Brain Topological Correlates of Motor Performance Changes After Repetitive Transcranial Magnetic Stimulation

Repetitive transcranial magnetic stimulation (rTMS) influences the brain temporally beyond the stimulation period and spatially beyond the stimulation site. Application of rTMS over the primary motor cortex (M1) has been shown to lead to plastic changes in interregional connectivity over the motor system as well as alterations in motor performance. With a sequential combination of rTMS over the M1 and functional magnetic resonance imaging (fMRI), we sought changes in the topology of brain networks and specifically the association of brain topological changes with motor performance changes. In a sham-controlled parallel group experimental design, real or sham rTMS was administered to each of the 15 healthy subjects without prior motor-related dysfunctions, over the right M1 at a high frequency of 10 Hz. Before and after the intervention, fMRI data were acquired during a sequential finger motor task using the left, nondominant hand. Changes in the topology of brain networks were assessed in terms of global and local efficiency, which measures the efficiency in transporting information at global and local scales, respectively, provided by graph-theoretical analysis. Greater motor performance changes toward improvements after real rTMS were shown in individuals who exhibited more increases in global efficiency and more decreases in local efficiency. The enhancement of motor performance after rTMS is supposed to be associated with brain topological changes, such that global information exchange is facilitated, while local information exchange is restricted.

[1]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[2]  M. Hallett,et al.  Responses to rapid-rate transcranial magnetic stimulation of the human motor cortex. , 1994, Brain : a journal of neurology.

[3]  M. Hallett,et al.  Depression of motor cortex excitability by low‐frequency transcranial magnetic stimulation , 1997, Neurology.

[4]  J. Lorberbaum,et al.  Echoplanar BOLD fMRI of brain activation induced by concurrent transcranial magnetic stimulation. , 1998, Investigative radiology.

[5]  Á. Pascual-Leone,et al.  Interindividual variability of the modulatory effects of repetitive transcranial magnetic stimulation on cortical excitability , 2000, Experimental Brain Research.

[6]  Á. Pascual-Leone,et al.  Modulation of corticospinal excitability by repetitive transcranial magnetic stimulation , 2000, Clinical Neurophysiology.

[7]  S. Bestmann,et al.  Functional MRI of cortical activations induced by transcranial magnetic stimulation (TMS) , 2001, Neuroreport.

[8]  V Latora,et al.  Efficient behavior of small-world networks. , 2001, Physical review letters.

[9]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[10]  W. Paulus,et al.  Intra- and interindividual variability of motor responses to repetitive transcranial magnetic stimulation , 2002, Clinical Neurophysiology.

[11]  Karl J. Friston,et al.  Acute Remapping within the Motor System Induced by Low-Frequency Repetitive Transcranial Magnetic Stimulation , 2003, The Journal of Neuroscience.

[12]  Massimo Marchiori,et al.  Economic small-world behavior in weighted networks , 2003 .

[13]  S. Bestmann,et al.  On the synchronization of transcranial magnetic stimulation and functional echo‐planar imaging , 2003, Journal of magnetic resonance imaging : JMRI.

[14]  Sung Ho Jang,et al.  Facilitative effect of high frequency subthreshold repetitive transcranial magnetic stimulation on complex sequential motor learning in humans , 2004, Neuroscience Letters.

[15]  Walter Paulus,et al.  Toward Establishing a Therapeutic Window for rTMS by Theta Burst Stimulation , 2005, Neuron.

[16]  Karl J. Friston,et al.  Frequency specific changes in regional cerebral blood flow and motor system connectivity following rTMS to the primary motor cortex , 2005, NeuroImage.

[17]  J. Rothwell,et al.  Stimulus intensity and coil characteristics influence the efficacy of rTMS to suppress cortical excitability , 2006, Clinical Neurophysiology.

[18]  M. Hallett,et al.  Repetitive Transcranial Magnetic Stimulation–Induced Corticomotor Excitability and Associated Motor Skill Acquisition in Chronic Stroke , 2006, Stroke.

[19]  Danielle Smith Bassett,et al.  Small-World Brain Networks , 2006, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[20]  P. Haggard,et al.  Dorsal premotor cortex exerts state-dependent causal influences on activity in contralateral primary motor and dorsal premotor cortex. , 2008, Cerebral cortex.

[21]  Mark Hallett,et al.  High frequency rTMS modulation of the sensorimotor networks: Behavioral changes and fMRI correlates , 2008, NeuroImage.

[22]  J. Rothwell,et al.  Consensus: Motor cortex plasticity protocols , 2008, Brain Stimulation.

[23]  E. Bullmore,et al.  Human brain networks in health and disease , 2009, Current opinion in neurology.

[24]  P. Rossini,et al.  Consensus paper: Combining transcranial stimulation with neuroimaging , 2009, Brain Stimulation.

[25]  Alvaro Pascual-Leone,et al.  6-Hz primed low-frequency rTMS to contralesional M1 in two cases with middle cerebral artery stroke , 2010, Neuroscience Letters.

[26]  Simon B. Eickhoff,et al.  Modulating cortical connectivity in stroke patients by rTMS assessed with fMRI and dynamic causal modeling , 2010, NeuroImage.

[27]  Fabrizio De Vico Fallani,et al.  A graph-theoretical approach in brain functional networks. Possible implications in EEG studies , 2010, Nonlinear biomedical physics.

[28]  Jorge L. Armony,et al.  Effects of rTMS on Parkinson’s disease: a longitudinal fMRI study , 2011, Journal of Neurology.

[29]  M. Nitsche,et al.  Modulating functional connectivity patterns and topological functional organization of the human brain with transcranial direct current stimulation , 2011, Human brain mapping.

[30]  Nick S. Ward,et al.  Age-related changes in the topological architecture of the brain during hand grip , 2012, Neurobiology of Aging.