Reorganization of cerebral networks after stroke: new insights from neuroimaging with connectivity approaches

Christian Grefkes, Gereon R Fink, Christian Grefkes, Gereon R Fink

Abstract

The motor system comprises a network of cortical and subcortical areas interacting via excitatory and inhibitory circuits, thereby governing motor behaviour. The balance within the motor network may be critically disturbed after stroke when the lesion either directly affects any of these areas or damages-related white matter tracts. A growing body of evidence suggests that abnormal interactions among cortical regions remote from the ischaemic lesion might also contribute to the motor impairment after stroke. Here, we review recent studies employing models of functional and effective connectivity on neuroimaging data to investigate how stroke influences the interaction between motor areas and how changes in connectivity relate to impaired motor behaviour and functional recovery. Based on such data, we suggest that pathological intra- and inter-hemispheric interactions among key motor regions constitute an important pathophysiological aspect of motor impairment after subcortical stroke. We also demonstrate that therapeutic interventions, such as repetitive transcranial magnetic stimulation, which aims to interfere with abnormal cortical activity, may correct pathological connectivity not only at the stimulation site but also among distant brain regions. In summary, analyses of connectivity further our understanding of the pathophysiology underlying motor symptoms after stroke, and may thus help to design hypothesis-driven treatment strategies to promote recovery of motor function in patients.

Figures

Figure 1
Figure 1
Neural activity during movement of the left or right hand in healthy subjects and in stroke patients with left-sided subcortical lesions (P < 0.05, corrected on the cluster level). Activation clusters were surface rendered onto a canonical brain. In stroke patients, movements of the impaired hand were associated with significant activations in ipsilateral (= contralesional) motor areas, which were absent in the healthy controls (A) or when moving the unaffected hand (B) (adapted from Grefkes et al., 2008b, with permission).
Figure 2
Figure 2
Connectivity among motor regions in healthy subjects and patients with hemiparesis caused by subcortical stroke. Coupling parameters (rate constants in 1/s) indicate connection strength, which is also coded in the size and colour of the arrows representing effective connectivity. Positive (green) values represent facilitatory, negative (red) values inhibitory influences on neuronal activity. The greater the absolute value, the more predominant the effect one area has over another. (A) Neural coupling in healthy subjects. In healthy subjects, the intrinsic coupling of motor areas is well balanced within and across hemispheres, while movements of the right hand induce a hemispheric-specific modulation of inter-regional coupling. (B) Significant changes of coupling parameters in stroke patients. Grey arrows denote no significant difference to healthy control subjects, while white arrows indicate a loss of coupling in the patient group. Patients with subcortical stroke show a significant reduction in intrinsic SMA-M1 coupling in the lesioned hemisphere, and a decoupling of ipsilesional areas from contralesional SMA (white arrows). Movements of the paretic hand are associated with a pathological inhibition of ipsilesional M1 exerted by contralesional M1, which does not occur in healthy subjects and correlates with the motor deficit of the paretic hand (adapted from Grefkes et al., 2008b, with permission). PMC = ventral premotor cortex
Figure 3
Figure 3
Synopsis of altered connectivity between cortical areas after stroke. To date, five studies have reported changes in cortical connectivity in patients suffering from motor deficits after stroke. The figure summarizes those regions that were included in the respective connectivity models: primary motor cortex (M1), dorsal and ventral premotor cortex (dPM, vPM), supplementary motor area (SMA), parietal cortex (PAR, including postcentral gyrus), secondary somatosensory cortex (S2) and prefrontal cortex (PFC). Among these regions of interest, a number of intra-hemispheric (blue-coloured) and inter-hemispheric (orange-coloured) connections were identified to be altered in stroke patients and/or to correlate with motor symptoms. Numbers on connections refer to the publication in which a change in neural coupling was reported. Arrow heads were added to the connections whenever directional information was available (i.e. in studies assessing effective connectivity). Strongest convergence across studies was found for the inter-hemispheric interactions between the primary motor cortices.

