Advertisement

Brain Structure and Function

, Volume 221, Issue 8, pp 4221–4234 | Cite as

Deep sleep divides the cortex into opposite modes of anatomical–functional coupling

  • Enzo Tagliazucchi
  • Nicolas Crossley
  • Edward T. Bullmore
  • Helmut Laufs
Original Article

Abstract

The coupling of anatomical and functional connectivity at rest suggests that anatomy is essential for wake-typical activity patterns. Here, we study the development of this coupling from wakefulness to deep sleep. Globally, similarity between whole-brain anatomical and functional connectivity networks increased during deep sleep. Regionally, we found differential coupling: during sleep, functional connectivity of primary cortices resembled more the underlying anatomical connectivity, while we observed the opposite in associative cortices. Increased anatomical–functional similarity in sensory areas is consistent with their stereotypical, cross-modal response to the environment during sleep. In distinction, looser coupling—relative to wakeful rest—in higher order integrative cortices suggests that sleep actively disrupts default patterns of functional connectivity in regions essential for the conscious access of information and that anatomical connectivity acts as an anchor for the restoration of their functionality upon awakening.

Keywords

Sleep Consciousness Anatomical connectivity Functional connectivity 

Notes

Acknowledgments

This work was supported by the Bundesministerium für Bildung und Forschung (grant number 01 EV 0703) and the LOEWE Neuronale Koordination Forschungsschwerpunkt Frankfurt (NeFF). We are indebted to Helmuth Steinmetz and Günther Deuschl for their patronage; Astrid Morzelewski for data acquisition and sleep scoring together with Kolja Jahnke; Sandra Anti, Ralf Deichmann and Steffen Volz for extensive MRI support; Thomas Sattler for excellent IT infrastructure maintenance; and our volunteers for participation in the study. We thank an anonymous reviewer and Olaf Sporns for most constructive comments on this manuscript.

Supplementary material

429_2015_1162_MOESM1_ESM.pdf (16.2 mb)
Supplementary material 1 (PDF 16626 kb)

