Application and Progress of Real-time Interleaved Transcranial Magnetic Stimulation Functional Magnetic Resonance Imaging

MA Yi-qi, XIE Ruo-xi, ZHENG Zhong, MA Dan, WU Min

Abstract

Transcranial magnetic stimulation (TMS), as a non-invasive neuromodulation technique, has achieved certain results in the study of brain function localization, treatment of nervous and mental diseases, but its mechanism of action and physiological effects are difficult to be clarified. The signals in blood oxygenation level dependent functional magnetic resonance imaging (BOLD-fMRI) is capable of reflecting the activities of brain tissue neurons. TMS-fMRI combines the advantages of two techniques to monitor changes in excitability of the TMS stimulation site and the distal brain region with which it is functionally linked. In this review, we elaborates the advances, limitations and future expectations of real-time interleaved TMS-fMRI. From the perspective of application progress, in the field of brain functional connectivity network research, TMS-fMRI can observe the dynamic connection between brain networks with a resolution of 100 ms, which is an important progress in the exploration of time-specific functional connectivity of brain regions. However, the TMS-fMRI on spatial specificity of functional connectivity of brain regions is still unclear, and future studies can focus on this aspect. In addition, TMS-fMRI can assess the effect of TMS on the cerebral cortex and the interaction between brain regions, help us understand the neural mechanism behind attention control, and study the brain's processing of somatosensory sensation. Nevertheless, TMS-fMRI can only observe the correlation between excitability of different brain regions under the stimulation of TMS, but the mechanism of this phenomenon and whether the correlation between brain regions is specific needs more research. Futhermore, TMS-fMRI can also be used to study the pathogenesis and therapeutic effect of neurological and psychiatric diseases, and the effects of psychoactive compounds on brain regions. Nonetheless, currently TMS-fMRI is still difficult to be widely used in clinical practice, so more efforts are needed in the study of clinical indications of TMS-fMRI. There are two major technical problems of TMS-fMRI. One major problem is that it is difficult for TMS coils to accurately position specific areas of cerebral cortex in MRI scanner. Another major problem is that TMS coils affect the static magnetic field (B0), resulting in image artifacts, spatial distortion and local signal loss of echo-Planar (EP) images. Nowadays, researchers have solved the two major problems through continuous technical updates, but TMS-fMRI still has problems in parameter setting, user experience, simplicity and universality of application and other aspects, which is the direction of future technological progress.

 

Keywords: Interleavedtranscranial magnetic stimulation functional magnetic resonance imaging, Functional magnetic resonance imaging, Transcranial magnetic stimulation

 

Full Text:

PDF


References


BARKER A T， JALINOUS R， FREESTON I L. Non-invasive magnetic stimulation of human motor cortex. Lancet，1985，325(8437): 1106–1107.

HUANG Y Z， EDWARDS M J， ROUNIS E， et al. Theta burst stimulation of the human motor cortex. Neuron，2005，45(2): 201–206.

BOHNING D E， SHASTRI A， NAHAS Z， et al. Echoplanar bold fmri of brain activation induced by concurrent transcranial magnetic stimulation. Invest Radiol，1998，33(6): 336–340.

HAWCO C， ARMONY J L， DASKALAKIS Z J， et al. Differing time of onset of concurrent TMS-fMRI during associative memory encoding: a measure of dynamic connectivity. Front Hum Neurosci， 2017， 11: 404[2020-04-01]. https://www.frontiersin.org/articles/10.3389/fnhum. 2017.00404/full. doi: 10.3389/fnhum.2017.00404.

HAWCO C， VOINESKOS A N， STEEVES J K E， et al. Spread of activity following TMS is related to intrinsic resting connectivity to the salience network: a concurrent TMS-fMRI study. Cortex，2018，108: 160–172.

RUFF C C， DRIVER J， BESTMANN S. Combining TMS and fMRI: from ‘virtual lesions’ to functional-network accounts of cognition. Cortex， 2009，45(9): 1043–1049.

LEITAO J， THIELSCHER A， WERNER S， et al. Effects of parietal TMS on visual and auditory processing at the primary cortical level—a concurrent TMS-fMRI study. Cereb Cortex，2013，23(4): 873–884. LEITAO J， THIELSCHER A， TUNNERHOFF J， et al. Concurrent TMS-fMRI reveals interactions between dorsal and ventral attentional systems. J Neurosci，2015，35(32): 11445–11457.

