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Chapter 1

The Transcranial Magnetic Stimulation (TMS)


Device and Foundational Techniques
Alexander Rotenberg, Jared Cooney Horvath,
and Alvaro Pascual-Leone

Abstract
Transcranial magnetic stimulation (TMS) is a technique that is constantly evolving. Today, not only are
there a number of technical options to consider, but also a number of methodological and experimental
options. In this chapter, we supply a comprehensive overview of these many considerations. We first exam-
ine the physical and hardware foundations of TMS (including electromagnetic induction, stimulator char-
acteristics, and coil variations). Following this, we briefly outline the most utilized and efficacious
stimulation paradigms (including varied single and repetitive pulse patterns). Finally, we offer several prac-
tical procedural techniques universal to all devices and protocols.

Key words Transcranial magnetic stimulation, Coils, Hardware, Techniques

1 Introduction

Transcranial magnetic stimulation (TMS) is a neurophysiologic


technique that allows for noninvasive stimulation of the human
brain. Since its introduction close to 30 years ago [1], TMS, often
in conjunction with other neuroscientific methods, has been used
to study intracortical, cortico-cortical, and cortico-subcortical
interactions (for review: [2–4]), assess causal relations between
brain activity and behavior, and investigate the neurophysiologic
substrate of the symptoms and pathophysiology of various neuro-
logical and psychiatric disorders (for review: [2–4]). In addition,
repetitive transcranial magnetic stimulation (rTMS) has the capacity
to modulate brain activity beyond the duration of application and
holds therapeutic promise in a range of neuropsychiatric conditions
such as major depression, chronic pain, and epilepsy (for review:
[5–8]). In the past 5 years, two TMS devices and protocols have
received United States Food and Drug Administration (FDA) for
the treatment of medication-refractory depression (FDA approval

Alexander Rotenberg et al. (eds.), Transcranial Magnetic Stimulation, Neuromethods, vol. 89,
DOI 10.1007/978-1-4939-0879-0_1, © Springer Science+Business Media New York 2014

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K061053; FDA approval K122288) and one TMS device has been
approved for presurgical motor and speech mapping (FDA approval
K112881). In Europe several devices have been awarded European
CE Mark approval and are increasingly used for diagnostic and
therapeutic indications in clinical practice.

2 Electromagnetic Induction

TMS induces electrical currents in the brain via Faraday’s principle


of electromagnetic induction [9]. Put simply, Faraday discovered
that a pulse of electric current sent through a wire coil generates a
magnetic field. The rate of change of this magnetic field deter-
mines the induction of a secondary current in a nearby conductor.
With regard to TMS, an electric pulse, which grows to peak
strength and diminishes back to zero in a short period of time
(<1 ms), is sent through the conductive wiring within the TMS
coil. The rapid fluctuation of this current produces a magnetic field
perpendicular to the plane of the coil that similarly rises (up to
about 2.5 T) and falls rapidly in time. This rapidly fluctuating mag-
netic field passes unimpeded through the subject’s scalp and skull
and induces a current in the brain that flows in a plane parallel to
that of the coil but in the opposite direction of the original current
[5, 10]. Thus, TMS might be best conceptualized as “electrodeless
electric stimulation of the brain via electromagnetic induction.”
Electromagnetic induction adheres to the inverse cube law:
namely, the power of the magnetic field decreases exponentially as
the distance from the original current increases. Thus, the induced
current in the brain also decreases rapidly with distance from the
coil. Because of this, the majority of TMS stimulation is restricted
to superficial layers on the convexity of the brain (1.5–2 cm deep
from the scalp: see [11]). Although techniques do exist that allow
for deeper brain stimulation, with current TMS devices and coils,
superficial areas of the brain closer to the plane of the coil will
always be exposed to greater induced currents than deeper brain
regions [12–14].