References

    1. Achard S, Bullmore E. Efficiency and cost of economical brain functional networks. PLoS Comput Biol. 2007;3:e17.
    1. Alstott J, Breakspear M, Hagmann P, Cammoun L, Sporns O. Modeling the impact of lesions in the human brain. PLoS Comput Biol. 2009;5:e1000408.
    1. Bassett DS, Bullmore E. Small-world brain networks. Neuroscientist. 2006;12:512–23.
    1. Bartolomei F, Bosma I, Klein M, Baayen JC, Reijneveld JC, Postma TJ, et al. How do brain tumors alter functional connectivity? A magnetoencephalography study. Ann Neurol. 2006;59:128–38.
    1. Bestmann S, Baudewig J, Siebner HR, Rothwell JC, Frahm J. BOLD MRI responses to repetitive TMS over human dorsal premotor cortex. Neuroimage. 2005;28:22–9.
    1. Biswal B, Yetkin FZ, Haughton VM, Hyde JS. Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Mag Res Med. 1995;34:537–41.
    1. Bollobás B. Random graphs. London: Academic Press; 1985.
    1. Box GEP, Draper NR. Empirical model-building and response surfaces. Wiley: New York; 1987.
    1. Breakspear M, Terry JR, Friston KJ. Modulation of excitatory synaptic coupling facilitates synchronization and complex dynamics in a biophysical model of neuronal dynamics. Network. 2003;14:703–32.
    1. Brodmann K. Vergleichende Lokalisationslehre der Großhirnrinde. Leipzig: Barth; 1909.
    1. Bullmore E, Sporns O. Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci. 2009;10:186–98.
    1. Burge J, Lane T, Link H, Qiu S, Clark VP. Discrete dynamic Bayesian network analysis of fMRI data. Hum Brain Mapp. 2009;30:122–37.
    1. Buxton RB, Wong EC, Frank LR. Dynamics of blood flow and oxygenation changes during brain activation: the balloon model. Magn Reson Med. 1998;39:855–64.
    1. Buzsaki G, Draguhn A. Neuronal oscillations in cortical networks. Science. 2004;304:1926–9.
    1. Carter AR, Astafiev SV, Lang CE, Connor LT, Rengachary J, Strube MJ, et al. Resting interhemispheric functional magnetic resonance imaging connectivity predicts performance after stroke. Ann Neurol. 2010;67:365–75.
    1. Chollet F, DiPiero V, Wise RJ, Brooks DJ, Dolan RJ, Frackowiak RS. The functional anatomy of motor recovery after stroke in humans: a study with positron emission tomography. Ann Neurol. 1991;29:63–71.
    1. Chouinard PA, Leonard G, Paus T. Changes in effective connectivity of the primary motor cortex in stroke patients after rehabilitative therapy. Exp Neurol. 2006;201:375–87.
    1. Chouinard PA, Van Der Werf YD, Leonard G, Paus T. Modulating neural networks with transcranial magnetic stimulation applied over the dorsal premotor and primary motor cortices. J Neurophysiol. 2003;90:1071–83.
    1. Corbetta M, Kincade MJ, Lewis C, Snyder AZ, Sapir A. Neural basis and recovery of spatial attention deficits in spatial neglect. Nat Neurosci. 2005;8:1603–10.
    1. Cramer SC. Repairing the human brain after stroke: I. Mechanisms of spontaneous recovery. Ann Neurol. 2008;63:272–87.
    1. Crofts JJ, Higham DJ. A weighted communicability measure applied to complex brain networks. J R Soc Interface. 2009;6:411–4.
    1. David O, Cosmelli D, Friston KJ. Evaluation of different measures of functional connectivity using a neural mass model. Neuroimage. 2004;21:659–73.
    1. David O, Guillemain I, Saillet S, Reyt S, Deransart C, Segebarth C, et al. Identifying neural drivers with functional MRI: an electrophysiological validation. PLoS Biol. 2008;6:2683–97.
