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Open Access 01-09-2015 | Original Article

Grey matter volumetric changes related to recovery from hand paresis after cortical sensorimotor stroke

Authors: E. Abela, A. Seiler, J. H. Missimer, A. Federspiel, C. W. Hess, M. Sturzenegger, B. J. Weder, R. Wiest

Published in: Brain Structure and Function | Issue 5/2015

Abstract

Preclinical studies using animal models have shown that grey matter plasticity in both perilesional and distant neural networks contributes to behavioural recovery of sensorimotor functions after ischaemic cortical stroke. Whether such morphological changes can be detected after human cortical stroke is not yet known, but this would be essential to better understand post-stroke brain architecture and its impact on recovery. Using serial behavioural and high-resolution magnetic resonance imaging (MRI) measurements, we tracked recovery of dexterous hand function in 28 patients with ischaemic stroke involving the primary sensorimotor cortices. We were able to classify three recovery subgroups (fast, slow, and poor) using response feature analysis of individual recovery curves. To detect areas with significant longitudinal grey matter volume (GMV) change, we performed tensor-based morphometry of MRI data acquired in the subacute phase, i.e. after the stage compromised by acute oedema and inflammation. We found significant GMV expansion in the perilesional premotor cortex, ipsilesional mediodorsal thalamus, and caudate nucleus, and GMV contraction in the contralesional cerebellum. According to an interaction model, patients with fast recovery had more perilesional than subcortical expansion, whereas the contrary was true for patients with impaired recovery. Also, there were significant voxel-wise correlations between motor performance and ipsilesional GMV contraction in the posterior parietal lobes and expansion in dorsolateral prefrontal cortex. In sum, perilesional GMV expansion is associated with successful recovery after cortical stroke, possibly reflecting the restructuring of local cortical networks. Distant changes within the prefrontal-striato-thalamic network are related to impaired recovery, probably indicating higher demands on cognitive control of motor behaviour.

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Brede database, http://hendrix.imm.dtu.dk/services/jerne/brede/brede.html.

Abela E, Missimer J, Wiest R, Federspiel A, Hess C, Sturzenegger M, Weder B (2012) Lesions to primary sensory and posterior parietal cortices impair recovery from hand paresis after stroke. PLoS One 7(2):e31275. doi:10.1371/journal.pone.0031275 PubMedCentralPubMedCrossRef

Agosta F, Gorno-Tempini ML, Pagani E, Sala S, Caputo D, Perini M, Bartolomei I, Fruguglietti ME, Filippi M (2009) Longitudinal assessment of grey matter contraction in amyotrophic lateral sclerosis: a tensor based morphometry study. Amyotroph Later Scler 10(3):168–174. doi:10.1080/17482960802603841 CrossRef

Alexander GE, DeLong MR, Strick PL (1986) Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci 9:357–381. doi:10.1146/annurev.ne.09.030186.002041 PubMedCrossRef

Amunts K, Lenzen M, Friederici AD, Schleicher A, Morosan P, Palomero-Gallagher N, Zilles K (2010) Broca’s region: novel organizational principles and multiple receptor mapping. PLoS Biol 8(9). doi:10.1371/journal.pbio.1000489

Andersen SM, Rapcsak SZ, Beeson PM (2010) Cost function masking during normalization of brains with focal lesions: still a necessity? NeuroImage 53(1):78–84. doi:10.1016/j.neuroimage.2010.06.003 PubMedCentralPubMedCrossRef

Anderson DR, Burnham KP (2010) Model selection and multi-model inference: a practical information theoretic approach. Springer, New York

Ashburner J, Friston KJ (2000) Voxel-based morphometry—the methods. NeuroImage 11(6 Pt 1):805–821. doi:10.1006/nimg.2000.0582 PubMedCrossRef

Ashburner J, Friston KJ (2005) Unified segmentation. NeuroImage 26(3):839–851. doi:10.1016/j.neuroimage.2005.02.018 PubMedCrossRef

