Brain Structure and Function

, Volume 220, Issue 2, pp 745–762 | Cite as

Differentially disrupted functional connectivity of the subregions of the inferior parietal lobule in Alzheimer’s disease

  • Zhiqun Wang
  • Mingrui Xia
  • Zhengjia Dai
  • Xia Liang
  • Haiqing Song
  • Yong He
  • Kuncheng Li
Original Article


Recent research on Alzheimer’s disease (AD) has shown that the altered structure and function of the inferior parietal lobule (IPL) provides a promising indicator of AD. However, little is known about the functional connectivity of the IPL subregions in AD subjects. In this study, we collected resting-state functional magnetic resonance imaging data from 32 AD patients and 38 healthy controls. We defined seven subregions of the IPL according to probabilistic cytoarchitectonic atlases and mapped the whole-brain resting-state functional connectivity for each subregion. Using hierarchical clustering analysis, we identified three distinct functional connectivity patterns of the IPL subregions: the anterior IPL connected with the sensorimotor network (SMN) and salience network (SN); the central IPL had connectivity with the executive-control network (ECN); and the posterior IPL exhibited connections with the default-mode network (DMN). Compared with the controls, the AD patients demonstrated distinct disruptive patterns of the IPL subregional connectivity with these different networks (SMN, SN, ECN and DMN), which suggests the impairment of the functional integration in the IPL. Notably, we also observed that the IPL subregions showed increased connectivity with the posterior part of the DMN in AD patients, which potentially indicates a compensatory mechanism. Finally, these abnormal IPL functional connectivity changes were closely associated with cognitive performance. Collectively, we show that the subregions of the IPL present distinct functional connectivity patterns with various functional networks that are differentially impaired in AD patients. Our results also suggest that functional disconnection and compensation in the IPL may coexist in AD.


Supramarginal gyrus Angular gyrus Network fMRI Alzheimer disease 



This work was supported by the Natural Science Foundation of China (grant nos. 81030028, 81000606 and 81370037), the Beijing Natural Science Foundation (grant no. Z111107067311036 and Z101107052210002) and the National Science Fund for Distinguished Young Scholars (grant no. 81225012).

Conflict of interest

The authors declare no competing financial interests.

Supplementary material

429_2013_681_MOESM1_ESM.docx (20 kb)
Supplementary material 1 (DOCX 20 kb)
429_2013_681_MOESM2_ESM.tif (3.7 mb)
Supplementary material 2 (TIFF 3809 kb)


  1. Agosta F, Rocca MA, Pagani E, Absinta M, Magnani G, Marcone A, Falautano M, Comi G, Gorno-Tempini ML, Filippi M (2010) Sensorimotor network rewiring in mild cognitive impairment and Alzheimer’s disease. Hum Brain Mapp 31(4):515–525PubMedGoogle Scholar
  2. Agosta F, Pievani M, Geroldi C, Copetti M, Frisoni GB, Filippi M (2012) Resting state fMRI in Alzheimer’s disease: beyond the default mode network. Neurobiol Aging 33(8):1564–1578CrossRefPubMedGoogle Scholar
