Neuronal-glial alterations in non-primary motor areas in chronic subcortical stroke

Brain Research

Volumn 1463, Issue , 2012, Pages 75-84

  Cirstea, Carmen M ^a   Nudo, Randolph J ^a   Craciunas, Sorin C ^a,b   Popescu, Elena A ^a   Choi, In Young ^a   Lee, Phil ^a   Yeh, Hung Wen ^a   Savage, Cary R ^a   Brooks, William M ^a  

^a UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

^b Bagdasar Arseni Hospital   (Romania)

Author keywords

1H MRS; Neuronal and glial compartments; Non primary motor areas; Subcortical stroke

Indexed keywords

GLUTAMIC ACID; GLUTAMINE; INOSITOL; N ACETYLASPARTIC ACID;

ADULT; AGED; ARTICLE; BRAIN ISCHEMIA; CHRONIC SUBCORTICAL STROKE; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; GLIA CELL; HEMISPHERE; HUMAN; MALE; METABOLITE; MOTOR DYSFUNCTION; NERVE CELL; PARESIS; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; STROKE; SUPPLEMENTARY MOTOR AREA; SURVIVOR;

ADULT; AGED; CHRONIC DISEASE; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; MOTOR CORTEX; NEUROGLIA; NEURONS; STROKE;

EID: 84861849617     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2012.04.052     Document Type: Article

References (74)

