Location via proxy:   [ UP ]  
[Report a bug]   [Manage cookies]                
Skip to main content

Advertisement

Springer Nature Link
Log in

Prognostic Value of EEG Microstates in Acute Stroke

  • Original Paper
  • Published:
Brain Topography Aims and scope Submit manuscript

Abstract

Given the importance of neuronal plasticity in recovery from a stroke and the huge variability of recovery abilities in patients, we investigated neuronal activity in the acute phase to enhance information about the prognosis of recovery in the stabilized phase. We investigated the microstates in 47 patients who suffered a first-ever mono-lesional ischemic stroke in the middle cerebral artery territory and in 20 healthy control volunteers. Electroencephalographic (EEG) activity at rest with eyes closed was acquired between 2 and 10 days (T0) after ischemic attack. Objective criteria allowed for the selection of an optimal number of microstates. Clinical condition was quantified by the National Institute of Health Stroke Scale (NIHSS) both in acute (T0) and stabilized (T1, 5.4 ± 1.7 months) phases and Effective Recovery (ER) was calculated as (NIHSS(T1)-NIHSS(T0))/NIHSS(T0). The microstates A, B, C and D emerged as the most stable. In patients with a left lesion inducing a language impairment, microstate C topography differed from controls. Microstate D topography was different in patients with a right lesion inducing neglect symptoms. In patients, the C vs D microstate duration differed after both a left and a right lesion with respect to controls (C lower than D in left and D lower than C in right lesion). A preserved microstate B in acute phase correlated with a better effective recovery. A regression model indicated that the microstate B duration explained the 11% of ER variance. This first ever study of EEG microstates in acute stroke opens an interesting path to identify neuronal impairments with prognostic relevance, to develop enriched compensatory treatments to drive a better individual recovery.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

References

  • Assenza G, Zappasodi F, Squitti R, Altamura C, Ventriglia M, Ercolani M, Quattrocchi CC, Lupoi D, Passarelli F, Vernieri F, Rossini PM, Tecchio F (2009) Neuronal functionality assessed by magnetoencephalography is related to oxidative stress system in acute ischemic stroke. NeuroImage 44:1267–1273

    Article  PubMed  Google Scholar 

  • Assenza G, Zappasodi F, Pasqualetti P, Vernieri F, Tecchio F (2013) A contralesional EEG power increase mediated by interhemispheric disconnection provides negative prognosis in acute stroke. Restor Neurol Neurosci 31:177–188

    CAS  PubMed  Google Scholar 

  • Baldassarre A, Ramsey L, Rengachary J, Zinn K, Siegel JS, Metcalf NV, Strube MJ, Snyder AZ, Corbetta M, Shulman GL. Dissociated functional connectivity profiles for motor and attention deficits in acute right-hemisphere stroke. Brain 139:2024–2038. doi:10.1093/brain/aww107

  • Barbati G, Porcaro C, Zappasodi F, Rossini PM, Tecchio F (2004) Optimization of ICA approach for artifact identification and removal in MEG signals. Clin Neurophys 115: 1220–1232

    Article  Google Scholar 

  • Beese U, Langer H, Lang W, Dinkel M (1998) Comparison of near-infrared spectroscopy and somatosensory evoked potentials for the detection of cerebral ischemia during carotid endarterectomy. Stroke 29:2032–2037

    Article  CAS  PubMed  Google Scholar 

  • Biernaskie J, Chernenko G, Corbett D (2004) Efficacy of rehabilitative experience declines with time after focal ischemic brain injury. J Neurosci 24:1245–1254

    Article  CAS  PubMed  Google Scholar 

  • Brandeis D, Lehmann D (1986) Event-related potentials of the brain and cognitive processes: approaches and applications. Neuropsychologia 24:151–168

    Article  CAS  PubMed  Google Scholar 

  • Britz J, Van De Ville D, Michel CM (2010) BOLD correlates of EEG topography reveal rapid resting-state network dynamics. Neuroimage 52:1162–1170. doi:10.1016/j.neuroimage.2010.02.052