  3. Allen G, Barnard H, McColl R, Hester AL, Fields JA, Weiner MF, Ringe WK, Lipton AM, Brooker M, McDonald E, Rubin CD, Cullum CM (2007) Reduced hippocampal functional connectivity in Alzheimer disease. Arch Neurol 64(10):1482–1487CrossRefPubMedGoogle Scholar
  4. Ashburner J, Friston KJ (2000) Voxel-based morphometry—the methods. Neuroimage 11(6 Pt 1):805–821CrossRefPubMedGoogle Scholar
  5. Ashburner J, Friston KJ (2005) Unified segmentation. NeuroImage 26(3):839–851CrossRefPubMedGoogle Scholar
  6. Bai F, Shu N, Yuan Y, Shi Y, Yu H, Wu D, Wang J, Xia M, He Y, Zhang Z (2012) Topologically convergent and divergent structural connectivity patterns between patients with remitted geriatric depression and amnestic mild cognitive impairment. J Neurosci 32(12):4307–4318CrossRefPubMedGoogle Scholar
  7. Barrantes FJ, Borroni V, Valles S (2010) Neuronal nicotinic acetylcholine receptor-cholesterol crosstalk in Alzheimer’s disease. FEBS Lett 584(9):1856–1863CrossRefPubMedGoogle Scholar
  8. Becker JT, Mintun MA, Aleva K, Wiseman MB, Nichols T, DeKosky ST (1996) Compensatory reallocation of brain resources supporting verbal episodic memory in Alzheimer’s disease. Neurology 46(3):692–700CrossRefPubMedGoogle Scholar
  9. Binkofski F, Buccino G, Stephan KM, Rizzolatti G, Seitz RJ, Freund HJ (1999) A parieto-premotor network for object manipulation: evidence from neuroimaging. Exp Brain Res Experimentelle Hirnforschung 128(1–2):210–213CrossRefGoogle Scholar
  10. Biswal B, Yetkin FZ, Haughton VM, Hyde JS (1995) Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med 34(4):537–541CrossRefPubMedGoogle Scholar
  11. Braak H, Braak E (1991) Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 82(4):239–259CrossRefPubMedGoogle Scholar
  12. Brier MR, Thomas JB, Snyder AZ, Benzinger TL, Zhang D, Raichle ME, Holtzman DM, Morris JC, Ances BM (2012) Loss of intranetwork and internetwork resting state functional connections with Alzheimer’s disease progression. J Neurosci 32(26):8890–8899CrossRefPubMedCentralPubMedGoogle Scholar
  13. Buckner RL, Andrews-Hanna JR, Schacter DL (2008) The brain’s default network: anatomy, function, and relevance to disease. Ann N Y Acad Sci 1124:1–38CrossRefPubMedGoogle Scholar
  14. Buckner RL, Sepulcre J, Talukdar T, Krienen FM, Liu H, Hedden T, Andrews-Hanna JR, Sperling RA, Johnson KA (2009) Cortical hubs revealed by intrinsic functional connectivity: mapping, assessment of stability, and relation to Alzheimer’s disease. J Neurosci 29(6):1860–1873CrossRefPubMedCentralPubMedGoogle Scholar
  15. Busatto GF, Garrido GE, Almeida OP, Castro CC, Camargo CH, Cid CG, Buchpiguel CA, Furuie S, Bottino CM (2003) A voxel-based morphometry study of temporal lobe gray matter reductions in Alzheimer’s disease. Neurobiol Aging 24(2):221–231CrossRefPubMedGoogle Scholar
  16. Caspers S, Geyer S, Schleicher A, Mohlberg H, Amunts K, Zilles K (2006) The human inferior parietal cortex: cytoarchitectonic parcellation and interindividual variability. NeuroImage 33(2):430–448CrossRefPubMedGoogle Scholar
  17. Caspers S, Eickhoff SB, Geyer S, Scheperjans F, Mohlberg H, Zilles K, Amunts K (2008) The human inferior parietal lobule in stereotaxic space. Brain Struct Funct 212(6):481–495CrossRefPubMedGoogle Scholar
