Functional and structural cortical characteristics after restricted focal motor cortical infarction evaluated at chronic stage - Indications from a preliminary study

Clinical Neurophysiology

Volumn 127, Issue 8, 2016, Pages 2775-2784

  Julkunen, Petro ^a,b   Määttä, Sara ^a,b   Säisänen, Laura ^a,b   Kallioniemi, Elisa ^a,b   Könönen, Mervi ^a   Jäkälä, Pekka ^a,b   Vanninen, Ritva ^a,b   Vaalto, Selja ^c,d  

^a KUOPIO UNIVERSITY HOSPITAL   (Finland)

^b UNIVERSITY OF EASTERN FINLAND   (Finland)

^c HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

^d AALTO UNIVERSITY   (Finland)

Author keywords

Diffusion weighted imaging; Infarction; Motor cortex; Motor evoked potential; Navigated transcranial magnetic stimulation; Stroke

Indexed keywords

ADULT; AGED; ARTICLE; BRAIN INFARCTION; CLINICAL ARTICLE; COMPUTER ASSISTED TOMOGRAPHY; CONTROLLED STUDY; DIFFUSION WEIGHTED IMAGING; FEMALE; HAND MUSCLE; HUMAN; ICD-10; MALE; MIDDLE AGED; MOTOR CORTEX; MOTOR EVOKED POTENTIAL; NERVOUS SYSTEM PARAMETERS; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; RESTING MOTOR THRESHOLD; RESTRICTED FOCAL CORTICAL INFARCTION; STROKE PATIENT; SUPPLEMENTARY MOTOR AREA; TRANSCRANIAL MAGNETIC STIMULATION; TRANSCRANIAL MAGNETIC STIMULATION SYSTEM; CEREBROVASCULAR ACCIDENT; DIAGNOSTIC IMAGING; ELECTROMYOGRAPHY; HEMISPHERIC DOMINANCE; NERVE CELL INHIBITION; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SKELETAL MUSCLE; THALAMUS;

AGED; BRAIN INFARCTION; DIFFUSION MAGNETIC RESONANCE IMAGING; ELECTROMYOGRAPHY; EVOKED POTENTIALS, MOTOR; FEMALE; FUNCTIONAL LATERALITY; HUMANS; MALE; MIDDLE AGED; MOTOR CORTEX; MUSCLE, SKELETAL; NEURAL INHIBITION; STROKE; THALAMUS; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 84974849229     PISSN: 13882457     EISSN: 18728952     Source Type: Journal    
DOI: 10.1016/j.clinph.2016.05.013     Document Type: Article

References (70)

