Skip to main content

Advertisement

SpringerLink
Log in

A historical perspective on the evolution of resting-state functional connectivity with MRI

  • Review Article
  • Published:
Magnetic Resonance Materials in Physics, Biology and Medicine Aims and scope Submit manuscript

Abstract

In this review article, I discuss initial and recent studies of the assessment of functional connectivity in the human brain using low-frequency BOLD fluctuations in the resting state. By putting the studies in their historical context, the goal is to give the reader an appreciation of the evolution of the field and the pivotal events and studies that have led to the widespread acceptance of the method as a neuroscience tool for investigating functional connectivity in the human brain.

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

Similar content being viewed by others

References

  1. Jezzard P, LeBihan D, Cuenod D, Pannier L, Prinster A, Turner R (1992) An investigation of the contribution of physiological noise in human functional MRI studies at 1.5 tesla and 4 tesla. In: Proceedings of society of magnetic resonance in medicine 12th annual meeting, New York, p 1392

  2. Weisskoff RM, Baker J, Belliveau J, Davis TL, Kwong KK, Cohen MS, Rosen BR (1992) Power spectrum analysis of functionally weighted MR data: what’s in the noise? In: Proceedings of society of magnetic resonance in medicine 12th annual meeting, New York, p 7

  3. Biswal B, DeYoe AE, Hyde JS (1996) Reduction of physiological fluctuations in fMRI using digital filters. Magn Reson Med 35: 107–113

    Article  CAS  PubMed  Google Scholar 

  4. Biswal B, Yetkin FZ, Haughton VM, Hyde JS (1995) Functional connectivity in the motor cortex of resting human brain. Magn Reson Med 34: 537–541

    Article  CAS  PubMed  Google Scholar 

  5. Biswal B, Hudetz AG, Yetkin FZ, Haughton VM, Hyde JS (1997) Hypercapnia reversibly suppresses low-frequency fluctuations in the human motor cortex during rest using echo-planar MRI. J Cereb Blood Flow Metab 17: 301–308

    Article  CAS  PubMed  Google Scholar 

  6. Biswal BB, Van Kylen J, Hyde JS (1997) Simultaneous assessment of flow and BOLD signals in resting-state. NMR Biomed 10: 165–170

    Article  CAS  PubMed  Google Scholar 

  7. Wong EC, Bandettini PA, Hyde JS (1992) Echo-planar imaging of the human brain using a three axis local gradient coil. In: Proceedings of SMRM 11th annual meeting, Berlin, p 105

  8. Lowe MJ, Mock BJ, Sorenson JA (1998) Functional connectivity in single and multislice echoplanar imaging using resting-state fluctuations. Neuroimage 7: 119–132

    Article  CAS  PubMed  Google Scholar 

  9. Li SJ, Biswal B, Li Z, Risinger R, Rainey C, Cho JK, Salmeron BJ, Stein EA (2000) Cocaine administration decreases functional connectivity in human primary visual and motor cortex as detected by functional MRI. Magn Reson Med 43: 45–51

    Article  CAS  PubMed  Google Scholar 

  10. Stein T, Moritz C, Quigley M, Cordes D, Haughton V, Meyerand E (2000) Functional connectivity in the thalamus and hippocampus studied with functional MR imaging. AJNR Am J Neuroradiol 21: 1397–1401

    CAS  PubMed  Google Scholar 

  11. Arfanakis K, Cordes D, Haughton VM, Moritz CH, Quigley MA, Meyerand ME (2000) Combining independent component analysis and correlation analysis to probe interregional connectivity in fMRI task activation datasets. Magn Reson Imaging 18: 921–930

    Article  CAS  PubMed  Google Scholar 

  12. Cordes D, Haughton VM, Arfanakis K, Carew JD, Turski PA, Moritz CH, Quigley MA, Meyerand ME (2001) Frequencies contributing to functional connectivity in the cerebral cortex in “resting-state” data. AJNR Am J Neuroradiol 22: 1326–1333

    CAS  PubMed  Google Scholar 

  13. Lowe MJ, Dzemidzic M, Lurito JT, Mathews VP, Phillips MD (2000) Correlations in low-frequency BOLD fluctuations reflect cortico-cortical connections. Neuroimage 12: 582–587