    1. De Vico Fallani F, Astolfi L, Cincotti F, Mattia D, la RD, Maksuti E, et al. Evaluation of the brain network organization from EEG signals: a preliminary evidence in stroke patient. Anat Rec. 2009;292:2023–31.
    1. Dong Y, Fukuyama H, Nabatame H, Yamauchi H, Shibasaki H, Yonekura Y. Assessment of benzodiazepine receptors using iodine-123-labeled iomazenil single-photon emission computed tomography in patients with ischemic cerebrovascular disease. A comparison with PET study. Stroke. 1997;28:1776–82.
    1. Dum RP, Strick PL. Motor areas in the frontal lobe of the primate. Physiol Behav. 2002;77:677–82.
    1. Duque J, Hummel F, Celnik P, Murase N, Mazzocchio R, Cohen LG. Transcallosal inhibition in chronic subcortical stroke. Neuroimage. 2005;28:940–6.
    1. Erdös P, Rényi A. On the evolution of random graphs. Publ Math Inst Hung Acad Sci. 1960;5:17–61.
    1. Estrada H, Hatano N. Communicability in complex networks. Phys Rev E. 2008;77:036 111.
    1. Feeney DM, Baron JC. Diaschisis. Stroke. 1986;17:817–30.
    1. Ferbert A, Priori A, Rothwell JC, Day BL, Colebatch JG, Marsden CD. Interhemispheric inhibition of the human motor cortex. J Physiol. 1992;453:525–46.
    1. Fink GR, Frackowiak RS, Pietrzyk U, Passingham RE. Multiple nonprimary motor areas in the human cortex. J Neurophysiol. 1997;77:2164–74.
    1. Foerster O. The motor cortex in man in the light of Hughling Jackson’s Doctrines. Brain. 1936;59:135–59.
    1. Fornito A, Zalesky A, Bullmore ET. Network scaling effects in graph analytic studies of human resting-state FMRI data. Front Syst Neurosci. 2010;4:22.
    1. Fox MD, Raichle ME. Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev Neurosci. 2007;8:700–11.
    1. Fridman EA, Hanakawa T, Chung M, Hummel F, Leiguarda R, Cohen LG. Reorganization of human premotor cortex after stroke recovery. Brain. 2004;127:747–58.
    1. Friston K. Beyond phrenology: what can neuroimaging tell us about distributed circuitry? Ann Rev Neurosci. 2002a;25:221–50.
    1. Friston K. Dynamic causal modeling and Granger causality. Comments on: The identification of interacting networks in the brain using fMRI: Model selection, causality and deconvolution. Neuroimage. 2009 doi:10.1016/j.neuroimage.2009.09.031.
    1. Friston KJ. Functional and effective connectivity in neuroimaging: a synthesis. Hum Brain Mapp. 1994;2:56–78.
    1. Friston KJ. Statistics I: Experimental design and statistical parametric mapping. In: Toga AW, Mazziotta JC, editors. Human brain function. San Diego: Academic Press; 2002b. pp. 605–32.
    1. Friston KJ, Buechel C, Fink GR, Morris J, Rolls E, Dolan RJ. Psychophysiological and modulatory interactions in neuroimaging. Neuroimage. 1997;6:218–29.
    1. Friston KJ, Frith CD, Liddle PF, Frackowiak RS. Functional connectivity: the principal-component analysis of large (PET) data sets. J Cereb Blood Flow Metab. 1993;13:5–14.
    1. Friston KJ, Harrison L, Penny W. Dynamic causal modelling. Neuroimage. 2003;19:1273–302.
    1. Gee DG, Biswal BB, Kelly C, Stark DE, Margulies DS, Shehzad Z, et al. Low frequency fluctuations reveal integrated and segregated processing among the cerebral hemispheres. Neuroimage. 2011;54:517–27.