    Article  PubMed  Google Scholar 

  • Brownsett SLE, Warren JE, Geranmayeh F, Woodhead Z, Leech R, Wise RJS (2014) Cognitive control and its impact on recovery from aphasic stroke. Brain 137:242–254

    Article  PubMed  Google Scholar 

  • Brunet D, Murray MM, Michel CM (2011) Spatiotemporal analysis of multichannel EEG: CARTOOL. Comput Intell Neurosci 2011:813870. doi:10.1155/2011/813870

    Article  PubMed  PubMed Central  Google Scholar 

  • Caliandro P, Vecchio F, Miraglia F, Reale G, Della Marca G, La Torre G, Lacidogna G, Iacovelli C, Padua L, Bramanti P, Rossini PM (2016) Small-world characteristics of cortical connectivity changes in acute stroke. Neurorehabil Neural Repair 31:81–94

    Article  PubMed  Google Scholar 

  • Carter AR, Astafiev SV, Lang CE, Connor LT, Rengachary J, Strube MJ, Pope DL, Shulman GL, Corbetta M (2010) Resting interhemispheric functional magnetic resonance imaging connectivity predicts performance after stroke. Ann Neurol 67:365–375

    PubMed  PubMed Central  Google Scholar 

  • Corbetta M (2012) Functional connectivity and neurological recovery. Dev Psychobiol 54: 239–253

    Article  PubMed  Google Scholar 

  • Crichton SL, Bray BD, McKevitt C, Rudd AG, Wolfe CDA (2016) Patient outcomes up to 15 years after stroke: survival, disability, quality of life, cognition and mental health. J Neurol Neurosurg Psychiatry 87:1091–1098

    Article  PubMed  Google Scholar 

  • Cuspineda E, Machado C, Aubert E, Galan L, Llopis F, Avila Y (2003) Predicting outcome in acute stroke: a comparison between QEEG and the Canadian Neurological Scale. Clin Electroencephalogr 34:1–4

    Article  CAS  PubMed  Google Scholar 

  • Cuspineda E, Machado C, Galan L, Aubert E, Alvarez MA, Llopis F, Portela L, Garcıa M, Manero JM, Avila Y (2007) QEEG prognostic value in acute stroke. Clin EEG Neurosci 38:155–160

    Article  CAS  PubMed  Google Scholar 

  • Duncan PW, Goldstein LB, Matchar D, Divine GW, Feussner J (1992) Measurement of motor recovery after stroke. Outcome assessment and sample size requirements. Stroke 23:1084–1089

    Article  CAS  PubMed  Google Scholar 

  • Evans N, Gale S, Schurger A, Blanke O (2015) Visual feedback dominates the sense of agency for brain-machine actions. PLoS ONE 10:e0130019

    Article  PubMed  PubMed Central  Google Scholar 

  • Feigin VL et al (2014) Global and regional burden of stroke during 1990–2010: findings from the global burden of disease study 2010. Lancet 383:245–254

    Article  PubMed  PubMed Central  Google Scholar 

  • Fernandez-Bouzas A, Harmony T, Fernandez T, Silva-Pereyra J, Valdés P, Bosch J, Aubert E, Casián G, Otero Ojeda G, Ricardo J, Hernández-Ballesteros A, Santiago E (2000) Sources of abnormal EEG activity in brain infarctions. Clin Electroencephalogr 31:165–169

    Article  CAS  PubMed  Google Scholar 

  • Finnigan SP, Rose SE, Walsh M, Griffin M, Janke AL, McMahon KL, Gillies R, Strudwick MW, Pettigrew CM, Semple J, Brown J, Brown P, Chalk JB (2004) Correlation of quantitative EEG in acute ischemic stroke with 30-day NIHSS score. Comparison with diffusion and perfusion MRI. Stroke 35:899–903