  18. Caspers S, Eickhoff SB, Rick T, von Kapri A, Kuhlen T, Huang R, Shah NJ, Zilles K (2011) Probabilistic fibre tract analysis of cytoarchitectonically defined human inferior parietal lobule areas reveals similarities to macaques. NeuroImage 58(2):362–380CrossRefPubMedGoogle Scholar
  19. Caspers S, Schleicher A, Bacha-Trams M, Palomero-Gallagher N, Amunts K, Zilles K (2013) Organization of the human inferior parietal lobule based on receptor architectonics. Cereb Cortex 23(3):615–628CrossRefPubMedCentralPubMedGoogle Scholar
  20. Cavada C, Goldman-Rakic PS (1989a) Posterior parietal cortex in rhesus monkey: I. Parcellation of areas based on distinctive limbic and sensory corticocortical connections. J Comp Neurol 287(4):393–421CrossRefPubMedGoogle Scholar
  21. Cavada C, Goldman-Rakic PS (1989b) Posterior parietal cortex in rhesus monkey: II. Evidence for segregated corticocortical networks linking sensory and limbic areas with the frontal lobe. J Comp Neurol 287(4):422–445CrossRefPubMedGoogle Scholar
  22. Chai XJ, Castanon AN, Ongur D, Whitfield-Gabrieli S (2012) Anticorrelations in resting state networks without global signal regression. Neuroimage 59(2):1420–1428CrossRefPubMedCentralPubMedGoogle Scholar
  23. Crone EA, Wendelken C, Donohue SE, Bunge SA (2006) Neural evidence for dissociable components of task-switching. Cereb Cortex 16(4):475–486CrossRefPubMedGoogle Scholar
  24. Dai W, Lopez OL, Carmichael OT, Becker JT, Kuller LH, Gach HM (2009) Mild cognitive impairment and alzheimer disease: patterns of altered cerebral blood flow at MR imaging. Radiology 250(3):856–866CrossRefPubMedCentralPubMedGoogle Scholar
  25. Dai Z, Yan C, Wang Z, Wang J, Xia M, Li K, He Y (2012) Discriminative analysis of early Alzheimer’s disease using multi-modal imaging and multi-level characterization with multi-classifier (M3). NeuroImage 59(3):2187–2195CrossRefPubMedGoogle Scholar
  26. Desikan RS, Cabral HJ, Fischl B, Guttmann CR, Blacker D, Hyman BT, Albert MS, Killiany RJ (2009) Temporoparietal MR imaging measures of atrophy in subjects with mild cognitive impairment that predict subsequent diagnosis of Alzheimer disease. Ajnr 30(3):532–538CrossRefPubMedCentralPubMedGoogle Scholar
  27. Dickerson BC, Sperling RA (2009) Large-scale functional brain network abnormalities in Alzheimer’s disease: insights from functional neuroimaging. Behav Neurol 21(1):63–75CrossRefPubMedCentralPubMedGoogle Scholar
  28. Dosenbach NU, Fair DA, Miezin FM, Cohen AL, Wenger KK, Dosenbach RA, Fox MD, Snyder AZ, Vincent JL, Raichle ME, Schlaggar BL, Petersen SE (2007) Distinct brain networks for adaptive and stable task control in humans. Proc Natl Acad Sci USA 104(26):11073–11078CrossRefPubMedCentralPubMedGoogle Scholar
  29. Downar J, Crawley AP, Mikulis DJ, Davis KD (2002) A cortical network sensitive to stimulus salience in a neutral behavioral context across multiple sensory modalities. J Neurophysiol 87(1):615–620PubMedGoogle Scholar
  30. Dubois B, Feldman HH, Jacova C, Dekosky ST, Barberger-Gateau P, Cummings J, Delacourte A, Galasko D, Gauthier S, Jicha G, Meguro K, O’Brien J, Pasquier F, Robert P, Rossor M, Salloway S, Stern Y, Visser PJ, Scheltens P (2007) Research criteria for the diagnosis of Alzheimer’s disease: revising the NINCDS-ADRDA criteria. Lancet Neurol 6(8):734–746CrossRefPubMedGoogle Scholar
