Skip to main content

Advertisement

SpringerLink
Log in

Altered functional connectivity within and between the default model network and the visual network in primary open-angle glaucoma: a resting-state fMRI study

  • Original Research
  • Published:
Brain Imaging and Behavior Aims and scope Submit manuscript

Abstract

To explore the alterations of functional connectivity (FC) and connections within and between the subnetworks of the visual network and the default mode network in glaucoma. We applied the independent component analysis to obtain two resting-state networks (RSNs), which were the visual network and the default mode network (DMN), from the resting-state fMRI data of 25 primary open-angle glaucoma (POAG) patients and 25 well-matched normal controls. Then FC analysis was performed to obtain the altered FC within the RSNs, whereas the functional network connectivity (FNC) analysis was performed within and between these two RSNs. The abnormalities were correlated with clinical measures in glaucoma to investigate the abnormality-clinical relationship. FC analysis showed that the FC in the occipital pole of the visual network was decreased in POAG patients while no alterations were found in the FC of the DMN in patients. FNC analysis of connections within the RSNs found that two of the three connections within the visual network were decreased while no connection alterations were found within the DMN. FNC analysis of connections between these two RSNs found two increased connections and one decreased connection. The decreased connection between these two RSNs was positively correlated with the visual field mean deviation. These findings shed light on the importance of the reorganization of resting state networks in glaucoma mechanism, which may facilitate the understanding of glaucoma.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Notes

  1. Practically, more emphasis should be put on visual field MD and CDR than RNFL.

References

  • Alba, C., Vidal, L., Diaz, F., Villena, A., & de Vargas, I. P. (2004). Ultrastructural and quantitative age-related changes in capillaries of the dorsal lateral geniculate nucleus. Brain Research Bulletin, 64(2), 145–153. doi:10.1016/j.brainresbull.2004.06.006.

    Article  CAS  PubMed  Google Scholar 

  • Baird, B., Smallwood, J., Mrazek, M. D., Kam, J. W., Franklin, M. S., & Schooler, J. W. (2012). Inspired by distraction: mind wandering facilitates creative incubation. Psychological Science, 23(10), 1117–1122. doi:10.1177/0956797612446024.

    Article  PubMed  Google Scholar 

  • Bell, A. J., & Sejnowski, T. J. (1995). An information maximization approach to blind separation and blind deconvolution. Neural Computation, 7(6), 1129–1159. doi:10.1162/Neco.1995.7.6.1129.

    Article  CAS  PubMed  Google Scholar 

  • Bola, M., & Sabel, B. A. (2015). Dynamic reorganization of brain functional networks during cognition. NeuroImage, 114, 398–413. doi:10.1016/j.neuroimage.2015.03.057.

    Article  PubMed  Google Scholar 

  • Bola, M., Gall, C., Moewes, C., Fedorov, A., Hinrichs, H., & Sabel, B. A. (2014). Brain functional connectivity network breakdown and restoration in blindness. [randomized controlled trial research support, non-U.S. Gov’t]. Neurology, 83(6), 542–551. doi:10.1212/WNL.0000000000000672.

    Article  PubMed  Google Scholar 

  • Bola, M., Gall, C., & Sabel, B. A. (2015). Disturbed temporal dynamics of brain synchronization in vision loss. Cortex, 67, 134–146. doi:10.1016/j.cortex.2015.03.020.

    Article  PubMed  Google Scholar 

  • Bressler, D. W., Fortenbaugh, F. C., Robertson, L. C., & Silver, M. A. (2013). Visual spatial attention enhances the amplitude of positive and negative fMRI responses to visual stimulation in an eccentricity-dependent manner. Vision Research, 85, 104–112. doi:10.1016/j.visres.2013.03.009.

    Article  PubMed  PubMed Central  Google Scholar 

  • Calhoun, V. D., Adali, T., Pearlson, G. D., & Pekar, J. J. (2001). A method for making group inferences from functional MRI data using independent component analysis. Human Brain Mapping, 14(3), 140–151.

    Article  CAS  PubMed  Google Scholar 

  • Chen, W., Kato, T., Zhu, X. H., Strupp, J., Ogawa, S., & Ugurbil, K. (1998). Mapping of lateral geniculate nucleus activation during visual stimulation in human brain using fMRI. [Clinical Trial Research Support, U.S. Gov’t, P.H.S.]. Magn Reson Med,, 39(1), 89–96.

    Article  CAS  Google Scholar 

  • Chen, W. W., Wang, N., Cai, S., Fang, Z., Yu, M., Wu, Q., et al. (2013). Structural brain abnormalities in patients with primary open-angle glaucoma: a study with 3 T MR imaging. [comparative study research support, non-U.S. Gov’t]. Investigative Ophthalmology & Visual Science, 54(1), 545–554. doi:10.1167/iovs.12-9893.