3 Inside the Brain

Currents induced in the brain by TMS primarily flow parallel to the


brain’s cortical surface (when the coil is held tangentially to the
scalp). Exactly which neural elements are activated by TMS, how-
ever, remains unclear and might be variable across different brain
regions and different subjects ([14, 15]; for review: [16]).
Ultimately, the effect of TMS might be conceptualized as an inter-
action between the induced current and the affected brain tissue
(both in terms of its specific structure as well as in terms of its state
The Transcranial Magnetic Stimulation (TMS) Device and Foundational Techniques 5

of activation). Therefore it is important not only to consider the


anatomy of the neural structures, but also the state of activity in the
neural elements affected by the TMS.

4 TMS Hardware

The design and components of TMS devices are relatively straight-


forward and universal. Each machine consists of a main unit and a
stimulating coil. The main unit is composed of several components
(see Fig. 1):
– Charging system—The charging system generates the current
used to generate the magnetic field essential to TMS. A typical
charging system can generate 8,000 A within several 100 ms.
– One or more energy storage capacitors—Capacitors allow for
multiple energetic pulses to be generated, stored, and
discharged in quick succession (typical voltage rating of
7.5 kV). Multiple storage capacitors are required for repetitive
TMS protocols.
– Energy recovery circuitry—Energy recovery units allow for the
main unit to recharge following discharge.
– Thyristor—Thyristors are electrical devices capable of switching
large currents over a short period of time. In this case, the
Thyristor acts as the bridge between the capacitor and coil,
transferring 500 J between the two in less than 100 ms.
– Pulse-shape circuitry—Specialized circuitry can be used to gener-
ate either monophasic or biphasic pulses (for discussion: [17]).
The stimulating coil consists of one or more well-insulated
coils of copper wire (frequently housed in a molded plastic cover).
As current passes through these coils, varied patterns of magnetic
fields are generated which, in turn, generate a current in the oppos-
ing direction in any nearby conductor. Coils can be arrayed in a
variety of shapes and sizes (Fig. 2). The specific geometry of each

Fig. 1 Simplified circuit diagram of a single-pulse magnetic stimulator (V voltage


source, S switch, C capacitor, D diode, R resistor, T thyristor. Modified from [16])
6 Alexander Rotenberg et al.

Fig. 2 Schematic drawings of different types of TMS coils. (From left to right) Round Coil, Figure-of-Eight Coil,
Double Coil, H-Coil

coil determines the shape, strength, and overall focality of the


resultant induced electric field, and thus of the brain stimulation.
– Circular or Round Coil—The circular coil is the oldest and
simplest TMS coil design. A single, centrally located coil gen-
erates a spherical magnetic field perpendicular to the coil itself
(as such, a magnetic sink will occur in the middle). Although
not very focal, this type of coil is useful for protocols requiring
single pulses and peripheral stimulation.
– Figure-of-8 Coil (also referred to as Butterfly Coil)—Easily the
most recognizable and utilized of coil designs, the figure-of-8-
coil is formed by abutting two single, circular coils against one
another. Although the pattern from each individual coil may
be relatively non-focal, the combined magnetic field (summed
at the contact point between coils) is stronger than in sur-
rounding regions and is relatively easy to determine spatially.
This type of coil is often preferred for most clinical and aca-
demic uses of TMS—including repetitive and chronometric
measures. Although not fully experimentally confirmed, math-
ematical modeling suggests a small figure-of-8 coil (each wing
measuring 4 cm in diameter) can achieve a spatial resolution of
approximately 5 mm3 of the brain volume.
– H-Coil (see Chap. 3)—Recently obtaining FDA approval for the
treatment of medication-resistant depression, the H-Coil aims to
stimulate deeper, non-superficial cortical layers. This is achieved
by having a more complex coil design with several planes such
that the decay function of the generated magnetic field is less
steep and the current reaches deeper into the brain (although the
superficial cortical layers still are exposed to the strongest field).
Research suggests the H-Coil may be able to stimulate neural
structures up to 6 cm below the cortical surface [13].
Coils can be made to specification. As such, a number of exper-
imental coil designs have been created, including the horizontal
racetrack, the vertical racetrack, and small-animal sized coils.
The Transcranial Magnetic Stimulation (TMS) Device and Foundational Techniques 7

