Magnetic Fields in Noninvasive Brain Stimulation

91145 2013 NRO20210.1177/1073858413491145The NeuroscientistVidal-Dourado and others Article Magnetic Fields in Noninvasive Brain Stimulation The ...
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91145

2013

NRO20210.1177/1073858413491145The NeuroscientistVidal-Dourado and others

Article

Magnetic Fields in Noninvasive Brain Stimulation

The Neuroscientist 2014, Vol. 20(2) 112­–121 © The Author(s) 2013 Reprints and permissions: sagepub.com/journalsPermissions.nav DOI: 10.1177/1073858413491145 nro.sagepub.com

Marcos Vidal-Dourado1, Adriana Bastos Conforto2,3, Luis Otávio Sales Ferreira Caboclo1, Milberto Scaff2, Laura Maria de Figueiredo Ferreira Guilhoto1, and Elza Márcia Targas Yacubian1

Abstract The idea that magnetic fields could be used therapeutically arose 2000 years ago. These therapeutic possibilities were expanded after the discovery of electromagnetic induction by the Englishman Michael Faraday and the American Joseph Henry. In 1896, Arsène d’Arsonval reported his experience with noninvasive brain magnetic stimulation to the scientific French community. In the second half of the 20th century, changing magnetic fields emerged as a noninvasive tool to study the nervous system and to modulate neural function. In 1985, Barker, Jalinous, and Freeston presented transcranial magnetic stimulation, a relatively focal and painless technique. Transcranial magnetic stimulation has been proposed as a clinical neurophysiology tool and as a potential adjuvant treatment for psychiatric and neurologic conditions. This article aims to contextualize the progress of use of magnetic fields in the history of neuroscience and medical sciences, until 1985. Keywords neuroscience, magnetic fields, transcranial magnetic stimulation (TMS), brain stimulation

Introduction The search for noninvasive brain stimulation modalities has occurred throughout history. Hundreds of years ago, it was suggested that magnetism (circa 1000 BC) and electricity (circa 600 BC) might be effective for treatment of psychiatric and neurologic conditions. Over the centuries, transcranial stimulation (Fig. 1) of the central nervous system by use of electrical currents or magnetic fields has been used in different ways, ranging from animal electricity to electrical devices, from lodestones to electromagnetic coils. This historical review aims to contextualize the use of magnetic fields in noninvasive brain stimulation, until the development of transcranial magnetic stimulators by Barker and others (1985).

Greece, the Magnesia (Thessaly for some authors) with abundant magnetic minerals in the ground (Mottelay 1893). Lucretius (99-55 BC), in De Rerum Natura (On the Nature of Things), Book VI, wrote about the opposite effects of magnetic forces (Arnold and Potamian 1904): Oft from the magnet, too, the steel recedes, Repelled by turns and re-attracted close.

Petrus Peregrinus reported his observations about the direction of magnetic flux (Epistola 1269). He showed that magnetic lines were concentrated in opposite extremes of lodestone and named them magnetic “poles” in analogy 1

Electric Currents and Magnetic Fields There are different versions concerning the discovery of magnetism. Western versions attribute it to the shepherd Magnes. He observed that the nails of his sandals were attracted by stones on the ground. Another version associates magnetism to a region of uncertain location in

Department of Neurology and Neurosurgery, Division of Neurology, Universidade Federal de São Paulo (UNIFESP), São Paulo, Brazil 2 Department of Neurology, Universidade de São Paulo (USP), São Paulo, Brazil 3 Instituto de Ensino e Pesquisa, Hospital Israelita Albert Einstein, Morumbi, São Paulo, Brazil Corresponding Author: Marcos Vidal-Dourado, Universidade Federal de São Paulo (UNIFESP), Rua Botucatu, 740 Vila Clementino, CEP 04040-000, São Paulo, Brazil. Email: [email protected]

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Figure 1.  Transcranial stimulation with the general faradization method (Cowen 1900, p. 51, Fig. 28). Courtesy of Wellcome Library, London.