1. Avirame K., Lesemann A., List J., Witte A.V., Schreiber S.J., Floel A. Cerebral autoregulation and brain networks in occlusive processes of the internal carotid artery. J Cereb Blood Flow Metab 2015, 35:240-247.
2. Brown C.E., Aminoltejari K., Erb H., Winship I.R., Murphy T.H. In vivo voltage-sensitive dye imaging in adult mice reveals that somatosensory maps lost to stroke are replaced over weeks by new structural and functional circuits with prolonged modes of activation within both the peri-infarct zone and distant sites. J Neurosci 2009, 29:1719-1734.
3. Bütefisch C.M., Netz J., Wessling M., Seitz R.J., Homberg V. Remote changes in cortical excitability after stroke. Brain 2003, 126:470-481.
4. Calautti C., Leroy F., Guincestre J.Y., Baron J.C. Dynamics of motor network overactivation after striatocapsular stroke: a longitudinal PET study using a fixed-performance paradigm. Stroke 2001, 32:2534-2542.
5. Calautti C., Leroy F., Guincestre J.Y., Marie R.M., Baron J.C. Sequential activation brain mapping after subcortical stroke: changes in hemispheric balance and recovery. Neuroreport 2001, 12:3883-3886.
6. Chen J.L., Schlaug G. Resting state interhemispheric motor connectivity and white matter integrity correlate with motor impairment in chronic stroke. Front Neurol 2013, 4:178.
7. Chen R., Tam A., Butefisch C., Corwell B., Ziemann U., Rothwell J.C., Cohen L.G. Intracortical inhibition and facilitation in different representations of the human motor cortex. J Neurophysiol 1998, 80:2870-2881.
8. Cicinelli P., Pasqualetti P., Zaccagnini M., Traversa R., Oliveri M., Rossini P.M. Interhemispheric asymmetries of motor cortex excitability in the postacute stroke stage: a paired-pulse transcranial magnetic stimulation study. Stroke 2003, 34:2653-2658.
9. Clarkson A.N., Huang B.S., Macisaac S.E., Mody I., Carmichael S.T. Reducing excessive GABA-mediated tonic inhibition promotes functional recovery after stroke. Nature 2010, 468:305-309.
10. Cunningham D.A., Machado A., Janini D., Varnerin N., Bonnett C., Yue G., Jones S., Lowe M., Beall E., Sakaie K., Plow E.B. Assessment of inter-hemispheric imbalance using imaging and noninvasive brain stimulation in patients with chronic stroke. Arch Phys Med Rehabil 2015, 96:S94-103.
11. Danner N., Könönen M., Säisänen L., Laitinen R., Mervaala E., Julkunen P. Effect of individual anatomy on resting motor threshold-computed electric field as a measure of cortical excitability. J Neurosci Methods 2012, 203:298-304.
12. Demirtas-Tatlidede A., Alonso-Alonso M., Shetty R.P., Ronen I., Pascual-Leone A., Fregni F. Long-term effects of contralesional rTMS in severe stroke: safety, cortical excitability, and relationship with transcallosal motor fibers. NeuroRehabilitation 2015, 36:51-59.
13. Devanne H., Lavoie B.A., Capaday C. Input-output properties and gain changes in the human corticospinal pathway. Exp Brain Res 1997, 114:329-338.
14. Di Lazzaro V., Oliviero A., Profice P., Saturno E., Pilato F., Tonali P. Motor cortex excitability changes within 8 hours after ischaemic stroke may predict the functional outcome. Eur J Emerg Med 1999, 6:119-121.
15. Dijkhuizen R.M., Singhal A.B., Mandeville J.B., Wu O., Halpern E.F., Finklestein S.P., Rosen B.R., Lo E.H. Correlation between brain reorganization, ischemic damage, and neurologic status after transient focal cerebral ischemia in rats: a functional magnetic resonance imaging study. J Neurosci 2003, 23:510-517.
16. Eliassen J.C., Boespflug E.L., Lamy M., Allendorfer J., Chu W.J., Szaflarski J.P. Brain-mapping techniques for evaluating poststroke recovery and rehabilitation: a review. Top Stroke Rehabil 2008, 15:427-450.