References

  1. AASM (2007) The AASM manual for the scoring of sleep and associated events- rules, terminology and technical specifications. American Academy of Sleep Medicine, ChicagoGoogle Scholar
  2. Allen PJ, Polizzi G, Krakow K, Fish DR, Lemieux L (1998) Identification of EEG events in the MR scanner: the problem of pulse artifact and a method for its subtraction. Neuroimage 8:229–239CrossRefPubMedGoogle Scholar
  3. Barttfeld P, Uhrig L, Sitt JD, Sigman M, Jarraya B, Dehaene S (2015) Signature of consciousness in the dynamics of resting-state brain activity. Proc Natl Acad Sci USA 112:887–892CrossRefPubMedPubMedCentralGoogle Scholar
  4. Beckmann CF, DeLuca M, Devlin JT, Smith SM (2005) Investigations into resting-state connectivity using independent component analysis. Phil Trans Roy Soc B 360:1001–1013CrossRefGoogle Scholar
  5. Boly M, Phillips C, Tshibanda L, Vanhaudenhuyse A, Schabus M, Dang-Vu TT, Moonen G, Hustinx R, Maquet P, Laureys S (2008) Intrinsic brain activity in altered states of consciousness: how conscious is the default mode of brain function? Ann N Y Acad Sci 1129:119–129CrossRefPubMedPubMedCentralGoogle Scholar
  6. Boly M, Garrido MI, Gosseries O, Bruno MA, Boveroux P, Schnakers C, Massimini M, Litvak V, Laureys S, Friston K (2011) Preserved feedforward but impaired top-down processes in the vegetative state. Science 332:858–862CrossRefPubMedGoogle Scholar
  7. Bullmore E, Sporns O (2012) The economy of brain network organization. Nat Rev Neurosci 13:336–349PubMedGoogle Scholar
  8. Chialvo DR (2010) Emergent complex neural dynamics. Nat Phys 6:744–750CrossRefGoogle Scholar
  9. 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 22:1326–1333PubMedGoogle Scholar
  10. Crossley NA, Mechelli A, Scott J, Carletti F, Fox PT, McGuire P, Bullmore ET (2014) The hubs of the human connectome are generally implicated in the anatomy of brain disorders. Brain 137:2382–2395CrossRefPubMedPubMedCentralGoogle Scholar
  11. Deco G, Kringelbach ML (2014) Great expectations: using whole-brain computational connectomics for understanding neuropsychiatric disorders. Neuron 84:892–905CrossRefPubMedGoogle Scholar
  12. Deco G, McIntosh AR, Shen K, Hutchison RM, Menon RS, Everling S, Hagmann P, Jirsa VK (2014) Identification of optimal structural connectivity using functional connectivity and neural modeling. J Neurosci 34:7910–7916CrossRefPubMedGoogle Scholar
  13. DeFelipe J (2010) From the connectome to the synaptome: an epic love story. Science 330:1198–1201CrossRefPubMedGoogle Scholar
  14. Gabbott PL, Rolls ET (2013) Increased neuronal firing in resting and sleep in areas of the macaque medial prefrontal cortex. Eur J Neurosci 37:1737–1746CrossRefPubMedGoogle Scholar
  15. Glover GH, Li TQ, Ress D (2000) Image-based method for retrospective correction of physiological motion effects in fMRI: RETROICOR. Magn Reson Med 44:162–167CrossRefPubMedGoogle Scholar
  16. Greicius MD, Supekar K, Menon V, Dougherty RF (2009) Resting-state functional connectivity reflects structural connectivity in the default mode network. Cereb Cortex 19:72–78CrossRefPubMedGoogle Scholar
  17. Hagmann P, Cammoun L, Gigandet X, Meuli R, Honey CJ, Wedeen VJ, Sporns O (2008) Mapping the structural core of human cerebral cortex. PLoS Biol 6:e159CrossRefPubMedPubMedCentralGoogle Scholar
  18. Haimovici A, Tagliazucchi E, Balenzuela P, Chialvo DR (2013) Brain organization into resting state networks emerges at criticality on a model of the human connectome. Phys Rev Lett 110:178101CrossRefPubMedGoogle Scholar
  19. Herrick CL (1893) The Evolution of Consciousness and of the Cortex. Science 21:351–352CrossRefPubMedGoogle Scholar
  20. Hofman MA (2014) Evolution of the human brain: when bigger is better. Front Neuroanat 8:15CrossRefPubMedPubMedCentralGoogle Scholar
  21. Honey CJ, Sporns O, Cammoun L, Gigandet X, Thiran JP, Meuli R, Hagmann P (2009) Predicting human resting-state functional connectivity from structural connectivity. Proc Natl Acad Sci USA 106:2035–2040CrossRefPubMedPubMedCentralGoogle Scholar
  22. Jahnke K, von Wegner F, Morzelewski A, Borisov S, Maischein M, Steinmetz H, Laufs H (2012) To wake or not to wake? The two-sided nature of the human K-complex. Neuroimage 59(2):1631–1638. doi: 10.1016/j.neuroimage.2011.09.013
  23. Kaas JH, Gharbawie OA, Stepniewska I (2013) Cortical networks for ethologically relevant behaviors in primates. Am J Primatol 75:407–414CrossRefPubMedGoogle Scholar
  24. Kandel ER, Markram H, Matthews PM, Yuste R, Koch C (2013) Neuroscience thinks big (and collaboratively). Nat Rev Neurosci 14:659–664CrossRefPubMedGoogle Scholar
  25. Lee SH, Dan Y (2012) Neuromodulation of brain states. Neuron 76(1):209–222CrossRefPubMedPubMedCentralGoogle Scholar