When used for a repetitive TMS paradigm, the conductive


material of the stimulation coils heat up potentially limiting the
duration of rTMS trains. Therefore, it is essential to keep coils cool
during stimulation. To this end, several coils have been developed
with an internal liquid or air cooling systems, as well as other
methods to offer heat sinks and reduce coil heating.

5 Pulse Waveforms

As noted above, specialized circuitry within the TMS main unit can
generate varied TMS pulse shapes (see Fig. 3).
– Monophasic—Monophasic pulses generate only unidirectional
voltage. As the initial course of voltage (positive) through a
coil would induce an opposing (negative) oscillation, in order
to generate a monophasic pulse a shunting diode and power
resistor must be used to dampen this natural cycle [18]. Due
to this pulse-shaping, monophasic pulses can only be delivered
singularly (unless multiple energy sources are utilized).
– Biphasic (Polyphasic)—Biphasic pulses generate full positive/
negative voltage oscillations [19]. This oscillation, in turn,
causes a rapid directional shift of the initial and induced cur-
rents. This type of pulse can be terminated after a single
cycle (biphasic) or after several oscillatory cycles (polyphasic
pulses: [20]).

6 Pulse Strength

The amount of voltage passed through the stimulating coil can be


adjusted up or down as needed. The strength of this initial current
contributes to the strength of the induced current (however, the
rate of change of the magnetic field amplitude is still tantamount in
stimulation). Devices often express output current as percent of

Fig. 3 Pulse-shaped graphs. (From left to right) Monophasic, biphasic, and polyphasic
8 Alexander Rotenberg et al.

maximal output, rather than as absolute current values as these are


different depending on the coils used. Frequently the applied stim-
ulation strength will be referenced in terms of a subject’s motor
threshold at a specified baseline.

7 Stimulation Paradigms

An important feature of TMS is the variability of its functional


parameters. Through different pulse patterns and durations, clini-
cians and researchers can examine a vast number of interesting
questions.
– Single-Pulse (see Chap. 5): Single-pulse TMS paradigms utilize
isolated, uniquely modulated pulses applied to a specific corti-
cal location. Single-pulse TMS paradigms are useful for the
diagnostic (for review: [21]) and exploratory measurement of
cortical reaction to each pulse [22–24]. Important parameters
to consider when utilizing single-pulse stimulation include
cortical location, pulse intensity, and response measurement.
When applied to the primary motor cortex, single-pulse stimu-
lation can induce contralateral muscle activity which can be
recorded by electromyography (EMG) as motor-evoked potentials
(MEPs). MEPs serve as a quantification of the TMS effect and can
be utilized both in mapping and intercessory protocols [25, 26].
When applied to the primary visual cortex, single-pulse stimulation
can produce phosphenes (subjective sensations of flashes of light)
in the visual field. Similar to MEPs, phosphenes can be used to
determine the threshold for cortical activation by TMS (for review:
[27]). The effects of single-pulse stimulation can also be recorded
using electroencephalography (EEG) as TMS-evoked potentials
(TEPs) which provide a metric of cortical reactivity.
– Paired-Pulse (see Chap. 6): Paired-pulse TMS paradigms utilize
two isolated pulses delivered in close succession. Each pulse can
be applied to the same cortical region or to separate regions and
used to assess their functionally connectivity [28]. In paired-
pulse paradigms, the cortical effects of the first (or condition-
ing) pulse can be measured via variations in the effect of the
second (or test) pulse. The effects of both pulses will depend on
their unique intensities and the duration of the inter-pulse
interval [29].
Paired-pulse paradigms are useful for examining cortical exci-
tation/inhibition ratio in healthy subjects and in patients.
Important parameters to consider when utilizing paired-pulse
stimulation include cortical location, conditioning and test pulse
intensities, and the inter-pulse interval duration [29].
The Transcranial Magnetic Stimulation (TMS) Device and Foundational Techniques 9

