Noninvasive Brain Stimulation for Neurorehabilitation in Post-Stroke Patients: Comparison
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Please note this is a comparison between Version 4 by Catherine Yang and Version 3 by Jianguang Xu.

Noninvasive brain stimulation (NIBS) is a popular neuromodulatory technology of rehabilitation focusing on the local cerebral cortex, which can improve clinical functions by regulating the excitability of corresponding neurons. Increasing evidence has been obtained from the clinical application of NIBS in post-stroke patients, especially repetitive transcranial magnetic stimulation (rTMS) and transcranial direct current stimulation (tDCS). With advances in neuronavigation technologies, functional near-infrared spectroscopy, and functional MRI, specific brain regions can be precisely located for stimulation, which also presents the possibility that neuromodulation in post-stroke rehabilitation evolving from a single target to multiple targets, circuits and even networks. It is essential to review the findings of current research, discuss future directions of NIBS application, and finally promote the use of NIBS in post-stroke rehabilitation.

  • noninvasive brain stimulation
  • repetitive transcranial magnetic stimulation
  • transcranial direct current stimulation
  • transcranial focused ultrasound stimulation
  • transcutaneous vagus nervestimulation
  • post-stroke

1 Introduction

Stroke is the second-leading cause of death and the third-leading cause of disability in the world, and patients with stroke often suffer from functional impairments and deficits [1]. Motor weakness, sensory dysfunction, speech disturbances, dysphagia, unilateral neglect, cognitive dysfunction, and emotional impairment in post-stroke patients will need long-term rehabilitation [2][3][4]. The pathology of stroke involves both the focal neurologic deficits and the impairment of the neural circuit or brain networks [5][6]. As a means of physical factor therapy, noninvasive brain stimulation (NIBS) is a physical therapy that can regulate specific regions in brain by electrical, magnetic, or ultrasound stimulation in vivo, thereby modulating the excitability of neurons and multiple brain functions [7][8][9][10].

The effects of NIBS on physical functions in post-stroke patients have been reported by extensive clinical research [11][12]. However, due to the small sample size (less than 30 individuals) and unstandardized stimulation parameters of clinical studies [13][14][15], NIBS has not yet been included in the standardized treatment protocols for post-stroke rehabilitation.

2. Overview of Neuromodulation and NIBS

Neuromodulation technology refers to the use of implantable or non-implantable techniques (e.g., electrical, magnetic, or ultrasonic methods) to obtain therapeutic effects by changing the function or state of the nervous system. Through this approach, neurons or nerve signal transduction in adjacent or distant parts of the stimulation site are excited, inhibited, or regulated, thereby changing nerve function and improving the quality of life of patients [10][11][12]. Noninvasive neuromodulation techniques mainly include transcranial magnetic stimulation (TMS), transcranial electrical stimulation (tES), transcranial focused ultrasound stimulation (tFUS), transcranial unfocused ultrasound stimulation (tUUS), and transcutaneous vagus nerve stimulation (tVNS), among which repetitive transcranial magnetic stimulation (rTMS) and tDCS have proven effective in treating depression and pain [16][17][18]. Due to the specific advantages of being noninvasive, painless, safe, and cheap, in addition to having different parameters and treatment modes, NIBS shows broad prospects for development.

3. Technology and Research Situation of NIBS

3.1 TMS

TMS induces electrical currents in the brain through electromagnetic induction caused by an energized coil placed on the scalp that is a highly effective, painless, and noninvasive brain stimulation procedure, causing changes in excitability and plasticity of the targeted cortical neuronal populations. Magnetic fields can penetrate the scalp and skull and generate subthreshold- or suprathreshold-induced currents in the cerebral cortex concurrently, which depolarize neurons to generate action potentials to modulate and stimulate neuronal activity in target areas, and then can mostly affect the cortex function by synchronizing activity in related brain regions [15]. The regulatory effect of TMS on the cerebral cortex is influenced by factors such as coil shape, stimulation site, frequency, intensity, dosage (number of pulses, time, and duration) and other parameters.

