Advertisement

Experimental Brain Research

, Volume 236, Issue 4, pp 1117–1127 | Cite as

Transcranial direct current stimulation generates a transient increase of small-world in brain connectivity: an EEG graph theoretical analysis

  • Fabrizio Vecchio
  • Riccardo Di Iorio
  • Francesca Miraglia
  • Giuseppe Granata
  • Roberto Romanello
  • Placido Bramanti
  • Paolo Maria Rossini
Research Article

Abstract

Transcranial direct current stimulation (tDCS) is a non-invasive technique able to modulate cortical excitability in a polarity-dependent way. At present, only few studies investigated the effects of tDCS on the modulation of functional connectivity between remote cortical areas. The aim of this study was to investigate—through graph theory analysis—how bipolar tDCS modulate cortical networks high-density EEG recordings were acquired before and after bipolar cathodal, anodal and sham tDCS involving the primary motor and pre-motor cortices of the dominant hemispherein 14 healthy subjects. Results showed that, after bipolar anodal tDCS stimulation, brain networks presented a less evident “small world” organization with a global tendency to be more random in its functional connections with respect to prestimulus condition in both hemispheres. Results suggest that tDCS globally modulates the cortical connectivity of the brain, modifying the underlying functional organization of the stimulated networks, which might be related to changes in synaptic efficiency of the motor network and related brain areas. This study demonstrated that graph analysis approach to EEG recordings is able to intercept changes in cortical functions mediated by bipolar anodal tDCS mainly involving the dominant M1 and related motor areas. Concluding, tDCS could be an useful technique to help understanding brain rhythms and their topographic functional organization and specificity.

Keywords

EEG Brain networks Graph analysis Smallworld tDCS 

Notes

Acknowledgements

Authors thank Drs Florinda Ferreri and Andrea Guerra for their support. Project’s founders :Italian Ministry of Health for Institutional Research (Ricerca corrente) and Young Researchers, Project GR-2011-02349998.

Compliance with ethical standards

Conflict of interest

The authors declare no competing financial interests.