to the Earth’s pole, “Magnetic North pole and South pole” (Arnold and Potamian 1904). Concepts about polarity, electrostatic and magnetic forces; properties of magnetic materials and medical applications of lodestones were compiled by William Gilbert, Queen Elizabeth I’s physician in De Magnete, magneticis que corporibus, et de magno magnete tellure: Physiologia nova, plurimis et argumentis & experimentis demonstrate (1600) (Mottelay 1893). Magnetic fields have properties of attraction and repulsion on specific materials. Lines of magnetic force determine the magnetic flux. Until the 19th century, electricity and magnetism have been described as distinct phenomena. However, this view began to change in May 1802, when the Italian amateur physicist, Gian Domenico Romagnosi, observed that a magnetic needle could be deviated by the influence of a voltaic pile. He published this observation in Ristretto dei Foglietti Universali, Trento/Italy (Romagnosi 1802). In 1819, Danish physicist Hans Christian Oersted also observed that a magnetic needle compass could be deflected by the influence of an electric current (Althaus 1860; Oersted 1820). Oersted

hypothesized that there are magnetic fields in space surrounding the electric currents. Faraday as well as the Frenchmen Arago, Andre-Marie Ampère, Jean-Baptiste Biot, and Felix Savart conceived the concept that electricity and magnetism are interactive phenomena, between 1820 and 1822 (Ampère 1820, 1826; Haüy 1821). Faraday and Henry reported on electromagnetic induction as follows: “a brief electric current in copper coil generating a time-varying magnetic field which induces a new electric current in nearby conductors.” However, it was only Faraday who announced the discovery of induction of electric currents by time-varying magnetic fields in 1831 (Faraday 1832; Kaempffert 1950). In 1833, the Russian physicist Heinrich Friedrich Emil Lenz observed that “the direction of the electric current induced by the magnetic field is opposite to the electric current flow that produces it.” Later, this phenomenon was called “Lenz’s law” (Lenz 1834). Magnetic fields are categorized as static magnetic fields and time-varying magnetic fields. Static magnetic field is constant over time and can be generated by permanent magnets or electromagnetic coils with direct electric current (DC). Electromagnetic coils with alternating current (AC) produce time-varying magnetic fields. These fields are named DC and AC magnetic fields, respectively.

Development of Electromagnetic Coils Electric current generators were developed during the 17th century, but coils able to produce magnetic fields only emerged in the 19th century. Coils, also known as electromagnets, are devices that generate electromagnetic fields. They consist of coils of electric current conducting wires with one or more turns around an imaginary axis. Ampère and Arago created spiral and helical magnetic coil models, from December 1820 to June 1822 (Ampère 1822, 1826; Barral 1854). William Sturgeon (1824) built the first U-shaped coil with a winding spiral core to generate DC magnetic fields (Fig. 2) (Sturgeon 1825). Henry (1827, 1828) improved Sturgeon’s electromagnet by insulating its wiring with silk thread, and increasing the number of magnetic coils to augment the intensity of the magnetic field (Henry 1830, 1831). In 1832, Hippolyte Pixii developed the first AC magnetic field device with two coils and a permanent horseshoe magnet (Fig. 3). A mechanical generator produced AC magnetic fields, with a hand crank attached to the base of the horseshoe magnet. When the position was changed, it reversed the electric and magnetic polarities (Pixii and others 1832).

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Figure 2.  Direct electric current device to induce magnetic fields, built by William Sturgeon (Trans Soc Arts 1825, 43: Plate 3, Fig. 13).