  31. Dubois B, Feldman HH, Jacova C, Cummings JL, Dekosky ST, Barberger-Gateau P, Delacourte A, Frisoni G, Fox NC, Galasko D, Gauthier S, Hampel H, Jicha GA, Meguro K, O’Brien J, Pasquier F, Robert P, Rossor M, Salloway S, Sarazin M, de Souza LC, Stern Y, Visser PJ, Scheltens P (2010) Revising the definition of Alzheimer’s disease: a new lexicon. Lancet Neurol 9(11):1118–1127CrossRefPubMedGoogle Scholar
  32. Eickhoff SB, Stephan KE, Mohlberg H, Grefkes C, Fink GR, Amunts K, Zilles K (2005) A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. NeuroImage 25(4):1325–1335CrossRefPubMedGoogle Scholar
  33. Fox MD, Zhang D, Snyder AZ, Raichle ME (2009) The global signal and observed anticorrelated resting state brain networks. J Neurophysiol 101(6):3270–3283CrossRefPubMedCentralPubMedGoogle Scholar
  34. Frisoni GB, Testa C, Zorzan A, Sabattoli F, Beltramello A, Soininen H, Laakso MP (2002) Detection of grey matter loss in mild Alzheimer’s disease with voxel based morphometry. J Neurol Neurosurg Psychiatry 73(6):657–664CrossRefPubMedCentralPubMedGoogle Scholar
  35. Grady CL, McIntosh AR, Beig S, Keightley ML, Burian H, Black SE (2003) Evidence from functional neuroimaging of a compensatory prefrontal network in Alzheimer’s disease. J Neurosci 23(3):986–993PubMedGoogle Scholar
  36. Greene SJ, Killiany RJ (2010) Subregions of the inferior parietal lobule are affected in the progression to Alzheimer’s disease. Neurobiol Aging 31(8):1304–1311CrossRefPubMedCentralPubMedGoogle Scholar
  37. Gregoriou GG, Borra E, Matelli M, Luppino G (2006) Architectonic organization of the inferior parietal convexity of the macaque monkey. J Comp Neurol 496(3):422–451CrossRefPubMedGoogle Scholar
  38. Greicius MD, Srivastava G, Reiss AL, Menon V (2004) Default-mode network activity distinguishes Alzheimer’s disease from healthy aging: evidence from functional MRI. Proc Natl Acad Sci USA 101(13):4637–4642CrossRefPubMedCentralPubMedGoogle Scholar
  39. Guo X, Wang Z, Li K, Li Z, Qi Z, Jin Z, Yao L, Chen K (2010) Voxel-based assessment of gray and white matter volumes in Alzheimer’s disease. Neurosci Lett 468(2):146–150CrossRefPubMedCentralPubMedGoogle Scholar
  40. Hampson M, Driesen N, Roth JK, Gore JC, Constable RT (2010) Functional connectivity between task-positive and task-negative brain areas and its relation to working memory performance. Magn Reson Imaging 28(8):1051–1057CrossRefPubMedCentralPubMedGoogle Scholar
  41. Hanakawa T, Dimyan MA, Hallett M (2008) Motor planning, imagery, and execution in the distributed motor network: a time-course study with functional MRI. Cereb Cortex 18(12):2775–2788CrossRefPubMedCentralPubMedGoogle Scholar
  42. Hanyu H, Kume K, Sato T, Hirao K, Kanetaka H, Sakurai H, Iwamoto T (2012) Regional differences in cortical benzodiazepine receptors of Alzheimer, vascular, and mixed dementia patients. J Neurol Sci 323(1–2):71–76CrossRefPubMedGoogle Scholar
  43. Hao J, Li K, Li K, Zhang D, Wang W, Yang Y, Yan B, Shan B, Zhou X (2005) Visual attention deficits in Alzheimer’s disease: an fMRI study. Neurosci Lett 385(1):18–23CrossRefPubMedGoogle Scholar
  44. He Y, Wang L, Zang Y, Tian L, Zhang X, Li K, Jiang T (2007) Regional coherence changes in the early stages of Alzheimer’s disease: a combined structural and resting-state functional MRI study. NeuroImage 35(2):488–500CrossRefPubMedGoogle Scholar