17. Feydy A., Carlier R., Roby-Brami A., Bussel B., Cazalis F., Pierot L., Burnod Y., Maier M.A. Longitudinal study of motor recovery after stroke: recruitment and focusing of brain activation. Stroke 2002, 33:1610-1617.
18. Fridman E.A., Hanakawa T., Chung M., Hummel F., Leiguarda R.C., Cohen L.G. Reorganization of the human ipsilesional premotor cortex after stroke. Brain 2004, 127:747-758.
19. Gauthier L.V., Taub E., Perkins C., Ortmann M., Mark V.W., Uswatte G. Remodeling the brain: plastic structural brain changes produced by different motor therapies after stroke. Stroke 2008, 39:1520-1525.
20. Hagemann G., Redecker C., Neumann-Haefelin T., Freund H.J., Witte O.W. Increased long-term potentiation in the surround of experimentally induced focal cortical infarction. Ann Neurol 1998, 44:255-258.
21. Hallett M. Plasticity of the human motor cortex and recovery from stroke. Brain Res Brain Res Rev 2001, 36:169-174.
22. Hervé D., Molko N., Pappata S., Buffon F., LeBihan D., Bousser M.G., Chabriat H. Longitudinal thalamic diffusion changes after middle cerebral artery infarcts. J Neurol Neurosurg Psychiatry 2005, 76:200-205.
23. Hickmott P.W., Merzenich M.M. Local circuit properties underlying cortical reorganization. J Neurophysiol 2002, 88:1288-1301.
24. Hodics T., Cohen L.G., Cramer S.C. Functional imaging of intervention effects in stroke motor rehabilitation. Arch Phys Med Rehabil 2006, 87:S36-42.
25. Jang S.H., Seo J.P. Aging of corticospinal tract fibers according to the cerebral origin in the human brain: a diffusion tensor imaging study. Neurosci Lett 2015, 585:77-81.
26. Janssen A.M., Rampersad S.M., Lucka F., Lanfer B., Lew S., Aydin U., Wolters C.H., Stegeman D.F., Oostendorp T.F. The influence of sulcus width on simulated electric fields induced by transcranial magnetic stimulation. Phys Med Biol 2013, 58:4881-4896.
27. Janssen A.M., Oostendorp T.F., Stegeman D.F. The effect of local anatomy on the electric field induced by TMS: evaluation at 14 different target sites. Med Biol Eng Comput 2014, 52:873-883.
28. Jones T.A., Schallert T. Overgrowth and pruning of dendrites in adult rats recovering from neocortical damage. Brain Res 1992, 581:156-160.
29. Julkunen P., Säisänen L., Danner N., Niskanen E., Hukkanen T., Mervaala E., Könönen M. Comparison of navigated and non-navigated transcranial magnetic stimulation for motor cortex mapping, motor threshold and motor evoked potentials. Neuroimage 2009, 44:790-795.
30. Julkunen P., Ruohonen J., Sääskilahti S., Säisänen L., Karhu J. Threshold curves for transcranial magnetic stimulation to improve reliability of motor pathway status assessment. Clin Neurophysiol 2011, 122:975-983.
31. Julkunen P., Säisänen L., Danner N., Awiszus F., Könönen M. Within-subject effect of coil-to-cortex distance on cortical electric field threshold and motor evoked potentials in transcranial magnetic stimulation. J Neurosci Methods 2012, 206:158-164.
32. Julkunen P., Säisänen L., Hukkanen T., Danner N., Könönen M. Does second-scale intertrial interval affect motor evoked potentials induced by single-pulse transcranial magnetic stimulation?. Brain Stimul 2012, 5:526-532.
33. Kallioniemi E., Könönen M., Julkunen P. Repeatability of functional anisotropy in navigated transcranial magnetic stimulation - coil-orientation versus response. Neuroreport 2015, 26:515-521.
34. Kallioniemi E., Könönen M., Säisänen L., Gröhn H., Julkunen P. Functional neuronal anisotropy assessed with neuronavigated transcranial magnetic stimulation. J Neurosci Methods 2015, 256:82-90.
35. Kujirai T., Caramia M.D., Rothwell J.C., Day B.L., Thompson P.D., Ferbert A., Wroe S., Asselman P., Marsden C.D. Corticocortical inhibition in human motor cortex. J Physiol 1993, 471:501-519.