Behrens TE, Johansen-Berg H, Woolrich MW, Smith SM, Wheeler-Kingshott CA, Boulby PA, Barker GJ, Sillery EL, Sheehan K, Ciccarelli O, Thompson AJ, Brady JM, Matthews PM (2003) Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging. Nat Neurosci 6(7):750–757. doi:10.1038/nn1075 PubMedCrossRef

Binkofski F, Buccino G (2004) Motor functions of the Broca’s region. Brain Lang 89(2):362–369. doi:10.1016/S0093-934X(03)00358-4 PubMedCrossRef

Binkofski F, Buccino G, Zilles K, Fink GR (2004) Supramodal representation of objects and actions in the human inferior temporal and ventral premotor cortex. Cortex 40(1):159–161PubMedCrossRef

Bonita R, Beaglehole R (1988) Recovery of motor function after stroke. Stroke 19(12):1497–1500PubMedCrossRef

Brambati SM, Renda NC, Rankin KP, Rosen HJ, Seeley WW, Ashburner J, Weiner MW, Miller BL, Gorno-Tempini ML (2007) A tensor based morphometry study of longitudinal gray matter contraction in FTD. NeuroImage 35(3):998–1003. doi:10.1016/j.neuroimage.2007.01.028 PubMedCentralPubMedCrossRef

Brambati SM, Rankin KP, Narvid J, Seeley WW, Dean D, Rosen HJ, Miller BL, Ashburner J, Gorno-Tempini ML (2009) Atrophy progression in semantic dementia with asymmetric temporal involvement: a tensor-based morphometry study. Neurobiol Aging 30(1):103–111. doi:10.1016/j.neurobiolaging.2007.05.014 PubMedCentralPubMedCrossRef

Brett M, Leff AP, Rorden C, Ashburner J (2001) Spatial normalization of brain images with focal lesions using cost function masking. NeuroImage 14(2):486–500. doi:10.1006/nimg.2001.0845 PubMedCrossRef

Brodtmann A, Pardoe H, Li Q, Lichter R, Ostergaard L, Cumming T (2012) Changes in regional brain volume three months after stroke. J Neurol Sci 322(1–2):122–128. doi:10.1016/j.jns.2012.07.019 PubMedCrossRef

Brott T, Adams HP Jr, Olinger CP, Marler JR, Barsan WG, Biller J, Spilker J, Holleran R, Eberle R, Hertzberg V et al (1989) Measurements of acute cerebral infarction: a clinical examination scale. Stroke 20(7):864–870PubMedCrossRef

Brown JA, Lutsep HL, Weinand M, Cramer SC (2008) Motor cortex stimulation for the enhancement of recovery from stroke: a prospective, multicenter safety study. Neurosurgery 62(Suppl 2):853–862. doi:10.1227/01.neu.0000316287.37618.78 PubMed

Carmichael ST, Wei L, Rovainen CM, Woolsey TA (2001) New patterns of intracortical projections after focal cortical stroke. Neurobiol Dis 8(5):910–922. doi:10.1006/nbdi.2001.0425 PubMedCrossRef

Caspers S, Eickhoff SB, Geyer S, Scheperjans F, Mohlberg H, Zilles K, Amunts K (2008) The human inferior parietal lobule in stereotaxic space. Brain Struct Funct 212(6):481–495. doi:10.1007/s00429-008-0195-z PubMedCrossRef

Castiello U (2005) The neuroscience of grasping. Nat Rev Neurosci 6(9):726–736. doi:10.1038/nrn1744 PubMedCrossRef

Ceccarelli A, Rocca MA, Pagani E, Falini A, Comi G, Filippi M (2009) Cognitive learning is associated with gray matter changes in healthy human individuals: a tensor-based morphometry study. NeuroImage 48(3):585–589. doi:10.1016/j.neuroimage.2009.07.009 PubMedCrossRef

Cieslik EC, Zilles K, Caspers S, Roski C, Kellermann TS, Jakobs O, Langner R, Laird AR, Fox PT, Eickhoff SB (2012) Is there “One” DLPFC in cognitive action control? Evidence for heterogeneity from co-activation-based parcellation. Cereb Cortex. doi:10.1093/cercor/bhs256