– Repetitive TMS (see Chap. 7): Repetitive TMS (rTMS) paradigms


utilize trains of pulses to induce cortical effects that outlast the
stimulation duration [6]. As with paired-pulse, the stimulation
intensity, the frequency of stimulation, the overall duration of
the trains and their pattern (continuous or intermittent burst
interrupted by pauses) determine the effect of each particular
rTMS protocol.
– Low-frequency rTMS (typically 1 Hz) applied for several min-
utes will typically lead to a suppression of cortical activity at the
stimulation location for a period lasting for about half the
duration of the stimulation train [30]. High-frequency rTMS
(typically >5 Hz) is typically applied in bursts interrupted by
pauses in order to comply with current safety guidelines and
prevent complications (particularly the induction of a seizure).
Such high-frequency or fast rTMS trains typically lead to an
increase in cortical activity at the stimulation location for a
period lasting for about half the duration of the stimulation
train [31].
rTMS allows clinicians to effect long lasting changes in cortical
reactivity and plasticity. Additionally, rTMS allows researchers to
modify cortical function during task performance, which can help
reveal causal relations between brain activity and behavior, and
might impair or enhance behavior and cognition [16].
In a specialized form of rTMS, theta-burst stimulation (TBS)
protocols deliver a novel pattern of stimulation that mimics neural
oscillatory patterns thought to correspond with effective cognitive
processing [32]. As other forms of rTMS, TBS protocols can be
used to induce cortical plasticity across both healthy subjects and
clinical pathologies and to modify brain activity for scientific and
clinical applications [33].
– Virtual Lesion (see Chap. 8): Virtual lesion paradigms aim to
temporarily disrupt cortical processing within specific cortical
regions via the introduction of extraneous noise. These
“lesions” can be generated in any number of ways: single pulses
generated at the proper time, low-frequency rTMS generated
for an effective duration, continuous TBS for 600 pulses, etc.
Virtual lesions allow researchers to examine both functional
connectivity and unique cognitive processing [34].
– Online and Off-Line Protocols: Online TMS protocols refer to
cognitive studies undertaken whilst TMS is being adminis-
tered. For instance, generating pulses during a language task
to disrupt speech production would be considered an “online”
paradigm [35].
Off-line TMS protocols refer to cognitive studies undertaken
after TMS has been administered. For instance, testing language
10 Alexander Rotenberg et al.

skills after 15 min of 1 Hz. TMS would be considered an “off-line”


paradigm [35].
– Chronometric Protocols: Chronometric paradigms seek to
explore when during a given task specific neural regions become
critical. Exclusively online and often single or paired-pulse,
chronometric designs contain arguably the greatest potential
for determining the time course of neural processing [34].
– Triple-Pulse Stimulation: Triple-pulse stimulation combines
TMS with electrical stimulators to examine corticospinal tract
integrity. By correctly timing a TMS pulse to M1 with two
peripheral stimulatory pulses (typically at Erb’s point and the
ulnar nerve), clinicians can accurately measure the percentage
of corticospinal fibers excited by the TMS pulse and thus cal-
culate the integrity of the corticospinal tract. The lower the
percentage, the more corticospinal tract compromise can be
assumed [36].
– Quadripulse Stimulation: Quadripulse stimulation is a unique
pattern of rTMS that can be utilized to explore and induce
neural plasticity [37]. During quadripulse stimulation, 300–
400 trains (separated by ~5 s) of four monophasic pulses are
delivered to the neural region of interest. If the interstimulus
interval of each of the four pulses is short (<15 ms), facilitation
is typically engendered for a period lasting 45–75 min. If the
interstimulus interval of each of the four pulses is long (25–
100 ms), depression is typically engendered for a period lasting
45–75 min.