    Article  PubMed  Google Scholar 

  • Finnigan SP, Walsh M, Rose SE, Chalk JB (2007) Quantitative EEG indices of sub-acute ischaemic stroke correlate with clinical outcomes. Clin Neurophysiol 118:2525–2532

    Article  PubMed  Google Scholar 

  • Graziadio S, Tomasevic L, Assenza G, Tecchio F, Eyre JA (2012) The myth of the ‘unaffected’ side after unilateral stroke: Is reorganisation of the non-infarcted corticospinal system to re-establish balance the price for recovery? Exp Neurol 238:168–175

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grefkes C, Fink GR (2011) Reorganization of cerebral networks after stroke: new insights from neuroimaging with connectivity approachs. Brain 134:1264–1276

    Article  PubMed  PubMed Central  Google Scholar 

  • Grefkes C, Novak DA, Eickhoff SB, Dafotakis M, Küst J, Karbe H, Fink GR (2008) Cortical connectivity after subcortical stroke assessed with functional magnetic resonance imaging. Ann Neurol 63:236–246

    Article  PubMed  Google Scholar 

  • Gschwind M, Hardmeier M, Van De Ville D, Tomescu M I, Penner I K, Negelin Y, Fuhr P, Michel C M, Seeck M (2016) Fluctuations of spontaneous EEG topographies predict disease state in relapsing-remitting multiple sclerosis. NeuroImage 12:466–477

    Article  PubMed  PubMed Central  Google Scholar 

  • Hatz F, Hardmeier M, Bousleiman H, Rüegg S, Schindler C, Fuhr P (2016) Reliability of functional connectivity of EEG applying microstates-segmented versus classical calculation of phase lag index. Brain Connect 6:461–469

    Article  PubMed  Google Scholar 

  • James GA, Lu ZL, VanMeter JW, Sathian K, Hu XP, Butler AJ (2009) Changes in resting state effective connectivity in the motor network following rehabilitation of upper extremity poststroke paresis. Top Stroke Rehabil 16:270–281

    Article  PubMed  PubMed Central  Google Scholar 

  • Jerret SA, Corsak J (1988) Clinical utility of topographic EEG brain mapping. Clin Electroencephalogr 19:134–143

    Article  Google Scholar 

  • Khanna A, Pascual-Leone A, Michel CM, Farzan F (2015) Microstates in resting-state EEG: current status and future directions. Neurosci Biobehav Rev 49:105–113. doi:10.1016/j.neubiorev.2014.12.010

    Article  PubMed  Google Scholar 

  • Koenig T, Melie-Garcia L (2009) Statistical analysis of multichannel scalp field data. In: Michel CM, Koenig T, Brandeis D, Gianotti LRR, Wackermann J (eds) Electrical neuroimaging. Medicine, Cambridge, pp 169–180

    Chapter  Google Scholar 

  • Koenig T, Lehmann D, Merlo MC, Kochi K, Hell D, Koukkou M (1999) A deviant EEG brain microstate in acute, neuroleptic-naive schizophrenics at rest. Eur Arch Psychiatry Clin Neurosci 249:205–211

    Article  CAS  PubMed  Google Scholar 

  • Koenig T, Prichep L, Lehman D, Valdes Sosa P, Braeker E, Kleinlogel H, Isenhart R, John ER (2002) Millisecond by millisecond, year by year: normative EEG microstates and developmental stages. NeuroImage 16:41–48.

    Article  PubMed  Google Scholar 

  • Lehmann D, Skrandies W (1980) Reference-free identification of components of checkboard-evoked multichannel potential field. Electroencephalogr Clin Neurophysiol 48:609–621

    Article  CAS  PubMed  Google Scholar 

  • Lehmann D, Ozaki H, Pal I (1987) EEG alpha map series: brain micro-states by space-oriented adaptive segmentation. Electroencephalogr Clin Neurophysiol 67:271–288

    Article  CAS  PubMed  Google Scholar 

  • Lehmann D, Strik WK, Henggeler B, Koenig T, Koukkou M (1998) Brain electric microstates and momentary conscious mind states as building bloks of spontaneous thinking: I. Visual imagery and abstract thoughts. Int J Psychophysiol 29:1–11

