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rTMS for the Treatment of Depression: a Comprehensive Review of Effective

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rTMS for the Treatment of Depression:
a Comprehensive Review of Effective
Protocols on Right DLPFC

Ali Yadollahpour, Seyed Ahmad

Hosseini & Ahmad Shakeri

International Journal of Mental

Health and Addiction

ISSN 1557-1874

Int J Ment Health Addiction

DOI 10.1007/s11469-016-9669-z

1 23
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 Author's personal copy
Int J Ment Health Addiction
DOI 10.1007/s11469-016-9669-z

rTMS for the Treatment of Depression: a Comprehensive

Review of Effective Protocols on Right DLPFC

Ali Yadollahpour 1 & Seyed Ahmad Hosseini 2 &

Ahmad Shakeri 1

# Springer Science+Business Media New York 2016

Abstract Major depressive disorders (MDDs) are the most common and debilitating diseases
worldwide. Repetitive transcranial magnetic stimulation (rTMS) has been widely used as an
alternative or adjunctive treatment for different types of depression disorders, including drug-
resistant major depressions. Despite controversial findings on the therapeutic outcomes of this
technique, the general consent is developing this technique as an alternative treatment for
depression disorders. Notwithstanding one protocol of rTMS has been approved by FDA for
the acute treatment of major depression, studies are ongoing for finding more efficient
protocols. This study aimed to comprehensively overview the effective rTMS protocols
applied on left dorsolateral prefrontal cortex DLPFC for MDDs. The databases of PubMed
(1985–2015), Web of Sciences (1985–2015), and Google Scholar (1980–2015) were searched
using the set terms. The obtained results were screened for the relevant contents by two
authors, and the appropriate studies were selected for further review. The most widely used
protocols for depression are 1Hz for right and 10Hz for left DLPFC. In addition, the main
parameters of these protocols and the main neurophysiological mechanisms of two common
frequencies of 1 and 10 Hz are summarized. Different protocols of rTMS, particularly low
versus high frequencies, result in significantly different electrophysiological and
neurocognitive changes in the subject. Low frequency rTMS modulates frontal alpha power
asymmetry and high frequency protocols influence more broader regions and wider electro-
physiological characteristics of the brain.

Keywords Repetitive transcranial magnetic stimulation . Depression . Treatment .

Effective protocols . Right dorsolateral prefrontal cortex

* Ali Yadollahpour
yadollahpour.a@gmail.com

1
Department of Medical Physics, School of Medicine, Ahvaz Jundishapur University of Medical
Sciences, Golestan Blv., Ahvaz, Iran 6135715794
2
Nutrition and Metabolic Diseases Research Center, Ahvaz Jundishapur University of Medical
Sciences, Ahvaz, Iran
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Depression is a mental illness and neuropsychological dysfunction with relatively high

prevalence worldwide (Kazdin 2000; Marcus et al. 2012). The America Psychological Asso-
ciation reports that depression is the most common disease worldwide (Kazdin 2000; Lepine
and Briley 2011). World Health Organization predicts that by 2020, depression will be the
second largest cause of disability, after heart ischemic disease (Parikh and Lam 2001).
Neuroimaging, neurophysiological and hemodynamic images of brains of the depressed
patients have show that certain regions of the depressed brain involved in the development
of depression, including the dorsolateral prefrontal cortex (DLPF), subgenual cingulate gyrus,
and limbic nucleus (Jaracz and Rybakowski 2002). Functional images of the brain in depressed
patients have shown that in addition to electrical activity of different brain regions, different
functions of the brain are disturbed during depression. Infrared spectroscopy studies have
shown that metabolic activity of specific regions of the brain is modulated in depression
(Fukuda et al. 2003). Positron emission tomography (PET) has shown dysfunction of serotonin
hormone receptors (Drevets et al. 1999) and disturbance of glucose local metabolism in the
prefrontal cortex (Kling et al. 1986). In depression, excitability of the brain cortex generally
decreases (Fountoulakis et al. 2008). Therefore, one of the main approaches for treatment of
this disorder is increasing the excitability of brain cortex (Maeda et al. 2000).