  45. Iacoboni M (2005) Neural mechanisms of imitation. Curr Opin Neurobiol 15(6):632–637CrossRefPubMedGoogle Scholar
  46. Jacobs HI, Van Boxtel MP, Uylings HB, Gronenschild EH, Verhey FR, Jolles J (2011) Atrophy of the parietal lobe in preclinical dementia. Brain Cogn 75(2):154–163CrossRefPubMedGoogle Scholar
  47. Jacobs HI, Van Boxtel MP, Heinecke A, Gronenschild EH, Backes WH, Ramakers IH, Jolles J, Verhey FR (2012) Functional integration of parietal lobe activity in early Alzheimer disease. Neurology 78(5):352–360CrossRefPubMedGoogle Scholar
  48. Jenkinson M, Bannister P, Brady M, Smith S (2002) Improved optimization for the robust and accurate linear registration and motion correction of brain images. NeuroImage 17(2):825–841CrossRefPubMedGoogle Scholar
  49. Johannsen P, Jakobsen J, Bruhn P, Gjedde A (1999) Cortical responses to sustained and divided attention in Alzheimer’s disease. NeuroImage 10(3 Pt 1):269–281CrossRefPubMedGoogle Scholar
  50. Kemppainen N, Ruottinen H, Nagren K, Rinne JO (2000) PET shows that striatal dopamine D1 and D2 receptors are differentially affected in AD. Neurology 55(2):205–209CrossRefPubMedGoogle Scholar
  51. Keysers C, Gazzola V (2009) Expanding the mirror: vicarious activity for actions, emotions, and sensations. Curr Opin Neurobiol 19(6):666–671CrossRefPubMedGoogle Scholar
  52. Lai MK, Tsang SW, Alder JT, Keene J, Hope T, Esiri MM, Francis PT, Chen CP (2005) Loss of serotonin 5-HT2A receptors in the postmortem temporal cortex correlates with rate of cognitive decline in Alzheimer’s disease. Psychopharmacology 179(3):673–677CrossRefPubMedGoogle Scholar
  53. Laureys G, Clinckers R, Gerlo S, Spooren A, Wilczak N, Kooijman R, Smolders I, Michotte Y, De Keyser J (2010) Astrocytic beta(2)-adrenergic receptors: from physiology to pathology. Prog Neurobiol 91(3):189–199CrossRefPubMedGoogle Scholar
  54. Ledberg A, Akerman S, Roland PE (1998) Estimation of the probabilities of 3D clusters in functional brain images. NeuroImage 8(2):113–128CrossRefPubMedGoogle Scholar
  55. Liang P, Wang Z, Yang Y, Jia X, Li K (2011) Functional disconnection and compensation in mild cognitive impairment: evidence from DLPFC connectivity using resting-state fMRI. PLoS One 6(7):e22153CrossRefPubMedCentralPubMedGoogle Scholar
  56. Limon A, Reyes-Ruiz JM, Miledi R (2012) Loss of functional GABA(A) receptors in the Alzheimer diseased brain. Proc Natl Acad Sci USA 109(25):10071–10076CrossRefPubMedCentralPubMedGoogle Scholar
  57. Makris N, Kennedy DN, McInerney S, Sorensen AG, Wang R, Caviness VS Jr, Pandya DN (2005) Segmentation of subcomponents within the superior longitudinal fascicle in humans: a quantitative, in vivo. DT-MRI study. Cereb Cortex 15(6):854–869CrossRefPubMedGoogle Scholar
  58. Mars RB, Jbabdi S, Sallet J, O’Reilly JX, Croxson PL, Olivier E, Noonan MP, Bergmann C, Mitchell AS, Baxter MG, Behrens TE, Johansen-Berg H, Tomassini V, Miller KL, Rushworth MF (2011) Diffusion-weighted imaging tractography-based parcellation of the human parietal cortex and comparison with human and macaque resting-state functional connectivity. J Neurosci 31(11):4087–4100CrossRefPubMedCentralPubMedGoogle Scholar