    Article  CAS  PubMed  Google Scholar 

  • Lehmann D, Faber PL, Galderisi S, Mucci A (2005) EEG microstate duration and syntax in acute, medication-naïve, first-episode schizophrenia: a multi-center study. Psychiatry Res 138:141–156

    Article  PubMed  Google Scholar 

  • Logar C, Boswell M (1991) The value of EEG mapping in focal cerebral lesions. Brain Topogr 3:441–446

    Article  CAS  PubMed  Google Scholar 

  • Mayhew SD, Porcaro C, Tecchio F, Bagshaw AP (2017) fMRI characterization of widespread brain networks relevant for behavioural variability in fine hand control with and without visual feedback. Neuroimage 148:330–342

    Article  PubMed  Google Scholar 

  • Michel CM, Thut G, Morand S, Khateb A, Pegna AJ, Peralta RG, Gonzales S, Seeck M, Landis T (2001) Electric source imaging of human brain functions. Brain Res Rev 36:108–118

    Article  CAS  PubMed  Google Scholar 

  • Milz P, Faber PL, Lehmann D, Koenig T, Kochi K, Pascual-Marqui RD (2016) The functional significance of EEG microstates-Associations with modalities of thinking. Neuroimage 125:643–656

    Article  CAS  PubMed  Google Scholar 

  • Moritz S, Kasprzak P, Arlt M, Taeger K, Metz C (2007) Accuracy of cerebral monitoring in detecting cerebral ischemia during carotid endarterectomy: a comparison of transcranial Doppler sonography, near-infrared spectroscopy, stump pressure, and somatosensory evoked potentials. Anesthesiology 107:563–569

    Article  PubMed  Google Scholar 

  • Murray MM, Brunet D, Michel CM (2008) Topographic ERP analyses: a step-by-step tutorial review. Brain Topogr 20:249–264. doi:10.1007/s10548-008-0054-5

    Article  PubMed  Google Scholar 

  • Murri L, Gori S, Massetani R, Bonanni E, Marcella F, Milani S (1998) Evaluation of acute ischemic stroke using quantitative EEG: a comparison with conventional EEG and CT scan. Neurophysiol Clin 28:249–257

    Article  CAS  PubMed  Google Scholar 

  • Musso F, Brinkmeyer J, Mobascher A, Warbrick T, Winterer G (2010) Spontaneous brain activity and EEG microstates. A novel EEG/fMRI analysis approach to explore resting-state networks. Neuroimage 52:1149–1161. doi:10.1016/j.neuroimage.2010.01.093

    Article  CAS  PubMed  Google Scholar 

  • Niedermeyer E (1997) Cerebrovascular disorders and EEG. In: Niedermeyer E, Lopes Da Silva F. (eds), Electroencephalography: basic principles, clinical applications and related fields, 4th edn., Williams & Wilkins, Baltimore, pp 320–321

    Google Scholar 

  • Nuwer MR, Jordan SE, Ahn SS (1987) Evaluation of stroke using EEG frequency analysis and topographyc mapping. Neurology 37:1153–1159

    Article  CAS  PubMed  Google Scholar 

  • Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113

    Article  CAS  PubMed  Google Scholar 

  • Oliveri M, Rossini PM, Traversa R, Cicinelli P, Filippi MM, Pasqualetti P, Tomaiuolo F, Caltagirone C (1999) Left frontal transcranial magnetic stimulation reduces contralesional extinction in patients with unilateral right brain damage. Brain 122:1731–1739

    Article  PubMed  Google Scholar 

  • Oliveri M, Rossini PM, Filippi MM, Traversa R, Cicinelli P, Palmieri MG, Pasqualetti P, Caltagirone C (2000) Time-dependent activation of parieto-frontal networks for directing attention to tactile space. A study with paired transcranial magnetic stimulation pulses in right-brain-damaged patients with extinction. Brain 123:1939–1947

    Article  PubMed  Google Scholar 

  • Oliviero A, Tecchio F, Zappasodi F, Pasqualetti P, Salustri C, Lupoi D, Ercolani M, Romani GL, Rossini PM (2004) Brain sensorimotor hand area functionality in acute stroke: insights from magnetoencephalography. NeuroImage 23: 542–550.

