Regional functional connectivity predicts distinct cognitive impairments in Alzheimer's disease spectrum

NeuroImage: Clinical

Volumn 5, Issue , 2014, Pages 385-395

  Ranasinghe, Kamalini G ^a   Hinkley, Leighton B ^b   Beagle, Alexander J ^a   Mizuiri, Danielle ^b   Dowling, Anne F ^b   Honma, Susanne M ^b   Finucane, Mariel M ^c   Scherling, Carole ^a   Miller, Bruce L ^a   Nagarajan, Srikantan S ^b   Vossel, Keith A ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c GLADSTONE INSTITUTE OF NEUROLOGICAL DISEASE   (United States)

Author keywords

Alzheimer's disease spectrum; Logopenic variant PPA; Magnetoencephalography (MEG); Network dysfunction; Posterior cortical atrophy; Resting state functional connectivity

Indexed keywords

ADULT; ALPHA RHYTHM; ALZHEIMER DISEASE; ARTICLE; BRAIN CORTEX ATROPHY; BRAIN REGION; CLINICAL ARTICLE; COGNITION; COGNITIVE DEFECT; CONNECTOME; DISEASE SEVERITY; EPISODIC MEMORY; EXECUTIVE FUNCTION; FEMALE; FRONTAL CORTEX; HUMAN; MAGNETOENCEPHALOGRAPHY; MAGNETOENCEPHALOGRAPHY SYSTEM; MALE; MENTAL PERFORMANCE; MIDDLE AGED; MILD COGNITIVE IMPAIRMENT; PARIETAL CORTEX; PREDICTIVE VALUE; PRIMARY PROGRESSIVE APHASIA; PRIORITY JOURNAL; RESTING STATE NETWORK; AGED; BRAIN; COGNITION DISORDERS; COMPLICATION; COMPUTER ASSISTED DIAGNOSIS; NERVE TRACT; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; SIGNAL PROCESSING;

AGED; ALZHEIMER DISEASE; BRAIN; COGNITION DISORDERS; FEMALE; HUMANS; IMAGE INTERPRETATION, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MAGNETOENCEPHALOGRAPHY; MALE; MIDDLE AGED; NEURAL PATHWAYS; NEUROPSYCHOLOGICAL TESTS; SIGNAL PROCESSING, COMPUTER-ASSISTED;

EID: 84907302906     PISSN: None     EISSN: 22131582     Source Type: Journal    
DOI: 10.1016/j.nicl.2014.07.006     Document Type: Article

References (63)