References

  1. Achard S, Bullmore E (2007) Efficiency and cost of economical brain functional networks. PLoS Comput Biol 3:e17CrossRefPubMedPubMedCentralGoogle Scholar
  2. Basar E (2012) A review of alpha activity in integrative brain function: fundamental physiology, sensory coding, cognition and pathology. Int J Psychophysiol 86:1–24CrossRefPubMedGoogle Scholar
  3. Başar E, Başar-Eroğlu C, Güntekin B, Yener GG (2013) Brain’s alpha, beta, gamma, delta, and theta oscillations in neuropsychiatric diseases: proposal for biomarker strategies. Suppl Clin Neurophysiol 62:19–54CrossRefPubMedGoogle Scholar
  4. Bassett DS, Bullmore E (2006) Small-world brain networks. Neuroscientist 12:512–523CrossRefPubMedGoogle Scholar
  5. Bassett DS, Bullmore ET (2009) Human brain networks in health and disease. Curr Opin Neurol 22:340–347CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bazanova OM, Vernon D (2014) Interpreting EEG alpha activity. Neurosci Biobehav Rev 44:94–110CrossRefPubMedGoogle Scholar
  7. Bell AJ, Sejnowski TJ (1995) An information-maximization approach to blind separation and blind deconvolution. Neural Comput 7:1129–1159CrossRefPubMedGoogle Scholar
  8. Ben-Simon E, Podlipsky I, Arieli A, Zhdanov A, Hendler T (2008) Never resting brain: simultaneous representation of two alpha related processes in humans. PLoS One 3:e3984CrossRefPubMedPubMedCentralGoogle Scholar
  9. Boggio PS, Castro LO, Savagim EA, Braite R, Cruz VC, Rocha RR, Rigonatti SP, Silva MT, Fregni F (2006) Enhancement of non-dominant hand motor function by anodal transcranial direct current stimulation. Neurosci Lett 404:232–236CrossRefPubMedGoogle Scholar
  10. Bola M, Sabel BA (2015) Dynamic reorganization of brain functional networks during cognition. Neuroimage 114:398–413CrossRefPubMedGoogle Scholar
  11. Bola M, Gall C, Moewes C, Fedorov A, Hinrichs H, Sabel BA (2014) Brain functional connectivity network breakdown and restoration in blindness. Neurology 83:542–551CrossRefPubMedGoogle Scholar
  12. Bola M, Gall C, Sabel BA (2015) Disturbed temporal dynamics of brain synchronization in vision loss. Cortex 67:134–146CrossRefPubMedGoogle Scholar
  13. Bollimunta A, Mo J, Schroeder CE, Ding M (2011) Neuronal mechanisms and attentional modulation of corticothalamic alpha oscillations. J Neurosci 31:4935–4943CrossRefPubMedPubMedCentralGoogle Scholar
  14. Boros K, Poreisz C, Munchau A, Paulus W, Nitsche MA (2008) Premotor transcranial direct current stimulation (tDCS) affects primary motor excitability in humans. Eur J Neurosci 27:1292–1300CrossRefPubMedGoogle Scholar
  15. Cordes D, Haughton VM, Arfanakis K, Wendt GJ, Turski PA, Moritz CH, Quigley MA, Meyerand ME (2000) Mapping functionally related regions of brain with functional connectivity MR imaging. AJNR Am J Neuroradiol 21:1636–1644PubMedGoogle Scholar
  16. Datta A, Bansal V, Diaz J, Patel J, Reato D, Bikson M (2009 Oct) Gyri-precise head model of transcranial direct current stimulation: improved spatial focality using a ring electrode versus conventional rectangular pad. Brain Stimul 2(4):201–207 (207.e1) CrossRefGoogle Scholar
  17. Ferreri F, Rossini PM (2013) TMS and TMS-EEG techniques in the study of the excitability, connectivity, and plasticity of the human motor cortex. Rev Neurosci 24:431–442CrossRefPubMedGoogle Scholar
  18. Ferreri F, Pasqualetti P, Maatta S, Ponzo D, Ferrarelli F, Tononi G, Mervaala E, Miniussi C, Rossini PM (2011) Human brain connectivity during single and paired pulse transcranial magnetic stimulation. Neuroimage 54:90–102CrossRefPubMedGoogle Scholar
