**4. rTMS in attention-deficit/hyperactivity disorder treatment**

ADHD, in the ICD-10 represented by hyperkinetic disorder, is one of the most common mental disorders among children, with a prevalence of 3–7% [81]. ADHD was long viewed as a childhood diagnosis; however, many studies in the last decades have demonstrated that symptoms persist to adulthood in up to 80% of patients [82]. The latest revision of the Diagnostic and Statistical Manual of Mental Disorders (DSM-V) reexamined the diagnostic criteria and allowed the classification of ADHD as a lifelong disorder with the condition of onset before the 12th year of life [55]. ADHD symptom heredity is considered to be as high as 75% [83]. Like many neuropsychiatric disorders, ADHD seems to be a result of the complex interplay of genetic and environmental factors and has been recently viewed as a neurodevelopmental disorder [81].

The three typical symptoms of childhood ADHD—attention deficit, hyperactivity, and impulsivity—are partially modified during the lifespan. In adulthood, feelings of internal restlessness, disorganization, and unrestrainability, and some behavioral difficulties, including impaired executive functions, prevail [84]. The treatment of ADHD in children as well as in adults is an ongoing topic in psychiatry. There are several possible treatment options in ADHD therapy. Treatment guidelines for both children and adult patients recommend using drugs such as methylphenidate and atomoxetine. However, about 20–50% of patients are considered nonresponders due to insufficient symptom reduction or severe side effects. Moreover, combining pharmacotherapy with psychotherapy (cognitive behavioral therapy, education, and focused complex programs) and other nonpharmacological methods is recommended in all cases [85].

#### **4.1. Neurobiology and neurophysiology of impulsivity in ADHD**

Neuroimaging studies indicate that ADHD might be a neurobiologically heterogeneous category of diseases. This would mean that there are several different disorder patterns which manifest by similar clinical symptoms or that dysfunctions in different functional systems could lead to similar symptoms. Data-mining techniques suggest three clusters of neuropsychological abnormities in ADHD: cognitive-behavioral management, time processing, and motivation. These clusters did not significantly overlap between individual subjects [86]. Similarly, a systematic review of the findings in executive function areas suggests that not all ADHD patients are impaired in the same region [87].

ADHD is characterized by a delay in cortical maturation, which is most substantial in the prefrontal regions [88]. Earlier neuroimaging studies described structural and functional abnormalities in patients with ADHD, suggesting a hypofunction of catecholamine projection from the basal ganglia into the PFC. This dysfunction manifests as a relative hypoactivity of the cortical dopamine system with a relative hyperactivity of striatal dopamine [89]. A metaanalysis of functional studies showed hypoactivity in the frontal regions (DLPFC, inferior PFC, OFC), anterior cingulum, superior parietal regions, caudate nucleus, and thalamus [90]. Duerden et al. [91] also observed that adolescents with ADHD had a significantly greater cortical thickness in the pre-supplementary motor area (SMA) than controls. Further, impaired functional connectivity between the frontal and parietal cortex and between the frontal and cerebellar cortex have been found in patients with ADHD during interference control tasks and time discrimination tasks [92] associated with interference control, activity timing, and time predictions. Striatal hypoactivation in ADHD can lead to the insufficient detection of behaviorally important stimuli, inability to orientate one's activities to long-term goals, and insufficient feedback effect from behavioral modification [93–95].

Several studies used TMS to investigate neurophysiological parameters in ADHD. A metaanalysis by Dutra et al. [96] identified no significant differences between ADHD and control groups in CSP, resting MT, and motor-evoked potential. However, there was a consistent finding in reduced short intracortical inhibition (SICI) in both children with ADHD [97–100] and adult ADHD patients [67]. SICI is a subthreshold conditioning stimulus followed by a suprathreshold test stimulus with an interstimulus interval of 1–6 ms. The motor-evoked potential which was evoked by the second suprathreshold stimulus should be reduced by 50–90% [101]. The SICI is described as probably measuring GABAA-mediated cortical inhibition [66, 102]. A study by Hasan et al. [103] also reported increased intracortical facilitation (ICF) in adult ADHD patients compared to healthy controls when considering an interstimulus interval of 7 ms between paired pulses applied to the left hemisphere. ICF is measured by TMS when the magnetic evoked potential generated by the suprathreshold is usually facilitated at an interstimulus interval of 8–30 ms [101]. However, there are too few studies to make a more robust conclusion.