8 Basic TMS Techniques

Although TMS devices and design necessarily differ between man-


ufacturers, there are several procedural techniques universal to
practitioners irrespective of which device is utilized.
– Activating the Pulse: The TMS pulse can typically be activated
in one of the three ways: via an activation button on the coil
handle, through an activation pedal controlled by the foot, or
through an activation button on the TMS device itself. Some
devices, in order to increase safety and prevent accidental pulse
discharges, actually require several of these steps to be done
together. Although many consider the button on the coil han-
dle to be the simplest, this configuration is not always available
(as some devices do not include an on handle button and others
must be disengaged when connecting coil trackers for neuro-
navigation). When utilizing the foot pedal, it is a good idea to
place the pedal in a location that is comfortable for your foot
(some practitioners prefer to use the ball of their foot, others
The Transcranial Magnetic Stimulation (TMS) Device and Foundational Techniques 11

the heel) and allows room for coil movement and repositioning.
Finally, as can be predicted, when utilizing the onboard activa-
tion button, it is advisable to have two operators: one to hold
the coil steady, the other to manipulate the buttons on the
device (this ensures no coil movement during stimulation).
– Localization (see Chap. 3): Stimulation localization can be
achieved in any number of ways. The first involves measuring
and marking the head (typically using a washable grease pencil)
according to the common 10–20 international system of EEG
electrode placement. Once established, the 10–20 landmarks
can be utilized to roughly determine cerebral regions and
develop small pulse grids to find specific neural locations.
Another localization technique involves utilizing a tight-fitting
swimming cap. With this, any number of scalp references can
be noted (such as vertex, inion, 10–20 points) using a dark and
easily observed marker. In addition, the swim cap allows for
the creation of small point-grids (again, using a marker) around
neural regions of interest to obtain specific localization. Finally,
several neuronavigation systems have recently been developed.
With these systems, anatomical landmarks are co-registered
with a participant’s structural MRI or PET scan and the head
and coil are both tracked in time and space utilizing either
infrared or ultra-frequency pulses. In addition to real-time nav-
igation, several of these systems allow for the tracking of each
pulse and the modeling of the stimulated region within the
brain itself (as determined via the anatomical scan).
– Long-Duration Stimulation Paradigms: When administering
long-duration stimulation protocols, it is common for the arm
and/or shoulder supporting the coil to tire. To combat this,
practitioners have tried a number of tricks—from hooking the
arm into a neck sling to allow for relaxation to locking the coil
into a T-Stand pressed against the participant’s scalp. As can be
imagined, nothing yet tried has proven ideal and, unfortu-
nately, arm fatigue may lead to subtle coil shifting over the
course of stimulation. Although there are no fast answers to
this issue, it is important to keep this in mind during long-
duration stimulation and try to combat fatigue and coil shift as
best as possible.

9 Conclusion

TMS has proven useful and efficacious in numerous medical and


research settings (as will be explored and expanded upon through-
out this book). As such, it appears to have staying power and will
soon likely complement the set of more established imaging and
brain mapping tools utilized in most hospitals and academic
12 Alexander Rotenberg et al.

laboratories. TMS is deceivingly simple, but appropriate utilization


requires a keen and up-to-date understanding of TMS devices as
they evolve, methodological techniques as they develop, and stim-
ulation paradigms as they emerge. Hopefully this and subsequent
chapters will facilitate these goals.

