Abstract
Following a nonlinear dynamics approach, we investigated the emergence of functional clusters which are related with spontaneous brain activity during sleep. Based on multichannel EEG traces from 10 healthy subjects, we compared the functional connectivity across different sleep stages. Our exploration commences with the conjecture of a small-world patterning, present in the scalp topography of the measured electrical activity. The existence of such a communication pattern is first confirmed for our data and then precisely determined by means of two distinct measures of non-linear interdependence between time-series. A graph encapsulating the small-world network structure along with the relative interdependence strength is formed for each sleep stage and subsequently fed to a suitable clustering procedure. Finally the delineated graph components are comparatively presented for all stages revealing novel attributes of sleep architecture. Our results suggest a pivotal role for the functional coupling during the different stages and indicate interesting dynamic characteristics like its variable hemispheric asymmetry and the isolation between anterior and posterior cortical areas during REM.
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References
Achard S, Salvador R, Whitcher B, Suckling J, Bullmore E (2006) A resilient, low-frequency, small-world human brain functional network with highly connected association cortical hubs. J Neurosci 26:63–72
Astola J, Haavisto P, Neuvo Y (1990) Vector median filters. Proc IEEE 78:678–689
Barahona M, Pecora LM (2002) Synchronization in small-world systems. Phys Rev Lett 89:054101
Bertini M, Ferrara M, Gennaro L, Curcio G, Moroni F, Vecchio F, Gasperis M, Rossini PM, Babiloni C (2007) Directional information flows between brain hemispheres during presleep wake and early sleep stages. Cereb Cortex 17:1970–1978
Breakspear M, Williams L, Stam CJ (2004) A novel method for the topographic analysis of neural activity reveals formation and dissolution of “Dynamic Cell Assemblies”. J Comput Neurosci 16:49–69
Corsi-Cabrera M, Miró E, del-Río-Portilla Y, Pérez-Garci E, Villanueva Y, Guevara MA (2003) Rapid eye movement sleep dreaming is characterized by uncoupled EEG activity between frontal and perceptual cortical regions. Brain Cogn 51:337–345
Corsi-Cabrera M, Muñoz-Torres Z, del Río Portilla Y, Guevara MA (2006) Power and coherent oscillations distinguish REM sleep, stage 1 and wakefulness. Int J Psychophysiol 60(1):59–66
Ferri R, Rundo F, Brunt O, Terzano MG, Stam CJ (2007) Small-world network organization of functional connectivity of EEG slow wave activity during sleep. Clin Neurophysiol 118:449–456
Fraser AM, Swinney HL (1986) Independent coordinates for strange attractors from mutual information. Phys Rev A 33:1134–1140
Friston KJ (2000a) The labile brain. I. Neuronal transients and nonlinear coupling. Phil Trans R Soc Lond B 355:215–236
Friston KJ (2000b) The labile brain. II. Transients, complexity and selection. Phil Trans R Soc Lond B 355:237–252
Friston KJ (2000c) The labile brain. III. Transients and spatio-temporal receptive fields. Phil Trans R Soc Lond B 355:253–265
Fujisaka H, Yamada T (1983) Stability theory of synchronized motion in coupled-oscillator systems. Prog Theor Phys 69:32–47
Grassberger P, Procaccia I (1983) Characterization of strange attractors. Phys Rev Lett 50:346–348
Gray C, Koenig P, Engel A, Singer W (1989) Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties. Nature 338:334–337
Guevara-Perez MA, Ramos-Loyo J, Hernández-González M, Madera-Carrillo H, Corsi-Cabrera M (2000) CAPTUSEN:un sistema para la adquisición computarizada del EEG y los potenciales relacionados a eventos. Rev Mex Psychol 17:77–88
He Y, Chen ZJ, Evans AC (2007) Small-world anatomical networks in the human brain revealed by cortical thickness from MRI. Cereb Cortex 17:2407–2419
Honey CJ, Kötter R, Breakspear M, Sporns O (2007) Network structure of cerebral cortex shapes functional connectivity on multiple time scales. Proc Natl Acad Sci USA 104:10240–10245
Ioannides AA (2006) Magnetoencephalography as a research tool in neuroscience: state of the art. Neuroscientist 12:524–544
Jeong J, Gore JC, Peterson BS (2001) Mutual information analysis of the EEG in patients withAlzheimer’s disease. ClinNeurophysiol 112:827–835
Kajimura N, Uchiyama M, Takayama Y, Uchida S, Uema T, Kato M, Sekimoto M, Watanabe T, Nakajima T, Horikoshi S, Ogawa K, Nishikawa M, Hiroki M, Kudo Y, Matsuda H, Okawa M, Takahashi K (2002) Functional neuroanatomy of human non-rapid eye movement sleep: a study using a positron emission tomography. Int Congress Ser 1232:801–805