#### **4.2. Review of rTMS treatment studies in ADHD**

**3.4. Summary of rTMS treatment in BPD**

50 Transcranial Magnetic Stimulation in Neuropsychiatry

therapeutic effects should be assessed.

The existing studies suggest that rTMS is a well-tolerated treatment in patients with BPD and is a potentially highly useful tool for reducing BPD symptoms including impulsivity and emotion regulation. There is a lack of double-blind randomized controlled studies with sufficient sample sizes. Current studies differ substantially in both rTMS cortical targets and stimulation protocols. Most studies have found an effect of high-frequency rTMS over the right DLPFC, but there are also studies that found low-frequency DLPFC, left-sided DLPFC, and cerebellar rTMS effective. More double-blind placebo-controlled studies and studies directly comparing different stimulation protocols in BPD are needed, and the duration of the

ADHD, in the ICD-10 represented by hyperkinetic disorder, is one of the most common mental disorders among children, with a prevalence of 3–7% [81]. ADHD was long viewed as a childhood diagnosis; however, many studies in the last decades have demonstrated that symptoms persist to adulthood in up to 80% of patients [82]. The latest revision of the Diagnostic and Statistical Manual of Mental Disorders (DSM-V) reexamined the diagnostic criteria and allowed the classification of ADHD as a lifelong disorder with the condition of onset before the 12th year of life [55]. ADHD symptom heredity is considered to be as high as 75% [83]. Like many neuropsychiatric disorders, ADHD seems to be a result of the complex interplay of genetic and environmental factors and has been recently viewed as a neurodevelopmental disorder [81]. The three typical symptoms of childhood ADHD—attention deficit, hyperactivity, and impulsivity—are partially modified during the lifespan. In adulthood, feelings of internal restlessness, disorganization, and unrestrainability, and some behavioral difficulties, including impaired executive functions, prevail [84]. The treatment of ADHD in children as well as in adults is an ongoing topic in psychiatry. There are several possible treatment options in ADHD therapy. Treatment guidelines for both children and adult patients recommend using drugs such as methylphenidate and atomoxetine. However, about 20–50% of patients are considered nonresponders due to insufficient symptom reduction or severe side effects. Moreover, combining pharmacotherapy with psychotherapy (cognitive behavioral therapy, education, and focused complex programs) and other nonpharmacological methods is recommended in all cases [85].

**4. rTMS in attention-deficit/hyperactivity disorder treatment**

**4.1. Neurobiology and neurophysiology of impulsivity in ADHD**

ADHD patients are impaired in the same region [87].

Neuroimaging studies indicate that ADHD might be a neurobiologically heterogeneous category of diseases. This would mean that there are several different disorder patterns which manifest by similar clinical symptoms or that dysfunctions in different functional systems could lead to similar symptoms. Data-mining techniques suggest three clusters of neuropsychological abnormities in ADHD: cognitive-behavioral management, time processing, and motivation. These clusters did not significantly overlap between individual subjects [86]. Similarly, a systematic review of the findings in executive function areas suggests that not all We searched for relevant studies through the PubMed (http://www.ncbi.nlm.nih.gov/ pubmed/), Web of Science (https://apps.webofknowledge.com/), and Scopus (https://www. scopus.com/) databases published before August 13, 2017. The following terms were used to search in the publication titles: (ADHD OR "attention deficit hyperactivity disorder") AND (TMS OR rTMS OR "transcranial magnetic stimulation"). We found 20 (PubMed), 32 (Web of Science), and 25 (Scopus) articles. After excluding duplicates and nonrelevant contributions (e.g. theoretical articles), seven studies were included in the review.

Current studies examining the treatment of ADHD by rTMS use two main protocols. The first protocol is the low-frequency (LF) stimulation of the SMA, intended to suppress motor symptoms of hyperactivity. The other protocol uses HF rTMS over the DLPFC, intended to facilitate dopaminergic neurotransmission in the PFC and induce the release of endogenous dopamine in the nucleus caudate nucleus and NAcc [104]. This kind of stimulation could improve the symptoms of ADHD mostly in the cognitive domain (deficit of attention and impulsive cognitive style).