  26. Messé A, Rudrauf D, Benali H, Marrelec G (2014) Relating structure and function in the human brain: relative contributions of anatomy, stationary dynamics, and non-stationarities. PLoS Comp Biol 10(3):e1003530CrossRefGoogle Scholar
  27. 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):893–905CrossRefPubMedGoogle Scholar
  28. Newman ME (2006) Modularity and community structure in networks. Proc Natl Acad Sci USA 103:8577–8582CrossRefPubMedPubMedCentralGoogle Scholar
  29. Newman ME, Girvan M (2004) Finding and evaluating community structure in networks. Phys Rev E 69:026113CrossRefGoogle Scholar
  30. Park HJ, Friston K (2013) Structural and functional brain networks: from connections to cognition. Science 342:1238411CrossRefPubMedGoogle Scholar
  31. Passingham RE, Stephan KE, Kotter R (2002) The anatomical basis of functional localization in the cortex. Nat Rev Neurosci 3:606–616CrossRefPubMedGoogle Scholar
  32. 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):2142–2154CrossRefPubMedGoogle Scholar
  33. Rand WM (1971) Objective criteria for the evaluation of clustering methods. JASA 66:846–850CrossRefGoogle Scholar
  34. Reveley C, Seth AK, Pierpaoli C, Silva AC, Yu D, Saunders RC, Leopold D, Ye FQ (2015) Superficial white matter fiber systems impede detection of long-range cortical connections in diffusion MR tractography. Proc Natl Acad Sci USA 112(21):E2820–E2828CrossRefPubMedPubMedCentralGoogle Scholar
  35. Rilling JK (2014) Comparative primate neuroimaging: insights into human brain evolution. Trends Cogn Sci 18:46–55CrossRefPubMedGoogle Scholar
  36. Rubinov M, Sporns O (2010) Complex network measures of brain connectivity: uses and interpretations. Neuroimage 52:1059–1069CrossRefPubMedGoogle Scholar
  37. 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 43:554–561CrossRefPubMedPubMedCentralGoogle Scholar
  38. Stam CJ, van Straaten ECW, Van Dellen E, Tewarie P, Gong G, Hillebrand A, Meier J, Van Mieghem P (2015) The relation between structural and functional connectivity patterns in complex brain networks. Int J Psychophysiol. doi: 10.1016/j.ijpsycho.2015.02.011 PubMedGoogle Scholar
  39. Storey JD (2002) A direct approach to false discovery rates. J Roy Stat Soc B 64(3):479–498CrossRefGoogle Scholar
  40. Tagliazucchi E, Behrens M, Laufs H (2013a) Sleep neuroimaging and models of consciousness. Front Psychol 4:256CrossRefPubMedPubMedCentralGoogle Scholar
  41. Tagliazucchi E, von Wegner F, Morzelewski A, Brodbeck V, Jahnke K, Laufs H (2013b) Breakdown of long-range temporal dependence in default mode and attention networks during deep sleep. Proc Natl Acad Sci USA 110:15419–15424CrossRefPubMedPubMedCentralGoogle Scholar
  42. Tagliazucchi E, Carhart-Harris R, Leech R, Nutt D, Chialvo DR (2014) Enhanced repertoire of brain dynamical states during the psychedelic experience. Hum Brain Mapp 35:5442–5456CrossRefPubMedGoogle Scholar
  43. Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Mazoyer B, Joliot M (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15:273–289CrossRefPubMedGoogle Scholar
  44. Van Essen DC (1997) A tension-based theory of morphogenesis and compact wiring in the central nervous system. Nature 385:313–318CrossRefPubMedGoogle Scholar
  45. Van Essen DC (2013) Cartography and connectomes. Neuron 80:775–790CrossRefPubMedGoogle Scholar
  46. Xia M, Wang J, He Y (2013) BrainNet Viewer: a network visualization tool for human brain connectomics. PLoS One 8(7):e68910CrossRefPubMedPubMedCentralGoogle Scholar
  47. Zalesky A, Fornito A, Harding IH, Cocchi L, Yücel M, Pantelis C, Bullmore ET (2010) Whole-brain anatomical networks: does the choice of nodes matter? Neuroimage 50:970–983CrossRefPubMedGoogle Scholar
  48. Zilles K, Palomero-Gallagher N, Amunts K (2013) Development of cortical folding during evolution and ontogeny. Trends Neurosci 36:275–284CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Enzo Tagliazucchi
    • 1
    • 2
  • Nicolas Crossley
    • 3
  • Edward T. Bullmore
    • 4
    • 5
    • 6
  • Helmut Laufs
    • 1
    • 7
    • 8
  1. 1.Department of Neurology and Brain Imaging CenterGoethe University Frankfurt am Main. Frankfurt am MainFrankfurt Am MainGermany
  2. 2.Institute for Medical PsychologyChristian Albrechts University KielKielGermany
  3. 3.Department of Psychosis Studies, Institute of Psychiatry, Psychology and NeurosciencesKing’s College LondonLondonUK
  4. 4.Department of PsychiatryUniversity of CambridgeCambridgeUK
  5. 5.Cambridgeshire and Peterborough NHS Foundation TrustCambridgeUK
  6. 6.GlaxoSmithKline, Alternative Discovery and DevelopmentBrentfordUK
  7. 7.Department of NeurologyChristian Albrechts University KielKielGermany
  8. 8.Department of NeurologyUKSHKielGermany

Personalised recommendations