36. Le Bihan D., Breton E., Lallemand D., Grenier P., Cabanis E., Laval-Jeantet M. MR imaging of intravoxel incoherent motions: application to diffusion and perfusion in neurologic disorders. Radiology 1986, 161:401-407.
37. Li Y., Wu P., Liang F., Huang W. The microstructural status of the corpus callosum is associated with the degree of motor function and neurological deficit in stroke patients. PLoS One 2015, 10:e0122615.
38. Liepert J., Hamzei F., Weiller C. Motor cortex disinhibition of the unaffected hemisphere after acute stroke. Muscle Nerve 2000, 23:1761-1763.
39. List J., Hertel-Zens S., Kubke J.C., Lesemann A., Schreiber S.J., Floel A. Cortical reorganization due to impaired cerebral autoregulation in individuals with occlusive processes of the internal carotid artery. Brain Stimul 2014, 7:381-387.
40. Maeda F., Gangitano M., Thall M., Pascual-Leone A. Inter- and intra-individual variability of paired-pulse curves with transcranial magnetic stimulation (TMS). Clin Neurophysiol 2002, 113:376-382.
41. Malcolm M.P., Vaughn H.N., Greene D. Inhibitory and excitatory motor cortex dysfunction persists in the chronic poststroke recovery phase. J Clin Neurophysiol 2015, 32:251-256.
42. Manganotti P., Patuzzo S., Cortese F., Palermo A., Smania N., Fiaschi A. Motor disinhibition in affected and unaffected hemisphere in the early period of recovery after stroke. Clin Neurophysiol 2002, 113:936-943.
43. Mills K.R., Nithi K.A. Corticomotor threshold to magnetic stimulation: normal values and repeatability. Muscle Nerve 1997, 20:570-576.
44. Mittmann T., Luhmann H.J., Schmidt-Kastner R., Eysel U.T., Weigel H., Heinemann U. Lesion-induced transient suppression of inhibitory function in rat neocortex in vitro. Neuroscience 1994, 60:891-906.
45. Neumann-Haefelin T., Staiger J.F., Redecker C., Zilles K., Fritschy J.M., Mohler H., Witte O.W. Immunohistochemical evidence for dysregulation of the GABAergic system ipsilateral to photochemically induced cortical infarcts in rats. Neuroscience 1998, 87:871-879.
46. Peurala S.H., Muller-Dahlhaus J.F., Arai N., Ziemann U. Interference of short-interval intracortical inhibition (SICI) and short-interval intracortical facilitation (SICF). Clin Neurophysiol 2008, 119:2291-2297.
47. Pitcher J.B., Ogston K.M., Miles T.S. Age and sex differences in human motor cortex input-output characteristics. J Physiol 2003, 546:605-613.
48. Prashantha D.K., Sriranjini S.J., Sathyaprabha T.N., Nagaraja D., Pal P.K. Evaluation of the motor cortical excitability changes after ischemic stroke. Ann Indian Acad Neurol 2013, 16:394-397.
49. Rossini P.M., Altamura C., Ferreri F., Melgari J.M., Tecchio F., Tombini M., Pasqualetti P., Vernieri F. Neuroimaging experimental studies on brain plasticity in recovery from stroke. Eura Medicophys 2007, 43:241-254.
50. Rossini P.M., Burke D., Chen R., Cohen L.G., Daskalakis Z., Di Iorio R., Di Lazzaro V., Ferreri F., Fitzgerald P.B., George M.S., Hallett M., Lefaucheur J.P., Langguth B., Matsumoto H., Miniussi C., Nitsche M.A., Pascual-Leone A., Paulus W., Rossi S., Rothwell J.C., Siebner H.R., Ugawa Y., Walsh V., Ziemann U. 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 2015, 126:1071-1107.
51. Rothwell J.C., Hallett M., Berardelli A., Eisen A., Rossini P., Paulus W. Magnetic stimulation: motor evoked potentials. The International Federation of Clinical Neurophysiology. Electroencephalogr Clin Neurophysiol Suppl 1999, 52:97-103.
52. Säisänen L., Julkunen P., Niskanen E., Danner N., Hukkanen T., Lohioja T., Nurkkala J., Mervaala E., Karhu J., Könönen M. Motor potentials evoked by navigated transcranial magnetic stimulation in healthy subjects. J Clin Neurophysiol 2008, 25:367-372.