In his pilot study, Niederhofer [105] presented a case study of an adult ADHD patient. This study used LF 1 Hz rTMS protocol over the SMA in order to reduce the symptoms of hyperactivity. The results describe a significant improvement that lasted for at least 4 weeks. Three years later, Niederhofer repeated the same protocol with a 42-year-old female ADHD patient on a 20 mg daily dose of methylphenidate (MPH). After 21 days of 1 Hz rTMS (1200 pulses per session, each session lasting 1 h) over the SMA, the daily MPH dose was lowered to 10 mg; simultaneously, the 10 hyperactivity-associated items of the Conners scale improved from the initial 25 to 17 points (measured during the therapy and a week after the termination). The attention items did not show any difference [106].

of the patients was stimulated for 2 weeks (10 sessions). Results showed an overall significant improvement in the clinical global impression-improvement (CGI-I) and the ADHD-IV scales in both groups combined (*P* < 0.01); no significant differences between active and sham stimulation were described. The study also described no negative side effects of the stimulation.

Repetitive Transcranial Magnetic Stimulation Treating Impulsivity in Borderline Personality…

http://dx.doi.org/10.5772/intechopen.72787

53

In another study [112], 25 children with ADHD underwent rTMS treatment. The primary motor cortex (M1) was stimulated using LF 1 Hz rTMS at low intensity—80% of the individual MT. This study did not evaluate the clinical effect of the stimulation, it only measured the effect of rTMS on electrophysiological parameters of the cortical excitability by EEG. The result of this study was a significant decrease of the N100 which was evoked by rTMS and lasted for at least 10 min after the stimulation. EEG source analysis indicated that the TMSevoked N100 change reflected rTMS effects in the stimulated motor cortex and therefore the TMS-evoked N100 could represent a promising candidate marker to monitor rTMS effects on cortical excitability in children with ADHD. No serious side effects of the stimulation were

Another study with child ADHD patients was conducted by Gómez et al. [113]. The aim of the study was to evaluate the tolerability and safety of LF rTMS in children with ADHD. The study group included 10 children aged from 7 to 12 years. These patients received 1 Hz stimulation (a total of 1500 stimuli in each session) over the left DLPFC (the site for stimulation was defined by the F3 electrode position (10/20 International System)) for 5 consecutive days, the intensity was set to 90% of the individual MT. The assumption was that 1 Hz stimulation over the left DLPFC could be as effective as 10 Hz stimulation to the homologous right area. Seventy percent of the patients reported a mild headache or a local discomfort lasting for few minutes as the most frequent side effect, 20% reported also a mild neck pain. Their parents and teachers were asked to fill out the symptoms checklist (SCL) for ADHD from DSM-IV, before and 1 week after completing the rTMS sessions. There was improvement in inattentiveness symptoms at school (score dropped from 16.7 to 8.6) and in hyperactivity/impulsivity at

None of these studies reported any severe side effects of rTMS; the only common side effect was a temporary and mild headache. Theoretically, there is a higher risk of paroxysmal reaction on rTMS in child patients due to their lower seizure threshold, but so far no study has reported such a side effect. If the personal history, entry EEG exam, and safety limits are per-

Using rTMS in treating ADHD symptoms is still a relatively unexplored area. However, current studies suggest it might be a promising nonpharmacological approach or it could be used in combination with pharmacotherapy. The benefit of using rTMS in ADHD treatment is the minimal occurrence of side effects among current studies, none of which is a serious side effect. Studies have explored the effect of rTMS in only small numbers of patients using different methodology, including different stimulation parameters and application targets. Current studies focus mostly on reducing inattention and impulsivity by stimulating the DLPFC. The

formed properly, the risk of provoking a paroxysmal reaction is very low [114].

**4.3. Conclusions and future directions of rTMS treatment paradigms in ADHD**

described; three patients reported a mild headache.

home (score dropped from 30.8 to 11.4).