Non-pharmacological Treatment

According to the guidelines of the American Psychiatric Association, current approved

treatment options for MDD include drug therapy, psychotherapy, drug therapy with psycho-
therapy, and electroconvulsive therapy (ECT) (Ali and Mahmud 2014; American Psychiatric
Association 2001). Despite using different antidepressants drugs, some portion of depressed
patients are resistant to drug treatment (Fava and Davidson 1996). Therefore, developing
nonpharmacologic treatments is necessary.
Developing nonpharmacologic techniques with no side effects and safety has always been
of interest to researchers and clinicians in any disorders. During the recent years, physical
agents such as electrical and magnetic fields, sound waves and laser have been extensively
used as alternative or adjunctive treatments for different disorders ranging from musculoskel-
etal and metabolic disorders, wounds, and neuropsychiatric disorders (Mostafa et al. 2015;
Yadollahpour and Rashidi 2014a, b; Yadollahpour et al. 2014b; Yadollahpour and Rezaee
2014; Zohre et al. 2015). This is the same for depression, particularly for drug-resistant cases.
In this regard, several therapeutic techniques have been developed for the treatment of various
types of depression (Aarre et al. 2003; Chistyakov et al. 2005a, b; Cooke 2003; Cordes et al.
2005). Electroconvulsive therapy (ECT), Vagus nerve stimulation (VNS), and deep brain
stimulation (DBS) are some of these techniques with promising potentials (Chistyakov et al.
2005a, b; Loo et al. 2011; Howland et al. 2011; Knotkova et al. 2012; Sparing and Mottaghy
2008). Although these techniques have shown therapeutic potentials for depression, they are
invasive and each of them has their own side effects. Transcranial direct current stimulation
(tDCS), repetitive transcranial magnetic stimulation (rTMS), and neurofeedback, which are
non-invasive, are relatively new developed techniques for the treatment of depression (Sparing
and Mottaghy 2008; Wagner et al. 2007). The rTMS has shown promising therapeutic
outcome for different types of depressive disorders especially for drug-treatment resistant
cases. This non-invasive technique is safe, cost-effective, and easy to use, which has been
reportedly capable of modulating the brain in neurophysiological, behavioral, and cognitive
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function levels. Various protocols of rTMS have been used for the treatment of depression.
These techniques used different stimulation parameters including frequency, field intensity,
number of total pulses, number of sessions per week, and number of total sessions. In addition,
site of stimulation is another important rTMS treatment parameters. The therapeutic efficacy of
these protocols and mechanisms of action are not fully understood. The present study aims to
comprehensively and descriptively overview the common rTMS protocols applied on DLPFC,
particularly left DLPFC, and the proposed mechanisms of action for depression treatment.

Methods

We searched the databases of PubMed (1985–2015), Web of Sciences (1985–2015), and

Google Scholar (1980–2015) using the following keywords: Bdepression treatment^, or
Bmajor depressive disorder^, and BrTMS^ or Brepetitive transcranial magnetic stimulation^,
and BDLPFC^ or Bdorsolateral prefrontal cortex^, and Bmechanisms of action^. The obtained
results were screened for the title and abstract by two authors, who came to consensus whether
the studies are related to the review. Because of the immense body of literature in this field, this
study was not aimed to provide a systematic review; but to provide a comprehensive and
descriptive overview of efficient rTMS protocols for depression treatment applied to DLPFC.
In addition, the main parameters of these protocols and the main neurophysiological mecha-
nisms of two common frequencies of 1 and 10 Hz are summarized.

Results and Discussion

Basic Principles of rTMS in Depression

Transcranial magnetic stimulation (TMS) is a common technique used in the field of non-
invasive brain stimulation since its first introduction by Barker et al. in 1985 (Barker et al.
1987). TMS operates based on the Faraday’s principle of electromagnetic induction. In this
technique, transmission of high intensity and rapidly rising electrical current (about 10 kA in
100–200 μs) through loops of wire in the form of figure-of-eight or circular coil induces a
time-varying magnetic field vertical to the plane of the coil, inducing an orthogonal electric
field which subsequently induces local current in conductive material surrounding coil such as
the brain. In this method, the magnetic field (up to 4 T) is used to enter extremely resistant
structures, such as the skull, while the electric field creates secondary currents leading to
neuronal activation (Wagner et al. 2007; Kobayashi and Pascual-Leone 2003; Hallett 2007).
Ionic current generated in the brain can cause neuronal depolarization and action potential
(Hoffman and Cavus 2002). Because of the nature of the brain and the fact that it is mainly
stimulated through electrical current, the brain is very sensitive to external electromagnetic
fields. The induced currents can modulate the neurophysiological functions of neural cells,
which in turn can lead to modulation of hemodynamic, physiological, and cognitive and
behavioral functions of different regions and systems of the brain. This technique has been
used in treatment of several disorders, such as epilepsy, anxiety, tinnitus, mania, addiction,
obsessive compulsive disorder, etc. (Howland et al. 2011; Hoffman and Cavus 2002;
Yadollahpour et al. 2014a; Höppner et al. 2011; George et al. 1999). In several studies,
these techniques are used to investigate the cause-effect relationships in cortical areas and
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alteration of different neurophysiological properties of brain, such as plasticity, motor