Lago-Fernandez LF, Huerta R, Corbacho F, Siguenza JA (2000) Fast response and temporal coherent oscillations in small-world networks. Phys Rev Lett 87:198701
Laskaris NA, Ioannides AA (2002) Semantic geodesic maps:a unifying geometrical approach for studying the structure and dynamics of single trial evoked responses. Clin Neurophysiol 113(8):1209–1226
Laskaris NA, Fotopoulos S, Ioannides AA (2004) Mining information from event-related recordings. IEEE SP Mag 21(3):66–77
Latora V, Marchiori M (2001) Efficient behavior of small-world networks. Phys Rev Lett 87:198701
Masuda N, Aihara K (2004) Global and local synchrony of coupled neurons in small-world networks. Biol Cybern 90:302–309
Meila M (2007) Comparing clusterings-an information based distance. J Multivariate Anal 98:873–895
Micheloyannis S, Pachou E, Stam CJ, Vourkas M, Erimaki S, Tsirka V (2006) Using graph theoretical analysis of multi channel EEG to evaluate the neural efficiency hypothesis. Neurosci Lett 402:273–277
Pavan M, Pelillo M (2007) Dominant sets and pairwise clustering. IEEE Trans PAMI 29(1):167–172
Pecora LM, Carroll TL (1990) Synchronization in chaotic systems. Phys Rev Lett 64:821–824
Perez-Garci E, del Rio-Portilla Y, Guevara MA, Arce C, Corsi-Cabrera M (2001) Paradoxical sleep is characterized by uncoupled gamma activity between frontal and perceptual cortical regions. Sleep 24:118–126
Pikovsky AS (1984) On the interaction of strange attractors. Physik B 55:149–154
Quiroga R Kraskov A Kreuz T, Grassberger P (2002) Performance of different synchronization measures in real data: a case study on electroencephalographic signals. Phys Rev E (online) 65:041903
Rechtschaffen A, Kales A (eds) (1968) A manual of standardized terminology, techniques and scoring system for sleep stages of human subjects. Brain Information Service, Brain Research Institute, University of California, Lost Angeles, CA
Roth C, Achermann P, Borbely AA (1999) Frequency and state specific hemispheric asymmetries in the human sleep EEG. Neurosci Lett 271:139–142
Rulkov NF, Sushchik MM, Tsimring LS, Abarbanel HDI (1995) Generalized synchronization of chaos: the auxiliary system approach. Phys Rev E 51:980–994
Schultz JV, Hubert L (1976) A nonparametric test for the correspondence between two proximity matrices. J Educ Stat 1:59–67
Sporns O, Zwi J (2004) The small world of the cerebral cortex. Neuroinformatics 2:145–162
Sporns O, Chialvo DR, Kaiser M, Hilgetag CC (2004) Organization, development and function of complex brain networks. Trends Cogn Sci 8:418–425
Sporns O, Tononi G, Kotter R (2006) The human connectome: a structural description of the human brain. PLoS Comput Biol 1:245–251
Stam CJ, Van Dijk BW (2002) Synchronization likelihood: an unbiased measure of generalized synchronization in multivariate data sets. Physica D 163:236–251
Stam CJ, Breakspear M, Cappellen Van, Van Walsum AM, Van Dijk BW (2004) Nonlinear synchronization in EEG and whole-head MEG recordings of healthy subjects. Hum Brain Mapp 19:63–78
Stam CJ, Jones BF, Nolte G, Breakspear M, Scheltens Ph (2007) Small-world networks and functional connectivity in Alzheimer’s disease. Cereb Cortex 17:92–99
Strogatz SH (2001) Exploring complex networks. Nature 410:268–276
Takens F (1981) Detecting strange attractors in turbulence. Lect Notes Math 898:366–381
Theiler J (1986) Spurious dimension from correlation algorithms applied to limited time-series data. Phys Rev A 34:2427–2432
Watts DJ, Strogatz SH (1998) Collective dynamics of ‹small-world’networks. Nature 393:440–442
Werth E, Acherman P, Borbely A (1996) Brain topography of the human sleep EEG: antero-posterior shifts of spectral power. NeuroReport 8:123–127
Werth E, Acherman P, Borbely A (1997) Fronto-occipital EEG power gradients in human sleep. J Sleep Res 6:102–112
Yamada T, Fujisaka H (1983) Stability theory of synchronized motion in coupled-oscillator systems 2: the mapping approach”. Prog Theor Phys 70:1240–1248
Acknowledgements
The authors wish to thank Edmundo Gonzalez Zamorano for technical assistance and the Laboratorio de Sueño, Facultad de Psicología, Universidad Nacional Autónoma de México for the concession of EEG data. Prof. Corsi-Cabrera was warmly thanked for thoughtful comments on an earlier version and invaluable related discussions.
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Dimitriadis, S.I., Laskaris, N.A., Del Rio-Portilla, Y. et al. Characterizing Dynamic Functional Connectivity Across Sleep Stages from EEG. Brain Topogr 22, 119–133 (2009). https://doi.org/10.1007/s10548-008-0071-4
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DOI: https://doi.org/10.1007/s10548-008-0071-4