Establishing group-level brain structural connectivity incorporating anatomical knowledge under latent space modeling.

Selena Wang, Yiting Wang, Frederick H Xu, Li Shen, Yize Zhao, Alzheimer���s Disease Neuroimaging Initiative
Author Information
  1. Selena Wang: Department of Biostatistics and Health Data Science, Indiana University School of Medicine, United States of America. Electronic address: selewang@iu.edu.
  2. Yiting Wang: Department of Statistics, Virginia University, United States of America.
  3. Frederick H Xu: Department of Bioengineering, University of Pennsylvania, United States of America.
  4. Li Shen: Department of Biostatistics, Epidemiology and Informatics, University of Pennsylvania, United States of America.
  5. Yize Zhao: Department of Biostatistics, Yale Univeristy, United States of America.

Abstract

Brain structural connectivity, capturing the white matter fiber tracts among brain regions inferred by diffusion MRI (dMRI), provides a unique characterization of brain anatomical organization. One fundamental question to address with structural connectivity is how to properly summarize and perform statistical inference for a group-level connectivity architecture, for instance, under different sex groups, or disease cohorts. Existing analyses commonly summarize group-level brain connectivity by a simple entry-wise sample mean or median across individual brain connectivity matrices. However, such a heuristic approach fully ignores the associations among structural connections and the topological properties of brain networks. In this project, we propose a latent space-based generative network model to estimate group-level brain connectivity. Within our modeling framework, we incorporate the anatomical information of brain regions as the attributes of nodes to enhance the plausibility of our estimation and improve biological interpretation. We name our method the attributes-informed brain connectivity (ABC) model, which compared with existing group-level connectivity estimations, (1) offers an interpretable latent space representation of the group-level connectivity, (2) incorporates the anatomical knowledge of nodes and tests its co-varying relationship with connectivity and (3) quantifies the uncertainty and evaluates the likelihood of the estimated group-level effects against chance. We devise a novel Bayesian MCMC algorithm to estimate the model. We evaluate the performance of our model through extensive simulations. By applying the ABC model to study brain structural connectivity stratified by sex among Alzheimer's Disease (AD) subjects and healthy controls incorporating the anatomical attributes (volume, thickness and area) on nodes, our method shows superior predictive power on out-of-sample structural connectivity and identifies meaningful sex-specific network neuromarkers for AD.