1. Albert M.S., DeKosky S.T., Dickson D., Dubois B., Feldman H.H., Fox N.C., Gamst A., Holtzman D.M., Jagust W.J., and Petersen R.C. 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 Alzheimer's & Dementia: the Journal of the Alzheimer's Association 7 2011 270 279 10.1016/j.jalz.2011.03.008 21514249
2. Ashburner J., and Friston K.J. Nonlinear spatial normalization using basis functions Human Brain Mapping 7 1999 254 266 10408769 (Pubitemid 29269964)
3. Baldo J.V., Schwartz S., Wilkins D., and Dronkers N.F. Role of frontal versus temporal cortex in verbal fluency as revealed by voxel-based lesion symptom mapping Journal of the International Neuropsychological Society: JINS 12 2006 896 900 10.1017/S1355617706061078 17064451 (Pubitemid 46415894)
4. Baldo J.V., and Shimamura A.P. Letter and category fluency in patients with frontal lobe lesions Neuropsychology 12 1998 259 267 9556772 (Pubitemid 28188866)
5. Benjamini Y., and Hochberg Y. Controlling the false discovery rate: A practical and powerful approach to multiple testing Journal of Royal Statistical Society 57 1995 289 300
6. Brenner R.P., Ulrich R.F., Spiker D.G., Sclabassi R.J., Reynolds C.F. 3rd, Marin R.S., and Boller F. Computerized EEG spectral analysis in elderly normal, demented and depressed subjects Electroencephalography and Clinical Neurophysiology 64 1986 483 492 2430770 (Pubitemid 17181929)
7. Buckner R.L., Snyder A.Z., Shannon B.J., LaRossa G., Sachs R., Fotenos A.F., Sheline Y.I., Klunk W.E., Mathis C.A., and Morris J.C. et al. Molecular, structural, and functional characterization of Alzheimer's disease: Evidence for a relationship between default activity, amyloid, and memory Journal of Neuroscience: the Official Journal of the Society for Neuroscience 25 2005 7709 7717 10.1523/JNEUROSCI.2177-05.2005 16120771 (Pubitemid 41208641)
8. Cabeza R., and Nyberg L. Imaging cognition II: An empirical review of 275 PET and fMRI studies Journal of Cognitive Neuroscience 12 2000 1 47 10769304 (Pubitemid 30142782)
9. Cohen J. A power primer Psychological Bulletin 112 1992 155 159 19565683
10. Dalal S.S., Guggisberg A.G., Edwards E., Sekihara K., Findlay A.M., Canolty R.T., Berger M.S., Knight R.T., Barbaro N.M., and Kirsch H.E. et al. Five-dimensional neuroimaging: Localization of the time-frequency dynamics of cortical activity NeuroImage 40 2008 1686 1700 10.1016/j.neuroimage.2008.01.023 18356081
11. Dalal S.S., Zumer J.M., Guggisberg A.G., Trumpis M., Wong D.D., Sekihara K., and Nagarajan S.S. MEG/EEG source reconstruction, statistical evaluation, and visualization with NUTMEG Computational Intelligence and Neuroscience 2011 2011 758973 10.1155/2011/758973 21437174
12. de Haan W., Mott K., van Straaten E.C., Scheltens P., and Stam C.J. Activity dependent degeneration explains hub vulnerability in Alzheimer's disease PLoS Computational Biology 8 2012 10.1371/journal.pcbi.1002582 22915996
13. de Haan W., Stam C.J., Jones B.F., Zuiderwijk I.M., van Dijk B.W., and Scheltens P. Resting-state oscillatory brain dynamics in Alzheimer disease Journal of Clinical Neurophysiology: Official Publication of the American Electroencephalographic Society 25 2008 187 193 10.1097/WNP.0b013e31817da184 18677182
14. de Haan W., van der Flier W.M., Koene T., Smits L.L., Scheltens P., and Stam C.J. Disrupted modular brain dynamics reflect cognitive dysfunction in Alzheimer's disease Neuroimage 59 2012 3085 3093 10.1016/j.neuroimage.2011.11. 055 22154957
15. Devanand D.P., Pradhaban G., Liu X., Khandji A., De Santi S., Segal S., Rusinek H., Pelton G.H., Honig L.S., and Mayeux R. et al. Hippocampal and entorhinal atrophy in mild cognitive impairment: Prediction of Alzheimer disease Neurology 68 2007 828 836 10.1212/01.wnl.0000256697.20968.d7 17353470 (Pubitemid 46568534)
16. Dosenbach N.U., Fair D.A., Miezin F.M., Cohen A.L., Wenger K.K., Dosenbach R.A., Fox M.D., Snyder A.Z., Vincent J.L., and Raichle M.E. et al. Distinct brain networks for adaptive and stable task control in humans Proceedings of the National Academy of Sciences of the United States of America 104 2007 11073 11078 10.1073/pnas.0704320104 17576922 (Pubitemid 47175228)