function, cortical excitability, and augmentation of synaptic strength (Hallett 2000;
Wassermann and Lisanby 2001).
Since the approval of rTMS application for the treatment of depression by FDA, various
protocols of stimulation have been investigated and evaluated for their therapeutic efficacy.
Some of these protocols showed high therapeutic efficacy. The main parameters influencing
the treatment outcome of rTMS in depression are frequency, magnetic field intensity (defined
as percentage of motor threshold of the subject), site of stimulation, number of pulse per
session, and number of sessions per day (Cooke 2003; Hoffman and Cavus 2002; Grunhaus
et al. 2000). The LDLPFC and RDLPFC are the most common sites for the rTMS applications.
The low frequencies rTMS (≤10 Hz) are usually applied on RDLPFC, whereas high frequen-
cies rTMS are used for LDLPFC (Berlim et al. 2011; Berman et al. 2000; Eche et al. 2012;
Eschweiler et al. 2000; McDonald et al. 2011).

rTMS Protocols for Depression Treatment

Table 1 presents the different protocols of rTMS applied on RDLPF. The DLPFC is the main
target for stimulation in depression. Findings of neuroimaging and neurophysiological studies
of the brain demonstrate that mood is regulated by a network of brain regions, including the
prefrontal, cingulate, parietal, and temporal cortical regions. This network is functionally
connected to different parts of the striatum, thalamus, and hypothalamus. Therefore, we can
expect that focal lesions in any section of this network can result in mood disturbances.
Furthermore, depressed patients show alterations in cerebral blood flow and metabolism in
different regions of this network, mainly the dorsolateral, orbitofrontal, and medial frontal
regions. One of the regions within the network responsible for depression is accessible by
rTMS and highly connected with other crucial nodes in the network, such as other prefrontal
and anterior cingulate regions is DLPFC. Therefore, the first line studies of rTMS for treatment
of depression focused on the DLPFC as a site of stimulation.
The mostly wide used protocol of rTMS for RDLPFC is 1Hz. The typical intensity range is
90 to 110 % of the subject’s motor threshold. The majority of the studies reviewed applied
2 weeks stimulations containing one session daily for five consecutive days per week. The
number of total pulses is usually 1200. In addition to these standard protocols, different
protocols have been proposed for the stimulation of RDLPFC, in which the majority increases
the number of total pulses or number of total sessions. It seems increasing the number of total
pulses or number of total sessions can increase the therapeutic efficacy. However, there are
somehow contradictory findings in this regard where increasing the number of total pulses or
total sessions did not result in better outcome (Aarre et al. 2003; McDonald et al. 2011;
Höppner et al. 2010). In addition, increasing the number of sessions or number of total pulses
can increase the patent’s agitation and stopping the treatment process. The site for stimulation
of DLPFC is based on the motor evoked potential (MEP) elicited by single pulse rTMS and
recording or observing the response of contralateral hand muscle. The site is usually located
5 cm anterior to the optimal location for producing MEPs in a hand muscle.
High frequency (10 Hz) focal stimulation of the LDLPF C is the most widely used
frequency for treatment of MDD. However, studies have shown that low frequency (1HZ)
stimulation on RDLPFC is also effective treatment. Currently, the therapeutic efficacy of
simultaneous stimulation affects different regions of brain such as right and left DLPFC,
stimulating other cortical and subcortical foci, and general stimulation of the whole brain are
Table 1 rTMS protocols applied on right dorsolateral prefrontal cortex (RDLPFC)