  59. Medeiros R, Kitazawa M, Caccamo A, Baglietto-Vargas D, Estrada-Hernandez T, Cribbs DH, Fisher A, LaFerla FM (2011) Loss of muscarinic M1 receptor exacerbates Alzheimer’s disease-like pathology and cognitive decline. Am J Pathol 179(2):980–991CrossRefPubMedCentralPubMedGoogle Scholar
  60. Mishizen-Eberz AJ, Rissman RA, Carter TL, Ikonomovic MD, Wolfe BB, Armstrong DM (2004) Biochemical and molecular studies of NMDA receptor subunits NR1/2A/2B in hippocampal subregions throughout progression of Alzheimer’s disease pathology. Neurobiol Dis 15(1):80–92CrossRefPubMedGoogle Scholar
  61. Morris JC (1993) The clinical dementia rating (CDR): current version and scoring rules. Neurology 43(11):2412–2414CrossRefPubMedGoogle Scholar
  62. Murphy K, Birn RM, Handwerker DA, Jones TB, Bandettini PA (2009) The impact of global signal regression on resting state correlations: are anti-correlated networks introduced? NeuroImage 44(3):893–905CrossRefPubMedCentralPubMedGoogle Scholar
  63. Nelson PT, Abner EL, Scheff SW, Schmitt FA, Kryscio RJ, Jicha GA, Smith CD, Patel E, Markesbery WR (2009) Alzheimer’s-type neuropathology in the precuneus is not increased relative to other areas of neocortex across a range of cognitive impairment. Neurosci Lett 450(3):336–339CrossRefPubMedCentralPubMedGoogle Scholar
  64. Pariente J, Cole S, Henson R, Clare L, Kennedy A, Rossor M, Cipoloti L, Puel M, Demonet JF, Chollet F, Frackowiak RS (2005) Alzheimer’s patients engage an alternative network during a memory task. Ann Neurol 58(6):870–879CrossRefPubMedGoogle Scholar
  65. Peeters R, Simone L, Nelissen K, Fabbri-Destro M, Vanduffel W, Rizzolatti G, Orban GA (2009) The representation of tool use in humans and monkeys: common and uniquely human features. J Neurosci 29(37):11523–11539CrossRefPubMedGoogle Scholar
  66. Pievani M, de Haan W, Wu T, Seeley WW, Frisoni GB (2011a) Functional network disruption in the degenerative dementias. Lancet Neurol 10(9):829–843CrossRefPubMedCentralPubMedGoogle Scholar
  67. Pievani M, Galluzzi S, Thompson PM, Rasser PE, Bonetti M, Frisoni GB (2011b) APOE4 is associated with greater atrophy of the hippocampal formation in Alzheimer’s disease. NeuroImage 55(3):909–919CrossRefPubMedGoogle Scholar
  68. Power JD, Barnes KA, Snyder AZ, Schlaggar BL, Petersen SE (2012) Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. NeuroImage 59(3):2142–2154CrossRefPubMedCentralPubMedGoogle Scholar
  69. Proctor DT, Coulson EJ, Dodd PR (2011) Post-synaptic scaffolding protein interactions with glutamate receptors in synaptic dysfunction and Alzheimer’s disease. Prog Neurobiol 93(4):509–521CrossRefPubMedGoogle Scholar
  70. Rushworth MF, Behrens TE, Johansen-Berg H (2006) Connection patterns distinguish 3 regions of human parietal cortex. Cereb Cortex 16(10):1418–1430CrossRefPubMedGoogle Scholar
  71. Sabbagh MN, Shah F, Reid RT, Sue L, Connor DJ, Peterson LK, Beach TG (2006) Pathologic and nicotinic receptor binding differences between mild cognitive impairment, Alzheimer disease, and normal aging. Arch Neurol 63(12):1771–1776CrossRefPubMedGoogle Scholar
  72. Satterthwaite TD, Wolf DH, Loughead J, Ruparel K, Elliott MA, Hakonarson H, Gur RC, Gur RE (2012) Impact of in-scanner head motion on multiple measures of functional connectivity: relevance for studies of neurodevelopment in youth. NeuroImage 60(1):623–632CrossRefPubMedCentralPubMedGoogle Scholar