    Article  CAS  PubMed  Google Scholar 

  14. Xiong J, Parsons LM, Gao JH, Fox PT (1999) Interregional connectivity to primary motor cortex revealed using MRI resting state images. Hum Brain Mapp 8: 151–156

    Article  CAS  PubMed  Google Scholar 

  15. Peltier SJ, Noll DC (2002) T(2)(*) dependence of low frequency functional connectivity. Neuroimage 16: 985–992

    Article  CAS  PubMed  Google Scholar 

  16. Lowe MJ (1999) Functional connectivity with continuous state fMRI assessed with structural equations. In: Proceedings of fifth international conference on functional mapping of the human brain, Dusseldorf, Germany, p 197

  17. Alexander GE, DeLong MR, Strick PL (1986) Parallell organization of functionally segregated circuits linking basal ganglia and cortex. Ann Rev Neurosci 9: 357–381

    Article  CAS  PubMed  Google Scholar 

  18. Lowe M, Rutecki P, Woodard A, Turski P, Sorenson J (1997) Auditory cortex fMRI noise correlations in callosal agenesis. Hum Brain Mapp 5: S194

    Article  Google Scholar 

  19. Quigley M, Cordes D, Turski P, Moritz C, Haughton V, Seth R, Meyerand ME (2003) Role of the corpus callosum in functional connectivity. AJNR Am J Neuroradiol 24: 208–212

    PubMed  Google Scholar 

  20. Adams RD, Victor M, Ropper AH (1997) Principles of Neurology. In: Adams RD, Victor M, Ropper AH (eds) McGraw-Hill, New York, pp 903–921

  21. Lowe MJ, Phillips MD, Lurito JT, Mattson D, Dzemidzic M, Mathews VP (2002) Multiple sclerosis: low-frequency temporal blood oxygen level-dependent fluctuations indicate reduced functional connectivity initial results. Radiology 224: 184–192

    Article  PubMed  Google Scholar 

  22. Greicius MD, Supekar K, Menon V, Dougherty RF (2009) Resting-state functional connectivity reflects structural connectivity in the default mode network. Cereb Cortex 19: 72–78

    Article  PubMed  Google Scholar 

  23. Lowe MJ, Beall EB, Sakaie KE, Koenig KA, Stone L, Marrie RA, Phillips MD (2008) Resting state sensorimotor functional connectivity in multiple sclerosis inversely correlates with transcallosal motor pathway transverse diffusivity. Hum Brain Mapp 29: 818–827

    Article  PubMed  Google Scholar 

  24. Skudlarski P, Jagannathan K, Calhoun VD, Hampson M, Skudlarska BA, Pearlson G (2008) Measuring brain connectivity: diffusion tensor imaging validates resting state temporal correlations. Neuroimage 43: 554–561

    Article  PubMed  Google Scholar 

  25. van den Heuvel M, Mandl R, Luigjes J, Hulshoff Pol H (2008) Microstructural organization of the cingulum tract and the level of default mode functional connectivity. J Neurosci 28: 10844–10851

    Article  PubMed  Google Scholar 

  26. Koch MA, Norris DG, Hund-Georgiadis M (2002) An investigation of functional and anatomical connectivity using magnetic resonance imaging. Neuroimage 16: 241–250

    Article  PubMed  Google Scholar 

  27. Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, Shulman GL (2001) A default mode of brain function. Proc Natl Acad Sci USA 98: 676–682

    Article  CAS  PubMed  Google Scholar 

  28. Binder JR, Frost JA, Hammeke TA, Bellgowan PS, Rao SM, Cox RW (1999) Conceptual processing during the conscious resting state A functional MRI study. J Cogn Neurosci 11: 80–95

    Article  CAS  PubMed  Google Scholar 

  29. Greicius MD, Krasnow B, Reiss AL, Menon V (2003) Functional connectivity in the resting brain: a network analysis of the default mode hypothesis. Proc Natl Acad Sci USA 100: 253–258

    Article  CAS  PubMed  Google Scholar 

  30. Fair DA, Cohen AL, Dosenbach NU, Church JA, Miezin FM, Barch DM, Raichle ME, Petersen SE, Schlaggar BL (2008) The maturing architecture of the brain’s default network. Proc Natl Acad Sci USA 105: 4028–4032