Study Study design Stimulation site/F No. of No. of No. of Sess./Sess. Total Assessment Outcome
(Hz)/Int.(%MT) sham active per week pulses
patients patients

Klein et al. 1999 DB placebo-controlled RDLPFC/1/%110 32 35 10/5 1200 HDRS 17- A significant difference in
itema responsec between two groups
MADRSb
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Lisanby et al. 2001 DB comparing active 10 RDLPFC/1/%110 12 12 10/5 16,000 HDRS Mean %reduction dHRSD: 20 %
(Hz) LDLPFC rTMS vs. in active group vs. Mean %
active 1 (Hz) RDLPFC reduction HRSD: 13 % in
rTMS vs. sham LDLPFC sham group
rTMS
Fitzgerald et al. 2003a, b DB placebo-controlled RDLPFC/1/100 % 20 20 10–20/5 After two 3000–6000 MADRS A significant difference in
weeks if the response between two groups
participant did not
respond, more two
weeks stimulation
Höppner et al. 2003 Comparing active 20 (Hz) RDLPFC/1/%110 10 10 10/5 1200 HDRS A significant pre- to
LDLPFC vs. active 1 MADRS post-treatment difference in
(Hz) RDLPFC vs. sham BDIe response, no significant inter-
LDLPFC rTMS group difference in response
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between P = .025
Kauffmann et al. 2004 DB, placebo-controlled RDLPFC/1 %110 5 7 10/5 1200 N.Af No significant difference in
response between two groups
P = 0.56
Isenberg et al. 2005 DB, randomized, parallel RDLPFC/1/%110 NA 14 20/5 1200 HDRS BAI Response rate: 32 %
group, comparing active
20 (Hz) LDLPFC rTMS
vs. active 1 (Hz)
RDLPFC rTMS
Januel et al. 2006 DB sham controlled RDLPFC/1/%90 16 11 16/4 1920 HDRS
Table 1 (continued)

Study Study design Stimulation site/F No. of No. of No. of Sess./Sess. Total Assessment Outcome
(Hz)/Int.(%MT) sham active per week pulses
patients patients

A significant difference in
response between two groups
P = 0.032
Stern et al. 2007 DB, randomized, parallel RDLPFC/1 %110 15 10 10/5 16,000 N.A A significant difference in
group, sham- controlled response between two groups
trial P = 0.028
Pallanti et al. 2010 DB, randomized RDLPFC/1/%110 20 20 15/5 6300 HDRS significant difference in response
between two groups
Aguirre et al. 2011 Randomized, controlled, two RDLPFC/1/%110 15 15 20/5 24,000 HDRS Both treatment groups
arm, clinical trial. significantly improved, but no
statistical differences
Eche et al. 2012 Single blind randomized RDLPFC/1/%100 – 8 20/5 1200 MADRS Post-treatment 50 %
comparing active 10 (Hz) antidepressant effect
LPF rTMS vs. active 1
(Hz) RDLPFC

F frequency, Int. intensity, sess. session, db double-blind

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a
Hamilton Depression Rating Scale
b
Montgomery-Asberg Depression Rating Scale
c
Response: ≥50 % reduction in depression ratings from baseline
d
Mean % reduction HRSD scores are expressed as mean changes from endpoint compared with baseline
e
Beck Depression Inventory
f
Not available
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under investigation. During recent years, several new techniques have been developed to
predict disease progression and treatment response to therapeutic interventions (Yadollahpour
2014; Norouzi et al. 2016). Accordingly, quantitative electroencephalography has been dra-
matically used for objective diagnosis of depression as well as predicting treatment response to
the interventions such as rTMS. This line of research promises significant advances for near
future in developing efficient and patient specific treatments.