    Article  PubMed  Google Scholar 

  • Pascual-Marqui RD, Michel CM, Lehmann D (1995) Segmentation of brain electrical activity into microstates: model estimation and validation. IEEE Trans Biomed Eng 42:658–665

    Article  CAS  PubMed  Google Scholar 

  • Pellegrino G, Tomasevic L, Tombini M, Assenza G, Bravi M, Sterzi S, Giacobbe V, Zollo L, Guglielmelli E, Cavallo G, Vernieri F, Tecchio F (2012) Inter-hemispheric coupling changes associate with motor improvements after robotic stroke Rehabilitation. Restor Neurol Neurosci 30:497–510

    CAS  PubMed  Google Scholar 

  • Rossini PM, Altamura C, Ferretti A, Vernieri F, Zappasodi F, Caulo M, Pizzella V, Del Gratta C, Romani GL, Tecchio F (2004) Does cerebrovascular disease affect the coupling between neuronal activity and local haemodynamics? Brain 127:99–110

    Article  CAS  PubMed  Google Scholar 

  • Saleh S, Yarossi M, Manuweera T, Adamovich S, Tunik E (2017) Network interactions underlying mirror feedback in stroke: A dynamic causal modeling study. NeuroImage 13 46–54

    Article  PubMed  Google Scholar 

  • Seitzman BA, Abell M, Bartley SC, Erickson MA, Bolbecker AR, Hetrick WP (2017) Cognitive manipulation of brain electric microstates. Neuroimage 146:533–543. doi:10.1016/j.neuroimage.2016.10.002

    Article  PubMed  Google Scholar 

  • Sharma N, Baron J-C, Rowe JB (2009) Motor imagery after stroke: relating outcome to motor network connectivity. Ann Neurol 66:604–616

    Article  PubMed  PubMed Central  Google Scholar 

  • Siegel JS, Ramsey LE, Snyder AZ, Metcalf NV, Chacko RV, Weinberger K, Baldassarre A, Hacker CD, Shulman GL, Corbetta M (2016) Disruptions of network connectivity predict impairment in multiple behavioral domains after stroke. Proc Natl Acad Sci USA 113:E4367–E4376. doi:10.1073/pnas.1521083113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tecchio F, Zappasodi F, Pasqualetti P, Tombini M, Salustri C, Oliviero A, Pizzella V, Vernieri F, Rossini PM, (2005) Rhythmic brain activity at rest from rolandic areas in acute mono-hemispheric stroke: a magnetoencephalographic study. NeuroImage 28: 72–83.

    Article  PubMed  Google Scholar 

  • Tecchio F, Pasqualetti P, Zappasodi F, Tombini M, Lupoi D, Vernieri F, Rossini PM (2007) Outcome prediction in acute monohemispheric stroke via magnetoencephalography. J Neurol 254:296–305

    Article  PubMed  Google Scholar 

  • Traversa R, Cicinelli P, Bassi A, Rossini PM, Bernardi G (1997) Mapping of motor cortical reorganization after stroke. A brain stimulation study with focal magnetic pulses. Stroke 28:110–117

    Article  CAS  PubMed  Google Scholar 

  • Van De Ville D, Britz J, Michel CM (2010) EEG microstate sequences in healthy humans at rest reveal scale-free dynamics. Proc Natl Acad Sci USA 107:18179

    Article  PubMed  Google Scholar 

  • Von Monakow C (1914) Die Lokalisation im Grosshirn und Abbau der Funktion durch kortikale Herde - Localization in the cortex and the reduction of cortical function. JF Bergmann (ed.) Wiesbaden

