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Transcranial magnetic stimulation is an non-invasive method of neuromodulation. It uses magnetic field to induce generation of current for cortical stimulation. It can modulate the altered equilibrium in cortical excitability by magnetic field. Though it is famous for its application in treating psychiatric diseases, it has many other applications. Since its introduction in 1985, it has been used to check the integrity of motor pathway. With more understanding of the technique, it has been started to be used to check the integrity of other brain connections like speech and vision. Due to its ability of neuromodulation, it has also been used in cortical mapping in neurosurgery and neurological function rehabilitation.
Department of Neurosurgery, Queen Elizabeth Hospital, Hong Kong SAR, China
*Address all correspondence to: ymh_1985@yahoo.com.hk
1. Introduction
Transcranial magnetic stimulation, which is commonly abbreviated as TMS, is an non-invasive method of cortical stimulation by the use of electromagnetic field. It is a safe and effective method of neuromodulation. It has been used as a tool for checking the integrity of neuronal pathway for prognosis estimation after insult. It is an FDA approved treatment for several psychiatric diseases. It is now also used for rehabilitation of different neurological deficits, like motor rehabilitation and dysphasia. Its neuromodulation property is used in treating Parkinson’s disease and epilepsy. With the advancement in navigated TMS, it has been applied in cortical mapping, especially in neurosurgical operative planning.
The foundation of TMS is inspired by the ideas of Luigi Galvani, an Italian doctor, and Michael Faraday, a British physicist. The former first experimented the electrical stimulation of muscles and nerve fibers in the late eighteenth century while the latter in 1831 discovered that the relationship of electrical energy and magnetic field was reciprocal [1, 2]. Based on their theories, researchers had tried to study the effects of electromagnetic stimulation of brain, but most attempts were in vane due to technical limitations [3]. It was not until 1985 when Anthony Barker, a British engineer from the University of Sheffield, presented to the world about his invention of the first practical electromagnetic stimulation device for human use and his successful demonstration of the influence of electromagnetic stimulation on motor cortex of the human brain [4]. He and his associates placed a single Faraday coil to the scalp above the left cerebral motor strip of the subject to induce movement in the right hand. The outfit of the device was showed in Figure 1 [4]. Though this machine was slow in charging and the elevation of temperature of the coil limited its repetitive uses, it marked the start of modern TMS era.
Figure 1.
TMS machine invented by Dr. Anthony Barker [4].
Based on his inventions, researches were done to expand clinical applications of TMS. In 1995, the first pilot clinical trial was published reporting the results of TMS in treatment of depression [5]. In 2002, Canadian Association of Health approved the medical results and benefits of repetitive TMS (rTMS) [6]. The first The United States Food and Drug Administration (FDA) approval of TMS was given in 2008 in treatment of depression [3]. In 2009, FDA also approved TMS for cortical mapping. Since late 1990s, applications of TMS on neurological rehabilitation and treatment of different neurological diseases have been the focus of researches. TMS on motor rehabilitation and dysphasia is gaining more and more support from evidences in literature [7, 8, 9, 10]. With advancement in technology, introduction of navigated TMS provides more precise application of TMS in mapping and treatment.
There are several companies producing TMS-related equipment. The basic requirements of TMS service include a transcranial magnetic stimulator and coils. The examples of stimulators and coils are shown in Figures 2 and 3 [11, 12]. Circular coils are the basic type of coils. Figure-of-eight coils, or also known as butterfly coils, consist of two sets of coils arranged in a figure-of-eight fashion to make the strength of the magnetic field generated more focused when compared with traditional circular coils [13]. They are commonly used for treatment. Figure 4 shows the magnetic field strength induced by circular coil and figure-of-eight coil, respectively. Double-cone coil has two large cup-shaped windings positioned side by side. It is used to stimulate deep-seated structure. H-coil is a special designed coil that is also used to stimulate deep seated target. Apart from the appearance of the coils, treatment coils may also be equipped with specific cooling system for heat dissipation. Heat dissipation is particularly important in more aggressive treatment protocol like theta burst stimulation (TBS) protocol. Liquid cooling system and forced-air cooling system are the commonest cooling systems employed.
Figure 2.