1. Aboul-Enein, F., Krssak, M., Hoftberger, R., Prayer, D., Kristoferitsch, W., 2010. Reduced NAA-levels in the NAWM of patients with MS is a feature of progression. A study with quantitative magnetic resonance spectroscopy at 3 Tesla. PLoS One 5, e11625.
2. Boudrias, M.H., Lee, S.P., Svojanovsky, S., Cheney, P.D., 2010a. Forelimb muscle representations and output properties of motor areas in the mesial wall of rhesus macaques. Cereb. Cortex 20, 704-719.
3. Boudrias, M.H., McPherson, R.L., Frost, S.B., Cheney, P.D., 2010b. Output properties and organization of the forelimb representation of motor areas on the lateral aspect of the hemisphere in rhesus macaques. Cereb. Cortex 20, 169-186.
4. Calautti, C., Baron, J.C., 2003. Functional neuroimaging studies of motor recovery after stroke in adults: a review. Stroke 34, 1553-1566. (Pubitemid 36693533)
5. Calautti, C., Naccarato, M., Jones, P.S., Sharma, N., Day, D.D., Carpenter, A.T., Bullmore, E.T., Warburton, E.A., Baron, J.C., 2007. The relationship between motor deficit and hemisphere activation balance after stroke: a 3T fMRI study. Neuroimage 34, 322-331.
6. Capizzano, A.A., Jorge, R.E., Robinson, R.G., 2010. Limbic metabolic abnormalities in remote traumatic brain injury and correlation with psychiatric morbidity and social functioning. J. Neuropsychiatry Clin. Neurosci. 22, 370-377.
7. Carey, J.R., Kimberley, T.J., Lewis, S.M., Auerbach, E.J., Dorsey, L., Rundquist, P., Ugurbil, K., 2002. Analysis of fMRI and finger tracking training in subjects with chronic stroke. Brain 125, 773-788. (Pubitemid 34279773)
8. Chard, D.T., Griffin, C.M., McLean, M.A., Kapeller, P., Kapoor, R., Thompson, A.J., Miller, D.H., 2002. Brain metabolite changes in cortical grey and normal-appearing white matter in clinically early relapsing-remitting multiple sclerosis. Brain 125, 2342-2352.
9. Chu, W.J., Mason, G.F., Pan, J.W., Hetherington, H.P., Liu, H.G., San Pedro, E.C., Mountz, J.M., 2002. Regional cerebral blood flow and magnetic resonance spectroscopic imaging findings in diaschisis from stroke. Stroke 33, 1243-1248. (Pubitemid 34517042)
10. Cirstea, M.C., Brooks, W.M., Craciunas, S.C., Popescu, A.E., Choi, I., Lee, S., Bani-Ahmed, A., Yeh, H., Savage, C.R., Cohen, L.G., Nudo, R.J., 2011. Primary motor cortex - a functional MRI-guided proton magnetic resonance spectroscopic study. Stroke 42, 1004-1009.
11. Constable, R.T., Skudlarski, P., Mencl, E., Pugh, K.R., Fulbright, R.K., Lacadie, C., Shaywitz, S.E., Shaywitz, B.A., 1998. Quantifying and comparing region-of-interest activation patterns in functional brain MR imaging: methodology considerations. Magn. Reson. Imaging 16, 289-300. (Pubitemid 28264525)
12. Deiber, M.P., Wise, S.P., Honda, M., Catalan, M.J., Grafman, J., Hallett, M., 1997. Frontal and parietal networks for conditional motor learning: a positron emission tomography study. J. Neurophysiol. 78, 977-991. (Pubitemid 27353559)
13. Dum, R.P., Strick, P.L., 1991. The origin of corticospinal projections from the premotor areas in the frontal lobe. J. Neurosci. 11, 667-689.
14. Dum, R.P., Strick, P.L., 2005. Frontal lobe inputs to the digit representations of the motor areas on the lateral surface of the hemisphere. J. Neurosci. 25, 1375-1386. (Pubitemid 40250713)
15. Efron, B., Tibshirani, R.J., 1994. An Introduction to the Bootstrap, 1st edition. CRC Press, Boca Raton, FL. Vol.
16. Fang, P.C., Stepniewska, I., Kaas, J.H., 2008. Corpus callosum connections of subdivisions of motor and premotor cortex, and frontal eye field in a prosimian primate, Otolemur garnetti. J. Comp. Neurol. 508, 565-578. (Pubitemid 351656385)
17. Fridman, E.A., Hanakawa, T., Chung, M., Hummel, F., Leiguarda, R.C., Cohen, L.G., 2004. Reorganization of the human ipsilesional premotor cortex after stroke. Brain 127, 747-758. (Pubitemid 38478519)
18. Fries, W., Danek, A., Scheidtmann, K., Hamburger, C., 1993. Motor recovery following capsular stroke. Role of descending pathways from multiple motor areas. Brain 116 (Pt 2), 369-382. (Pubitemid 23104053)
19. Fugl-Meyer, A.R., Jaasko, L., Leyman, I., Olsson, S., Steglind, S., 1975. The post-stroke hemiplegic patient. 1. A method for evaluation of physical performance. Scand. J. Rehabil. Med. 7, 13-31.