  • Wackermann J, Lehmann D, Michel C, Strik W (1993) Adaptive segmentation of spontaneous EEG map series into spatially defined microstates. Int J Psychophysiol 14:269–283

    Article  CAS  PubMed  Google Scholar 

  • Wu W, Sun J, Jin Z, Guo X, Qiu Y, Zhu Y ,Tong S (2011) Impaired neuronal synchrony after focal ischemic stroke in elderly patients. Clin Neurophysiol 122:21–26

    Article  PubMed  Google Scholar 

  • Wu J, Quinlan EB, Dodakian L, McKenzie A, Kathuria N, Zhou RJ, Augsburger R, See J, Le VH, Srinivasan R, Cramer SC (2015) Connectivity measures are robust biomarkers of cortical function and plasticity after stroke. Brain 138:2359–2369. doi:10.1093/brain/awv156

    Article  PubMed  PubMed Central  Google Scholar 

  • Zappasodi F, Tombini M, Milazzo D, Rossini PM, Tecchio F (2007) Delta dipole density and strength in acute monohemispheric stroke. Neurosci Lett 416:310–314

    Article  CAS  PubMed  Google Scholar 

  • Zappasodi F, Olejarczyk E, Marzetti L, Assenza G, Pizzella V, Tecchio F (2014) Fractal dimension of EEG activity senses neuronal impairment in acute stroke. Plos ONE 9:e100199

    Article  PubMed  PubMed Central  Google Scholar 

  • Zeiler SR, Krakauer JW (2013) The interaction between training and plasticity in the poststroke brain. Curr Opin Neurol 26:609–616

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The research leading to these results has received funding from: (1) The Italian Ministry of Health, Cod. GR-2008-1138642; (2) PNR-CNR Aging Program 2012–2018; (3) FISM – Fondazione Italiana Sclerosi Multipla –Prot. N. 13/15/F14. The authors want to acknowledge Peter Angelo Taliaferro for language editing.

Author information

Authors and Affiliations

  1. Department of Neuroscience, Imaging and Clinical Sciences, “Gabriele d’Annunzio” University of Chieti-Pescara, via dei Vestini 31, 66100, Chieti, Italy

    Filippo Zappasodi & Pierpaolo Croce

  2. Institute for Advanced Biomedical Technologies, “Gabriele d’Annunzio” University of Chieti-Pescara, Chieti, Italy

    Filippo Zappasodi & Pierpaolo Croce

  3. Medical Statistics and Information Technology, Fatebenefratelli Foundation for Health Research and Education, AFaR Division, Rome, Italy

    Alessandro Giordani

  4. Clinical Neurology, Campus Biomedico University of Rome, Rome, Italy

    Giovanni Assenza

  5. Department of Geriatrics, Neurosciences & Orthopaedics, Institute of Neurology, Catholic University of Sacred Heart, Policlinic A. Gemelli Foundation, Rome, Italy

    Nadia M. Giannantoni, Paolo Profice, Giuseppe Granata & Paolo M. Rossini

  6. Laboratory of Electrophysiology for Translational neuroScience (LET’S) – ISTC – CNR, at Department of Neuroscience, Fatebenefratelli Hospital, Rome, Italy

    Nadia M. Giannantoni & Franca Tecchio

  7. IRCCS S. Raffaele-Pisana, Rome, Italy

    Paolo M. Rossini

Authors
  1. Filippo Zappasodi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Pierpaolo Croce
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alessandro Giordani
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Giovanni Assenza
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Nadia M. Giannantoni
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Paolo Profice
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Giuseppe Granata
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Paolo M. Rossini
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Franca Tecchio
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Filippo Zappasodi.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zappasodi, F., Croce, P., Giordani, A. et al. Prognostic Value of EEG Microstates in Acute Stroke. Brain Topogr 30, 698–710 (2017). https://doi.org/10.1007/s10548-017-0572-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10548-017-0572-0

Keywords

Search

Navigation