Evidence for interhemispheric imbalance in stroke patients as revealed by combining transcranial magnetic stimulation and electroencephalography

被引:69
作者
Casula, Elias Paolo [1 ,2 ]
Pellicciari, Maria Concetta [1 ]
Bonni, Sonia [1 ]
Spano, Barbara [3 ]
Ponzo, Viviana [1 ]
Salsano, Ilenia [3 ]
Giulietti, Giovanni [3 ]
Martino Cinnera, Alex [1 ]
Maiella, Michele [1 ]
Borghi, Ilaria [1 ]
Rocchi, Lorenzo [2 ]
Bozzali, Marco [3 ,4 ]
Sallustio, Fabrizio [5 ]
Caltagirone, Carlo [1 ]
Koch, Giacomo [1 ,5 ]
机构
[1] Santa Lucia Fdn, Dept Behav & Clin Neurol, Noninvas Brain Stimulat Unit, Rome, Italy
[2] UCL, UCL Queen Sq Inst Neurol, Dept Clin & Movement Neurosci, London, England
[3] Santa Lucia Fdn, Neuroimaging Lab, Rome, Italy
[4] Univ Sussex, Brighton & Sussex Med Sch, Brighton, E Sussex, England
[5] Tor Vergata Polyclin, Dept Neurosci, Stroke Unit, Rome, Italy
关键词
electroencephalography; interhemispheric dynamics; stroke; transcranial magnetic stimulation; MOTOR CORTEX EXCITABILITY; CORPUS-CALLOSUM; INHIBITION; RESPONSES; CIRCUITS; BRAIN; EEG; SYNCHRONIZATION; TOPOGRAPHY; MODULATION;
D O I
10.1002/hbm.25297
中图分类号
Q189 [神经科学];
学科分类号
071006 ;
摘要
Interhemispheric interactions in stroke patients are frequently characterized by abnormalities, in terms of balance and inhibition. Previous results showed an impressive variability, mostly given to the instability of motor-evoked potentials when evoked from the affected hemisphere. We aim to find reliable interhemispheric measures in stroke patients with a not-evocable motor-evoked potential from the affected hemisphere, by combining transcranial magnetic stimulation (TMS) and electroencephalography. Ninteen stroke patients (seven females; 61.26 +/- 9.8 years) were studied for 6 months after a first-ever stroke in the middle cerebral artery territory. Patients underwent four evaluations: clinical, cortical, corticospinal, and structural. To test the reliability of our measures, the evaluations were repeated after 3 weeks. To test the sensitivity, 14 age-matched healthy controls were compared to stroke patients. In stroke patients, stimulation of the affected hemisphere did not result in any inhibition onto the unaffected. The stimulation of the unaffected hemisphere revealed a preservation of the inhibition mechanism onto the affected. This resulted in a remarkable interhemispheric imbalance, whereas this mechanism was steadily symmetric in healthy controls. This result was stable when cortical evaluation was repeated after 3 weeks. Importantly, patients with a better recovery of the affected hand strength were the ones with a more stable interhemispheric balance. Finally, we found an association between microstructural integrity of callosal fibers, suppression of interhemispheric TMS-evoked activity and interhemispheric connectivity. We provide direct and sensitive cortical measures of interhemispheric imbalance in stroke patients. These measures offer a reliable means of distinguishing healthy and pathological interhemispheric dynamics.
引用
收藏
页码:1343 / 1358
页数:16
相关论文
共 60 条
[1]   Coherent oscillations in monkey motor cortex and hand muscle EMG show task-dependent modulation [J].
Baker, SN ;
Olivier, E ;
Lemon, RN .
JOURNAL OF PHYSIOLOGY-LONDON, 1997, 501 (01) :225-241
[2]   MR DIFFUSION TENSOR SPECTROSCOPY AND IMAGING [J].
BASSER, PJ ;
MATTIELLO, J ;
LEBIHAN, D .
BIOPHYSICAL JOURNAL, 1994, 66 (01) :259-267
[3]   Interhemispheric Control of Unilateral Movement [J].
Beaule, Vincent ;
Tremblay, Sara ;
Theoret, Hugo .
NEURAL PLASTICITY, 2012, 2012
[4]   Smallest real difference, a link between reproducibility and responsiveness [J].
Beckerman, H ;
Roebroeck, ME ;
Lankhorst, GJ ;
Becher, JG ;
Bezemer, PD ;
Verbeek, ALM .
QUALITY OF LIFE RESEARCH, 2001, 10 (07) :571-578
[5]   Targeting interhemispheric inhibition with neuromodulation to enhance stroke rehabilitation [J].
Boddington, L. J. ;
Reynolds, J. N. J. .
BRAIN STIMULATION, 2017, 10 (02) :214-222
[6]   Evaluating interhemispheric cortical responses to transcranial magnetic stimulation in chronic stroke: A TMS-EEG investigation [J].
Borich, Michael R. ;
Wheaton, Lewis A. ;
Brodie, Sonia M. ;
Lakhani, Bimal ;
Boyd, Lara A. .
NEUROSCIENCE LETTERS, 2016, 618 :25-30
[7]   Evaluation of differences in brain neurophysiology and morphometry associated with hand function in individuals with chronic stroke [J].
Borich, Michael R. ;
Neva, Jason L. ;
Boyd, Lara A. .
RESTORATIVE NEUROLOGY AND NEUROSCIENCE, 2015, 33 (01) :31-42
[8]   The reliability of commonly used electrophysiology measures [J].
Brown, K. E. ;
Lohse, K. R. ;
Mayer, I. M. S. ;
Strigaro, G. ;
Desikan, M. ;
Casula, E. P. ;
Meunier, S. ;
Popa, T. ;
Lamy, J. -C. ;
Odish, O. ;
Leavitt, B. R. ;
Durr, A. ;
Roos, R. A. C. ;
Tabrizi, S. J. ;
Rothwell, J. C. ;
Boyd, L. A. ;
Orth, M. .
BRAIN STIMULATION, 2017, 10 (06) :1102-1111
[9]   Extended brain disinhibition following small photothrombotic lesions in rat frontal cortex [J].
BuchkremerRatzmann, I ;
Witte, OW .
NEUROREPORT, 1997, 8 (02) :519-522
[10]   Relationship between interhemispheric inhibition and motor cortex excitability in subacute stroke patients [J].
Buetefisch, Cathrin M. ;
Wessling, Marion ;
Netz, Johannes ;
Seitz, Ruediger J. ;
Hoemberg, Volker .
NEUROREHABILITATION AND NEURAL REPAIR, 2008, 22 (01) :4-21