53. Säisänen L., Julkunen P., Niskanen E., Hukkanen T., Mervaala E., Karhu J., Könönen M. Short- and intermediate-interval cortical inhibition and facilitation assessed by navigated transcranial magnetic stimulation. J Neurosci Methods 2011, 195:241-248.
54. Schaechter J.D., Perdue K.L. Enhanced cortical activation in the contralesional hemisphere of chronic stroke patients in response to motor skill challenge. Cereb Cortex 2008, 18:638-647.
55. Schmidt S., Bathe-Peters R., Fleischmann R., Ronnefarth M., Scholz M., Brandt S.A. Nonphysiological factors in navigated TMS studies; confounding covariates and valid intracortical estimates. Hum Brain Mapp 2015, 36:40-49.
56. Shen J.M., Xia X.W., Kang W.G., Yuan J.J., Sheng L. The use of MRI apparent diffusion coefficient (ADC) in monitoring the development of brain infarction. BMC Med Imaging 2011, 11:2.
57. Shimizu T., Hosaki A., Hino T., Sato M., Komori T., Hirai S., Rossini P.M. Motor cortical disinhibition in the unaffected hemisphere after unilateral cortical stroke. Brain 2002, 125:1896-1907.
58. Sterr A., Dean P.J., Vieira G., Conforto A.B., Shen S., Sato J.R. Cortical thickness changes in the non-lesioned hemisphere associated with non-paretic arm immobilization in modified CI therapy. Neuroimage Clin 2013, 2:797-803.
59. Stroemer R.P., Kent T.A., Hulsebosch C.E. Neocortical neural sprouting, synaptogenesis, and behavioral recovery after neocortical infarction in rats. Stroke 1995, 26:2135-2144.
60. Swayne O.B., Rothwell J.C., Ward N.S., Greenwood R.J. Stages of motor output reorganization after hemispheric stroke suggested by longitudinal studies of cortical physiology. Cereb Cortex 2008, 18:1909-1922.
61. Takechi U., Matsunaga K., Nakanishi R., Yamanaga H., Murayama N., Mafune K., Tsuji S. Longitudinal changes of motor cortical excitability and transcallosal inhibition after subcortical stroke. Clin Neurophysiol 2014, 125:2055-2069.
62. Traversa R., Cicinelli P., Bassi A., Rossini P.M., Bernardi G. Mapping of motor cortical reorganization after stroke. A brain stimulation study with focal magnetic pulses. Stroke 1997, 28:110-117.
63. Traversa R., Cicinelli P., Oliveri M., Giuseppina Palmieri M., Filippi M.M., Pasqualetti P., Rossini P.M. Neurophysiological follow-up of motor cortical output in stroke patients. Clin Neurophysiol 2000, 111:1695-1703.
64. Vaalto S., Säisänen L., Könönen M., Julkunen P., Hukkanen T., Määttä S., Karhu J. Corticospinal output and cortical excitation-inhibition balance in distal hand muscle representations in nonprimary motor area. Hum Brain Mapp 2011, 32:1692-1703.
65. van Swieten J.C., Koudstaal P.J., Visser M.C., Schouten H.J., van Gijn J. Interobserver agreement for the assessment of handicap in stroke patients. Stroke 1988, 19:604-607.
66. Volz L.J., Hamada M., Rothwell J.C., Grefkes C. What makes the muscle twitch: motor system connectivity and TMS-induced activity. Cereb Cortex 2015, 25:2346-2353.
67. Ward N.S., Cohen L.G. Mechanisms underlying recovery of motor function after stroke. Arch Neurol 2004, 61:1844-1848.
68. Ward N.S., Brown M.M., Thompson A.J., Frackowiak R.S. Neural correlates of motor recovery after stroke: a longitudinal fMRI study. Brain 2003, 126:2476-2496.
69. Ward N.S., Newton J.M., Swayne O.B., Lee L., Thompson A.J., Greenwood R.J., Rothwell J.C., Frackowiak R.S. Motor system activation after subcortical stroke depends on corticospinal system integrity. Brain 2006, 129:809-819.
70. Wassermann E.M. Variation in the response to transcranial magnetic brain stimulation in the general population. Clin Neurophysiol 2002, 113:1165-1171.