Electric Currents in Brain Stimulation Scribonius Largus (circa 46 AD) applied electricity from live torpedo fish, on the scalp of patients with headaches. This procedure was reported to induce torpor and transient local pain. In the 1050s, the physician Ibn-Sidah prescribed the electrical properties of live catfish to treat epilepsy (Kellaway 1946). Electrical stimulation for medical purposes became more popular in the 18th century (Le Roy 1755). In 1752, Charles Le Roy applied DC electrical stimulation, a non– time-varying current, in a patient with rheumatic paralysis. Le Roy reported pain relief and improvement in paralysis. On December 6, 1753, Le Roy tried to treat another patient named Granger, with amaurosis due to optic neuritis. Granger was submitted to DC electrical stimulation through a wire encircling his head (Fig. 4). This wire was connected to three metallic plates (electrodes) that were positioned on the supraorbital and occipital areas, and on the right leg (Le Roy 1755). The patient described a descending flame that quickly appeared in front of his eyes. Nonetheless, he did not recover visual acuity.

The Neuroscientist 20(2)

Figure 3.  AC magnetic fields device built by Hippolyte Pixii. Courtesy of Wellcome Library, London.

Giovanni Aldini (1762-1834), Luigi Galvani’s nephew, performed DC stimulation over his own head evoking different responses: . . . First of all, the fluid (electric discharge) took over a great portion of my brain, promoting a strong jerk, similar to a quivering against to the skull wall. I felt a strong sensation on my head and prolonged insomnia during several days . . . (Aldini 1804, p 216–7)

Aldini’s experiments are considered a landmark in electrical stimulation for treatment of psychiatric disturbances. The farmer Luigi Lanzarini had been diagnosed with “melancholy” and was admitted to the Sant’Orsola Hospital, Bologna/Italy in 1801. Aldini applied DC stimulation to the moistened scalp in the parietal area (Fig. 5) and Lanzarini’s mood improved. Invasive mapping of human brain functions started in 1874 with Roberts Bartholow, professor of the Medical College of Ohio (EUA) who performed AC electrical stimulation in the exposed brain of Mary Raferty, a 30-year-old Irish woman with a parietal epithelioma. The tumor caused a festering ulceration in the skull with an approximate diameter of 2 inches, only covered by

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Figure 5.  Luigi Lanzarini is represented in the upper right image (Aldini 1804). Courtesy of Wellcome Library, London.

Figure 4.  Electrostimulation scheme applied in the patient Granger by Le Roy (Hist Acad Roy Sciences 1755, p. 98). Credit of Bibliothèque Nationale de France (Gallica).

granulation tissue. Bartholow inserted needle electrodes in the parietal area eliciting sensory and motor responses contralateral to the stimulated cortex. After consecutive high-intensity AC electrical stimulation, the patient presented stertorous breathing and loss of consciousness, followed by a generalized tonic–clonic seizure that lasted for 5 minutes. She recovered her consciousness but had another epileptic seizure followed by mydriasis, convergent strabismus, right hemiplegia, coma, and death (Bartholow 1874a). The procedure was harshly criticized by the American Medical Association (Bartholow 1874b; Cincinnati Medical News 1874). In 1882, Italian neuropsychiatrist Ezio Sciamanna administered DC and AC electrical stimulation to the exposed brain of farmer Ferdinando Rinalducci. He had undergone neurosurgery after head trauma caused by a horse-fall. The craniotomy to remove bone fragments resulted in an open wound almost 3 cm wide in the parietal area. AC stimulation evoked lifting of the left eyelid, deviation of the left mouth angle and jaw occlusion. Abduction of the left thumb was elicited by DC stimulation with the negative electrode positioned over different points of the exposed cortex (Sciamanna 1882). Alberto Alberti, an Italian physician who immigrated to Argentina, worked at the Hospital de San Nicolás de los Arroyos, Buenos Aires, and cared for Severa Velo, a 45-year-old woman suffering from epileptic seizures. She had Luetic osteitis eroding the skull, causing frontal,