References

1. Barker AT, Jalinous R, Freeston IL (1985) field induced in the brain by transcranial mag-
Non-invasive magnetic stimulation of human netic stimulation using figure-8 and deep
motor cortex. Lancet 325:1106–1107 H-coils. J Clin Neurophysiol 24(1):31–38
2. Pascual-Leone A, Davey M, Wassermann EM, 14. Amassian VE, Eberle L, Maccabee PJ, Cracco
Rothwell J, Puri B (eds) (2002) Handbook of RQ (1992) Modelling magnetic coil excitation
transcranial magnetic stimulation. Edward of human cerebral cortex with a peripheral
Arnold, London nerve immersed in a brain-shaped volume con-
3. Rotenberg A (2010) Prospects for clinical ductor: the significance of fiber bending in
applications of transcranial magnetic stimula- excitation. Electroencephalogr Clin
tion and real-time EEG in epilepsy. Brain Neurophysiol 85(5):291–301
Topogr 22(4):257–266 15. Maccabee PJ, Amassian VE, Eberle LP, Cracco
4. Horvath JC, Perez JM, Forrow L, Fregni F, RQ (1993) Magnetic coil stimulation of
Pascual-Leone A (2011) Transcranial magnetic straight and bent amphibian and mammalian
stimulation: a historical evaluation and future peripheral nerve in vitro: locus of excitation. J
prognosis of therapeutically relevant ethical con- Physiol 460(1):201–219
cerns. J Med Ethics 37(3):137–143 16. Wagner T, Valero-Cabre A, Pascual-Leone A
5. Kobayashi M, Pascual-Leone A (2003) (2007) Noninvasive human brain stimulation.
Transcranial magnetic stimulation in neurol- Annu Rev Biomed Eng 9:527–565
ogy. Lancet Neurol 2(3):145–156 17. Peterchev AV, Jalinous R, Lisanby SH (2008)
6. Fitzgerald PB, Fountain S, Daskalakis ZJ A transcranial magnetic stimulator inducing
(2006) A comprehensive review of the effects of near-rectangular pulses with controllable pulse
rTMS on motor cortical excitability and inhibi- width (cTMS). Biomed Eng IEEE Trans
tion. Clin Neurophysiol 117(12):2584–2596 55(1):257–266
7. Valero-Cabré A, Pascual-Leone A, Coubard 18. Barker AT, Freeston IL, Jalinous R, Jarratt JA
OA (2011) Transcranial magnetic stimulation (1987) Magnetic stimulation of the human
(TMS) in basic and clinical neuroscience brain and peripheral nervous system: an intro-
research. Neurol Rev 167(4):291–316 duction and the results of an initial clinical
8. Najib U, Bashir S, Edwards D, Rotenberg A, evaluation. Neurosurgery 20:100–109
Pascual-Leone A (2011) Transcranial brain 19. Dantec (2003) Instruction manual. Dantec
stimulation: clinical applications and future Medical A/S, Skovlunde, DK
directions. Neurosurg Clin N Am 22(2):233 20. Sommer M, Alfaro A, Rummel M, Speck S,
9. Faraday M (1839) Experimental researches in Lang N, Tings T, Paulus W (2006) Half sine,
electricity, vol 1. Bernard Quaritch, London monophasic and biphasic transcranial mag-
10. Hallett M (2000) Transcranial magnetic stim- netic stimulation of the human motor cortex.
ulation and the human brain. Nature Clin Neurophysiol 117(4):838–844
406(6792):147–150 21. Chen R, Cros D, Curra A, Di Lazzaro V,
11. Deng ZD, Lisanby SH, Peterchev AV (2012) Lefaucheur JP, Magistris MR, Mills K, Rösler
Electric field depth–focality tradeoff in transcra- KM, Triggs WJ, Ugawa Y, Ziemann U (2008)
nial magnetic stimulation: simulation compari- The clinical diagnostic utility of transcranial
son of 50 coil designs. Brain Stimul 6(1):1–13 magnetic stimulation: report of an IFCN com-
12. Wagner TA, Zahn M, Grodzinsky AJ, Pascual- mittee. Clin Neurophysiol 119(3):504–532
Leone A (2004) Three-dimensional head 22. Muri RM, Vermersch AI, Rivaud S, Gaymard
model simulation of transcranial magnetic B, Pierrot-Deseilligny C (1996) Effects of
stimulation. Biomed Eng IEEE Trans 51(9): single-pulse transcranial magnetic stimulation
1586–1598 over the prefrontal and posterior parietal corti-
13. Roth Y, Amir A, Levkovitz Y, Zangen A (2007) ces during memory-guided saccades in
Three-dimensional distribution of the electric humans. J Neurophysiol 76(3):2102–2106
The Transcranial Magnetic Stimulation (TMS) Device and Foundational Techniques 13