Keywords

References

  1. Neuroimage. 2018 Oct 1;179:357-372 [PMID: 29782994]
  2. J Neurol. 2007 Oct;254(10):1395-400 [PMID: 17934882]
  3. Psychometrika. 2023 Dec;88(4):1197-1227 [PMID: 37615903]
  4. Nat Commun. 2020 Jun 16;11(1):3038 [PMID: 32546755]
  5. PLoS One. 2013 Sep 03;8(9):e73021 [PMID: 24019889]
  6. Brain. 1980 Sep;103(3):525-54 [PMID: 6774795]
  7. Perception. 2008;37(12):1805-21 [PMID: 19227374]
  8. Proc Natl Acad Sci U S A. 2000 Sep 26;97(20):11050-5 [PMID: 10984517]
  9. Int J Comput Biol Drug Des. 2020;13(1):58-70 [PMID: 32095160]
  10. Arch Clin Neuropsychol. 2009 Dec;24(8):783-9 [PMID: 19889648]
  11. J Neurosci. 2006 Jan 4;26(1):63-72 [PMID: 16399673]
  12. J Stat Softw. 2008 Feb;24: [PMID: 28804272]
  13. J Neurosurg. 2017 Sep;127(3):613-621 [PMID: 27982771]
  14. J Am Stat Assoc. 2015;110(511):1047-1056 [PMID: 26848204]
  15. Ann Appl Stat. 2017 Sep;11(3):1217-1244 [PMID: 29721127]
  16. Stat Surv. 2018;12:105-135 [PMID: 31428219]
  17. Hum Brain Mapp. 1999;8(4):272-84 [PMID: 10619420]
  18. J Neurol. 2015 Jul;262(7):1780-90 [PMID: 25761375]
  19. J Nerv Ment Dis. 1955 Jan;121(1):50-2 [PMID: 14368313]
  20. Alzheimers Dement. 2013 Sep;9(5):e111-94 [PMID: 23932184]
  21. Psychol Med. 2017 Feb;47(3):495-506 [PMID: 27776563]
  22. Proceedings (IEEE Int Conf Bioinformatics Biomed). 2022 Dec;2022:1323-1328 [PMID: 37041884]
  23. Cereb Cortex. 1999 Dec;9(8):896-901 [PMID: 10601007]
  24. Alzheimers Dement. 2010 May;6(3):202-11.e7 [PMID: 20451868]
  25. Neuroimage. 2016 Jul 15;135:79-91 [PMID: 27132542]
  26. Psychometrika. 2020 Jun;85(2):251-274 [PMID: 32221792]
  27. Nat Rev Neurosci. 2009 Mar;10(3):186-98 [PMID: 19190637]
  28. J Int Neuropsychol Soc. 2005 Jan;11(1):30-9 [PMID: 15686606]
  29. J Neurosci. 2021 Jan 20;41(3):513-523 [PMID: 33229501]
  30. Neurosci Biobehav Rev. 2016 Oct;69:113-23 [PMID: 27473935]
  31. Cereb Cortex. 2012 Aug;22(8):1862-75 [PMID: 21968567]
  32. Neurology. 2007 Sep 4;69(10):986-97 [PMID: 17785667]
  33. Neuroimage. 2012 Aug 15;62(2):782-90 [PMID: 21979382]
  34. Nat Neurosci. 2017 Feb 23;20(3):353-364 [PMID: 28230844]
  35. AJNR Am J Neuroradiol. 2020 May;41(5):798-803 [PMID: 32381542]
  36. Neuroimage. 2010 Sep;52(3):1059-69 [PMID: 19819337]
  37. Nat Commun. 2021 Feb 1;12(1):721 [PMID: 33526780]
  38. Brain Cogn. 2009 Apr;69(3):451-9 [PMID: 18980790]
  39. J Int Neuropsychol Soc. 1999 Sep;5(6):502-9 [PMID: 10561930]
  40. Stat Sci. 2019 Aug;34(3):428-453 [PMID: 33235407]
  41. J Neurosci. 2009 Jan 28;29(4):1175-90 [PMID: 19176826]
  42. Gend Med. 2012 Feb;9(1):44-55 [PMID: 22333522]
  43. Neuropsychologia. 1994 Oct;32(10):1287-96 [PMID: 7845568]
  44. Front Aging Neurosci. 2021 Oct 05;13:705030 [PMID: 34675796]
  45. ScientificWorldJournal. 2015;2015:430735 [PMID: 25685840]
  46. World J Psychiatry. 2016 Mar 22;6(1):54-65 [PMID: 27014598]
  47. Front Psychol. 2021 Dec 09;12:773289 [PMID: 34955989]
  48. J Neurosci Methods. 2012 Jan 30;203(2):386-97 [PMID: 22001222]
  49. Proc SPIE Int Soc Opt Eng. 2021;11596: [PMID: 34354323]
  50. Front Neuroinform. 2009 Oct 30;3:37 [PMID: 19949480]
  51. Alzheimer Dis Assoc Disord. 2007 Apr-Jun;21(2):122-9 [PMID: 17545737]
  52. PLoS One. 2010 Aug 16;5(8):e12200 [PMID: 20808943]
  53. Neuroimage. 2016 Jan 1;124(Pt A):1054-1064 [PMID: 26427642]
  54. Optom Vis Sci. 1995 Mar;72(3):155-67 [PMID: 7609938]
  55. J Neurol Neurosurg Psychiatry. 1977 May;40(5):455-63 [PMID: 197211]
  56. Prog Neurobiol. 2018 Dec;171:90-113 [PMID: 30219248]
  57. Int J Geriatr Psychiatry. 2018 Jan;33(1):193-199 [PMID: 28295599]
  58. Neuroimage. 2021 Jan 15;225:117480 [PMID: 33099009]
  59. Neuropsychology. 1998 Jan;12(1):29-33 [PMID: 9460732]
  60. Brain Struct Funct. 2019 Jan;224(1):501-513 [PMID: 30390153]

Grants

  1. P30 AG021342/NIA NIH HHS
  2. R01 EB034720/NIBIB NIH HHS
  3. RF1 AG068191/NIA NIH HHS
  4. RF1 AG081413/NIA NIH HHS

MeSH Term

Humans
Brain
Female
Male
Alzheimer Disease
Algorithms
White Matter
Connectome
Diffusion Magnetic Resonance Imaging

Word Cloud

Created with Highcharts 10.0.0connectivitybraingroup-levelstructuralanatomicalmodelamonglatentnetworkmodelingnodesspaceBrainregionssummarizesexestimateattributesmethodABCknowledgeADincorporatingcapturingwhitematterfibertractsinferreddiffusionMRIdMRIprovidesuniquecharacterizationorganizationOnefundamentalquestionaddressproperlyperformstatisticalinferencearchitectureinstancedifferentgroupsdiseasecohortsExistinganalysescommonlysimpleentry-wisesamplemeanmedianacrossindividualmatricesHoweverheuristicapproachfullyignoresassociationsconnectionstopologicalpropertiesnetworksprojectproposespace-basedgenerativeWithinframeworkincorporateinformationenhanceplausibilityestimationimprovebiologicalinterpretationnameattributes-informedcomparedexistingestimations1offersinterpretablerepresentation2incorporatestestsco-varyingrelationship3quantifiesuncertaintyevaluateslikelihoodestimatedeffectschancedevisenovelBayesianMCMCalgorithmevaluateperformanceextensivesimulationsapplyingstudystratifiedAlzheimer'sDiseasesubjectshealthycontrolsvolumethicknessareashowssuperiorpredictivepowerout-of-sampleidentifiesmeaningfulsex-specificneuromarkersEstablishingAnatomicalstructureanalysisLatent

Similar Articles

Cited By