  19. Ferreri F, Ponzo D, Hukkanen T, Mervaala E, Kononen M, Pasqualetti P, Vecchio F, Rossini PM, Maatta S (2012) Human brain cortical correlates of short-latency afferent inhibition: a combined EEG-TMS study. J Neurophysiol 108:314–323CrossRefPubMedGoogle Scholar
  20. Ferreri F, Vecchio F, Ponzo D, Pasqualetti P, Rossini PM (2014) Time-varying coupling of EEG oscillations predicts excitability fluctuations in the primary motor cortex as reflected by motor evoked potentials amplitude: an EEG-TMS study. Hum Brain Mapp 35:1969–1980CrossRefPubMedGoogle Scholar
  21. Ferreri F, Vecchio F, Guerra A, Miraglia F, Ponzo D, Vollero L, Iannello G, Maatta S, Mervaala E, Rossini PM, Di Lazzaro V (2017) Age related differences in functional synchronization of EEG activity as evaluated by means of TMS-EEG coregistrations. Neurosci Lett 647:141–146.  https://doi.org/10.1016/j.neulet.2017.03.021 CrossRefPubMedGoogle Scholar
  22. Fox MD, Raichle ME (2007) Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev Neurosci 8:700–711CrossRefPubMedGoogle Scholar
  23. Fregni F, Boggio PS, Mansur CG, Wagner T, Ferreira MJ, Lima MC, Rigonatti SP, Marcolin MA, Freedman SD, Nitsche MA, Pascual-Leone A (2005) Transcranial direct current stimulation of the unaffected hemisphere in stroke patients. Neuroreport 16:1551–1555CrossRefPubMedGoogle Scholar
  24. Freyer F, Aquino K, Robinson PA, Ritter P, Breakspear M (2009) Bistability and non-Gaussian fluctuations in spontaneous cortical activity. J Neurosci 29:8512–8524CrossRefPubMedGoogle Scholar
  25. Guerra A, Petrichella S, Vollero L, Ponzo D, Pasqualetti P, Maatta S, Mervaala E, Kononen M, Bressi F, Iannello G, Rossini PM, Ferreri F (2015) Neurophysiological features of motor cortex excitability and plasticity in subcortical ischemic vascular dementia: a TMS mapping study. Clin Neurophysiol 126:906–913CrossRefPubMedGoogle Scholar
  26. Hern JE, Landgren S, Phillips CG, Porter R (1962) Selective excitation of corticofugal neurones by surface-anodal stimulation of the baboon’s motor cortex. J Physiol 161:73–90CrossRefPubMedPubMedCentralGoogle Scholar
  27. Hipp JF, Hawellek DJ, Corbetta M, Siegel M, Engel AK (2012) Large-scale cortical correlation structure of spontaneous oscillatory activity. Nat Neurosci 15:884–890CrossRefPubMedGoogle Scholar
  28. Hoffmann S, Falkenstein M (2008) The correction of eye blink artefacts in the EEG: a comparison of two prominent methods. PLoS One 3:e3004CrossRefPubMedPubMedCentralGoogle Scholar
  29. Hummel F, Cohen LG (2005) Improvement of motor function with noninvasive cortical stimulation in a patient with chronic stroke. Neurorehabil Neural Repair 19:14–19CrossRefPubMedGoogle Scholar
  30. Iriarte J, Urrestarazu E, Valencia M, Alegre M, Malanda A, Viteri C, Artieda J (2003) Independent component analysis as a tool to eliminate artifacts in EEG: a quantitative study. J Clin Neurophysiol 20:249–257CrossRefPubMedGoogle Scholar
  31. Jensen O, Mazaheri A (2010) Shaping functional architecture by oscillatory alpha activity: gating by inhibition. Front Hum Neurosci 4:186CrossRefPubMedPubMedCentralGoogle Scholar
  32. Klimesch W (1999) EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis. Brain Res Brain Res Rev 29:169–195CrossRefPubMedGoogle Scholar
  33. Klimesch W, Schimke H, Pfurtscheller G (1993) Alpha frequency, cognitive load and memory performance. Brain Topogr 5:241–251CrossRefPubMedGoogle Scholar
  34. Klimesch W, Schimke H, Schwaiger J (1994) Episodic and semantic memory: an analysis in the EEG theta and alpha band. Electroencephalogr Clin Neurophysiol 91:428–441CrossRefPubMedGoogle Scholar