HEINEN K， RUFF C C， BJOERTOMT O， et al. Concurrent TMS-fMRI reveals dynamic interhemispheric influences of the right parietal cortex during exogenously cued visuospatial attention. Eur J Neurosci，2011， 33(5): 991–1000.

SOLOMONHARRIS L M， RAFIQUE S A， STEEVES J K. Consecutive TMS-fMRI reveals remote effects of neural noise to the "occipital face area". Brain Res，2016，1650: 134–141.

RUFF C C， BESTMANN S， BLANKENBURG F， et al. Distinct causal influences of parietal versus frontal areas on human visual cortex: evidence from concurrent TMS-fMRI. Cereb Cortex，2008，18(4): 817–827.

MULLIN C R， STEEVES J K E. Consecutive TMS-fMRI reveals an inverse relationship in BOLD signal between object and scene processing. J Neurosci，2013，33(49): 19243–19249.

BESTMANN S， OLIVIERO A， VOSS M， et al. Cortical correlates of TMS-induced phantom hand movements revealed with concurrent TMS-fMRI. Neuropsychologia，2006，44(14): 2959–2971.

MCGREGOR K M， ZLATAR Z， KLEIM E， et al. Physical activity and neural correlates of aging: a combined TMS/fMRI study. Behav Brain Res，2011，222(1): 158–168.

RICHARDS L G， STEWART K C， WOODBURY M L， et al. Movement-dependent stroke recovery: a systematic review and meta-analysis of TMS and fMRI evidence. Neuropsychologia，2008，46(1): 3–11.

BESTMANN S， SWAYNE O， BLANKENBURG F， et al. The role of contralesional dorsal premotor cortex after stroke as studied with concurrent TMS-fMRI. J Neurosci，2010，30(36): 11926–11937.

DU J， HU J P， HU J Z， et al. Aberrances of cortex excitability and connectivity underlying motor deficit in acute stroke. Neural Plast， 2018， 1318093[2020-04-01]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6215555/. doi: 10.1155/2018/1318093.

CUNNINGHAM D A， MACHADO A， JANINI D， et al. Assessment of inter-hemispheric imbalance using imaging and noninvasive brain stimulation in patients with chronic stroke. Arch Phys Med Rehabil， 2015，96(4): S94–S103.

DU Z D， WANG R， PRAKASH R， et al. Transcranial magnetic stimulation in schizophrenia: the contribution of neuroimaging. Curr Top Med Chem，2012，12(21): 2452–2457.

LI X， LARGE C H， RICCI R， et al. Using interleaved transcranial magnetic stimulation/functional magnetic resonance imaging (fMRI) and dynamic causal modeling to understand the discrete circuit specific changes of medications: lamotrigine and valproic acid changes in motor or prefrontal effective connectivity. Psychiatry Res，2011，194(2): 141–148.

BOHNING D E， DENSLOW S， BOHNING P A， et al. A TMS coil positioning/holding system for MR image-guided TMS interleaved with fMRI. Clin Neurophysiol，2003，114(11): 2210–2219.

NAVARRO DE LARA L I， WINDISCHBERGER C， KUEHNE A， et al. A novel coil array for combined TMS/fMRI experiments at 3 T. Magn Reson Med，2015，74(5): 1492–1501.

NAVARRO DE LARA L I， TIK M， WOLETZ M， et al. High-sensitivity TMS/fMRI of the human motor cortex using a dedicated multichannel MR coil. NeuroImage，2017，150: 262–269.

YAU J M， JALINOUS R， CANTARERO G L， et al. Static field influences on transcranial magnetic stimulation: considerations for TMS in the scanner environment. Brain Stimul，2014，7(3): 388–393.

BUNGERT A， CHAMBERS C D， PHILLIPS M， et al. Reducing image artefacts in concurrent TMS/fMRI by passive shimming. Neuroimage， 2012，59(3): 2167–2174.

OH H， KIM J H， YAU J M. EPI distortion correction for concurrent human brain stimulation and imaging at 3T. J Neurosci Methods， 2019， 327: 108400[2020-04-01]. https://doi.org/10.1016/j.jneumeth.2019. 108400. doi: 10.1016/j.jneumeth.2019.108400.

COBOS SÁNCHEZ C， CABELLO M R， OLOZÁBAL Á Q， et al. Design of TMS coils with reduced Lorentz forces: application to concurrent TMS-fMRI. J Neural Eng， 2020， 17(1): 016056[2020-04-01]. https://iopscience.iop.org/article/10.1088/1741-2552/ab4ba2. doi: 10.1088/1741-2552/ab4ba2.


Refbacks

  • There are currently no refbacks.