parietal, and occipital bone defects. Alberti mapped this patient’s exposed brain between September, 1883 and April, 1884. He observed that speech, coughing, crying, abdominal and limb muscle contractions could be evoked by DC cortical stimulation. In 1884, Alberto Alberti won a prize for his monograph Contribuición Al Estudio de las Localizaciónes Cerebrales y a la Patogénesis de la Epilepsia (Contribution to the Study of the Brain Localization and the Pathogenesis of Epilepsy). It was only in 1985 that this monograph was accidentally discovered in the library of the Universidad de Buenos Aires, Argentina, by the professor of pathological anatomy Dr. Diego Luis Outes and by medical student Luis Florián. Alberti’s work was then recognized for his contribution to brain mapping research (Contreras and Crocco 2005). In 1938, Italian neurologists Ugo Cerletti and Luigi Bini developed electroconvulsive therapy (ECT) to induce generalized tonic–clonic seizures through strong electrical discharges changing psychiatric treatment paradigms (Shepley and McGregor 1940). ECT is mainly prescribed for major depression. Electrical dosage and electrode placement can determine efficacy and adverse events of ECT. Unilateral treatment is associated with less severe cognitive side effects when compared to the bilateral procedure (Sackeim and others 1993). In 1954, Gualtierotti and Paterson mapped the motor cortex in baboons and humans through noninvasive electrical stimuli by saw-tooth or square wave pulses with intensities ranging from 2 to 70 mA, and frequencies ranging from 20 to 150 Hz. The cathode (negative pole) was placed over the upper motor area and the anode (positive pole) either in the middle or lower area. Pain was the most undesirable effect of this method leading to its disuse (Gualtierotti and Paterson 1954).

116 Brindley and Lewin (1968) implanted molded electrodes to fit the calcarine and neighboring cortex of the right hemisphere in a 52-year-old blind patient. Intracranial electrodes were connected by a cable to 80 extracranial radio receivers stimulated by transmission coils of an oscillator tuned with frequencies that ranged from 25 to 4000 Hz. Electric stimulation elicited light visual sensations for up to 2 minutes after the end of the stimulation. Transcranial electrical stimulation was developed by Merton and Morton (1980) using a capacitor that charged up to 2000 V. This capacitor discharged suprathreshold pulses (100–1200 V) lasting for 50 to 500 µs through electrodes on the scalp using a push/pull switch of double function, a Morse key (Holdefer and others 2006). Transcranial electrical stimulation elicited phosphenes after occipital stimulation, and motor responses in the contralateral hand after frontal stimulation (Merton and Morton 1980).

Magnetic Fields in Brain Stimulation A changing electric current can induce a magnetic field (Faraday 1832). Effects of magnetic fields generated by AC devices (AC magnetic fields) in the human nervous system were reported 141 years after the DC interventions described by Charles Le Roy in 1752. In 1893, Jacques Arsène d’Arsonval, a physician and former student of French neurophysiologist Claude Bernard, employed high-frequency (about 500 kHz) time-varying magnetic fields with different types of coils of various sizes (d’Arsonval 1893). In 1896, d’Arsonval reported his experience with noninvasive brain magnetic stimulation to the scientific French community: To measure the strong-current intensity (from 2 to 100 amperes) that passes over a great solenoid, I proceeded this way . . . (d’Arsonval 1896, p. 450) In a verbal communication done about one month ago to the Society, I had announced that intense alternating magnetic fields (of 110 volts, 30 amperes and 42 cycles per second) . . . (d’Arsonval 1896, p. 451)

The intensity of the electric current in d’Arsonval’s magnetic coil was measured using a galvanometer developed by him. d’Arsonval and others placed their heads inside the coil, and reported some unexpected effects: . . . did arise, when anybody put the head there (inside the coil), phosphenes and vertigo can be triggered in anybody until a syncope . . . (d’Arsonval, 1896, p. 451)