  35. Klimesch W, Doppelmayr M, Russegger H, Pachinger T, Schwaiger J (1998) Induced alpha band power changes in the human EEG and attention Neurosci Lett 244(2):73–76CrossRefPubMedGoogle Scholar
  36. Klimesch W, Doppelmayr M, Stadler W, Pollhuber D, Sauseng P, Rohm D (2001) Episodic retrieval is reflected by a process specific increase in human electroencephalographic theta activity. Neurosci Lett 302:49–52CrossRefPubMedGoogle Scholar
  37. Klimesch W, Sauseng P, Hanslmayr S (2007) EEG alpha oscillations: the inhibition-timing hypothesis. Brain Res Rev 53:63–88CrossRefPubMedGoogle Scholar
  38. Krause B, Marquez-Ruiz J, Cohen KR (2013) The effect of transcranial direct current stimulation: a role for cortical excitation/inhibition balance? Front Hum Neurosci 7:602CrossRefPubMedPubMedCentralGoogle Scholar
  39. Lang N, Siebner HR, Ward NS, Lee L, Nitsche MA, Paulus W, Rothwell JC, Lemon RN, Frackowiak RS (2005) How does transcranial DC stimulation of the primary motor cortex alter regional neuronal activity in the human brain? Eur J Neurosci 22:495–504CrossRefPubMedPubMedCentralGoogle Scholar
  40. Liebetanz D, Nitsche MA, Tergau F, Paulus W (2002) Pharmacological approach to the mechanisms of transcranial DC-stimulation-induced after-effects of human motor cortex excitability. Brain 125:2238–2247CrossRefPubMedGoogle Scholar
  41. Lizier JT, Heinzle J, Horstmann A, Haynes JD, Prokopenko M (2011) Multivariate information-theoretic measures reveal directed information structure and task relevant changes in fMRI connectivity. J Comput Neurosci 30:85–107CrossRefPubMedGoogle Scholar
  42. Lockley SW, Evans EE, Scheer FA, Brainard GC, Czeisler CA, Aeschbach D (2006) Short-wavelength sensitivity for the direct effects of light on alertness, vigilance, and the waking electroencephalogram in humans. Sleep 29:161–168PubMedGoogle Scholar
  43. Marshall L, Molle M, Hallschmid M, Born J (2004) Transcranial direct current stimulation during sleep improves declarative memory. J Neurosci 24:9985–9992CrossRefPubMedGoogle Scholar
  44. Mathewson KE, Lleras A, Beck DM, Fabiani M, Ro T, Gratton G (2011) Pulsed out of awareness: EEG alpha oscillations represent a pulsed-inhibition of ongoing cortical processing. Front Psychol 2:99CrossRefPubMedPubMedCentralGoogle Scholar
  45. Micheloyannis S, Pachou E, Stam CJ, Breakspear M, Bitsios P, Vourkas M, Erimaki S, Zervakis M (2006) Small-world networks and disturbed functional connectivity in schizophrenia. Schizophr Res 87:60–66CrossRefPubMedGoogle Scholar
  46. Micheloyannis S, Vourkas M, Tsirka V, Karakonstantaki E, Kanatsouli K, Stam CJ (2009) The influence of ageing on complex brain networks: a graph theoretical analysis. Hum Brain Mapp 30:200–208CrossRefPubMedGoogle Scholar
  47. Michels L, Moazami-Goudarzi M, Jeanmonod D, Sarnthein J (2008) EEG alpha distinguishes between cuneal and precuneal activation in working memory. Neuroimage 40:1296–1310CrossRefPubMedGoogle Scholar
  48. Miniussi C, Harris JA, Ruzzoli M (2013) Modelling non-invasive brain stimulation in cognitive neuroscience. Neurosci Biobehav Rev 37:1702–1712CrossRefPubMedGoogle Scholar
  49. Miraglia F, Vecchio F, Bramanti P, Rossini PM (2015) Small-worldness characteristics and its gender relation in specific hemispheric networks. Neuroscience 310:1–11CrossRefPubMedGoogle Scholar
  50. Miraglia F, Vecchio F, Bramanti P, Rossini PM (2016) EEG characteristics in “eyes-open” versus “eyes-closed” conditions: small-world network architecture in healthy aging and age-related brain degeneration. Clin Neurophysiol 127:1261–1268CrossRefPubMedGoogle Scholar