20. Garnett, M.R., Blamire, A.M., Rajagopalan, B., Styles, P., Cadoux-Hudson, T.A., 2000. Evidence for cellular damage in normal-appearing white matter correlates with injury severity in patients following traumatic brain injury: a magnetic resonance spectroscopy study. Brain 123 (Pt 7), 1403-1409. (Pubitemid 30420940)
21. Gerloff, C., Bushara, K., Sailer, A., Wassermann, E.M., Chen, R., Matsuoka, T., Waldvogel, D., Wittenberg, G.F., Ishii, K., Cohen, L.G., Hallett, M., 2006. Multimodal imaging of brain reorganization in motor areas of the contralesional hemisphere of well recovered patients after capsular stroke. Brain 129, 791-808. (Pubitemid 43278240)
22. Giehl, K.M., Tetzlaff, W., 1996. BDNF and NT-3, but not NGF, prevent axotomy-induced death of rat corticospinal neurons in vivo. Eur. J. Neurosci. 8, 1167-1175. (Pubitemid 26174643)
23. Hattingen, E., Lanfermann, H., Menon, S., Neumann-Haefelin, T., de Rochement, R.D., Stamelou, M., Hoglinger, G.U., Magerkurth, J., Pilatus, U., 2009. Combined 1H and 31P MR spectroscopic imaging: impaired energy metabolism in severe carotid stenosis and changes upon treatment. MAGMA 22, 43-52.
24. He, S.Q., Dum, R.P., Strick, P.L., 1993. Topographic organization of corticospinal projections from the frontal lobe: motor areas on the lateral surface of the hemisphere. J. Neurosci. 13, 952-980. (Pubitemid 23067585)
25. He, S.Q., Dum, R.P., Strick, P.L., 1995. Topographic organization of corticospinal projections from the frontal lobe: motor areas on the medial surface of the hemisphere. J. Neurosci. 15, 3284-3306.
26. Heller, A., Wade, D.T., Wood, V.A., Sunderland, A., Hewer, R.L., Ward, E., 1987. Arm function after stroke: measurement and recovery over the first three months. J. Neurol. Neurosurg. Psychiatry 50, 714-719. (Pubitemid 17076283)
27. Henneberger, C., Papouin, T., Oliet, S.H., Rusakov, D.A., 2010. Long-term potentiation depends on release of D-serine from astrocytes. Nature 463, 232-236.
28. Hetherington, H.P., Pan, J.W., Mason, G.F., Adams, D., Vaughn, M.J., Twieg, D.B., Pohost, G.M., 1996. Quantitative 1H spectroscopic imaging of human brain at 4.1 T using image segmentation. Magn. Reson. Med. 36, 21-29. (Pubitemid 26196527)
29. Horenstein, C., Lowe, M.J., Koenig, K.A., Phillips, M.D., 2009. Comparison of unilateral and bilateral complex finger tapping-related activation in premotor and primary motor cortex. Hum. Brain Mapp. 30, 1397-1412.
30. Hummel, F.C., Steven, B., Hoppe, J., Heise, K., Thomalla, G., Cohen, L.G., Gerloff, C., 2009. Deficient intracortical inhibition (SICI) during movement preparation after chronic stroke. Neurology 72, 1766-1772.
31. Hutchins, K.D., Martino, A.M., Strick, P.L., 1988. Corticospinal projections from the medial wall of the hemisphere. Exp. Brain Res. 71, 667-672.
32. Inglese, M., Rusinek, H., George, I.C., Babb, J.S., Grossman, R.I., Gonen, O., 2008. Global average gray and white matter N-acetylaspartate concentration in the human brain. Neuroimage 41, 270-276.
33. Johansen-Berg, H., Rushworth, M.F., Bogdanovic, M.D., Kischka, U., Wimalaratna, S., Matthews, P.M., 2002. The role of ipsilateral premotor cortex in hand movement after stroke. Proc. Natl. Acad. Sci. U. S. A. 99, 14518-14523. (Pubitemid 35257703)
34. Kang, D.W., Roh, J.K., Lee, Y.S., Song, I.C., Yoon, B.W., Chang, K.H., 2000. Neuronal metabolic changes in the cortical region after subcortical infarction: a proton MR spectroscopy study. J. Neurol. Neurosurg. Psychiatry 69, 222-227. (Pubitemid 30466028)
35. Kobayashi, M., Takayama, H., Suga, S., Mihara, B., 2001. Longitudinal changes of metabolites in frontal lobes after hemorrhagic stroke of basal ganglia: a proton magnetic resonance spectroscopy study. Stroke 32, 2237-2245.
36. Liang, Z., Zeng, J., Zhang, C., Liu, S., Ling, X., Xu, A., Ling, L., Wang, F., Pei, Z., 2008. Longitudinal investigations on the anterograde and retrograde degeneration in the pyramidal tract following pontine infarction with diffusion tensor imaging. Cerebrovasc. Dis. 25, 209-216. (Pubitemid 351450423)