The Neuroscientist 20(2) In the 19th century, noninvasive magnetic stimulation focused on visual phenomena. Different investigators were able to evoke phosphenes with DC or AC magnetic fields. Bertold Beer (1902); Silvanus Thompson (1910), British Institution of Electrical Engineers; Knight Dunlap (1911), professor at John Hopkins University; Magnusson and Stevens (1911); Barlow and others (1947); Dieter Seidel (1968) and Lovsund and others (1980), summarized in Table 1. Historically, until the 20th century, greater developments in electric stimulation were reported, compared to those of magnetic stimulation. However, in 1976, magnetic stimulation started to be investigated by Anthony Barker (University of Sheffield, UK) and colleagues (Barker 1976; Barker and others 1979). Polson and others (1982) recorded muscle action potentials evoked by noninvasive magnetic stimulation in human motor nerves performed by a “prototype transcranial magnetic stimulation (TMS) device” (Fig. 6). Magnetic stimuli were delivered through a coil overlying the median nerve path and electrodes placed on the thenar eminence recorded muscle responses. In 1985, Barker presented TMS of the motor cortex at the London Congress of the International Federation of Clinical Neurophysiology (Fig. 7A). Barker and others (1985) described TMS as a contactless and noninvasive new neurophysiological tool (Fig. 7B). TMS discharges a brief pulse of electric current that flows through a magnetic coil placed on the scalp, generating a time-varying magnetic field where it induces an electric current flow in cortical neurons, consistent with the “law of electromagnetic induction and the Lenz’s Law” (Fig. 8). These currents produce an ion flux across the membrane on cortical axons, which is sufficiently powerful to depolarize the membrane triggering an action potential capable of inhibitory or excitatory neural responses (Barker and others 1985; Groppa and others 2012). Currently, magnetic fields induced by TMS can range from 1.0 to 4.0 Tesla (T) depending on setup parameters. The current intensity ranges from 4,000 A up to 10,000 A discharged in under 100 µs, with densities of electric current induced in the brain estimated at around 5.13 × 10−8 A/m2 (Wagner and others 2007). Pulse widths usually range between 70 and 280 µs (Toschi and others 2008). TMS can be applied by different kinds of coils: circular, double cone coil, and double circular, “figure-of-8” or “butterfly” coils with diameters ranging from 40 to 90 mm (Wagner and others 2007). The flux of the magnetic field applied by the figure-of-8 coil is more concentrated and more focused when compared to simple circular coils. TMS pulse in the figure-of-8 coil reaches a depth of

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Vidal-Dourado and others Table 1.  Timeline of the Visual Sensations Evoked by Magnetic Stimulation. Year

Author(s)

1902

Bertold Beer

1910

Silvanus Thompson

1911

Knight Dunlapa

1911

Magnusson and Stevens

1947

Barlow and others

1968

Seidel, Seidel and others

1980

Lovsund and others

Magnetic Stimuli

Method

15 to 30 amperes (A)

Coil positioned between 1 and 2 cm from the eyes and temporal region in own author AC magnetic fields 50 Hz, Thompson placed his head current intensity up to 180 between 2 large coils A and maximum magnetic with 32 turns measuring 8 intensity of 140 milliTesla inches in length by 9 inches (mT) in diameter AC magnetic fields, 25-60 Hz Coil with 8 inches length and and current intensity of 200 A elliptical in cross section, or 480 A the internal diameters being 10.5 inches and 9 inches DC and AC magnetic Five observers stimulated by stimulation with two coils, circular coil placed around 205 and 263 turns and current the head intensity from 17 A to 52 A (DC) and 5 A to 30 A (AC) Electric current intensity up Compared the results of to 1 mA and AC magnetic electric and AC magnetic fields, 10-90 Hz and 90 mT of stimulation on the retina, magnetic intensity temporal and occipital lobes AC magnetic stimulation, 10-60 Tested 30 blindfolded Hz and 20-100 mT students by toroidal coil placed around the head

AC magnetic fields, 10-50 Hz Magnetic stimulation on ranging from 0 to 40 mT, with the retina of 34 subjects, U-shaped coil including 2 blind patients