17. Duffy F.H., Albert M.S., and McAnulty G. Brain electrical activity in patients with presenile and senile dementia of the Alzheimer type Annals of Neurology 16 1984 439 448 10.1002/ana.410160404 6497353 (Pubitemid 14021822)
18. Engel A.K., Gerloff C., Hilgetag C.C., and Nolte G. Intrinsic coupling modes: Multiscale interactions in ongoing brain activity Neuron 80 2013 867 886 10.1016/j.neuron.2013.09.038 24267648
19. Fox M.D., and Raichle M.E. Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging Nature Reviews. Neuroscience 8 2007 700 711 10.1038/nrn2201 17704812 (Pubitemid 47283145)
20. Gelman A., Hill J., and Yajima M. Why we (usually) don't have to worry about multiple comparisons Journal of Research on Educational Effectiveness 5 2012 189 211
21. Gelman A., and Rubin D.B. Inference from iterative simulation using multiple sequences Statistical Science 1992 457 472
22. Goldman-Rakic P.S. Circuitry of primate prefrontal cortex and Regulation of Behavior by representational memory F. Plum, Handbook of Physiology, The Nervous System, Higher Functions of the Brain 1987 American Physiological Society Bethesda, MD 373 417
23. Goldman-Rakic P.S. Topography of cognition: Parallel distributed networks in primate association cortex Annual Review of Neuroscience 11 1988 137 156 10.1146/annurev.ne.11.030188.001033 3284439
24. Gorno-Tempini M.L., Hillis A.E., Weintraub S., Kertesz A., Mendez M., Cappa S.F., Ogar J.M., Rohrer J.D., Black S., and Boeve B.F. et al. Classification of primary progressive aphasia and its variants Neurology 76 2011 1006 1014 10.1212/WNL.0b013e31821103e6 21325651
25. Gershberg F.B., and Shimamura A.P. Impaired use of organizational strategies in free recall following frontal lobe damage Neuropsychologia 33 1995 1305 1333 8552230
26. Grogan A., Green D.W., Ali N., Crinion J.T., and Price C.J. Structural correlates of semantic and phonemic fluency ability in first and second languages Cerebral Cortex (New York, N.Y.: 1991) 19 2009 2690 2698 10.1093/cercor/bhp023 19293396
27. Guggisberg A.G., Honma S.M., Findlay A.M., Dalal S.S., Kirsch H.E., Berger M.S., and Nagarajan S.S. Mapping functional connectivity in patients with brain lesions Annals of Neurology 63 2008 193 203 10.1002/ana.21224 17894381 (Pubitemid 351355298)
28. Hampson M., Driesen N.R., Skudlarski P., Gore J.C., and Constable R.T. Brain connectivity related to working memory performance Journal of Neuroscience: the Official Journal of the Society for Neuroscience 26 2006 13338 13343 10.1523/JNEUROSCI.3408-06.2006 17182784 (Pubitemid 46011644)
29. Hanslmayr S., Gross J., Klimesch W., and Shapiro K.L. The role of alpha oscillations in temporal attention Brain Research Reviews 67 2011 331 343 10.1016/j.brainresrev.2011.04.002 21592583
30. Hindriks R., Bijma F., van Dijk B.W., van der Werf Y.D., van Someren E.J., and van der Vaart A.W. Dynamics underlying spontaneous human alpha oscillations: Adata-driven approach Neuroimage 57 2011 440 451 10.1016/j.neuroimage.2011.04.043 21558008
31. Hinkley L.B., Marco E.J., Findlay A.M., Honma S., Jeremy R.J., Strominger Z., Bukshpun P., Wakahiro M., Brown W.S., and Paul L.K. et al. The role of corpus callosum development in functional connectivity and cognitive processing PloS One 7 2012 e39804 10.1371/journal.pone.0039804 22870191
32. Hinkley L.B., Owen J.P., Fisher M., Findlay A.M., Vinogradov S., and Nagarajan S.S. Cognitive impairments in schizophrenia as assessed through activation and connectivity measures of magnetoencephalography (MEG) data Frontiers in Human Neuroscience 3 2010 73 10.3389/neuro.09.073.2009 21160543
33. Hinkley L.B., Vinogradov S., Guggisberg A.G., Fisher M., Findlay A.M., and Nagarajan S.S. Clinical symptoms and alpha band resting-state functional connectivity imaging in patients with schizophrenia: Implications for novel approaches to treatment Biological Psychiatry 70 2011 1134 1142 10.1016/j.biopsych.2011.06.029 21861988