37. Liepert, J., Hamzei, F., Weiller, C., 2000. Motor cortex disinhibition of the unaffected hemisphere after acute stroke. Muscle Nerve 23, 1761-1763.
38. Lotze, M., Markert, J., Sauseng, P., Hoppe, J., Plewnia, C., Gerloff, C., 2006. The role of multiple contralesional motor areas for complex hand movements after internal capsular lesion. J. Neurosci. 26, 6096-6102. (Pubitemid 44318375)
39. Loubinoux, I., Carel, C., Pariente, J., Dechaumont, S., Albucher, J.F., Marque, P., Manelfe, C., Chollet, F., 2003. Correlation between cerebral reorganization and motor recovery after subcortical infarcts. Neuroimage 20, 2166-2180. (Pubitemid 37543631)
40. Lu, P., Blesch, A., Tuszynski, M.H., 2001. Neurotrophism without neurotropism: BDNF promotes survival but not growth of lesioned corticospinal neurons. J. Comp. Neurol. 436, 456-470. (Pubitemid 32623064)
41. Mai, J.K., Paxinos, G., Voss, T., 2008. Atlas of the Human Brain. Elsevier, New York, NY. Vol.
42. Manganotti, P., Patuzzo, S., Cortese, F., Palermo, A., Smania, N., Fiaschi, A., 2002. Motor disinhibition in affected and unaffected hemisphere in the early period of recovery after stroke. Clin. Neurophysiol. 113, 936-943. (Pubitemid 34621201)
43. Mochizuki, H., Huang, Y.Z., Rothwell, J.C., 2004. Interhemispheric interaction between human dorsal premotor and contralateral primary motor cortex. J. Physiol. 561, 331-338. (Pubitemid 39549488)
44. Morecraft, R.J., Herrick, J.L., Stilwell-Morecraft, K.S., Louie, J.L., Schroeder, C.M., Ottenbacher, J.G., Schoolfield, M.W., 2002. Localization of arm representation in the corona radiata and internal capsule in the non-human primate. Brain 125, 176-198. (Pubitemid 34084047)
45. Munoz Maniega, S., Cvoro, V., Chappell, F.M., Armitage, P.A., Marshall, I., Bastin, M.E., Wardlaw, J.M., 2008. Changes in NAA and lactate following ischemic stroke: a serial MR spectroscopic imaging study. Neurology 71, 1993-1999.
46. Nachev, P., Kennard, C., Husain, M., 2008. Functional role of the supplementary and pre-supplementary motor areas. Nat. Rev. Neurosci. 9, 856-869.
47. Perez, M.A., Tanaka, S., Wise, S.P., Willingham, D.T., Cohen, L.G., 2008. Time-specific contribution of the supplementary motor area to intermanual transfer of procedural knowledge. J. Neurosci. 28, 9664-9669.
48. Provencher, S.W., 2001. Automatic quantitation of localized in vivo 1H spectra with LCModel. NMR Biomed. 14, 260-264. (Pubitemid 32611437)
49. Rango, M., Cogiamanian, F., Marceglia, S., Barberis, B., Arighi, A., Biondetti, P., Priori, A., 2008. Myoinositol content in the human brain is modified by transcranial direct current stimulation in a matter of minutes: a 1H-MRS study. Magn. Reson. Med. 60, 782-789.
50. Riecker, A., Groschel, K., Ackermann, H., Schnaudigel, S., Kassubek, J., Kastrup, A., 2010. The role of the unaffected hemisphere in motor recovery after stroke. Hum. Brain Mapp. 31, 1017-1029.
51. Sabet, A., Sibbitt Jr., W.L., Stidley, C.A., Danska, J., Brooks, W.M., 1998. Neurometabolite markers of cerebral injury in the antiphospholipid antibody syndrome of systemic lupus erythematosus. Stroke 29, 2254-2260. (Pubitemid 28511941)
52. Sastre-Garriga, J., Ingle, G.T., Chard, D.T., Ramio-Torrenta, L., McLean, M.A., Miller, D.H., Thompson, A.J., 2005. Metabolite changes in normal-appearing gray and white matter are linked with disability in early primary progressive multiple sclerosis. Arch. Neurol. 62, 569-573. (Pubitemid 40489887)
53. Seitz, R.J., Hoflich, P., Binkofski, F., Tellmann, L., Herzog, H., Freund, H.J., 1998. Role of the premotor cortex in recovery from middle cerebral artery infarction. Arch. Neurol. 55, 1081-1088. (Pubitemid 28367233)
54. Seitz, R.J., Azari, N.P., Knorr, U., Binkofski, F., Herzog, H., Freund, H.J., 1999. The role of diaschisis in stroke recovery. Stroke 30, 1844-1850. (Pubitemid 29411825)
55. Sharma, N., Baron, J.C., Rowe, J.B., 2009. Motor imagery after stroke: relating outcome to motor network connectivity. Ann. Neurol. 66, 604-616.
56. Sharma, N.K., McCarson, K., Van Dillen, L., Lentz, A., Khan, T., Cirstea, M.C., 2011. Primary somatosensory cortex in chronic low back pain - a H-MRS study. Journal of Pain Research 4, 143-150.