3.2 tES

tES refers to physical therapy using electrical current to stimulate the brain, and it has gained popularity as a long-term therapy for patients with neurological disorders due to its convenience and potential effects on the brain network [19]. tES is an NIBS technique in experimental and clinical fields, including transcranial direct current stimulation (tDCS), transcranial alternating current stimulation (tACS), transcranial pulsed current stimulation (tPCS), and transcranial random noise stimulation (tRNS). Unlike tACS and tDCS, tPCS can intrigue randomly generated quadratic pulses, which may in turn increase endogenously generated brain oscillations, thereby facilitating the synchronization of deep brain structures with cortical activity [20]. Another promising alternative, tRNS, is a noisy electrical stimulation that increases cortical excitability through a random “noise” resonance [21]. Both of them are currently lacking in research, herein, the two most widely used tES techniques, tDCS and tACS, are summarized in the following section.

3.2.1 tDCS

tDCS mainly delivers low direct current to brain tissue through electrodes placed on the scalp. A constant electric field can impact the neurons in the cerebral cortex, thereby activating sodium-potassium pumps, calcium-dependent channels, and NMDA receptor activity to depolarize or hyperpolarize neuronal membrane potential [22][23], thus regulating neuronal activity and cortical excitability. However, unlike TMS, tDCS does not induce action potentials directly, whereby stimulation sites are more scattered. Its effects are thought to be achieved by altering the polarity of the membrane to change their probability of triggering action potentials, thus modulating the activation of neurons in the stimulated area. The parameters of tDCS have a decisive effect on its biological effects [24], including electrode shape, size, number, placement, polarity, stimulation intensity, duration, and stimulation waveform [24][25][26], in which slight changes will produce distinctly different effects [27].

3.2.2 tACS

tACS selectively enhances synaptic connectivity in neuronal circuits and synaptic plasticity by modulating the brain’s intrinsic endogenous neural oscillatory patterns and altering neurotransmitter levels [28]. Then, tACS ultimately improves the coordinated activity between local brain areas and brain regions [19][29]. Unlike TMS and tDCS, tACS completely avoids skin irritations [19]. It stimulates cortical neurons with sinusoidal or biphasic alternating current, modulates endogenous brain oscillations, and induces changes in synaptic plasticity to improve long-term brain function and depressive symptoms [30][31][32]. tACS uses different parameter stimulation electrodes, alternating current to stimulate specific targets. There are no acknowledged parameters, including stimulation frequency, intensity, phase, and duration, which may influence the effects of tACS.

3.3 tFUS

Ultrasound is an acoustic wave with a frequency greater than the hearing detection level of the human ear (>20 kHz); it is a mechanical wave generated by the vibration of a sound source and propagated through a compressed and expanded medium. tFUS, especially MR-guided focused ultrasound (MRgFUS) [8], combines the properties of deep focus targeting with high spatial resolution. It can stimulate deep and relatively superficial brain tissue in a precise, stable, focused, and noninvasive manner [33], and it has become one of the hot spots in basic and clinical research. The neuromodulatory effect of tFUS is mainly produced by the mechanical, thermal, and cavitation effects of ultrasound. By changing the frequency, intensity, pulse repetition frequency, pulse width, and duration of the ultrasound, the neurons at the stimulation site are activated or inhibited, thus regulating the neural function [9].

3.4 tVNS

tVNS involves applying electrical stimulation to peripheral vagus nerves. It transmits signals to the brain, causing changes in brain electrical activity and neurotransmitters, thereby modulating the functional activity of neurons [34]. tVNS can be mainly classified into two types: one is transcutaneous auricular vagus nerve stimulation (taVNS), which consists of electrically stimulating the auricular branch of the vagus nerve [35] (especially the auricular vessels); and the other is transcutaneous cervical vagus nerve stimulation (tcVNS), which consists of electrically stimulating the vagus nerve in the carotid sheath of the anterolateral neck [36]. tVNS exerts neuromodulatory effects, mainly by transmitting electrical stimulation to the brain, as well as increasing the plasticity of neural activity in the left prefrontal cortex, motor cortex, sensory cortex [37], right caudate nucleus, middle cingulate gyrus, and cerebellum [38]. It also enhances the plasticity of corticospinal motor pathways by activating widely projected neuromodulatory systems [39], ultimately increasing synaptic connections to muscle tissue and enhancing motor function [40].

4. Application of NIBS in Post-Stroke Rehabilitation

The use of NIBS in clinical practice is continuously developing, and its role and position in neurological rehabilitation have become increasingly prominent. Combined with adjunctive exercises, the application of NIBS has been extrapolated from the treatment of post-stroke motor dysfunction to sensory disorders, aphasia, dysphagia, unilateral neglect, cognitive dysfunction, depression, and even disorders of consciousness in the acute phase [41].