    1. Gerloff C, Bushara K, Sailer A, Wassermann EM, Chen R, Matsuoka T, et al. Multimodal imaging of brain reorganization in motor areas of the contralesional hemisphere of well recovered patients after capsular stroke. Brain. 2006;129:791–808.
    1. Grefkes C, Eickhoff SB, Nowak DA, Dafotakis M, Fink GR. Dynamic intra- and interhemispheric interactions during unilateral and bilateral hand movements assessed with fMRI and DCM. Neuroimage. 2008a;41:1382–94.
    1. Grefkes C, Fink GR. Functional Neuroimaging and Neuromodulation: Effects of Transcranial Magnetic Stimulation on Cortical Networks in Healthy Subjects and Patients. Klin Neurophysiol. 2009;40:239–47.
    1. Grefkes C, Nowak DA, Eickhoff SB, Dafotakis M, Kust J, Karbe H, et al. Cortical connectivity after subcortical stroke assessed with functional magnetic resonance imaging. Ann Neurol. 2008b;63:236–46.
    1. Grefkes C, Nowak DA, Wang LE, Dafotakis M, Eickhoff SB, Fink GR. Modulating cortical connectivity in stroke patients by rTMS assessed with fMRI and dynamic causal modeling. Neuroimage. 2010a;50:234–43.
    1. Grefkes C, Wang LE, Eickhoff SB, Fink GR. Noradrenergic modulation of cortical networks engaged in visuomotor processing. Cereb Cortex. 2010b;20:783–97.
    1. Hallett M. Transcranial magnetic stimulation and the human brain. Nature. 2000;406:147–50.
    1. He BJ, Snyder AZ, Vincent JL, Epstein A, Shulman GL, Corbetta M. Breakdown of functional connectivity in frontoparietal networks underlies behavioral deficits in spatial neglect. Neuron. 2007;53:905–18.
    1. Hoerzer GM, Liebe S, Schloegl A, Logothetis NK, Rainer G. Directed coupling in local field potentials of macaque v4 during visual short-term memory revealed by multivariate autoregressive models. Front Comput Neurosci. 2010;4:14.
    1. Honey CJ, Sporns O. Dynamical consequences of lesions in cortical networks. Hum Brain Mapp. 2008;29:802–9.
    1. Horwitz B, Rumsey JM, Donohue BC. Functional connectivity of the angular gyrus in normal reading and dyslexia. Proc Natl Acad Sci USA. 1998;95:8939–44.
    1. Hummel F, Celnik P, Giraux P, Floel A, Wu WH, Gerloff C, et al. Effects of non-invasive cortical stimulation on skilled motor function in chronic stroke. Brain. 2005;128:490–9.
    1. Hummel FC, Cohen LG. Non-invasive brain stimulation: a new strategy to improve neurorehabilitation after stroke? Lancet Neurol. 2006;5:708–12.
    1. James GA, Lu ZL, VanMeter JW, Sathian K, Hu XP, Butler AJ. Changes in resting state effective connectivity in the motor network following rehabilitation of upper extremity poststroke paresis. Top Stroke Rehabil. 2009;16:270–81.
    1. Johansen-Berg H, Dawes H, Guy C, Smith SM, Wade DT, Matthews PM. Correlation between motor improvements and altered fMRI activity after rehabilitative therapy. Brain. 2002a;125:2731–42.
    1. Johansen-Berg H, Rushworth MF, Bogdanovic MD, Kischka U, Wimalaratna S, Matthews PM. The role of ipsilateral premotor cortex in hand movement after stroke. Proc Natl Acad Sci USA. 2002b;99:14518–23.
    1. Kazantsev VB, Nekorkin VI, Makarenko VI, Llinas R. Olivo-cerebellar cluster-based universal control system. Proc Natl Acad Sci USA. 2003;100:13064–8.
    1. Kinsbourne M. Hemi-neglect and hemisphere rivalry. In: Weinstein EAFRP, editor. Hemi-inattention and hemisphere specialization. Advances in neurology. New York: Raven Press; 1977.