Example of a transcranial magnetic stimulator [11].
Figure 3.
Different types of commonly used coils [12].
Figure 4.
Magnetic field strength induced by circular coil and figure-of-eight coil, respectively [13].
Some adjuncts can be used during TMS. Devices recording motor-evoked potential and electroencephalography (EEG) are frequently utilized. For navigated TMS (nTMS), sensor, localizers and software for MRI navigation are essential components on top of the basic requirements.
When current flows through the coil, magnetic field is generated by Ampere’s law. When the coil is placed over the scalp, the magnetic field strength generated passes through the scalp and skull then affects a nearby neuron. The magnetic field generates current in that particular neuron by Faraday’s law to cause depolarization of the neuron and propagation of action potential. If the neuron affected is located in motor cortex, the cascade process induced by TMS triggers a muscle movement which can be recorded by electromyography. This firing of impulse passes through the pathway to the end organ to produce a specific response. If this pathway is not intact, the impulse of action potential cannot reach the end organ, and no response can be produced. Figure 5 shows how TMS triggers the cascade [13]. The magnetic field strength generated ranged from 1.5 to 3 Tesla [14, 15]. Typical figure-of-eight coil is able to activate cortical neurons 1.5–3 cm beneath the scalp [16].
Figure 5.
Mechanism of action for TMS [13].
The method of pulse delivery leads to different neuromodulative outcomes. Single-pulse delivery produces immediate effect without causing any long-lasting effect, i.e., no after effect. This mode of pulse delivery is best used for cortical mapping and checking the integrity of neuronal pathways. Pattern TMS, including repetitive TMS (rTMS) and theta burst stimulation (TBS) pattern, on the other hand produces persistent effect beyond the stimulation period, i.e., it possesses after effect. This property is useful in provision of treatment and rehabilitation. rTMS is the delivery of a number of trains of repetitive stimulation at a fixed frequency. rTMS may have intervals of breaks in between trains of stimulation. rTMS delivered at 1 Hertz (Hz) is considered as low frequency, while rTMS delivered at 5 Hz or above is considered as high frequency. TBS pattern describes the delivery of 3 pulses at 50 Hz in every 200 microseconds. TBS pattern can be given in an intermittent fashion or in a continuous fashion. In the intermittent theta burst stimulation pattern (iTBS), 600 pulses of stimulations are given in 190 seconds in a fashion that a 2-second train of TBS stimulation followed by 8 seconds of break in every 10 seconds. In the continuous theta burst stimulation paradigm (cTBS), 600 pulses of stimulations are given in TBS pattern uninterruptedly for 40 seconds [16]. Neuromodulation makes use of the after effect which can be classified as excitatory or inhibitory. High-frequency rTMS and iTBS are found to have excitatory effects, while, on the contrary, low-frequency rTMS and cTBS are associated with inhibitory effects [16]. Figure 6 shows the summary of effects of rTMS and TBS [17].
Figure 6.
Summary of effects of rTMS and TBS [17].
The exact mechanism of how after effect of TMS helps in neuromodulation remains unclear. The most popular theory is interhemispheric balance theory, which is also known as interhemispheric rivalry theory [18, 19]. It is believed that each cerebral hemisphere inhibits its contralateral counterpart via the corpus callosum and the two sides are at a balanced status. When a pathology occurs in one side, this balance is disturbed. The inhibitory effect from the normal contralateral side will be uncounteracted in the lesioned side, leading to symptoms. Therefore, the aim of TMS is to restore the balance, either by inhibiting the normal contralateral side or stimulating the pathological side (Figure 7).
The contraindications are mostly related to the exposure of the magnetic field. The absolute contraindication is the presence of ferromagnetic implant in head and neck region, including tattoo on face. Though TMS can be one of the treatments for convulsion, known history of convulsion or suboptimally controlled convulsion, medications that potentially lower seizure threshold and alcoholism may be the exclusion criteria in some of the TMS centers [20]. Heating issue of metallic implant is another concern in patient selection. Eddy currents induced in conductive surface electrodes and implants can cause them to heat up [20]. The temperature increase depends on the shape, size, orientation, conductivity, and surrounding tissue properties of the electrode or implant as well as the TMS coil type, position, and stimulation parameters. Silver and gold are highly conductive and can produce heat excessively, potentially leading to skin burn or even brain tissue damage. Titanium tends to have low heating profile and is safe for TMS [20]. Although there are successful and uneventful TMS treatment done on pregnant ladies [20], pregnancy is still a concern in many centers. Pediatric safety is yet to be confirmed. A systematic review shows that TMS is apparently safe for pediatric patients aged 6 or above [21]. However, there is currently no enough data to demonstrate safety or hazard for individuals below 6 years of age [21].