  73. Seeley WW, Menon V, Schatzberg AF, Keller J, Glover GH, Kenna H, Reiss AL, Greicius MD (2007) Dissociable intrinsic connectivity networks for salience processing and executive control. J Neurosci 27(9):2349–2356CrossRefPubMedCentralPubMedGoogle Scholar
  74. Seeley WW, Crawford RK, Zhou J, Miller BL, Greicius MD (2009) Neurodegenerative diseases target large-scale human brain networks. Neuron 62(1):42–52CrossRefPubMedCentralPubMedGoogle Scholar
  75. Seidenberg M, Guidotti L, Nielson KA, Woodard JL, Durgerian S, Antuono P, Zhang Q, Rao SM (2009) Semantic memory activation in individuals at risk for developing Alzheimer disease. Neurology 73(8):612–620CrossRefPubMedCentralPubMedGoogle Scholar
  76. Song XW, Dong ZY, Long XY, Li SF, Zuo XN, Zhu CZ, He Y, Yan CG, Zang YF (2011) REST: a toolkit for resting-state functional magnetic resonance imaging data processing. PLoS One 6(9):e25031CrossRefPubMedCentralPubMedGoogle Scholar
  77. Truchot L, Costes N, Zimmer L, Laurent B, Le Bars D, Thomas-Anterion C, Mercier B, Hermier M, Vighetto A, Krolak-Salmon P (2008) A distinct [18F]MPPF PET profile in amnestic mild cognitive impairment compared to mild Alzheimer’s disease. NeuroImage 40(3):1251–1256CrossRefPubMedGoogle Scholar
  78. Uddin LQ, Supekar KS, Ryali S, Menon V (2011) Dynamic reconfiguration of structural and functional connectivity across core neurocognitive brain networks with development. J Neurosci 31(50):18578–18589CrossRefPubMedCentralPubMedGoogle Scholar
  79. Van Dijk KR, Sabuncu MR, Buckner RL (2012) The influence of head motion on intrinsic functional connectivity MRI. NeuroImage 59(1):431–438CrossRefPubMedCentralPubMedGoogle Scholar
  80. Vidoni ED, Thomas GP, Honea RA, Loskutova N, Burns JM (2012) Evidence of altered corticomotor system connectivity in early-stage Alzheimer’s disease. J Neurol Phys Ther: JNPT 36(1):8–16CrossRefPubMedCentralPubMedGoogle Scholar
  81. Vincent JL, Kahn I, Snyder AZ, Raichle ME, Buckner RL (2008) Evidence for a frontoparietal control system revealed by intrinsic functional connectivity. J Neurophysiol 100(6):3328–3342CrossRefPubMedCentralPubMedGoogle Scholar
  82. Walhovd KB, Fjell AM, Brewer J, McEvoy LK, Fennema-Notestine C, Hagler DJ Jr, Jennings RG, Karow D, Dale AM (2010) Combining MR imaging, positron-emission tomography, and CSF biomarkers in the diagnosis and prognosis of Alzheimer disease. Ajnr 31(2):347–354CrossRefPubMedCentralPubMedGoogle Scholar
  83. Wang L, Zang Y, He Y, Liang M, Zhang X, Tian L, Wu T, Jiang T, Li K (2006) Changes in hippocampal connectivity in the early stages of Alzheimer’s disease: evidence from resting state fMRI. NeuroImage 31(2):496–504CrossRefPubMedGoogle Scholar
  84. Wang K, Liang M, Wang L, Tian L, Zhang X, Li K, Jiang T (2007) Altered functional connectivity in early Alzheimer’s disease: a resting-state fMRI study. Hum Brain Mapp 28(10):967–978CrossRefPubMedGoogle Scholar
  85. Wang Z, Yan C, Zhao C, Qi Z, Zhou W, Lu J, He Y, Li K (2011) Spatial patterns of intrinsic brain activity in mild cognitive impairment and Alzheimer’s disease: a resting-state functional MRI study. Hum Brain Mapp 32:1720–1740CrossRefPubMedGoogle Scholar