Clos M, Amunts K, Laird AR, Fox PT, Eickhoff SB (2013) Tackling the multifunctional nature of Broca’s region meta-analytically: co-activation-based parcellation of area 44. NeuroImage 83C:174–188. doi:10.1016/j.neuroimage.2013.06.041 CrossRef

Dancause N, Barbay S, Frost SB, Plautz EJ, Chen D, Zoubina EV, Stowe AM, Nudo RJ (2005) Extensive cortical rewiring after brain injury. J Neurosci 25(44):10167–10179. doi:10.1523/JNEUROSCI.3256-05.2005 PubMedCrossRef

Deichmann R, Schwarzbauer C, Turner R (2004) Optimisation of the 3D MDEFT sequence for anatomical brain imaging: technical implications at 1.5 and 3 T. NeuroImage 21(2):757–767. doi:10.1016/j.neuroimage.2003.09.062 PubMedCrossRef

DeLong MR, Alexander GE, Mitchell SJ, Richardson RT (1986) The contribution of basal ganglia to limb control. Prog Brain Res 64:161–174. doi:10.1016/S0079-6123(08)63411-1 PubMedCrossRef

Eckert U, Metzger CD, Buchmann JE, Kaufmann J, Osoba A, Li M, Safron A, Liao W, Steiner J, Bogerts B, Walter M (2012) Preferential networks of the mediodorsal nucleus and centromedian–parafascicular complex of the thalamus—a DTI tractography study. Hum Brain Mapp 33(11):2627–2637. doi:10.1002/hbm.21389 PubMedCrossRef

Ehrsson HH, Fagergren E, Forssberg H (2001) Differential fronto-parietal activation depending on force used in a precision grip task: an fMRI study. J Neurophysiol 85(6):2613–2623PubMed

Eickhoff SB, Stephan KE, Mohlberg H, Grefkes C, Fink GR, Amunts K, Zilles K (2005) A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. NeuroImage 25(4):1325–1335. doi:10.1016/j.neuroimage.2004.12.034 PubMedCrossRef

Eickhoff SB, Heim S, Zilles K, Amunts K (2006) Testing anatomically specified hypotheses in functional imaging using cytoarchitectonic maps. NeuroImage 32(2):570–582. doi:10.1016/j.neuroimage.2006.04.204 PubMedCrossRef

Eisner-Janowicz I, Barbay S, Hoover E, Stowe AM, Frost SB, Plautz EJ, Nudo RJ (2008) Early and late changes in the distal forelimb representation of the supplementary motor area after injury to frontal motor areas in the squirrel monkey. J Neurophysiol 100(3):1498–1512. doi:10.1152/jn.90447.2008 PubMedCentralPubMedCrossRef

Fan F, Zhu C, Chen H, Qin W, Ji X, Wang L, Zhang Y, Zhu L, Yu C (2012) Dynamic brain structural changes after left hemisphere subcortical stroke. Hum Brain Mapp. doi:10.1002/hbm.22034 PubMed

Farbota KD, Sodhi A, Bendlin BB, McLaren DG, Xu G, Rowley HA, Johnson SC (2012) Longitudinal volumetric changes following traumatic brain injury: a tensor-based morphometry study. J Int Neuropsychol Soc 18(6):1006–1018. doi:10.1017/S1355617712000835 PubMedCentralPubMedCrossRef

Filippi M, Ceccarelli A, Pagani E, Gatti R, Rossi A, Stefanelli L, Falini A, Comi G, Rocca MA (2010) Motor learning in healthy humans is associated to gray matter changes: a tensor-based morphometry study. PLoS One 5(4):e10198. doi:10.1371/journal.pone.0010198 PubMedCentralPubMedCrossRef

Fridman EA, Hanakawa T, Chung M, Hummel F, Leiguarda RC, Cohen LG (2004) Reorganization of the human ipsilesional premotor cortex after stroke. Brain 127(Pt 4):747–758. doi:10.1093/brain/awh082 PubMedCrossRef

