Effect of 5 Hz repetitive transcranial magnetic stimulation on cognition during a Go/NoGo task

doi:10.1016/j.jpsychires.2004.01.006

Journal of Psychiatric Research

Volume 38, Issue 5, September–October 2004, Pages 513-520

https://doi.org/10.1016/j.jpsychires.2004.01.006 Get rights and content

Abstract

Repetitive transcranial magnetic stimulation (rTMS) has been developed as a novel tool for modulating cognition by delivering stimulation in the brain. However, the effects of rTMS on cognition are still controversial. This randomized, sham-controlled, crossover study was designed to determine whether rTMS of the left dorsolateral prefrontal cortex (DLPFC) interferes with the Go/NoGo task and whether personal parameters such as age affect rTMS. A total of 24 healthy subjects (12 male and 12 female, aged 20–37 years) underwent one session of active rTMS followed by sham rTMS (total of 1600 pulses, 100% of motor threshold, 5 Hz, 8 s), or vice versa. The results did not show any differences between active and sham rTMS stimulation in terms of performance accuracy, response speed, or choice reaction time (cRT) implicating that short-term rTMS will not enhance or deteriorate cognition. However, percentage cRT shortening induced by active rTMS was negatively correlated with age (r=−0.57, P=0.005), whereas that induced by sham rTMS was not (r=−0.23, P>0.05), suggesting that cognition of younger subjects might have greater modulation by active stimulation than older ones. This finding may help explain some of the controversies or paradoxical results observed in studies of the effect of left DLPFC rTMS on cognition.

Introduction

Repetitive transcranial magnetic stimulation (rTMS) is a novel, noninvasive tool for the manipulation of neuronal activities in the human brain. In several studies, cognitive function could be modulated through rTMS delivered over the cerebral cortex in healthy subjects and in patients with brain diseases (Grafman and Wassermann, 1999; Huber et al., 2003). Conversely, other studies failed to demonstrate the effect of rTMS on cognition (Jahanshahi and Rothwell, 2000). To date, the effects of rTMS on cognition are still controversial, and the mechanisms by which rTMS influences cognition also remains unclear. Many personal parameters are known to possibly affect the effect of rTMS in treating depression. These parameters include psychotic features, age, previous responses to rTMS, and underlying brain physiologic markers (Gershon et al., 2003). However, most studies of the effect of rTMS on cognition have focused on effectiveness only. Unlike the effect of rTMS in treating depression, little is known about how personal factors might account for the disparity of results from studies of cognition and rTMS. To see the effect of rTMS on performance of cognition, we used the Go/NoGo task as a test battery for attentional performance. Thus, our aims were (1) to investigate whether a single session of rTMS applied to the left dorsolateral prefrontal cortex (DLPFC) interferes with performance on a Go/NoGo task performance in healthy subjects and (2) to determine whether age might account for the disparity in results that has shown in the treatment of depression (Figiel et al., 1998; Kozel et al., 2000; Janicak et al., 2002).

Section snippets

Subjects

Twenty-four subjects (12 men and 12 women; age, 20–37 years; mean ± standard deviation [SD], 27.0 ± 4.7 years) were recruited through local advertisement. Subjects were all right-handed and were naive to transcranial magnetic stimulation (TMS) and the Go/NoGo task. Subjects were screened for psychiatric disorders and substance or alcohol abuse by means of the Mini-International Neuropsychiatric Interview (Sheehan et al., 1998) and excluded if these were present. Those with significant physical

Results

The two groups (active/sham vs. sham/active) were not significantly different in terms of age, years of education, MT, or baseline cRT and error rate scores. The results of comparison showed in Table 1. Further analysis also demonstrated no significant carry-over or period effects in on cRT (P>0.05) or error rate (P>0.05), indicating that the order effect did not influence the results. No subjective or objective adverse effects were observed in any subject during stimulation.

Discussion

The present study showed that a single rTMS session of either active or sham stimulation did not influence the accuracy of performance on a Go/NoGo task. Similarly, it did not influence the cRT on this cognitive test. However, we found that the response after active stimulation may have been faster in younger subjects than in older ones.

The Go/NoGo task is a common tool for assessing cognition. A previous study showed an impaired ability to perform Go/NoGo task with DLPFC lesions (Godefroy et

Conclusion

Consistent with most of previous results, our findings did not show changes in accuracy or influence in the speed of responses to a Go/NoGo task after rTMS with a single active session, implying that a short-term active rTMS will neither enhancing nor deteriorating cognition. Further analysis revealed that improvement of the speed response, correlated with age and suggested that age factor might be critical in determining the effect of rTMS applied to the left DLPFC on cognition. This is

Acknowledgements

This work was supported by a grant from Taipei Veterans General hospital (VGH-91-237).