  51. Miraglia F, Vecchio F, Rossini PM (2017) Searching for signs of aging and dementia in EEG through network analysis. Behav Brain Res 317:292–300CrossRefPubMedGoogle Scholar
  52. Monte-Silva K, Kuo MF, Liebetanz D, Paulus W, Nitsche MA (2010) Shaping the optimal repetition interval for cathodal transcranial direct current stimulation (tDCS). J Neurophysiol 103:1735–1740CrossRefPubMedGoogle Scholar
  53. Monte-Silva K, Kuo MF, Hessenthaler S, Fresnoza S, Liebetanz D, Paulus W, Nitsche MA (2013) Induction of late LTP-like plasticity in the human motor cortex by repeated non-invasive brain stimulation. Brain Stimul 6:424–432CrossRefPubMedGoogle Scholar
  54. Nitsche MA, Paulus W (2001) Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans. Neurology 57:1899–1901CrossRefPubMedGoogle Scholar
  55. Nitsche MA, Liebetanz D, Schlitterlau A, Henschke U, Fricke K, Frommann K, Lang N, Henning S, Paulus W, Tergau F (2004) GABAergic modulation of DC stimulation-induced motor cortex excitability shifts in humans. Eur J Neurosci 19:2720–2726CrossRefPubMedGoogle Scholar
  56. Notturno F, Marzetti L, Pizzella V, Uncini A, Zappasodi F (2014) Local and remote effects of transcranial direct current stimulation on the electrical activity of the motor cortical network. Hum Brain Mapp 35:2220–2232CrossRefPubMedGoogle Scholar
  57. Nunez PL, Wingeier BM, Silberstein RB (2001) Spatial-temporal structures of human alpha rhythms: theory, microcurrent sources, multiscale measurements, and global binding of local networks. Hum Brain Mapp 13:125–164CrossRefPubMedGoogle Scholar
  58. Onnela JP, Saramaki J, Kertesz J, Kaski K (2005) Intensity and coherence of motifs in weighted complex networks. Phys Rev E Stat Nonlin Soft Matter Phys 71:065103CrossRefPubMedGoogle Scholar
  59. Palva S, Palva JM (2011) Functional roles of alpha-band phase synchronization in local and large-scale cortical networks. Front Psychol 2:204CrossRefPubMedPubMedCentralGoogle Scholar
  60. Pascual-Marqui RD (2007a) Discrete 3D, distributed, linear imaging methods of electric neuronal activity. Part 1: exact, zero error localization. arXiv:0710.3341
  61. Pascual-Marqui RD (2007b) Instantaneous and lagged measurements of linear and nonlinear dependence between groups of multivariate time series: frequency decomposition. arXiv:0711.1455
  62. Pascual-Marqui RD (2009) Theory of the EEG inverse problem. In: House Artech B (ed) Quantitative EEG analysis: methods and clinical applications, pp 121–140Google Scholar
  63. Pascual-Marqui RD, Lehmann D, Koukkou M, Kochi K, Anderer P, Saletu B, Tanaka H, Hirata K, John ER, Prichep L, Biscay-Lirio R, Kinoshita T (2011) Assessing interactions in the brain with exact low-resolution electromagnetic tomography. Philos Trans A Math Phys Eng Sci 369:3768–3784CrossRefPubMedGoogle Scholar
  64. Paulus W, Peterchev AV, Ridding M (2013) Transcranial electric and magnetic stimulation: technique and paradigms. Handb Clin Neurol 116:329–342CrossRefPubMedGoogle Scholar
  65. Pfurtscheller G, Lopes da Silva FH (1999) Event-related EEG/MEG synchronization and desynchronization: basic principles. Clin Neurophysiol 110:1842–1857CrossRefPubMedGoogle Scholar
  66. Polania R, Nitsche MA, Paulus W (2011a) Modulating functional connectivity patterns and topological functional organization of the human brain with transcranial direct current stimulation. Hum Brain Mapp 32:1236–1249CrossRefPubMedGoogle Scholar