Gauthier LV, Taub E, Perkins C, Ortmann M, Mark VW, Uswatte G (2008) Remodeling the brain: plastic structural brain changes produced by different motor therapies after stroke. Stroke 39(5):1520–1525. doi:10.1161/STROKEAHA.107.502229 PubMedCentralPubMedCrossRef

Geyer S (2004) The microstructural border between the motor and the cognitive domain in the human cerebral cortex. Adv Anat Embryol Cell Biol 174(I–VIII):1–89CrossRef

Geyer S, Ledberg A, Schleicher A, Kinomura S, Schormann T, Burgel U, Klingberg T, Larsson J, Zilles K, Roland PE (1996) Two different areas within the primary motor cortex of man. Nature 382(6594):805–807. doi:10.1038/382805a0 PubMedCrossRef

Go AS, Mozaffarian D, Roger VL, Benjamin EJ, Berry JD, Borden WB, Bravata DM, Dai S, Ford ES, Fox CS, Franco S, Fullerton HJ, Gillespie C, Hailpern SM, Heit JA, Howard VJ, Huffman MD, Kissela BM, Kittner SJ, Lackland DT, Lichtman JH, Lisabeth LD, Magid D, Marcus GM, Marelli A, Matchar DB, McGuire DK, Mohler ER, Moy CS, Mussolino ME, Nichol G, Paynter NP, Schreiner PJ, Sorlie PD, Stein J, Turan TN, Virani SS, Wong ND, Woo D, Turner MB (2013) Heart disease and stroke statistics-2013 update: a report from the American Heart Association. Circulation 127(1):e6–e245. doi:10.1161/CIR.0b013e31828124ad PubMedCrossRef

Haber S, McFarland NR (2001) The place of the thalamus in frontal cortical–basal ganglia circuits. Neuroscientist 7(4):315–324PubMedCrossRef

Jebsen RH, Taylor N, Trieschmann RB, Trotter MJ, Howard LA (1969) An objective and standardized test of hand function. Arch Phys Med Rehabil 50(6):311–319PubMed

Keller SS, Crow T, Foundas A, Amunts K, Roberts N (2009) Broca’s area: nomenclature, anatomy, typology and asymmetry. Brain Lang 109(1):29–48. doi:10.1016/j.bandl.2008.11.005 PubMedCrossRef

Kipps CM, Duggins AJ, Mahant N, Gomes L, Ashburner J, McCusker EA (2005) Progression of structural neuropathology in preclinical Huntington’s disease: a tensor based morphometry study. J Neurol Neurosurg Psychiatry 76(5):650–655. doi:10.1136/jnnp.2004.047993 PubMedCentralPubMedCrossRef

Krakauer JW (2005) Arm function after stroke: from physiology to recovery. Semin Neurol 25(4):384–395. doi:10.1055/s-2005-923533 PubMedCrossRef

Lin DD, Kleinman JT, Wityk RJ, Gottesman RF, Hillis AE, Lee AW, Barker PB (2009) Crossed cerebellar diaschisis in acute stroke detected by dynamic susceptibility contrast MR perfusion imaging. AJNR Am J Neuroradiol 30(4):710–715. doi:10.3174/ajnr.A1435 PubMedCentralPubMedCrossRef

Maes F, Collignon A, Vandermeulen D, Marchal G, Suetens P (1997) Multimodality image registration by maximization of mutual information. IEEE Trans Med Imaging 16(2):187–198. doi:10.1109/42.563664 PubMedCrossRef

Mathiowetz V, Weber K, Volland G, Kashman N (1984) Reliability and validity of grip and pinch strength evaluations. J Hand Surg Am 9(2):222–226PubMedCrossRef

Matthews JN, Altman DG, Campbell MJ, Royston P (1990) Analysis of serial measurements in medical research. BMJ 300(6719):230–235PubMedCentralPubMedCrossRef

McNeill TH, Brown SA, Hogg E, Cheng HW, Meshul CK (2003) Synapse replacement in the striatum of the adult rat following unilateral cortex ablation. J Comp Neurol 467(1):32–43. doi:10.1002/cne.10907 PubMedCrossRef