  86. Wang J, Fan L, Zhang Y, Liu Y, Jiang D, Zhang Y, Yu C, Jiang T (2012a) Tractography-based parcellation of the human left inferior parietal lobule. NeuroImage 63(2):641–652CrossRefPubMedGoogle Scholar
  87. Wang Z, Jia X, Liang P, Qi Z, Yang Y, Zhou W, Li K (2012b) Changes in thalamus connectivity in mild cognitive impairment: evidence from resting state fMRI. Eur J Radiol 81:277–285CrossRefPubMedGoogle Scholar
  88. Wang J, Zuo X, Dai Z, Xia M, Zhao Z, Zhao X, Jia J, Han Y, He Y (2013) Disrupted functional brain connectome in individuals at risk for Alzheimer’s disease. Biol Psychiatry 73(5):472–481CrossRefPubMedGoogle Scholar
  89. Weissenbacher A, Kasess C, Gerstl F, Lanzenberger R, Moser E, Windischberger C (2009) Correlations and anticorrelations in resting-state functional connectivity MRI: a quantitative comparison of preprocessing strategies. NeuroImage 47(4):1408–1416CrossRefPubMedGoogle Scholar
  90. Xia M, Wang J, He Y (2013) BrainNet Viewer: a network visualization tool for human brain connectomics. PLoS One 8(7):e68910. doi: 10.1371/journal.pone.0068910 CrossRefPubMedCentralPubMedGoogle Scholar
  91. Xiong H, McCabe L, Costello J, Anderson E, Weber G, Ikezu T (2004) Activation of NR1a/NR2B receptors by soluble factors from APP-stimulated monocyte-derived macrophages: implications for the pathogenesis of Alzheimer’s disease. Neurobiol Aging 25(7):905–911CrossRefPubMedGoogle Scholar
  92. Xu Y, Yan J, Zhou P, Li J, Gao H, Xia Y, Wang Q (2012) Neurotransmitter receptors and cognitive dysfunction in Alzheimer’s disease and Parkinson’s disease. Prog Neurobiol 97(1):1–13CrossRefPubMedCentralPubMedGoogle Scholar
  93. Yan C, Zang Y (2010) DPARSF: a MATLAB toolbox for “Pipeline” data analysis of resting-state fMRI. Front Syst Neurosci 4:13Google Scholar
  94. Zhang D, Raichle ME (2010) Disease and the brain’s dark energy. Nat Rev Neurol 6(1):15–28CrossRefPubMedGoogle Scholar
  95. Zhang HY, Wang SJ, Liu B, Ma ZL, Yang M, Zhang ZJ, Teng GJ (2010) Resting brain connectivity: changes during the progress of Alzheimer disease. Radiology 256(2):598–606CrossRefPubMedGoogle Scholar
  96. Zilles K, Amunts K (2010) Centenary of Brodmann’s map—conception and fate. Nat Rev Neurosci 11(2):139–145CrossRefPubMedGoogle Scholar
  97. Zuo XN, Kelly C, Di Martino A, Mennes M, Margulies DS, Bangaru S, Grzadzinski R, Evans AC, Zang YF, Castellanos FX, Milham MP (2010) Growing together and growing apart: regional and sex differences in the lifespan developmental trajectories of functional homotopy. J Neurosci 30(45):15034–15043CrossRefPubMedCentralPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Department of RadiologyXuanwu Hospital of Capital Medical UniversityBeijingChina
  2. 2.State Key Laboratory of Cognitive Neuroscience and Learning and IDG/McGovern Institute for Brain ResearchBeijing Normal UniversityBeijingChina
  3. 3.Center for Collaboration and Innovation in Brain and Learning SciencesBeijing Normal UniversityBeijingChina
  4. 4.Department of NeurologyXuanwu Hospital of Capital Medical UniversityBeijingChina
  5. 5.Key Laboratory for Neurodegenerative DiseasesCapital Medical University, Ministry of EducationBeijingChina
  6. 6.Beijing Key Laboratory of Magnetic Resonance Imaging and Brain InformaticsBeijingChina

Personalised recommendations