The largest study was conducted by Bloch et al. [107]. They performed a randomized, crossover, double-blind pilot study in 13 adult ADHD patients. They applied a single session of HF stimulation (42 × 2 s, 20 Hz stimuli at 100% of individual MT intensity, with a 30 s interstimulus interval) over the right DLPFC (located by measuring 5 cm anterior to the motor threshold). One patient dropped out of the study because the stimulation was painful, the other 12 completed the treatment and reported no side effects. The result of the study was a significant improvement in self-reported attention with no effects on mood or anxiety [positive and negative affect schedule (PANAS), visual analogue scales (VAS), and Cambridge neuropsychological test automated battery (CANTAB) were used]. No difference was found in the attention score when comparing the pre- and post-sham rTMS results. The limitation of that study was the fact that the symptoms were evaluated only before the treatment and 10 min after; therefore, no claims can be made about the long-term effects of this therapy.

Ustohal et al. [108] used a similar design in their own pilot study. They treated a 36-year-old male subject who was diagnosed with ADHD in childhood and experienced three major depression episodes in adulthood. The authors used HF 10 Hz frequency in 120% intensity of individual MT (10 s train, 30 s inter train interval, 1500 pulses per session). The study was divided into three sections, each lasting 1 week. In the first week, sham stimulation was applied; in the second week, the left DLPFC was stimulated; and in the third week, the right DLPFC was stimulated. In the first week, there was already a significant improvement in the d2 test of attention (from the initial 86.4 percentile to 98.2 percentile) and a small reduction on the depression scale (from MADRS 14 to 12). In the second week, there was a further reduction on the depression scale (MADRS score decreased to 7) and improvement in the d2 test of attention (98.9 percentile). On the first session of the third week, the patient described serious side effects—dysphoria, hypobulia, and increased tension. The MADRS score increased significantly (21 points). Therefore, the authors changed the target to the left DLPFC, which led to improved symptoms, reduced depression scale score (MADRS = 9), and improvement in the d2 test of attention (99.2 percentile). The authors discussed that these side effects may be related to the fact that LF rTMS of the right DLPFC is used in the treatment of depression [109] and, on the contrary, HF rTMS of this area has been used in patients with mania [110].

In another study, Weaver et al. [111] stimulated nine adolescents and young adults diagnosed with ADHD. They targeted the right DLPFC (located by measuring 5 cm anterior to the motor threshold) and used HF stimulation (10 Hz, 4 s trains, 26 s inter train interval, 2000 pulses per session) with 100% intensity of individual MT. This study had a double-blind design and each of the patients was stimulated for 2 weeks (10 sessions). Results showed an overall significant improvement in the clinical global impression-improvement (CGI-I) and the ADHD-IV scales in both groups combined (*P* < 0.01); no significant differences between active and sham stimulation were described. The study also described no negative side effects of the stimulation.

In his pilot study, Niederhofer [105] presented a case study of an adult ADHD patient. This study used LF 1 Hz rTMS protocol over the SMA in order to reduce the symptoms of hyperactivity. The results describe a significant improvement that lasted for at least 4 weeks. Three years later, Niederhofer repeated the same protocol with a 42-year-old female ADHD patient on a 20 mg daily dose of methylphenidate (MPH). After 21 days of 1 Hz rTMS (1200 pulses per session, each session lasting 1 h) over the SMA, the daily MPH dose was lowered to 10 mg; simultaneously, the 10 hyperactivity-associated items of the Conners scale improved from the initial 25 to 17 points (measured during the therapy and a week after the termination). The

The largest study was conducted by Bloch et al. [107]. They performed a randomized, crossover, double-blind pilot study in 13 adult ADHD patients. They applied a single session of HF stimulation (42 × 2 s, 20 Hz stimuli at 100% of individual MT intensity, with a 30 s interstimulus interval) over the right DLPFC (located by measuring 5 cm anterior to the motor threshold). One patient dropped out of the study because the stimulation was painful, the other 12 completed the treatment and reported no side effects. The result of the study was a significant improvement in self-reported attention with no effects on mood or anxiety [positive and negative affect schedule (PANAS), visual analogue scales (VAS), and Cambridge neuropsychological test automated battery (CANTAB) were used]. No difference was found in the attention score when comparing the pre- and post-sham rTMS results. The limitation of that study was the fact that the symptoms were evaluated only before the treatment and 10 min after; therefore, no claims can be made about the long-term effects of this therapy.