    Article  CAS  PubMed  Google Scholar 

  31. Fox MD, Snyder AZ, Vincent JL, Corbetta M, Van Essen DC, Raichle ME (2005) The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc Natl Acad Sci USA 102: 9673–9678

    Article  CAS  PubMed  Google Scholar 

  32. Vincent JL, Patel GH, Fox MD, Snyder AZ, Baker JT, Van Essen DC, Zempel JM, Snyder LH, Corbetta M, Raichle ME (2007) Intrinsic functional architecture in the anaesthetized monkey brain. Nature 447: 83–86

    Article  CAS  PubMed  Google Scholar 

  33. Beckmann CF, DeLuca M, Devlin JT, Smith SM (2005) Investigations into resting-state connectivity using independent component analysis. Philos Trans R Soc Lond B Biol Sci 360: 1001–1013

    Article  PubMed  Google Scholar 

  34. Damoiseaux JS, Rombouts SA, Barkhof F, Scheltens P, Stam CJ, Smith SM, Beckmann CF (2006) Consistent resting-state networks across healthy subjects. Proc Natl Acad Sci USA 103: 13848–13853

    Article  CAS  PubMed  Google Scholar 

  35. Logothetis NK, Pauls J, Augath M, Trinath T, Oeltermann A (2001) Neurophysiological investigation of the basis of the fMRI signal. Nature 412: 150–157

    Article  CAS  PubMed  Google Scholar 

  36. Leopold DA, Murayama Y, Logothetis NK (2003) Very slow activity fluctuations in monkey visual cortex: implications for functional brain imaging. Cereb Cortex 13: 422–433

    Article  PubMed  Google Scholar 

  37. Kenet T, Bibitchkov D, Tsodyks M, Grinvald A, Arieli A (2003) Spontaneously emerging cortical representations of visual attributes. Nature 425: 954–956

    Article  CAS  PubMed  Google Scholar 

  38. Laufs H, Krakow K, Sterzer P, Eger E, Beyerle A, Salek-Haddadi A, Kleinschmidt A (2003) Electroencephalographic signatures of attentional and cognitive default modes in spontaneous brain activity fluctuations at rest. Proc Natl Acad Sci USA 100: 11053–11058

    Article  CAS  PubMed  Google Scholar 

  39. Basser JB, (1998) Fiber-tractography via diffusion tensor MRI. In: Proceeding of international society for magnetic resonance imaging in medicine. Sydney

  40. Conturo TE, Lori NF, Cull TS, Akbudak E, Snyder AZ, Shimony JS, McKinstry RC, Burton H, Raichle ME (1999) Tracking neuronal fiber pathways in the living human brain. Proc Natl Acad Sci USA 96: 10422–10427

    Article  CAS  PubMed  Google Scholar 

  41. Mori S, Crain BJ, Chacko VP, van Zijl PC (1999) Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging. Ann Neurol 45: 265–269

    Article  CAS  PubMed  Google Scholar 

  42. Mori S, Crain BJ, Zijl PCV (1998) 3D brain fiber reconstruction from diffusion MRI. In: Proceeding of international conference on functional mapping of the human brain. Montreal

  43. Poupon C, Clark CA, Frouin V, Regis J, Bloch I, Le Bihan D, Mangin J (2000) Regularization of diffusion-based direction maps for the tracking of brain white matter fascicles. Neuroimage 12: 184–195

    Article  CAS  PubMed  Google Scholar 

  44. Tuch DS, Belliveau JW, Wedeen V (2000) A path integral approach to white matter tractography. In: Proceedings of international society of magnetic resonance in medicine, Denver

  45. Song SK, Sun SW, Ju WK, Lin SJ, Cross AH, Neufeld AH (2003) Diffusion tensor imaging detects and differentiates axon and myelin degeneration in mouse optic nerve after retinal ischemia. Neuroimage 20: 1714–1722

    Article  PubMed  Google Scholar 

  46. Song SK, Sun SW, Ramsbottom MJ, Chang C, Russell J, Cross AH (2002) Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. Neuroimage 17: 1429–1436

    Article  PubMed  Google Scholar 

  47. Song SK, Yoshino J, Le TQ, Lin SJ, Sun SW, Cross AH, Armstrong RC (2005) Demyelination increases radial diffusivity in corpus callosum of mouse brain. Neuroimage 26: 132–1340