    Article  Google Scholar 

  • Dai, H., Mu, K. T., Qi, J. P., Wang, C. Y., Zhu, W. Z., Xia, L. M., et al. (2011). Assessment of lateral geniculate nucleus atrophy with 3 T MR imaging and correlation with clinical stage of glaucoma. [controlled clinical trial]. AJNR. American Journal of Neuroradiology, 32(7), 1347–1353. doi:10.3174/ajnr.A2486.

    Article  CAS  PubMed  Google Scholar 

  • Dai, H., Morelli, J. N., Ai, F., Yin, D., Hu, C., Xu, D., et al. (2013). Resting-state functional MRI: functional connectivity analysis of the visual cortex in primary open-angle glaucoma patients. [research support, non-U.S. Gov’t]. Human Brain Mapping, 34(10), 2455–2463. doi:10.1002/hbm.22079.

    Article  PubMed  Google Scholar 

  • Damoiseaux, J. S., Rombouts, S. A., Barkhof, F., Scheltens, P., Stam, C. J., Smith, S. M., et al. (2006). Consistent resting-state networks across healthy subjects. Proceedings of the National Academy of Sciences of the United States of America, 103(37), 13848–13853. doi:10.1073/pnas.0601417103.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ding, K., Liu, Y., Yan, X., Lin, X., & Jiang, T. (2013). Altered functional connectivity of the primary visual cortex in subjects with amblyopia. Neural Plasticity, 2013, 8. doi:10.1155/2013/612086.

    Article  Google Scholar 

  • Erhardt, E. B., Rachakonda, S., Bedrick, E. J., Allen, E. A., Adali, T., & Calhoun, V. D. (2011). Comparison of multi-subject ICA methods for analysis of fMRI data. Human Brain Mapping, 32(12), 2075–2095. doi:10.1002/hbm.21170.

    Article  PubMed  Google Scholar 

  • Fornito, A., Harrison, B. J., Zalesky, A., & Simons, J. S. (2012). Competitive and cooperative dynamics of large-scale brain functional networks supporting recollection. Proceedings of the National Academy of Sciences of the United States of America, 109(31), 12788–12793. doi:10.1073/pnas.1204185109.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frezzotti, P., Giorgio, A., Motolese, I., De Leucio, A., Iester, M., Motolese, E., et al. (2014). Structural and functional brain changes beyond visual system in patients with advanced glaucoma. PloS One, 9(8), e105931. doi:10.1371/journal.pone.0105931.

    Article  PubMed  PubMed Central  Google Scholar 

  • Garaci, F. G., Bolacchi, F., Cerulli, A., Melis, M., Spano, A., Cedrone, C., et al. (2009). Optic nerve and optic radiation neurodegeneration in patients with glaucoma: in vivo analysis with 3-T diffusion-tensor MR imaging. Radiology, 252(2), 496–501. doi:10.1148/radiol.2522081240.

    Article  PubMed  Google Scholar 

  • Gentili, C., Ricciardi, E., Gobbini, M. I., Santarelli, M. F., Haxby, J. V., Pietrini, P., et al. (2009). Beyond amygdala: default mode network activity differs between patients with social phobia and healthy controls. Brain Research Bulletin, 79(6), 409–413. doi:10.1016/j.brainresbull.2009.02.002.

    Article  PubMed  Google Scholar 

  • Greicius, M. D., Krasnow, B., Reiss, A. L., & Menon, V. (2003). Functional connectivity in the resting brain: a network analysis of the default mode hypothesis. Proceedings of the National Academy of Sciences of the United States of America, 100(1), 253–258. doi:10.1073/pnas.0135058100.

    Article  CAS  PubMed  Google Scholar 

  • Gupta, N., & Yucel, Y. H. (2007). Glaucoma as a neurodegenerative disease. Current Opinion in Ophthalmology, 18(2), 110–114. doi:10.1097/Icu.0b013e3280895aea.

    Article  PubMed  Google Scholar 

  • Gupta, N., Ang, L. C., de Tilly, L. N., Bidaisee, L., & Yucel, Y. H. (2006a). Human glaucoma and neural degeneration in intracranial optic nerve, lateral geniculate nucleus, and visual cortex. British Journal of Ophthalmology, 90(6), 674–678. doi:10.1136/bjo.2005.086769.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jafri, M. J., Pearlson, G. D., Stevens, M., & Calhoun, V. D. (2008). A method for functional network connectivity among spatially independent resting-state components in schizophrenia. NeuroImage, 39(4), 1666–1681. doi:10.1016/j.neuroimage.2007.11.001.

    Article  PubMed  Google Scholar 

  • Joel, S. E., Caffo, B. S., Zijl, P. C. M., & Pekar, J. J. (2011). On the relationship between seed-based and ICA-based measures of functional connectivity. Magnetic Resonance in Medicine, 66(3), 644–657. doi:10.1002/mrm.22818.