Transient hearing impairment, convulsion, syncope, local scalp discomfort, headache and acute psychiatric changes have been reported as TMS-related risks [20]. The incidence for significant complications is low. Therefore, TMS is overall a safe procedure. Summary of potential risks is shown in Table 1 [20].
Side effect
Single-pulse TMS
Paired-pulse TMS
Low-frequency rTMS
High-frequency rTMS
Theta burst
Seizure induction
Rare
Not reported
Rare (usually protective effect)
Possible (1.4% crude risk estimate in epileptic patients; less than 1% in normals)
Possible (one seizure in a normal subject during cTBS) (see para 3.3.3)
Transient acute hypomania induction
No
No
Rare
Possible following left prefrontal stimulation
Not reported
Syncope
Possible as epiphenomenon (i.e., not related to direct brain effect)
Possible
Transient headache, local pain, neck pain, toothache and paresthesia
Possible
Likely possible, but not reported/addressed
Frequent (see para. 3.3)
Frequent (see para. 3.3)
Possible
Transient hearing changes
Possible
Likely possible, but not reported
Possible
Possible
Not reported
Transient cognitive/neuropsychological changes
Not reported
No reported
Overall negligible (see Section 4.6)
Overall negligible (see Section 4.6)
Transient impairment of working memory
Burns from scalp electrodes
No
No
Not reported
Occasionally reported
Not reported, but likely possible
Induced currents in electrical circuits
Theoretically possible, but described malfunction only if TMS is delivered in close proximity with the electric device (pace-makers, brain stimulators, pumps, intracardiac lines and cochlear implants)
Structural brain changes
Not reported
Not reported
Inconsistent
Inconsistent
Not reported
Histoxicity
No
No
Inconsistent
Inconsistent
Not reported
Other biological transient effects
Not reported
Not reported
Not reported
Transient hormone (TSH), and blood lactate levels change
There are many indications and may be grossly divided into two categories, namely therapeutic and non-therapeutic.
6.1 Therapeutic
6.1.1 Depression
Major depression is the first FDA approved indication for TMS. Multiple meta-analyses suggest that rTMS has a comparable effect to electroconvulsive therapy and antidepressants. It shows significant improvement in both helpless and anhedonic symptoms, with squared deviation from mean (SDM) 1.34 and 1.87, respectively [22]. The standard protocol is to deliver 10 Hz stimulation to left dorsolateral prefrontal cortex over 4–6 week in once-daily stimulation session. Other treatment protocols are also available [22]. iTBS is also proven to be as effective as the standard rTMS protocol with response rate of 36.7% when compared with 33.3% in standard rTMS protocol [23].
6.1.2 Obsessive and compulsive disorders (OCD)
OCD is another FDA approved indication for TMS. Multiple meta-analyses suggest rTMS is effective [24]. There are a couple of rTMS protocols with different targets like supplementary motor area, orbitofrontal cortex and dorsolateral prefrontal cortex [25, 26]. cTBS may also show a therapeutic effect in treating OCD at 6 weeks in terms of Yale–Brown Obsessive–Compulsive Scale and Hamilton Anxiety Rating Scale [27].
6.1.3 Smoking cessation
FDA clearance for TMS on smoking cessation was granted in 2020. It was based on a pivotal randomized controlled trial sponsored by a pharmacological company [28]. It used H coil to stimulate lateral prefrontal cortex and insula by facilitatory rTMS and achieved 28.0% continuous quit rate at week 18 compared to 11.7% in sham group [28]. With this landmark paper, more evidence was concluded from systematic reviews and meta-analyses in proving the effectiveness of rTMS on smoking cessation [29].
