimulation and transcranial magnetic stimulation enhance motor learning and memory formation? Brain Stimulat (2008) 1:363-369. doi:10.1016/j.brs.2008.08.001
150. Manenti R, Cotelli M, Miniussi C. Successful physiological aging and episodic memory: A brain stimulation study. Behav Brain Res (2011) 216:153-158. doi:10.1016/j.bbr.2010.07.027
151. Rossi S. Age-Related Functional Changes of Prefrontal Cortex in Long-Term Memory: A Repetitive Transcranial Magnetic Stimulation Study. J Neurosci (2004) 24:7939-7944. doi:10.1523/JNEUROSCI.0703-04.2004
152. Solé-Padullés C, Bartrés-Faz D, Junqué C, Clemente IC, Molinuevo JL, Bargalló N, Sánchez-Aldeguer J, Bosch B, Falcón C, Valls-Solé J. Repetitive Transcranial Magnetic Stimulation Effects on Brain Function and Cognition among Elders with Memory Dysfunction. A Randomized Sham-Controlled Study. Cereb Cortex (2006) 16:1487-1493. doi:10.1093/cercor/bhj083
153. Cotelli M, Manenti R, Cappa SF, Zanetti O, Miniussi C. Transcranial magnetic stimulation improves naming in Alzheimer disease patients at different stages of cognitive decline. Eur J Neurol (2008) 15:1286-1292. doi:10.1111/j.1468-1331.2008.02202.x
154. Demirtas-Tatlidede A, Vahabzadeh-Hagh AM, Pascual-Leone A. Can noninvasive brain stimulation enhance cognition in neuropsychiatric disorders? Neuropharmacology (2013) 64:566-578. doi:10.1016/j.neuropharm.2012.06.020
155. Miniussi C, Cappa SF, Cohen LG, Floel A, Fregni F, Nitsche MA, Oliveri M, Pascual-Leone A, Paulus W, Priori A, et al. Efficacy of repetitive transcranial magnetic stimulation/transcranial direct current stimulation in cognitive neurorehabilitation. Brain Stimulat (2008) 1:326-336. doi:10.1016/j.brs.2008.07.002
156. Grefkes C, Nowak DA, Wang LE, Dafotakis M, EickhoffSB, Fink GR. Modulating cortical connectivity in stroke patients by rTMS assessed with fMRI and dynamic causal modeling. NeuroImage (2010) 50:233-242. doi:10.1016/j.neuroimage.2009.12.029
157. Hampstead BM, Gopinath K. Behavioral and fMRI changes associated with combined tDCS and cognitive rehabilitation in a case series of patients with mild cognitive impairment. Clin Neurophysiol (2013) 124:e123-e124. doi:10.1016/j.clinph.2013.04.202
158. Flöel A. tDCS-enhanced motor and cognitive function in neurological diseases. NeuroImage (2014) 85, Part 3:934-947. doi:10.1016/j.neuroimage.2013.05.098
159. Lautenschlager NT, Cox K, Kurz AF. Physical Activity and Mild Cognitive Impairment and Alzheimer's Disease. Curr Neurol Neurosci Rep (2010) 10:352-358. doi:10.1007/s11910-010-0121-7
160. Hahn EA, Andel R. Nonpharmacological Therapies for Behavioral and Cognitive Symptoms of Mild Cognitive Impairment. J Aging Health (2011) 23:1223-1245. doi:10.1177/0898264311422745
161. Piira A, van Walsem MR, Mikalsen G, Nilsen KH, Knutsen S, Frich JC. Effects of a One Year Intensive Multidisciplinary Rehabilitation Program for Patients with Huntington's Disease: a Prospective Intervention Study. PLoS Curr (2013) doi:10.1371/currents.hd.9504af71e0d1f87830c25c394be47027
162. Zinzi P, Salmaso D, Grandis RD, Graziani G, Maceroni S, Bentivoglio A, Zappata P, Frontali M, Jacopini G. Effects of an intensive rehabilitation programme on patients with Huntington's disease: a pilot study. Clin Rehabil (2007) 21:603-613. doi:10.1177/0269215507075495
163. Valenzuela M, Sachdev P. Can Cognitive Exercise Prevent the Onset of Dementia? Systematic Review of Randomized Clinical Trials with Longitudinal Follow-up. Am J Geriatr Psychiatry (2009) 17:179-187. doi:10.1097/JGP.0b013e3181953b57
164. Konsztowicz S, Anton J, Crane J, Moafmashhadi P, Koski L. A Pilot Study of Training and Compensation Interventions for Mild Cognitive Impairment. Dement Geriatr Cogn Disord EXTRA (2013) 3:192-201. doi:10.1159/000350026
165. Li H, Li J, Li N, Li B, Wang P, Zhou T. Cognitive intervention for persons with mild cognitive impairment: A meta-analysis. Ageing Res Rev (2011) 10:285-296. doi:10.1016/j.arr.2010.11.003
166. Jean L, Bergeron M-È, Thivierge S, Simard M. Cognitive Intervention Programs for Individuals With Mild Cognitive Impairment: Systematic Review of the Literature. Am J Geriatr Psychiatry (2010) 18:281-296. doi:10.1097/JGP.0b013e3181c37ce9
167. Simon SS, Yokomizo JE, Bottino CMC. Cognitive intervention in amnestic Mild Cognitive Impairment: A systematic review. Neurosci Biobehav Rev (2012) 36:1163-1178. doi:10.1016/j.neubiorev.2012.01.007
168. Stott J, Spector A. A review of the effectiveness of memory interventions in mild cognitive impairment (MCI). Int Psychogeriatr (2011) 23:526-538. doi:10.1017/S1041610210001973
169. Hampstead BM, Stringer AY, Stilla RF, Deshpande G, Hu X, Moore AB, Sathian K. Activation and Effective Connectivity Changes Following Explicit-Memory Training for Face-Name Pairs in Patients With Mild Cognitive Impairment A Pilot Study. Neurorehabil Neural Repair (2011) 25:210-222. doi:10.1177/1545968310382424
170. Carretti B, Borella E, Fostinelli S, Zavagnin M. Benefits of training working memory in amnestic mild cognitive impairment: specific and transfer effects. Int Psychogeriatr (2013) 25:617-626. doi:10.1017/S1041610212002177