Mordasini L, Weisstanner C, Rummel C, Thalmann GN, Verma RK, Wiest R, Kessler TM (2012) Chronic pelvic pain syndrome in men is associated with reduction of relative gray matter volume in the anterior cingulate cortex compared to healthy controls. J Urol 188(6):2233–2237. doi:10.1016/j.juro.2012.08.043 PubMedCrossRef

Napieralski JA, Butler AK, Chesselet MF (1996) Anatomical and functional evidence for lesion-specific sprouting of corticostriatal input in the adult rat. J Comp Neurol 373(4):484–497. doi:10.1002/(SICI)1096-9861(19960930)373 PubMedCrossRef

Nocun A, Wojczal J, Szczepanska-Szerej H, Wilczynski M, Chrapko B (2013) Quantitative evaluation of crossed cerebellar diaschisis, using voxel-based analysis of Tc-99m ECD brain SPECT. Nucl Med Rev Cent East Eur 16(1):31–34. doi:10.5603/NMR.2013.0006 PubMedCrossRef

Nudo RJ (1997) Remodeling of cortical motor representations after stroke: implications for recovery from brain damage. Mol Psychiatry 2(3):188–191PubMedCrossRef

Nudo RJ (2003) Functional and structural plasticity in motor cortex: implications for stroke recovery. Phys Med Rehabil Clin N Am 14(1 Suppl):57–76CrossRef

Nudo RJ, Friel KM (1999) Cortical plasticity after stroke: implications for rehabilitation. Rev Neurol 155(9):713–717PubMed

Ongur D, Price JL (2000) The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cereb Cortex 10(3):206–219PubMedCrossRef

Petrides M, Pandya DN (2009) Distinct parietal and temporal pathways to the homologues of Broca’s area in the monkey. PLoS Biol 7(8):e1000170. doi:10.1371/journal.pbio.1000170 PubMedCentralPubMedCrossRef

Prabhakaran S, Zarahn E, Riley C, Speizer A, Chong JY, Lazar RM, Marshall RS, Krakauer JW (2008) Inter-individual variability in the capacity for motor recovery after ischemic stroke. Neurorehabil Neural Repair 22(1):64–71. doi:10.1177/1545968307305302 PubMedCrossRef

Rehme AK, Eickhoff SB, Rottschy C, Fink GR, Grefkes C (2012) Activation likelihood estimation meta-analysis of motor-related neural activity after stroke. NeuroImage 59(3):2771–2782. doi:10.1016/j.neuroimage.2011.10.023 PubMedCrossRef

Ridgway GR, Omar R, Ourselin S, Hill DL, Warren JD, Fox NC (2009) Issues with threshold masking in voxel-based morphometry of atrophied brains. NeuroImage 44(1):99–111. doi:10.1016/j.neuroimage.2008.08.045 PubMedCrossRef

Ripolles P, Marco-Pallares J, de Diego-Balaguer R, Miro J, Falip M, Juncadella M, Rubio F, Rodriguez-Fornells A (2012) Analysis of automated methods for spatial normalization of lesioned brains. NeuroImage 60(2):1296–1306. doi:10.1016/j.neuroimage.2012.01.094 PubMedCrossRef

Rizzolatti G, Arbib MA (1998) Language within our grasp. Trends Neurosci 21(5):188–194PubMedCrossRef

Salmond CH, Ashburner J, Vargha-Khadem F, Connelly A, Gadian DG, Friston KJ (2002) Distributional assumptions in voxel-based morphometry. NeuroImage 17(2):1027–1030PubMedCrossRef

Schaechter JD, Perdue KL (2008) Enhanced cortical activation in the contralesional hemisphere of chronic stroke patients in response to motor skill challenge. Cereb Cortex 18(3):638–647. doi:10.1093/cercor/bhm096 PubMedCrossRef

Schaechter JD, Moore CI, Connell BD, Rosen BR, Dijkhuizen RM (2006) Structural and functional plasticity in the somatosensory cortex of chronic stroke patients. Brain 129(Pt 10):2722–2733. doi:10.1093/brain/awl214 PubMedCrossRef