Results Flickering light sensations were stronger with greater current intensities, eye closure, also during eye and head movements Visual and gustatory sensations appeared 2 or 3 minutes after the end 480 A and 25 Hz was better than 200 A and 60 Hz to elicit flickering lights AC magnetic stimulation between 20 and 30 Hz showed to be optimal to evoke visual sensations replicating Dunlap’s findings Phosphenes, usually colorless, could be equally triggered by electric or magnetic stimulation when applied on retina, but were not elicited by occipital stimulation Description of 39 geometric patterns of phosphenes with frequency of stimulation ranging from 10 to 50 Hz, better between 15 and 30 Hz, also concluding that were elicited by retinal stimulation AC magnetic fields, 20-30 Hz and 10-12 mT were the most effective parameters to evoke visual sensations

a

The sample may have been inaccurately described by author. Probably, more than seven subjects were tested.

Figure 6.  Polson operating a transcranial magnetic stimulation device developed by Barker, Jalinous, and Freeston. Courtesy of Anthony Barker.

1.5 to 3 cm (Rossi and others 2009; Thielscher and Kammer 2004; Zangen and others 2005). Deep stimulation of subcortical areas (4–6 cm deep) can be achieved

with Hesed coils, “H-coil” (Bersani and others 2013; Roth and others 2007). In humans, TMS may be neuronavigated and can be associated with other tools such as electroencephalogram, functional magnetic resonance image, positron emission tomography, and transcranial Doppler ultrasonography (Ahdab and others 2010; Bashir and others 2011; Denslow and others 2005; Julkunen and others 2009; Rollnik and others 2002; Sack and Linden 2003; Sparing and others 2008; Thut and Pascual-Leone 2010). The combination of the good temporal resolution of TMS with the good spatial resolution of other noninvasive tools provides complementary information that is relevant to understand mechanisms of cortical reactivity and connectivity (Walsh and Cowey 2000). TMS has been demonstrated to be useful for assessment of motor and sensory pathways (Chen and others 2008) and has become a reliable neuromodulation tool (Grefkes and others 2010; Rossi and others 2009). In

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Figure 7.  (A) Anthony T. Barker during demonstration of transcranial magnetic stimulation (TMS) in London, 1985. (B) Anthony T. Barker (right), Ian L. Freeston (middle), and Reza Jalinous (left) presenting a TMS device in 1985. Courtesy of Anthony Barker.

Figure 8.  (A) Time-varying electric current flowing in the coil. (B) Time-varying magnetic field generated by electric current of the coil. (C) Electric current in cortical layers induced by magnetic field is opposite to the electric current flow produced by coil, “Lenz’s law.” (D) Depolarization of cortical neurons activating the corticospinal tract during transcranial magnetic stimulation.

addition, repetitive TMS (rTMS), characterized by rhythmic administration of pulses, has been proposed as adjuvant treatment for brain hyperexcitability syndromes (Lefaucheur 2006; Rotenberg 2010; Tassinari and others 2003), cerebrovascular disease (Dodick and others 2010; Hummel and Cohen 2006), movement disorders (Cantello 2002) and psychiatric disturbances such as depression (Loo and others 2008; Wassermann and Lisanby 2001).

Conclusion Over the centuries, electric and magnetic fields were believed to mediate biological responses. More recently, in the 20th century, noninvasive electric stimulation of the brain by time-varying magnetic fields flourished as a novel tool to understand brain function, and to treat neurologic and psychiatric conditions. The number of TMS studies has steadily grown since year 2000. The Food and

Vidal-Dourado and others Drug Administration has approved clinical use of TMS for treatment of depression and for mapping the motor cortex prior to neurosurgery (Rossi and others 2009). Ongoing research of other therapeutic applications of TMS is promising and based on strong scientific principles. Hundreds of years after its discovery, magnetic field now occupies a key position in neuroscience and medicine. Acknowledgment Our thanks to Prof. Anthony Barker for providing and authorizing the publication of his photographs, as well as to Marcelo Vianna De Lima, MD, for his valuable suggestions.

Declaration of Conflicting Interests The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding The author(s) received no financial support for the research, authorship, and/or publication of this article.

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