    1. Kinsbourne M. From unilateral neglect to the brain basis of consciousness. Cortex. 2006;42:869–74.
    1. Kwakkel G, Kollen BJ, Wagenaar RC. Long term effects of intensity of upper and lower limb training after stroke: a randomised trial. J Neurol Neurosurg Psychiatry. 2002;72:473–9.
    1. Kwan LT, Reed BR, Eberling JL, Schuff N, Tanabe J, Norman D, et al. Effects of subcortical cerebral infarction on cortical glucose metabolism and cognitive function. Arch Neurol. 1999;56:809–14.
    1. Lee L, Siebner HR, Rowe JB, Rizzo V, Rothwell JC, Frackowiak RS, et al. Acute remapping within the motor system induced by low-frequency repetitive transcranial magnetic stimulation. J Neurosci. 2003;23:5308–18.
    1. Liu Y, Liang M, Zhou Y, He Y, Hao Y, Song M, et al. Disrupted small-world networks in schizophrenia. Brain. 2008;131:945–61.
    1. Llinas RR, Ribary U, Jeanmonod D, Kronberg E, Mitra PP. Thalamocortical dysrhythmia: A neurological and neuropsychiatric syndrome characterized by magnetoencephalography. Proc Natl Acad Sci USA. 1999;96:15222–7.
    1. Logothetis N. Can current fMRI techniques reveal the micro-architecture of cortex? Nat Neurosci. 2000;3:413–4.
    1. Logothetis NK, Kayser C, Oeltermann A. In vivo measurement of cortical impedance spectrum in monkeys: implications for signal propagation. Neuron. 2007;55:809–23.
    1. Lotze M, Markert J, Sauseng P, Hoppe J, Plewnia C, Gerloff C. The role of multiple contralesional motor areas for complex hand movements after internal capsular lesion. J Neurosci. 2006;26:6096–102.
    1. Lynall ME, Bassett DS, Kerwin R, McKenna PJ, Kitzbichler M, Muller U, et al. Functional connectivity and brain networks in schizophrenia. J Neurosci. 2010;30:9477–87.
    1. Mansur CG, Fregni F, Boggio PS, Riberto M, Gallucci-Neto J, Santos CM, et al. A sham stimulation-controlled trial of rTMS of the unaffected hemisphere in stroke patients. Neurology. 2005;64:1802–4.
    1. McIntosh AR, Gonzalez-Lima F. Structural equation modeling and its application to network analysis in functional brain imaging. Hum Brain Mapp. 1994;2:2–22.
    1. Murase N, Duque J, Mazzocchio R, Cohen LG. Influence of interhemispheric interactions on motor function in chronic stroke. Ann Neurol. 2004;55:400–9.
    1. Nachev P, Kennard C, Husain M. Functional role of the supplementary and pre-supplementary motor areas. Nat Rev Neurosci. 2008;9:856–69.
    1. Newton JM, Ward NS, Parker GJ, Deichmann R, Alexander DC, Friston KJ, et al. Non-invasive mapping of corticofugal fibres from multiple motor areas–relevance to stroke recovery. Brain. 2006;129:1844–58.
    1. Nomura EM, Gratton C, Visser RM, Kayser A, Perez F, D'Esposito M. Double dissociation of two cognitive control networks in patients with focal brain lesions. Proc Natl Acad Sci USA. 2010;107:12017–22.
    1. Nowak DA, Grefkes C, Dafotakis M, Eickhoff S, Küst J, Karbe H, et al. Effects of low-frequency repetitive transcranial magnetic stimulation of the contralesional primary motor cortex on movement kinematics and neural activity in subcortical stroke. Arch Neurol. 2008;65:741–7.
    1. Nowak DA, Grefkes C, Dafotakis M, Kust J, Karbe H, Fink GR. Dexterity is impaired at both hands following unilateral subcortical middle cerebral artery stroke. Eur J Neurosci. 2007;25:3173–84.