Ustohal et al. [108] used a similar design in their own pilot study. They treated a 36-year-old male subject who was diagnosed with ADHD in childhood and experienced three major depression episodes in adulthood. The authors used HF 10 Hz frequency in 120% intensity of individual MT (10 s train, 30 s inter train interval, 1500 pulses per session). The study was divided into three sections, each lasting 1 week. In the first week, sham stimulation was applied; in the second week, the left DLPFC was stimulated; and in the third week, the right DLPFC was stimulated. In the first week, there was already a significant improvement in the d2 test of attention (from the initial 86.4 percentile to 98.2 percentile) and a small reduction on the depression scale (from MADRS 14 to 12). In the second week, there was a further reduction on the depression scale (MADRS score decreased to 7) and improvement in the d2 test of attention (98.9 percentile). On the first session of the third week, the patient described serious side effects—dysphoria, hypobulia, and increased tension. The MADRS score increased significantly (21 points). Therefore, the authors changed the target to the left DLPFC, which led to improved symptoms, reduced depression scale score (MADRS = 9), and improvement in the d2 test of attention (99.2 percentile). The authors discussed that these side effects may be related to the fact that LF rTMS of the right DLPFC is used in the treatment of depression [109] and, on the contrary, HF rTMS

In another study, Weaver et al. [111] stimulated nine adolescents and young adults diagnosed with ADHD. They targeted the right DLPFC (located by measuring 5 cm anterior to the motor threshold) and used HF stimulation (10 Hz, 4 s trains, 26 s inter train interval, 2000 pulses per session) with 100% intensity of individual MT. This study had a double-blind design and each

attention items did not show any difference [106].

52 Transcranial Magnetic Stimulation in Neuropsychiatry

of this area has been used in patients with mania [110].

In another study [112], 25 children with ADHD underwent rTMS treatment. The primary motor cortex (M1) was stimulated using LF 1 Hz rTMS at low intensity—80% of the individual MT. This study did not evaluate the clinical effect of the stimulation, it only measured the effect of rTMS on electrophysiological parameters of the cortical excitability by EEG. The result of this study was a significant decrease of the N100 which was evoked by rTMS and lasted for at least 10 min after the stimulation. EEG source analysis indicated that the TMSevoked N100 change reflected rTMS effects in the stimulated motor cortex and therefore the TMS-evoked N100 could represent a promising candidate marker to monitor rTMS effects on cortical excitability in children with ADHD. No serious side effects of the stimulation were described; three patients reported a mild headache.

Another study with child ADHD patients was conducted by Gómez et al. [113]. The aim of the study was to evaluate the tolerability and safety of LF rTMS in children with ADHD. The study group included 10 children aged from 7 to 12 years. These patients received 1 Hz stimulation (a total of 1500 stimuli in each session) over the left DLPFC (the site for stimulation was defined by the F3 electrode position (10/20 International System)) for 5 consecutive days, the intensity was set to 90% of the individual MT. The assumption was that 1 Hz stimulation over the left DLPFC could be as effective as 10 Hz stimulation to the homologous right area. Seventy percent of the patients reported a mild headache or a local discomfort lasting for few minutes as the most frequent side effect, 20% reported also a mild neck pain. Their parents and teachers were asked to fill out the symptoms checklist (SCL) for ADHD from DSM-IV, before and 1 week after completing the rTMS sessions. There was improvement in inattentiveness symptoms at school (score dropped from 16.7 to 8.6) and in hyperactivity/impulsivity at home (score dropped from 30.8 to 11.4).

None of these studies reported any severe side effects of rTMS; the only common side effect was a temporary and mild headache. Theoretically, there is a higher risk of paroxysmal reaction on rTMS in child patients due to their lower seizure threshold, but so far no study has reported such a side effect. If the personal history, entry EEG exam, and safety limits are performed properly, the risk of provoking a paroxysmal reaction is very low [114].