    Article  PubMed  Google Scholar 

  48. Johnston JM, Vaishnavi SN, Smyth MD, Zhang D, He BJ, Zempel JM, Shimony JS, Snyder AZ, Raichle ME (2008) Loss of resting interhemispheric functional connectivity after complete section of the corpus callosum. J Neurosci 28: 6453–6458

    Article  CAS  PubMed  Google Scholar 

  49. Bell AJ, Sejnowski TJ (1995) An information-maximization approach to blind separation and blind deconvolution. Neural Comput 7: 1129–1159

    Article  CAS  PubMed  Google Scholar 

  50. Smith SM, Fox PT, Miller KL, Glahn DC, Fox PM, Mackay CE, Filippini N, Watkins KE, Toro R, Laird AR, Beckmann CF (2009) Correspondence of the brain’s functional architecture during activation and rest. Proc Natl Acad Sci USA 106: 13040–13045

    Article  CAS  PubMed  Google Scholar 

  51. Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TE, Johansen-Berg H, Bannister PR, De Luca M, Drobnjak I, Flitney DE, Niazy RK, Saunders J, Vickers J, Zhang Y, De Stefano N, Brady JM, Matthews PM (2004) Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23(Suppl 1): S208–S219

    Article  PubMed  Google Scholar 

  52. Calhoun VD, Liu J, Adali T (2009) A review of group ICA for fMRI data and ICA for joint inference of imaging, genetic, and ERP data. Neuroimage 45: S163–S172

    Article  PubMed  Google Scholar 

  53. Bianciardi M, Fukunaga M, van Gelderen P, Horovitz SG, de Zwart JA, Shmueli K, Duyn JH (2009) Sources of functional magnetic resonance imaging signal fluctuations in the human brain at rest: a 7 T study. Magn Reson Imaging 27: 1019–1029

    Article  PubMed  Google Scholar 

  54. Scholvinck ML, Maier A, Ye FQ, Duyn JH, Leopold DA (2010) Neural basis of global resting-state fMRI activity. Proc Natl Acad Sci USA 107: 10238–10243

    Article  CAS  PubMed  Google Scholar 

  55. Shmuel A, Leopold DA (2008) Neuronal correlates of spontaneous fluctuations in fMRI signals in monkey visual cortex: implications for functional connectivity at rest. Hum Brain Mapp 29: 751–761

    Article  PubMed  Google Scholar 

  56. 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: 893–905

    Article  PubMed  Google Scholar 

  57. Nir Y, Mukamel R, Dinstein I, Privman E, Harel M, Fisch L, Gelbard-Sagiv H, Kipervasser S, Andelman F, Neufeld MY, Kramer U, Arieli A, Fried I, Malach R (2008) Interhemispheric correlations of slow spontaneous neuronal fluctuations revealed in human sensory cortex. Nat Neurosci 11: 1100–1108

    Article  CAS  PubMed  Google Scholar 

  58. He BJ, Snyder AZ, Zempel JM, Smyth MD, Raichle ME (2008) Electrophysiological correlates of the brain’s intrinsic large-scale functional architecture. Proc Natl Acad Sci USA 105: 16039–16044

    Article  CAS  PubMed  Google Scholar 

  59. Petsche H, Kaplan S, von Stein A, Filz O (1997) The possible meaning of the upper and lower alpha frequency ranges for cognitive and creative tasks. Int J Psychophysiol 26: 77–97

    Article  CAS  PubMed  Google Scholar 

  60. Rodriguez E, George N, Lachaux JP, Martinerie J, Renault B, Varela FJ (1999) Perception’s shadow: long-distance synchronization of human brain activity. Nature 397: 430–433

    Article  CAS  PubMed  Google Scholar 

  61. Singer W (2001) Consciousness and the binding problem. Ann NY Acad Sci 929: 123–146

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Cleveland Clinic Foundation, 9500 Euclid Ave, Cleveland, OH, 44195, USA

    Mark J. Lowe

Authors
  1. Mark J. Lowe
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mark J. Lowe.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lowe, M.J. A historical perspective on the evolution of resting-state functional connectivity with MRI. Magn Reson Mater Phy 23, 279–288 (2010). https://doi.org/10.1007/s10334-010-0230-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10334-010-0230-y

Keywords

Search

Navigation