    1. Pascual-Leone A, Walsh V, Rothwell J. Transcranial magnetic stimulation in cognitive neuroscience - Virtual lesion, chronometry, and functional connectivity. Curr Opin Neurobiol. 2000;10:232–7.
    1. Penfield W, Rasmussen T. The cerebral cortex of man. New York: Macmillan; 1952.
    1. Penny WD, Stephan KE, Mechelli A, Friston KJ. Comparing dynamic causal models. Neuroimage. 2004a;22:1157–72.
    1. Penny WD, Stephan KE, Mechelli A, Friston KJ. Modelling functional integration: a comparison of structural equation and dynamic causal models. Neuroimage. 2004b;23(Suppl 1):S264–74.
    1. Pikovsky A, Rosenblum M, Kurths J. Synchronization. A universal concept in nonlinear sciences. Cambridge, UK: Cambridge University Press; 2001.
    1. Polania R, Nitsche MA, Paulus W. Modulating functional connectivity patterns and topological functional organization of the human brain with transcranial direct current stimulation. Hum Brain Mapp. 2010 doi: 10.1002/hbm.21104.
    1. Rehme AK, Fink GR, Cramon DY, Grefkes C. The role of the contralesional motor cortex for motor recovery in the early days after stroke assessed with longitudinal fMRI. Cereb Cortex. 2010 doi: 10.1093/cercor/bhq140.
    1. Rizzolatti G, Luppino G, Matelli M. The organization of the cortical motor system: New concepts. Electroenceph Clin Neurophysiol. 1998;106:283–96.
    1. Roebroeck A, Formisano E, Goebel R. Mapping directed influence over the brain using Granger causality and fMRI. Neuroimage. 2005;25:230–42.
    1. Roebroeck A, Formisano E, Goebel R. The identification of interacting networks in the brain using fMRI: Model selection, causality and deconvolution. Neuroimage. 2009 doi: 10.1016/j.neuroimage.2009.09.036.
    1. Roulston MS. Estimating the errors on measured entropy and mutual information. Physica. 1999;125:285–94.
    1. Rowe J, Stephan KE, Friston K, Frackowiak R, Lees A, Passingham R. Attention to action in Parkinson’s disease: impaired effective connectivity among frontal cortical regions. Brain. 2002;125:276–89.
    1. Saur D, Lange R, Baumgaertner A, Schraknepper V, Willmes K, Rijntjes M, et al. Dynamics of language reorganization after stroke. Brain. 2006;129:1371–84.
    1. Schieber M. New views of the primary motor cortex. Neuroscientist. 2000;6:380–9.
    1. Sharma N, Baron JC, Rowe JB. Motor imagery after stroke: relating outcome to motor network connectivity. Ann Neurol. 2009;66:604–16.
    1. Smith SM, Miller KL, Salimi-Khorshidi G, Webster M, Beckmann CF, Nichols TE, et al. Network modelling methods for FMRI. Neuroimage. 2011;54:875–91.
    1. Smith VA, Jarvis ED, Hartemink AJ. Evaluating functional network inference using simulations of complex biological systems. Bioinformatics. 2002;18(Suppl 1):S216–24.
    1. Smith VA, Yu J, Smulders TV, Hartemink AJ, Jarvis ED. Computational inference of neural information flow networks. PLoS Comput Biol. 2006;2:e161.
    1. Sporns O, Honey CJ, Kotter R. Identification and classification of hubs in brain networks. PLoS ONE. 2007;2:e1049.
    1. Sporns O, Tononi G, Kotter R. The human connectome: a structural description of the human brain. PLoS Comput Biol. 2005;1:e42.
    1. Stam CJ, Jones BF, Nolte G, Breakspear M, Scheltens P. Small-world networks and functional connectivity in Alzheimer’s disease. Cereb Cortex. 2007;17:92–9.