6.1.4 Schizophrenia
Stanford et al. suggested that negative symptoms appeared to be associated with hypoactivity of the dorsolateral prefrontal cortex of the brain while positive symptoms, particularly auditory hallucination, appeared to be associated with hyperactivity in the left temporo-parietal cortex [30]. Therefore, high-frequency rTMS at dorsolateral prefrontal cortex was suggested for negative symptoms and low-frequency rTMS at left temporo-parietal cortex for positive symptoms. Meta-analyses show the clinical improvement for the mentioned protocol with p value 0.002 [31, 32]. Goh et al. found that iTBS given to left dorsolateral prefrontal cortex was also effective in treating negative symptoms of schizophrenia with a p value of 0.004 [33].
6.1.5 Migraine with aura
Migraine with aura is another FDA approved indication which was announced in 2017. There are different protocols involving facilitatory stimulation over left dorsolateral prefrontal cortex or left motor cortex [34]. A meta-analysis shows effectiveness of TMS in treating migraine with aura [34]. Prophylactic inhibitory rTMS at vertex in patients with known migraine regardless of the presence of aura apparently also reduces migraine median frequency by 12 days per month and median intensity by 6 points [35].
6.1.6 Motor rehabilitation
Motor deficits after cranial or spinal insults are common. Stroke is one of the major causes. There is no standardized protocol. Inhibitory rTMS or cTBS over motor cortex of the non-lesional side and facilitatory rTMS or iTBS over motor cortex of lesional side are the common choices. Systematic reviews and meta-analyses show that rTMS and TBS are effective in improvement of motor function after insult of the brain with 95% confidence interval 0.24–9.71 for upper limb Fugl Meyer assessment [36, 37, 38].
Spinal insults, including trauma and post tumor excision, can also lead to motor deficits. Although there are no insults in brain, the corticospinal tract is affected by the spinal insult. A lot of studies support the use of TMS (rTMS or iTBS) in spinal insult patients, particularly incomplete spinal injury cases, and one of the studies shows improvement in lower limb motor score of 5 points with p value 0.004 compared to 1 point in sham group [39, 40, 41, 42, 43].
6.1.7 Parkinson’s disease
Parkinson’s disease is a relative common but disabling disease. Neuromodulation is one of the treatment approaches. Unlike deep brain stimulation, TMS provides a method of neuromodulation without the need of incision and anesthesia. Currently there are no consensus for the protocol TMS in managing Parkinson’s disease. There are different protocols available. Apparently motor symptoms of Parkinson’s disease improve after TMS [44, 45, 46, 47]. The Movement Disorder Society-Sponsored Revision of the Unified Parkinson’s Disease Rating Scale shows 6 points of improvement in Part III at 4 week post-treatment with p value 0.04 [45].
6.1.8 Other therapeutic uses
rTMS has been reported to be effective in improving nominal aphasia since 2005 [10]. It shows improvement by two standard deviations in Boston Diagnostic Aphasia Examination [10]. Since then, multiple trials have been conducted to test for the efficacy of rTMS on dysphasia. A recent systematic review confirmed that rTMS is an effective tool in post-stroke aphasia rehabilitation [9].
Tinnitus is one of disabling diseases that may not have any effective medical treatment. rTMS was found to be able to reduce the severity of tinnitus [48, 49, 50]. Over 16 points of improvement in Tinnitus handicap inventory scores at 6 months post-treatment was observed [49].
Spasticity is common after cerebral insults like stroke. A recent systematic review shows that TMS helps to improve Modified Ashworth Scale of the patients by 0.58 with p value <0.01 [51].
Neuropathic pain is one of the big topics in pain management, and TMS is shown to be an effective tool in managing those patients [52, 53].
rTMS is also shown to be effective in rehabilitation of dysphagia after stroke in recent published systematic reviews [54, 55]. The mean difference was −1.03 with p value <0.0001 in Penetration Aspiration Scale after completion of TMS [55].
There are some other fields that researchers and scholars are working on to see if TMS helps in the management. Examples include hemineglect, visual field impairment and epilepsy [56, 57, 58].