Scheperjans F, Eickhoff SB, Homke L, Mohlberg H, Hermann K, Amunts K, Zilles K (2008) Probabilistic maps, morphometry, and variability of cytoarchitectonic areas in the human superior parietal cortex. Cereb Cortex 18(9):2141–2157. doi:10.1093/cercor/bhm241 PubMedCentralPubMedCrossRef

Seitz RJ, Roland PE (1992) Learning of sequential finger movements in man: a combined kinematic and positron emission tomography (PET) study. Eur J Neurosci 4(2):154–165PubMedCrossRef

Smith SM, Nichols TE (2009) Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. NeuroImage 44(1):83–98. doi:10.1016/j.neuroimage.2008.03.061 PubMedCrossRef

Stern EB (1992) Stability of the Jebsen–Taylor hand function test across three test sessions. Am J Occup Ther 46(7):647–649PubMedCrossRef

Stinear C (2010) Prediction of recovery of motor function after stroke. Lancet Neurol 9(12):1228–1232. doi:10.1016/S1474-4422(10)70247-7 PubMedCrossRef

Stinear CM, Barber PA, Petoe M, Anwar S, Byblow WD (2012) The PREP algorithm predicts potential for upper limb recovery after stroke. Brain 135(Pt 8):2527–2535. doi:10.1093/brain/aws146 PubMedCrossRef

Tao G, Datta S, He R, Nelson F, Wolinsky JS, Narayana PA (2009) Deep gray matter atrophy in multiple sclerosis: a tensor based morphometry. J Neurol Sci 282(1–2):39–46. doi:10.1016/j.jns.2008.12.035 PubMedCentralPubMedCrossRef

Tardif CL, Collins DL, Pike GB (2009) Sensitivity of voxel-based morphometry analysis to choice of imaging protocol at 3 T. NeuroImage 44(3):827–838. doi:10.1016/j.neuroimage.2008.09.053 PubMedCrossRef

Tohka J, Zijdenbos A, Evans A (2004) Fast and robust parameter estimation for statistical partial volume models in brain MRI. NeuroImage 23(1):84–97. doi:10.1016/j.neuroimage.2004.05.007 PubMedCrossRef

Toni I, Ramnani N, Josephs O, Ashburner J, Passingham RE (2001) Learning arbitrary visuomotor associations: temporal dynamic of brain activity. NeuroImage 14(5):1048–1057. doi:10.1006/nimg.2001.0894 PubMedCrossRef

Ugurbil K, Garwood M, Ellermann J, Hendrich K, Hinke R, Hu X, Kim SG, Menon R, Merkle H, Ogawa S et al (1993) Imaging at high magnetic fields: initial experiences at 4 T. Magn Reson Q 9(4):259–277PubMed

Winship IR, Murphy TH (2008) In vivo calcium imaging reveals functional rewiring of single somatosensory neurons after stroke. J Neurosci 28(26):6592–6606. doi:10.1523/JNEUROSCI.0622-08.2008 PubMedCrossRef

Zatorre RJ, Fields RD, Johansen-Berg H (2012) Plasticity in gray and white: neuroimaging changes in brain structure during learning. Nat Neurosci 15(4):528–536. doi:10.1038/nn.3045 PubMedCentralPubMedCrossRef

Zeiler SR, Gibson EM, Hoesch RE, Li MY, Worley PF, O’Brien RJ, Krakauer JW (2013) Medial premotor cortex shows a reduction in inhibitory markers and mediates recovery in a mouse model of focal stroke. Stroke 44(2):483–489. doi:10.1161/STROKEAHA.112.676940 PubMedCentralPubMedCrossRef

Title: Grey matter volumetric changes related to recovery from hand paresis after cortical sensorimotor stroke
Authors: E. Abela
A. Seiler
J. H. Missimer
A. Federspiel
C. W. Hess
M. Sturzenegger
B. J. Weder
R. Wiest
Publication date: 01-09-2015
Publisher: Springer Berlin Heidelberg
Published in: Brain Structure and Function / Issue 5/2015
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-014-0804-y

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Grey matter volumetric changes related to recovery from hand paresis after cortical sensorimotor stroke

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