    Article  PubMed  PubMed Central  Google Scholar 

  • Lee, L., Harrison, L. M., & Mechelli, A. (2003). A report of the functional connectivity workshop, Dusseldorf 2002. NeuroImage, 19(2 Pt 1), 457–465.

    Article  PubMed  Google Scholar 

  • Li, Y. O., Adali, T., & Calhoun, V. D. (2007). Estimating the number of independent components for functional magnetic resonance imaging data. Human Brain Mapping, 28(11), 1251–1266. doi:10.1002/hbm.20359.

    Article  PubMed  Google Scholar 

  • Li, T., Liu, Z., Li, J., Liu, Z., Tang, Z., Xie, X., et al. (2015). Altered amplitude of low-frequency fluctuation in primary open-angle glaucoma: a resting-state FMRI study. Investigative Ophthalmology & Visual Science, 56(1), 322–329. doi:10.1167/iovs.14-14974.

    Article  Google Scholar 

  • Lin, X. M., Ding, K., Liu, Y., Yan, X. H., Song, S. J., & Jiang, T. Z. (2012). Altered spontaneous activity in anisometropic amblyopia subjects: revealed by resting-state fMRI. PloS One, 7(8). doi:10.1371/journal.pone.0043373.

  • McKeown, M. J., Makeig, S., Brown, G. G., Jung, T. P., Kindermann, S. S., Bell, A. J., et al. (1998). Analysis of fMRI data by blind separation into independent spatial components. Human Brain Mapping, 6(3), 160–188.

    Article  CAS  PubMed  Google Scholar 

  • Murphy, K., Birn, R. M., Handwerker, D. A., Jones, T. B., & Bandettini, P. A. (2009). The impact of global signal regression on resting state correlations: are anti-correlated networks introduced? NeuroImage, 44(3), 893–905. doi:10.1016/j.neuroimage.2008.09.036.

    Article  PubMed  Google Scholar 

  • Ongur, D., Lundy, M., Greenhouse, I., Shinn, A. K., Menon, V., Cohen, B. M., et al. (2010). Default mode network abnormalities in bipolar disorder and schizophrenia. Psychiatry Research, 183(1), 59–68. doi:10.1016/j.pscychresns.2010.04.008.

    Article  PubMed  PubMed Central  Google Scholar 

  • Raichle, M. E., MacLeod, A. M., Snyder, A. Z., Powers, W. J., Gusnard, D. A., & Shulman, G. L. (2001). A default mode of brain function. Proceedings of the National Academy of Sciences of the United States of America, 98(2), 676–682. doi:10.1073/pnas.98.2.676.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schwartz, S., Vuilleumier, P., Hutton, C., Maravita, A., Dolan, R. J., & Driver, J. (2005). Attentional load and sensory competition in human vision: modulation of fMRI responses by load at fixation during task-irrelevant stimulation in the peripheral visual field. Cerebral Cortex, 15(6), 770–786. doi:10.1093/cercor/bhh178.

    Article  PubMed  Google Scholar 

  • Shirer, W. R., Ryali, S., Rykhlevskaia, E., Menon, V., & Greicius, M. D. (2012). Decoding subject-driven cognitive states with whole-brain connectivity patterns. Cerebral Cortex, 22(1), 158–165. doi:10.1093/Cercor/Bhr099.

    Article  CAS  PubMed  Google Scholar 

  • Song, Y., Mu, K., Wang, J., Lin, F., Chen, Z., Yan, X., et al. (2014). Altered spontaneous brain activity in primary open angle glaucoma: a resting-state functional magnetic resonance imaging study. [Comparative Study Research Support, Non-U.S. Gov’t]. PLoS One, 9(2), e89493, doi:10.1371/journal.pone.0089493.

  • Tian, L., Ren, J., & Zang, Y. (2012). Regional homogeneity of resting state fMRI signals predicts stop signal task performance. NeuroImage, 60(1), 539–544. doi:10.1016/j.neuroimage.2011.11.098.

    Article  PubMed  Google Scholar 

  • van de Ven, V. G., Formisano, E., Prvulovic, D., Roeder, C. H., & Linden, D. E. J. (2004). Functional connectivity as revealed by spatial independent component analysis of fMRI measurements during rest. Human Brain Mapping, 22(3), 165–178. doi:10.1002/hbm.20022.

    Article  PubMed  Google Scholar 

  • van den Heuvel, M. P., & Hulshoff Pol, H. E. (2010). Exploring the brain network: a review on resting-state fMRI functional connectivity. [review]. European Neuropsychopharmacology, 20(8), 519–534. doi:10.1016/j.euroneuro.2010.03.008.