34. Hirshorn E.A., and Thompson-Schill S.L. Role of the left inferior frontal gyrus in covert word retrieval: Neural correlates of switching during verbal fluency Neuropsychologia 44 2006 2547 2557 10.1016/j.neuropsychologia.2006.03. 035 16725162 (Pubitemid 44062559)
35. Janowsky J.S., Shimamura A.P., Kritchevsky M., and Squire L.R. Cognitive impairment following frontal lobe damage and its relevance to human amnesia Behavioral Neuroscience 103 1989 548 560 2736069 (Pubitemid 19161168)
36. Jelic V., Shigeta M., Julin P., Almkvist O., Winblad B., and Wahlund L.O. Quantitative electroencephalography power and coherence in Alzheimer's disease and mild cognitive impairment Dementia (Basel, Switzerland) 7 1996 314 323 8915037 (Pubitemid 26341260)
37. Jeong J. EEG dynamics in patients with Alzheimer's disease Clinical Neurophysiology: Official Journal of the International Federation of Clinical Neurophysiology 115 2004 1490 1505 10.1016/j.clinph.2004.01.001 15203050 (Pubitemid 38760295)
38. Klimesch W. EEG alpha and theta oscillations reflect cognitive and memory performance: A review and analysis Brain Research. Brain Research Reviews 29 1999 169 195 10209231 (Pubitemid 29191338)
39. Kramer J.H., Jurik J., Sha S.J., Rankin K.P., Rosen H.J., Johnson J.K., and Miller B.L. Distinctive neuropsychological patterns in frontotemporal dementia, semantic dementia, and Alzheimer disease Cognitive and Behavioral Neurology: Official Journal of the Society for Behavioral and Cognitive Neurology 16 2003 211 218 14665820 (Pubitemid 37517826)
40. Libon D.J., McMillan C., Gunawardena D., Powers C., Massimo L., Khan A., Morgan B., Farag C., Richmond L., and Weinstein J. et al. Neurocognitive contributions to verbal fluency deficits in frontotemporal lobar degeneration Neurology 73 2009 535 542 10.1212/WNL.0b013e3181b2a4f5 19687454
41. Martin-Loeches M., Gil P., Jimenez F., Exposito F.J., Miguel F., Cacabelos R., and Rubia F.J. Topographic maps of brain electrical activity in primary degenerative dementia of the Alzheimer type and multiinfarct dementia Biological Psychiatry 29 1991 211 223 2015328
42. Martino J., Honma S.M., Findlay A.M., Guggisberg A.G., Owen J.P., Kirsch H.E., Berger M.S., and Nagarajan S.S. Resting functional connectivity in patients with brain tumors in eloquent areas Annals of Neurology 69 2011 521 532 10.1002/ana.22167 21400562
43. McKhann G.M., Knopman D.S., Chertkow H., Hyman B.T., Jack C.R. Jr., Kawas C.H., Klunk W.E., Koroshetz W.J., Manly J.J., and 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 Alzheimer's amp; Dementia: the Journal of the Alzheimer's Association 7 2011 263 269 10.1016/j.jalz.2011.03.005 21514250
44. Mendez M.F., Ghajarania M., and Perryman K.M. Posterior cortical atrophy: Clinical characteristics and differences compared to Alzheimer's disease Dementia and Geriatric Cognitive Disorders 14 2002 33 40 58331 ] [Pubmed: 12053130 ] (Pubitemid 34621579)
45. Morris J.C. The clinical dementia rating (CDR): Current version and scoring rules Neurology 43 1993 2412 2414 8232972 (Pubitemid 23346995)
46. Nolte G., Bai O., Wheaton L., Mari Z., Vorbach S., and Hallett M. Identifying true brain interaction from EEG data using the imaginary part of coherency Clinical Neurophysiology: Official Journal of the International Federation of Clinical Neurophysiology 115 2004 2292 2307 10.1016/j.clinph.2004. 04.029 15351371 (Pubitemid 39200796)
47. Osipova D., Ahveninen J., Jensen O., Ylikoski A., and Pekkonen E. Altered generation of spontaneous oscillations in Alzheimer's disease Neuroimage 27 2005 835 841 10.1016/j.neuroimage.2005.05.011 15961323 (Pubitemid 41317253)
48. Palva J.M., Monto S., Kulashekhar S., and Palva S. Neuronal synchrony reveals working memory networks and predicts individual memory capacity Proceedings of the National Academy of Sciences of the United States of America 107 2010 7580 7585 10.1073/pnas.0913113107 20368447