  67. Polania R, Paulus W, Antal A, Nitsche MA (2011b) Introducing graph theory to track for neuroplastic alterations in the resting human brain: a transcranial direct current stimulation study. Neuroimage 54:2287–2296CrossRefPubMedGoogle Scholar
  68. Polania R, Paulus W, Nitsche MA (2012) Modulating cortico-striatal and thalamo-cortical functional connectivity with transcranial direct current stimulation. Hum Brain Mapp 33:2499–2508CrossRefPubMedGoogle Scholar
  69. Ranck JB Jr (1975) Which elements are excited in electrical stimulation of mammalian central nervous system: a review. Brain Res 98:417–440CrossRefPubMedGoogle Scholar
  70. Reijneveld JC, Ponten SC, Berendse HW, Stam CJ (2007) The application of graph theoretical analysis to complex networks in the brain. Clin Neurophysiol 118:2317–2331CrossRefPubMedGoogle Scholar
  71. Reinacher M, Becker R, Villringer A, Ritter P (2009) Oscillatory brain states interact with late cognitive components of the somatosensory evoked potential. J Neurosci Methods 183:49–56CrossRefPubMedGoogle Scholar
  72. Rioult-Pedotti MS, Friedman D, Donoghue JP (2000) Learning-induced LTP in neocortex. Science 290:533–536CrossRefPubMedGoogle Scholar
  73. Rossini PM, Di SE, Stanzione P (1985) Nerve impulse propagation along central and peripheral fast conducting motor and sensory pathways in man. Electroencephalogr Clin Neurophysiol 60:320–334CrossRefPubMedGoogle Scholar
  74. Rossini PM, Burke D, Chen R, Cohen LG, Daskalakis Z, Di IR, Di L, Ferreri V, Fitzgerald F, George PB, Hallett MS, Lefaucheur M, Langguth JP, Matsumoto B, Miniussi H, Nitsche C, Pascual-Leone MA, Paulus A, Rossi W, Rothwell S, Siebner JC, Ugawa HR, Walsh Y, Ziemann VU (2015) Non-invasive electrical and magnetic stimulation of the brain, spinal cord, roots and peripheral nerves: basic principles and procedures for routine clinical and research application. An updated report from an I.F.C.N. Committee. Clin Neurophysiol 126:1071–1107CrossRefPubMedGoogle Scholar
  75. Rubinov M, Sporns O (2010) Complex network measures of brain connectivity: uses and interpretations. Neuroimage 52:1059–1069CrossRefPubMedGoogle Scholar
  76. Sadaghiani S, Scheeringa R, Lehongre K, Morillon B, Giraud AL, Kleinschmidt A (2010) Intrinsic connectivity networks, alpha oscillations, and tonic alertness: a simultaneous electroencephalography/functional magnetic resonance imaging study. J Neurosci 30:10243–10250CrossRefPubMedGoogle Scholar
  77. Siebner HR, Lang N, Rizzo V, Nitsche MA, Paulus W, Lemon RN, Rothwell JC (2004) Preconditioning of low-frequency repetitive transcranial magnetic stimulation with transcranial direct current stimulation: evidence for homeostatic plasticity in the human motor cortex. J Neurosci 24:3379–3385CrossRefPubMedGoogle Scholar
  78. Smit DJ, Stam CJ, Posthuma D, Boomsma DI, de Geus EJ (2008) Heritability of “small-world” networks in the brain: a graph theoretical analysis of resting-state EEG functional connectivity. Hum Brain Mapp 29:1368–1378CrossRefPubMedGoogle Scholar
  79. Spitoni GF, Cimmino RL, Bozzacchi C, Pizzamiglio L, Di RF (2013) Modulation of spontaneous alpha brain rhythms using low-intensity transcranial direct-current stimulation. Front Hum Neurosci 7:529CrossRefPubMedPubMedCentralGoogle Scholar
  80. Sporns O, Honey CJ (2006) Small worlds inside big brains. Proc Natl Acad Sci USA 103:19219–19220CrossRefPubMedPubMedCentralGoogle Scholar
  81. Sporns O, Zwi JD (2004) The small world of the cerebral cortex. Neuroinformatics 2:145–162CrossRefPubMedGoogle Scholar