#### **4.3. Conclusions and future directions of rTMS treatment paradigms in ADHD**

Using rTMS in treating ADHD symptoms is still a relatively unexplored area. However, current studies suggest it might be a promising nonpharmacological approach or it could be used in combination with pharmacotherapy. The benefit of using rTMS in ADHD treatment is the minimal occurrence of side effects among current studies, none of which is a serious side effect. Studies have explored the effect of rTMS in only small numbers of patients using different methodology, including different stimulation parameters and application targets. Current studies focus mostly on reducing inattention and impulsivity by stimulating the DLPFC. The most widely used stimulation is high frequency rTMS over the right DLPFC. However, a study by Ustohal et al. [108] showed that this protocol can have a negative effect on patient's depression symptoms and suggests another stimulation site, such as left DLPFC, at least for patients with a personal history of depression. However, this side effect has only been observed in a single patient. Another treatment protocol to consider is low frequency rTMS over the left DLPFC, which could possibly have a similar effect. Hyperactivity symptoms of ADHD could also be reduced by using low frequency rTMS over the SMA; however, only two patients have been stimulated by this protocol, and further research is needed. There is a lack of reliable data on the duration of the therapeutic effect. Further understanding of the neurophysiological mechanisms of the effect and assessment of adequate stimulation parameters are required.

**Author details**

Czech Republic

Czech Republic

**References**

Tomas Sverak1,2\*, Pavla Linhartova<sup>1</sup>

, Adam Fiala1

2 Central European Institute of Technology (CEITEC MU), Masaryk University, Brno,

[1] Smith JL, Mattick RP, Jamadar SD, Iredale JM. Deficits in behavioural inhibition in substance abuse and addiction: A meta-analysis. Drug and Alcohol Dependence. 2014;**145**:1-33

[2] Schag K, Schönleber J, Teufel M, Zipfel S, Giel KE. Food-related impulsivity in obesity and binge eating disorder—A systematic review. Obesity Reviews: An Official Journal

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[4] Turner D, Sebastian A, Tüscher O. Impulsivity and cluster B personality disorders.

[5] Ouzir M. Impulsivity in schizophrenia: A comprehensive update. Aggression and

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[8] Whiteside SP, Lynam DR. The five factor model and impulsivity: Using a structural model of personality to understand impulsivity. Personality and Individual Differences.

[9] Cyders MA, Smith GT. Mood-based rash action and its components: Positive and nega-

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1 Department of Psychiatry, Masaryk University and University Hospital Brno,

\*Address all correspondence to: tomas.sverak@mail.muni.cz

and Tomas Kasparek<sup>1</sup>

http://dx.doi.org/10.5772/intechopen.72787

55

Repetitive Transcranial Magnetic Stimulation Treating Impulsivity in Borderline Personality…

#### **4.4. Summary of rTMS treatment in ADHD**

Studies suggest that rTMS is a well-tolerated treatment in patients with ADHD and potentially a highly useful tool for reducing ADHD symptoms including impulsivity, motor hyperactivity, and reduced attention. There are not yet double-blind randomized controlled studies with sufficient sample sizes. The current studies differ substantially in both rTMS cortical targets and stimulation protocols. Most studies suggest stimulation over the right DLPFC by high frequency rTMS; another potentially promising protocol in ADHD is low frequency rTMS over the SMA. More double-blind placebo-controlled studies and evidence about the therapeutic effect of rTMS in ADHD patients are needed.

## **5. Conclusion**

The most important application of rTMS for impulsivity reduction in BDP and ADHD seems to be stimulation over the left or right DLPFC, the SMA, or the cerebellum. However, it should be stressed that the neural activity associated with impulsivity differs according to the task parameters used during neuroimaging. This applies for studies of behavioral inhibition, Delay Discounting, and emotion regulation. This problem might be overcome by navigating rTMS individually according to functional fMRI from a specific task administered to the patients before stimulation. rTMS seems to be well tolerated without any adverse events in BPD and ADHD patients. The results of rTMS impulsivity treatment studies are promising, but double-blind studies with larger active and sham group sizes are needed to optimize the treatment results.