49. Plummer M., Best N., Cowles K., and Vinesh K. CODA: Convergence diagnosis and output analysis for MCMC R News 6 2006 7 11
50. Possin K.L., Lamarre A.K., Wood K.A., Mungas D.M., and Kramer J.H. Ecological validity and neuroanatomical correlates of the NIH EXAMINER Executive composite score Journal of the International Neuropsychological Society: JINS 20 2014 20 28 10.1017/S1355617713000611 23764015
51. Rabinovici G.D., Furst A.J., Alkalay A., Racine C.A., O'Neil J.P., Janabi M., Baker S.L., Agarwal N., Bonasera S.J., and Mormino E.C. et al. Increased metabolic vulnerability in early-onset Alzheimer's disease is not related to amyloid burden Brain: A Journal of Neurology 133 2010 512 528 10.1093/brain/awp326 20080878
52. Schwartz S., and Baldo J. Distinct patterns of word retrieval in right and left frontal lobe patients: A multidimensional perspective Neuropsychologia 39 2001 1209 1217 11527558 (Pubitemid 32799149)
53. Seeley W.W., Crawford R.K., Zhou J., Miller B.L., and Greicius M.D. Neurodegenerative diseases target large-scale human brain networks Neuron 62 2009 42 52 10.1016/j.neuron.2009.03.024 19376066
54. Seeley W.W., Menon V., Schatzberg A.F., Keller J., Glover G.H., Kenna H., Reiss A.L., and Greicius M.D. Dissociable intrinsic connectivity networks for salience processing and executive control Journal of Neuroscience: the Official Journal of the Society for Neuroscience 27 2007 2349 2356 10.1523/JNEUROSCI. 5587-06.2007 17329432 (Pubitemid 46340968)
55. Singer W. Neuronal synchrony: A versatile code for the definition of relations? Neuron 24 1999 49 65 10677026 (Pubitemid 29466147)
56. Stam C.J., de Haan W., Daffertshofer A., Jones B.F., Manshanden I., van Cappellen van Walsum A.M., Montez T., Verbunt J.P., de Munck J.C., and van Dijk B.W. et al. Graph theoretical analysis of magnetoencephalographic functional connectivity in Alzheimer's disease Brain: A Journal of Neurology 132 2009 213 224 10.1093/brain/awn262 18952674
57. Stam C.J., Jones B.F., Manshanden I., van Cappellen van Walsum A.M., Montez T., Verbunt J.P., de Munck J.C., van Dijk B.W., Berendse H.W., and Scheltens P. Magnetoencephalographic evaluation of resting-state functional connectivity in Alzheimer's disease NeuroImage 32 2006 1335 1344 10.1016/j.neuroimage.2006.05.033 16815039 (Pubitemid 44278696)
58. Tarapore P.E., Martino J., Guggisberg A.G., Owen J., Honma S.M., Findlay A., Berger M.S., Kirsch H.E., and Nagarajan S.S. Magnetoencephalographic imaging of resting-state functional connectivity predicts postsurgical neurological outcome in brain gliomas Neurosurgery 71 2012 1012 1022 10.1227/NEU. 0b013e31826d2b78 22895403
59. Troyer A.K., Moscovitch M., Winocur G., Alexander M.P., and Stuss D. Clustering and switching on verbal fluency: The effects of focal frontal- and temporal-lobe lesions Neuropsychologia 36 1998 499 504 9705059 (Pubitemid 28342185)
60. Vincent J.L., Kahn I., Snyder A.Z., Raichle M.E., and Buckner R.L. Evidence for a frontoparietal control system revealed by intrinsic functional connectivity Journal of Neurophysiology 100 2008 3328 3342 10.1152/jn.90355.2008 18799601
61. Westlake K.P., Hinkley L.B., Bucci M., Guggisberg A.G., Byl N., Findlay A.M., Henry R.G., and Nagarajan S.S. Resting state alpha-band functional connectivity and recovery after stroke Experimental Neurology 237 2012 160 169 10.1016/j.expneurol.2012.06.020 22750324
62. Yeo B.T., Krienen F.M., Sepulcre J., Sabuncu M.R., Lashkari D., Hollinshead M., Roffman J.L., Smoller J.W., Zöllei L., and Polimeni J.R. et al. The organization of the human cerebral cortex estimated by intrinsic functional connectivity Journal of Neurophysiology 106 2011 1125 1165 10.1152/jn.00338.2011 21653723
63. Zhou J., Gennatas E.D., Kramer J.H., Miller B.L., and Seeley W.W. Predicting regional neurodegeneration from the healthy brain functional connectome Neuron 73 2012 1216 1227 10.1016/j.neuron.2012.03.004 22445348