    1. Stephan KE, Fink GR, Marshall JC. Mechanisms of hemispheric specialization: insights from analyses of connectivity. Neuropsychologia. 2007a;45:209–28.
    1. Stephan KE, Harrison LM, Kiebel SJ, David O, Penny WD, Friston KJ. Dynamic causal models of neural system dynamics:current state and future extensions. J Biosci. 2007b;32:129–44.
    1. Stephan KE. On the role of general system theory for functional neuroimaging. J Anat. 2004;205:443–70.
    1. Stephan KE, Kasper L, Harrison LM, Daunizeau J, den Ouden HE, Breakspear M, et al. Nonlinear dynamic causal models for fMRI. Neuroimage. 2008;42:649–62.
    1. Stephan KE, Weiskopf N, Drysdale PM, Robinson PA, Friston KJ. Comparing hemodynamic models with DCM. Neuroimage. 2007;38:387–401.
    1. Stinear CM, Barber PA, Smale PR, Coxon JP, Fleming MK, Byblow WD. Functional potential in chronic stroke patients depends on corticospinal tract integrity. Brain. 2007;130:170–80.
    1. Takeuchi N, Chuma T, Matsuo Y, Watanabe I, Ikoma K. Repetitive transcranial magnetic stimulation of contralesional primary motor cortex improves hand function after stroke. Stroke. 2005;36:2681–6.
    1. Talelli P, Greenwood RJ, Rothwell JC. Arm function after stroke: neurophysiological correlates and recovery mechanisms assessed by transcranial magnetic stimulation. Clin Neurophysiol. 2008;117:1641–59.
    1. Tombari D, Loubinoux I, Pariente J, Gerdelat A, Albucher JF, Tardy J, et al. A longitudinal fMRI study: in recovering and then in clinically stable sub-cortical stroke patients. Neuroimage. 2004;23:827–39.
    1. Turrigiano G. Homeostatic signaling: the positive side of negative feedback. Curr Opin Neurobiol. 2007;17:318–24.
    1. van Meer MP, van der Marel K, Wang K, Otte WM, El BS, Roeling TA, et al. Recovery of sensorimotor function after experimental stroke correlates with restoration of resting-state interhemispheric functional connectivity. J Neurosci. 2010;30:3964–72.
    1. von Monakow C. Die Lokalisation im Grosshirn und der Abbau der Funktion durch kortikale Herde. Wiesbaden/Germany: JF Bergmann; 1914.
    1. Wang L, Yu C, Chen H, Qin W, He Y, Fan F, et al. Dynamic functional reorganization of the motor execution network after stroke. Brain. 2010;133:1224–38.
    1. Ward NS, Brown MM, Thompson AJ, Frackowiak RS. Neural correlates of motor recovery after stroke: a longitudinal fMRI study. Brain. 2003;126:2476–96.
    1. Ward NS, Newton JM, Swayne OB, Lee L, Thompson AJ, Greenwood RJ, et al. Motor system activation after subcortical stroke depends on corticospinal system integrity. Brain. 2006;129:809–19.
    1. Warren JE, Crinion JT, Lambon Ralph MA, Wise RJ. Anterior temporal lobe connectivity correlates with functional outcome after aphasic stroke. Brain. 2009;132:3428–42.
    1. Watts DJ, Strogatz SH. Collective dynamics of ‘small-world’ networks. Nature. 1998;393:440–2.
    1. Weiller C, Chollet F, Friston KJ, Wise RJ, Frackowiak RS. Functional reorganization of the brain in recovery from striatocapsular infarction in man. Ann Neurol. 1992;31:463–72.
    1. Yamamoto S, Takasawa M, Kajiyama K, Baron JC, Yamaguchi T. Deterioration of hemiparesis after recurrent stroke in the unaffected hemisphere: Three further cases with possible interpretation. Cerebrovasc Dis. 2007;23:35–9.

Source: PubMed

スポンサーと協力者

医学的状態

薬物療法

3
購読する