    Article  PubMed  Google Scholar 

  • Vidal, L., Ruiz, C., Villena, A., Diaz, F., & Perez de Vargas, I. (2004). Quantitative age-related changes in dorsal lateral geniculate nucleus relay neurons of the rat. Neuroscience Research, 48(4), 387–396. doi:10.1016/j.neures.2003.12.004.

    Article  PubMed  Google Scholar 

  • von dem Hagen, E. A. H., Stoyanova, R. S., Baron-Cohen, S., & Calder, A. J. (2012). Reduced functional connectivity within and between ‘social’resting state networks in autism spectrum conditions. Social Cognitive and Affective Neuroscience, 8(6), 694–701. doi:10.1093/scan/nss053.

    Article  Google Scholar 

  • Wang, T. Y., Li, Q., Guo, M. X., Peng, Y. M., Li, Q. J., Qin, W., et al. (2014). Abnormal functional connectivity density in children with anisometropic amblyopia at resting-state. Brain Research, 1563, 41–51. doi:10.1016/J.Brainres.2014.03.015.

    Article  CAS  PubMed  Google Scholar 

  • Wang, J. Q., Li, T., Sabel, B. A., Chen, Z. Q., Wen, H. W., Li, J. H., et al. (2016a). Structural brain alterations in primary open angle glaucoma: a 3 T MRI study. Scientific Reports, 6. doi:10.1038/Srep18969.

  • Wang, J., Li, T., Wang, N., Xian, J., & He, H. (2016b). Graph theoretical analysis reveals the reorganization of the brain network pattern in primary open angle glaucoma patients. European Radiology. doi:10.1007/s00330-016-4221-x.

    Google Scholar 

  • Williams, A. L., Lackey, J., Wizov, S. S., Chia, T. M., Gatla, S., Moster, M. L., et al. (2013). Evidence for widespread structural brain changes in glaucoma: a preliminary voxel-based MRI study. [research support, non-U.S. Gov’t]. Investigative Ophthalmology & Visual Science, 54(8), 5880–5887. doi:10.1167/iovs.13-11776.

    Article  Google Scholar 

  • Yan, C. G., & Zang, Y. F. (2010). DPARSF: a MATLAB toolbox for "pipeline" data analysis of resting-state fMRI. Frontiers in Systems Neuroscience, 4. doi:10.3389/fnsys.2010.00013.

  • Yu, L., Xie, B., Yin, X., Liang, M., Evans, A. C., Wang, J., et al. (2013). Reduced cortical thickness in primary open-angle glaucoma and its relationship to the retinal nerve fiber layer thickness. [Research Support, Non-U.S. Gov’t]. PLoS One, 8(9), e73208, doi:10.1371/journal.pone.0073208.

  • Zeki, S., & Shipp, S. (1988). The functional logic of cortical connections. Nature, 335(6188), 311–317. doi:10.1038/335311a0.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by National Natural Science Foundation of China (61271151, 91520202, and 81571649) and Youth Innovation Promotion Association CAS.

Author information

Authors and Affiliations

  1. State Key Laboratory of Management and Control for Complex Systems, Institute of Automation, Chinese Academy of Sciences, Beijing, China

    Jieqiong Wang, Peng Zhou & Huiguang He

  2. University of Chinese Academy of Sciences, Beijing, China

    Jieqiong Wang, Peng Zhou & Huiguang He

  3. Department of Radiology, Beijing Tongren Hospital, Capital Medical University, Beijing, China

    Ting Li & Junfang Xian

  4. Department of Ophthalmology, Beijing Tongren Hospital, Capital Medical University, Beijing, China

    Ningli Wang

  5. Center for Excellence in Brain Science and Intelligence Technology, Chinese Academy of Sciences, Beijing, China

    Huiguang He

Authors
  1. Jieqiong Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ting Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Peng Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ningli Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Junfang Xian
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Huiguang He
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Junfang Xian or Huiguang He.

Ethics declarations

Disclosures

Author Jieqiong Wang, Author Ting Li, Author Peng Zhou, Author Ningli Wang, Author Junfang Xian, Author Huiguang He declare that they have no conflict of interest.

All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation (institutional and national) and with the Helsinki Declaration of 1975, and the applicable revisions at the time of the investigation. Informed consent was obtained from all patients for being included in the study.

Electronic supplementary material

ESM 1 Table S1

(DOCX 18 kb)

ESM 2 Table S2

(DOCX 14 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, J., Li, T., Zhou, P. et al. Altered functional connectivity within and between the default model network and the visual network in primary open-angle glaucoma: a resting-state fMRI study. Brain Imaging and Behavior 11, 1154–1163 (2017). https://doi.org/10.1007/s11682-016-9597-3

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11682-016-9597-3

Keywords

Search

Navigation