6.2 Non-therapeutic
6.2.1 Diagnostic and prognostic tool
Single-pulse TMS has been used to stimulate motor cortex to produce motor response since its first introduction in 1985 [1]. With the successful production of motor response, it proves the integrity of motor pathway, from neurons in motor cortex via corticospinal tract to muscle fibers. Disruption in any part along the tract causes failure of motor response production. This property has been used to evaluate the severity of the insult for both diagnosis and estimation of prognosis and to monitor the progress of rehabilitation [59, 60].
6.2.2 Cortical mapping
FDA first cleared the use of nTMS in cortical mapping in 2009. It can be used for both motor and language mapping. Intraoperative direct cortical stimulation has been the gold standard for cortical mapping. nTMS has been shown to have good accuracy (<10 mm) in motor mapping compared to direct cortical stimulation [61, 62]. The accuracy of nTMS is comparable or even better than functional MRI according to the results from some studies [61]. nTMS has been in used in preoperative planning in neurosurgical operations to maximize the resection of tumors in eloquent areas while preserving neurological functions [63, 64].
Connectome, the concept first introduced by Professor Sporns, is the connection matrix of human brain, which refers to the complete set of structural connections between neurons of the brain [65]. Diseases or cerebral insults cause disruption of the connectome. Diaschesis and vicaration of function, together with homeostatic mechanism of neuroplasticity, help to restore neurological functions which can be demonstrated by TMS in cortical remapping, i.e., detection of shift of stimulation hotspots compared with premorbid state. TMS, at the same time, is also considered as an non-invasive and safe tool to modulate the reconstruction of connectome after insult during the rehabilitation phase [18].
EEG is an non-invasive method of recording brain activity. TMS can produce TMS-related potential and induce different brain oscillation patterns in different parts of the brain [66]. EEG can be used to record TMS-induced activity when TMS stimulated a non-motor function-related circuit. This was first reported by Dr. Cracco in 1989 [67], but it was not in clinical use until recent decades. Concurrent use of TMS and EEG requires the use of specific TMS compatible EEG system due to risks of eddy current generation with traditional EEG electrodes and early saturation of traditional EEG amplifiers by TMS-induced current [68]. Either single pulse, paired pulses or pattern TMS can be used for different assessment purposes [68]. It is often used with functional MRI and navigated TMS to stimulate a specific target or circuit. Researchers have found that changes in TMS-EEG parameters in various psychiatric and neurological diseases [69]. This may lead to future development as a tool for diagnosis and monitor of treatment response [69].
Our department first introduced TMS service for neuro-rehabilitation for our patients with intracranial or spinal insults in 2018 in outpatient setting (Figure 8). To facilitate early inpatient rehabilitation, TMS service was introduced to our in-hospital patients in 2021 as a routine tool of rehabilitation. rTMS and TBS are employed for motor and dysphasia rehabilitation. Despite service cut during COVID-19 period, over 100 cases had received TMS service in our unit. We conducted a prospective pilot trial to compare the 6-month outcome in motor rehabilitation in stroke patients receiving iTBS to stroke patients receiving conventional physiotherapy. There were significant improvement in upper limb Fugl Meyer assessment score and limb power in patients completing ten sessions of iTBS on motor hotspot of the pathological hemisphere.
TMS is an non-invasive and safe tool for neuromodulation. It makes use of electromagnetic theory for stimulation of neuronal pathways. It has both diagnostic, prognostic and therapeutic applications. Its applications reflect and demonstrate the connectome inside brain.
Conflict of interest
The authors declare no conflict of interest.
Thanks
Special thanks to Dr. Cheung FC1, Dr. Poon TL1, Ms. Luk H2, Mr. Chee B2, Mr. Au A3 & colleagues involved in TMS service provision in Queen Elizabeth Hospital, HKSAR
Department of Neurosurgery, Queen Elizabeth Hospital, HKSAR.
Department of Physiotherapy, Queen Elizabeth Hospital, HKSAR.
Department of Speech Therapy, Queen Elizabeth Hospital, HKSAR.
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Written By
Ming-Him Yuen
Submitted: 27 December 2022Reviewed: 11 January 2023Published: 16 March 2023
Open access peer-reviewed chapter