  82. Stagg CJ, Best JG, Stephenson MC, O’Shea J, Wylezinska M, Kincses ZT, Morris PG, Matthews PM, Johansen-Berg H (2009) Polarity-sensitive modulation of cortical neurotransmitters by transcranial stimulation. J Neurosci 29:5202–5206CrossRefPubMedGoogle Scholar
  83. Steinke GK, Galan RF (2011) Brain rhythms reveal a hierarchical network organization. PLoS Comput Biol 7:e1002207CrossRefPubMedPubMedCentralGoogle Scholar
  84. Steriade M, Llinas RR (1988) The functional states of the thalamus and the associated neuronal interplay. Physiol Rev 68:649–742CrossRefPubMedGoogle Scholar
  85. Tenke CE, Kayser J (2005) Reference-free quantification of EEG spectra: combining current source density (CSD) and frequency principal components analysis (fPCA). Clin Neurophysiol 116:2826–2846CrossRefPubMedGoogle Scholar
  86. Vecchio F, Miraglia F, Bramanti P, Rossini PM (2014a) Human brain networks in physiological aging: a graph theoretical analysis of cortical connectivity from EEG data. J Alzheimers Dis 41:1239–1249PubMedGoogle Scholar
  87. Vecchio F, Miraglia F, Marra C, Quaranta D, Vita MG, Bramanti P, Rossini PM (2014b) Human brain networks in cognitive decline: a graph theoretical analysis of cortical connectivity from EEG data. J Alzheimers Dis 41:113–127PubMedGoogle Scholar
  88. Vecchio F, Miraglia F, Curcio G, Altavilla R, Scrascia F, Giambattistelli F, Quattrocchi CC, Bramanti P, Vernieri F, Rossini PM (2015a) Cortical brain connectivity evaluated by graph theory in dementia: a correlation study between functional and structural data. J Alzheimers Dis 45:745–756PubMedGoogle Scholar
  89. Vecchio F, Miraglia F, Curcio G, Della MG, Vollono C, Mazzucchi E, Bramanti P, Rossini PM (2015b) Cortical connectivity in fronto-temporal focal epilepsy from EEG analysis: a study via graph theory. Clin Neurophysiol 126:1108–1116CrossRefPubMedGoogle Scholar
  90. Vecchio F, Miraglia F, Quaranta D, Granata G, Romanello R, Marra C, Bramanti P, Rossini PM (2015c) Cortical connectivity and memory performance in cognitive decline: a study via graph theory from EEG data. Neuroscience 316:143–150.  https://doi.org/10.1016/j.neuroscience.2015.12.036 CrossRefPubMedGoogle Scholar
  91. Vecchio F, Pellicciari MC, Miraglia F, Brignani D, Miniussi C, Rossini PM (2016) Effects of transcranial direct current stimulation on the functional coupling of the sensorimotor cortical network. Neuroimage 140:50–56CrossRefPubMedGoogle Scholar
  92. Vecchio F, Miraglia F, Piludu F, Granata G, Romanello R, Caulo M, Onofrj V, Bramanti P, Colosimo C, Rossini PM (2017) “Small World” architecture in brain connectivity and hippocampal volume in Alzheimer's disease: a study via graph theory from EEG data. Brain Imaging Behav 11(2):473–485.  https://doi.org/10.1007/s11682-016-9528-3 CrossRefPubMedGoogle Scholar
  93. Vines BW, Nair D, Schlaug G (2008) Modulating activity in the motor cortex affects performance for the two hands differently depending upon which hemisphere is stimulated. Eur J Neurosci 28:1667–1673CrossRefPubMedGoogle Scholar
  94. Vogt F, Klimesch W, Doppelmayr M (1998) High-frequency components in the alpha band and memory performance. J Clin Neurophysiol 15(2):167–172CrossRefPubMedGoogle Scholar
  95. Watts DJ, Strogatz SH (1998) Collective dynamics of ‘small-world’ networks. Nature 393:440–442CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Brain Connectivity LaboratoryIRCCS San Raffaele-PisanaRomeItaly
  2. 2.Department Geriatrics, Neurosciences, Orthopedics, Policlinic A. Gemelli, Institute of NeurologyCatholic UniversityRomeItaly
  3. 3.IRCCS Centro Neurolesi Bonino-PulejoMessinaItaly

Personalised recommendations