57. Shelton, F.N., Reding, M.J., 2001. Effect of lesion location on upper limb motor recovery after stroke. Stroke 32, 107-112. (Pubitemid 32063832)
58. Shibuya, M., 2009. Brain angiogenesis in developmental and pathological processes: therapeutic aspects of vascular endothelial growth factor. FEBS J. 276, 4636-4643.
59. Siegel, G.J.B., Agranoff, B.W., Albers, G.W., Fisher, S.K., Uhler, M.D., 2005. Basic Neurochemistry: Molecular, Cellular and Medical Aspects, 7th ed. Academic Press, Oxford, UK. Vol.
60. Stepniewska, I., Preuss, T.M., Kaas, J.H., 1993. Architectonics, somatotopic organization, and ipsilateral cortical connections of the primary motor area (M1) of owl monkeys. J. Comp. Neurol. 330, 238-271. (Pubitemid 23095325)
61. Suhy, J., Rooney, W.D., Goodkin, D.E., Capizzano, A.A., Soher, B.J., Maudsley, A.A., Waubant, E., Andersson, P.B., Weiner, M.W., 2000. 1H MRSI comparison of white matter and lesions in primary progressive and relapsing-remitting MS. Mult. Scler. 6, 148-155. (Pubitemid 30392111)
62. Swayne, O.B., Rothwell, J.C., Ward, N.S., Greenwood, R.J., 2008. Stages of motor output reorganization after hemispheric stroke suggested by longitudinal studies of cortical physiology. Cereb. Cortex 18, 1909-1922. (Pubitemid 352019912)
63. Tarkka, I.M., Kononen, M., Pitkanen, K., Sivenius, J., Mervaalat, E., 2008. Alterations in cortical excitability in chronic stroke after constraint-induced movement therapy. Neurol. Res. 30, 504-510. (Pubitemid 352008710)
64. van der Grond, J., Balm, R., Kappelle, L.J., Eikelboom, B.C., Mali, W.P., 1995. Cerebral metabolism of patients with stenosis or occlusion of the internal carotid artery. A 1H-MR spectroscopic imaging study. Stroke 26, 822-828.
65. van der Grond, J., Balm, R., Klijn, C.J., Kapelle, L.J., Eikelboom, B.C., Mali, W.P., 1996. Cerebral metabolism of patients with stenosis of the internal carotid artery before and after endarterectomy. J. Cereb. Blood Flow Metab. 16, 320-326. (Pubitemid 26062825)
66. Van Zijl, P.C., Barker, P.B., 1997. Magnetic resonance spectroscopy and spectroscopic imaging for the study of brain metabolism. Ann. N. Y. Acad. Sci. 820, 75-96. (Pubitemid 27343074)
67. Walker, P.M., Ben Salem, D., Giroud, M., Brunotte, F., 2006. Is NAA reduction in normal contralateral cerebral tissue in stroke patients dependent on underlying risk factors? J. Neurol. Neurosurg. Psychiatry 77, 596-600. (Pubitemid 43844581)
68. Wang, Y., Li, S.J., 1998. Differentiation of metabolic concentrations between gray matter and white matter of human brain by in vivo 1H magnetic resonance spectroscopy. Magn. Reson. Med. 39, 28-33. (Pubitemid 28028335)
69. Wannier, T., Schmidlin, E., Bloch, J., Rouiller, E.M., 2005. A unilateral section of the corticospinal tract at cervical level in primate does not lead to measurable cell loss in motor cortex. J. Neurotrauma 22, 703-717. (Pubitemid 40840384)
70. Ward, N.S., Newton, J.M., Swayne, O.B., Lee, L., Thompson, A.J., Greenwood, R.J., Rothwell, J.C., Frackowiak, R.S., 2006. Motor system activation after subcortical stroke depends on corticospinal system integrity. Brain 129, 809-819. (Pubitemid 43278241)
71. Watanabe, T., Shiino, A., Akiguchi, I., 2010. Absolute quantification in proton magnetic resonance spectroscopy is useful to differentiate amnesic mild cognitive impairment from Alzheimer's disease and healthy aging. Dement. Geriatr. Cogn. Disord. 30, 71-77.
72. Werring, D.J., Clark, C.A., Barker, G.J., Miller, D.H., Parker, G.J., Brammer, M.J., Bullmore, E.T., Giampietro, V.P., Thompson, A.J., 1998. The structural and functional mechanisms of motor recovery: complementary use of diffusion tensor and functional magnetic resonance imaging in a traumatic injury of the internal capsule. J. Neurol. Neurosurg. Psychiatry 65, 863-869. (Pubitemid 128710426)
73. Wise, S.P., di Pellegrino, G., Boussaoud, D., 1996. The premotor cortex and nonstandard sensorimotor mapping. Can. J. Physiol. Pharmacol. 74, 469-482. (Pubitemid 26261957)
74. Zemke, A.C., Heagerty, P.J., Lee, C., Cramer, S.C., 2003. Motor cortex organization after stroke is related to side of stroke and level of recovery. Stroke 34, e23-e28.