rTMS Mechanisms of Actions in Depression Treatment

According to different neurophysiological and behavioral effects, there are distinctions be-
tween low (≤1 HZ) and high frequencies (>5 HZ) rTMS (Wassermann and Lisanby 2001).
Generally, low frequencies rTMS exert inhibiting effects, whereas high frequencies induce
excitatory effects (Hoffman and Cavus 2002; Maeda et al. 2000).
In depression, left dorsolateral prefrontal cortex (RDLPFC) shows hypoactivation or lower
metabolism compared with healthy brains. In contrast, right dorsolateral prefrontal cortex
(RDLPFC) undergoes hyperactivation or higher metabolism than the healthy brains. Hypo-
and hyper-activation is respectively manifested by higher and lower alpha activity in EEG.
Decreasing frontal alpha asymmetry reportedly is an index of recovering from depression.
Neurophysiological studies have found that depressed patients show an asymmetry of activa-
tion between left and right hemispheres in different regions of brains such as frontal, central,
temporal, superior frontolateral, and medial regions. These asymmetries are observed for
different frequency bands of EEG such as alpha, beta and delta bands. Left-to-right
asymmetries of the depressed patients are higher than the healthy subjects. For example,
depressed patients have increased alpha current density in the left hemisphere compared to the
right hemisphere (Allen et al. 2004; Deslandes et al. 2008; Gordon et al. 2010; Knott et al.
2011). We can say that in depression, the left-to-right balance of activity is disturbed. For the
treatment of depression with rTMS, considering the imbalanced asymmetry and based on the
theory of resonance, researchers usually use high frequency rTMS (higher than 10 Hz) to
LDLPFC or low frequency rTMS to RDLPFC to balance the left/right frontal asymmetry
(Fitzgerald et al. 2003b; Isenberg et al. 2005; Leuchter et al. 2013). Generally low frequency
rTMS reduces excitability of brain cortex, and high frequency rTMS increases excitability of
cortex (Hoffman and Cavus 2002; Eche et al. 2012). The main effects of rTMS exerting the
therapeutic effects are oscillatory rhythms of brains, modulating motor function, and altering
mood states (Howland et al. 2011; Wagner et al. 2007; Leuchter et al. 2013). Various studies
have been performed on the mechanisms of action of rTMS for the treatment of depression
(Valiulis et al. 2012; Gershon et al. 2003; Speer et al. 2000). The findings of the previous
studies have shown that different protocols of rTMS, particularly low versus high frequencies,
result in significantly different electrophysiological changes (Chistyakov et al. 2005a, b;
Howland et al. 2011; Speer et al. 2000; Kim et al. 2006; Hoogendam et al. 2010). However,
some studies comparing low and high frequencies rTMS on right and left DLPFC have failed
to show clinical outcome differences between the two protocols (Isenberg et al. 2005;
Fitzgerald et al. 2003a, 2009; Höppner et al. 2003). High frequency (≥10 Hz) rTMS on
DLPFC result in broader changes off EEG band power, such as increasing delta power on the
left hemisphere and alpha power growth on the right, as well as increasing of theta power in
parietal-occipital regions. In contrast, low frequencies (1 Hz) rTMS do not significantly alter
the power of basic EEG bands (Valiulis et al. 2012; Speer et al. 2000). However, some studies
have reported low frequencies rTMS modulate left-right alpha power asymmetrical indices of
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frontal area towards the right hemisphere, and this modification is correlated with the clinical
outcome. Various studies have shown that the neurobiological and electrophysiological mech-
anisms of the two common rTMS protocols (1 Hz RDLPFC vs. 10 Hz LDLPFC) are
significantly different. Low frequency rTMS modulates frontal alpha power asymmetry and
high frequency protocols influence more broader regions and wider electrophysiological
characteristics of the brain.
This study overviews the common protocols of rTMS applied on the DLPFC, focusing on
the main contributing parameters and mechanisms of action. The most widely used site of
stimulation for depression treatment is left and right DLPFC with corresponding 10 and 1 Hz
stimulation. The neurophysiological effects of low frequency rTMS are significantly different
from the high frequency stimulation. Low frequency rTMS modulates frontal alpha power
asymmetry, whereas high frequency protocols influence more broader regions and wider
electrophysiological characteristics of the brain.

Acknowledgments The authors would like to thank research deputy of Ahvaz Jundishapur University of
Medical Sciences who financially support the work. We also thank the faculty members of medical physics
department, school of medicine for their comment in conducting this study.

Compliance with Ethical Standards

Source of Funding This study was a part of MSc thesis in Medical Physics, and was financially supported by
Ahvaz Jundishapur University of Medical Sciences (Grant No.: 940189).

Disclosures Authors have equally contributed in the designing, conducting, and preparation of this manuscript
and have no conflict of interests on publishing this manuscript.

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