23. Amassian VE, Cracco RQ, Maccabee PJ, (1997) Depression of motor cortex excitability
Cracco JB, Rudell AP, Eberle L (1998) by low‐frequency transcranial magnetic stimu-
Transcranial magnetic stimulation in study of lation. Neurology 48(5):1398–1403
the visual pathway. J Clin Neurophysiol 31. Guse B, Falkai P, Wobrock T (2010) Cognitive
15(4):288–304 effects of high-frequency repetitive transcranial
24. Thut G, Northoff G, Ives JR, Kamitani Y, magnetic stimulation: a systematic review. J
Pfennig A, Kampmann F, Schomer DL, Neural Transm 117(1):105–122
Pascual-Leone A (2003) Effects of single-pulse 32. Huang YZ, Edwards MJ, Rounis E, Bhatia KP,
transcranial magnetic stimulation (TMS) on Rothwell JC (2005) Theta burst stimulation of
functional brain activity: a combined event- the human motor cortex. Neuron 45(2):
related TMS and evoked potential study. Clin 201–206
Neurophysiol 114(11):2071–2080 33. Chen R, Udupa K (2009) Measurement and
25. Rothwell JC (1997) Techniques and mecha- modulation of plasticity of the motor system in
nisms of action of transcranial stimulation of humans using transcranial magnetic stimula-
the human motor cortex. J Neurosci Methods tion. Mot Control 13(4):442–453
74(2):113–122 34. Pascual-Leone A, Walsh V, Rothwell J (2000)
26. Chen R (2000) Studies of human motor physi- Transcranial magnetic stimulation in cognitive
ology with transcranial magnetic stimulation. neuroscience–virtual lesion, chronometry, and
Muscle Nerve Suppl 9:S26–S32 functional connectivity. Curr Opin Neurobiol
27. Merabet LB, Theoret H, Pascual-Leone A 10(2):232–237
(2003) Transcranial magnetic stimulation as 35. Terao Y, Ugawa Y (2006) Studying higher cere-
an investigative tool in the study of visual func- bral functions by transcranial magnetic stimula-
tion. Optom Vis Sci 80(5):356–368 tion. Suppl Clin Neurophysiol 59:9–17
28. Rothwell JC (1999) Paired-pulse investiga- 36. Ni Z, Müller-Dahlhaus F, Chen R, Ziemann U
tions of short-latency intracortical facilitation (2011) Triple-pulse TMS to study interactions
using TMS in humans. Electroencephalogr between neural circuits in human cortex. Brain
Clin Neurophysiol Suppl 51:113–119 Stimul 4(4):281–293
29. Currà A, Modugno N, Inghilleri M, Manfredi 37. Hamada M, Terao Y, Hanajima R, Shirota Y,
M, Hallett M, Berardelli A (2002) Transcranial Nakatani-Enomoto S, Furubayashi T, Matsumoto
magnetic stimulation techniques in clinical H, Ugawa Y (2008) Bidirectional long-term
investigation. Neurology 59(12):1851–1859 motor cortical plasticity and metaplasticity
30. Chen R, Classen J, Gerloff C, Celnik P, induced by quadripulse transcranial magnetic
Wassermann EM, Hallett M, Cohen LG stimulation. J Physiol 586(16):3927–3947

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