5. Current Status and Prospects

5.1 Effectiveness and Sustainability

Due to the heterogeneity of stroke injury location and the differences in the site, frequency, and duration of NIBS stimulation, it is difficult to use uniform criteria to judge the effectiveness and long-term efficacy of NIBS. However, there is a time-dependent effect of NIBS. In particular, cognitive function is significantly correlated with the number and duration of stimulation [42], which has been well-validated by recent studies. The session of commonly used treatments for NIBS reported in studies generally ranges from 5 to 20 (1–4 weeks), with follow-up usually after the end of treatment; the longest reported effective duration is 1 year [43].

5.2 Limitations and Future Trends

5.2.1. Small Samples, and Insufficient and Short Follow-Up Studies

Firstly, most studies on the application of NIBS in stroke only included small sample sizes, usually fewer than 30 individuals in each group [44][45][46]. Secondly, most of the current studies focused on motor function, speech, and cognitive function after stroke, mainly using rTMS and tDCS for intervention, while there are fewer studies investigating other functional impairments or using alternate NIBS techniques. Lastly, the follow-up duration after NIBS intervention in stroke patients was relatively short. Most studies assessed outcome indicators at the end of the intervention course, with the longest follow-up duration being 1 year [47].

5.2.2. Variety of Therapeutic Options and Prospects

In previous studies, M1 and DLPFC were most frequently used as single stimulation targets, while other brain regions such as supplementary motor areas, S1, dACC, thalamus, and hippocampus have been rarely reported. Some recent studies found that functional connections are damaged in post-stroke patients [48]. Stimulating one or two targets of the same neural circuit can modulate the whole circuit and achieve better functional recovery. PAS protocols [49] including within-system, cross-system, and cortico–cortical, which are composed of rTMS or peripheral stimulation, provide the concept and feasibility of bi-targeted neuromodulation, especially cortico–cortical PAS [50][51]. On the basis of the understanding of brain network doctrine and the summary analysis of existing studies, we believe that neuromodulation can go from single-target stimulation to two-target stimulation, and then to multi-target stimulation of the same circuit, eventually achieving stimulation of the whole brain network, which will be a future development direction. Animal experiments have reported similar approaches, such as modulation of touch being able to improve dexterous motor function [52].

Secondly, the protocols of these neuromodulation techniques in NIBS applied in stroke patients still need further optimization and can be combined into exponentially increasing stimulation programs depending on the choice of stimulation location, intensity, frequency, total time, and whether the stimulation is continuous or not [53], among which the treatment parameters that may lead to adverse effects need further modification [54]. The optimal parameters for TMS, tES, tFUS, and tVNS need to be more clearly defined and harmonized, and more comprehensive well-designed high-quality studies on the selection of optimal parameters are expected to provide evidence for the early development of standardized therapeutic protocols for various techniques of NIBS.

Lastly, most of the available studies focused on examining the therapeutic effects and neuromodulatory mechanisms of a particular technique in stroke, but the possibility of combining different NIBS techniques in stroke is often ignored. The main reasons for this may be the difficulty in assessing the effects of combining various techniques and the difficulty in explaining the interactions between the combinations. Given the differences in the mechanisms of various NIBS, the integration of different techniques may enhance the neuromodulatory effect, and different NIBS combination models have been reported in the literature for application in stroke patients, such as rTMS-tDCS and TMS-tACS [55]. There are also many studies combining NIBS with fMRI or EEG [51] techniques, for example, TMS-EEG, and TMS-fMRI can be used in combination to better individualize and synchronize neuromodulation in stroke patients, revealing possible remote top-down effect at the neural population level [56]. Furthermore, the combination of cathodal cerebellar tDCS and visual feedback was reported to improve balance control in a healthy population [57] and these findings should also be considered to deeply elaborate the mechanism of NIBS techniques in post-stroke dysfunction, which will be a future direction of development.

6. Conclusions

NIBS can be used as a therapeutic measure in post-stroke neurorehabilitation to promote recovery of functional impairment in patients when combined with movement training or other rehabilitation treatments. Overcoming the current limitations, NIBS can provide better and more precise modulation of neural circuits and neural networks, reduce adverse effects, and improve therapeutic effectiveness.

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