References (33)

C.M. Epstein et al.
Asymmetries of prefrontal cortex in human episodic memory: effects of transcranial magnetic stimulation on learning abstract patterns
Neuroscience Letters
(2002)
T.J. Huber et al.
Gender differences in the effect of repetitive transcranial magnetic stimulation in schizophrenia
Psychiatry Research
(2003)
P.G. Janicak et al.
Repetitive transcranial magnetic stimulation versus electroconvulsive therapy for major depression: preliminary results of a randomized trials
Biological Psychiatry
(2002)
R. Kawashima et al.
Functional anatomy of GO/NO-GO discrimination and response selection – A PET study in man
Brain Research
(1996)
T.M. Lee et al.
Neural correlates of response inhibition for behavioral regulation in humans assessed by functional magnetic resonance imaging
Neuroscience Letters
(2001)
D. Liebetanz et al.
Safety aspects of chronic low-frequency transcranial magnetic stimulation based on localized proton magnetic resonance spectroscopy and histology of the rat brain
Journal of Psychiatric Research
(2003)
F.M. Mottaghy et al.
Modulation of a brain-behavior relationship in verbal working memory by rTMS
Brain Research and Cognitive Brain Research
(2003)
B.R. Mull et al.
Transcranial magnetic stimulation of left prefrontal cortex impairs working memory
Clinical Neurophysiology
(2001)
A. Pascual-Leone et al.
Safety of rapid-rate transcranial magnetic stimulation in normal volunteers
Electroencephalography and Clinical Neurophysiology
(1993)
E.M. Wassermann et al.
Use and safety of a new repetitive transcranial magnetic stimulator
Electroencephalography and Clinical Neurophysiology
(1996)

B. Boroojerdi et al.

Enhancing analogic reasoning with rTMS over the left prefrontal cortex

Neurology

(2001)

S.L. Bridgers et al.

Transcranial magnetic stimulation: an assessment of cognitive and other cerebral effects

Neurology

(1989)

S.F. Cappa et al.

The role of the left frontal lobe in action naming: rTMS evidence

Neurology

(2002)

S. Evers et al.

The impact of transcranial magnetic stimulation on cognitive processing: an event-related potential study

Neuroreport

(2001)

G.S. Figiel et al.

The use of rapid-rate transcranial magnetic stimulation (rTMS) in refractory depressed patients

Journal of Neuropsychiatry and Clinical Neuroscience

(1998)

S.S. Flitman et al.

Linguistic processing during repetitive transcranial magnetic stimulation

Neurology

(1998)

Cited by (29)

Repetitive transcranial magnetic stimulation promotes response inhibition in patients with major depression during the stop-signal task
2022, Journal of Psychiatric Research
Citation Excerpt :
In the study of Tovar-Perdomo et al., the patients ranged in age from 18 to 40, with an average age of 46.25 ± 11.47 years. In healthy people, it has been reported that rTMS improved cognitive function more significantly in younger participants (age ≤28) than in older (Huang et al., 2004). The relatively older age of the patients in this study may limit the effectiveness of rTMS.
Response inhibition (RI) deficit is an aspect of cognitive impairment in depressed individuals, but currently no effective treatment has been established. This study aimed to explore the effect of individualized repetitive transcranial magnetic stimulation (rTMS) targeting the left dorsolateral prefrontal cortex (lDLPFC)-nucleus accumbens (NAcc) network on RI in patients with major depressive disorder (MDD).
Fourty-four patients diagnosed with MDD were randomized to receive 15 once-daily sessions of active (10 Hz, 100% of resting motor threshold) or sham rTMS within a double-blind, sham-controlled trial. We measured the efficacy of rTMS by the improvements in behavioral and neurological manifestations during the stop-signal task. The Hamilton Depression Rating Scale-17 items (HAMD-17) was used to assess depressive symptoms. We analyzed the differences in RI performance between MDD patients and 30 healthy controls (HCs) at baseline and assessed whether MDD patients who completed rTMS treatment had comparable RI ability to HCs.
At baseline, the depressed patients showed longer stop-signal response time (SSRT), smaller P3 amplitudes, and weaker theta-band power in successful stop trials (SSTs) than HCs. The active group exhibited RI ability comparable to that of HCs after rTMS treatment, but the improvements were not significant in the sham group. The active group showed significant remission in depression symptoms post-treatment compared to the sham group, and the changes in P3 amplitudes and theta-band power during SSTs were negatively correlated with the decrease of HAMD-17 scores.
The depressed patients have impaired RI and treatment with the individualized rTMS protocol may be an effective approach.
The effect of non-invasive brain stimulation on executive functioning in healthy controls: A systematic review and meta-analysis
2021, Neuroscience and Biobehavioral Reviews
Citation Excerpt :
Three studies assessed the effect of HF-rTMS stimulation. Although Hwang et al. (2010) found improved GNG performance after left DLPFC stimulation, the other studies did not replicate this effect (Huang et al., 2004; Schaller et al., 2013). Because the quantitative data of Huang et al. (2004) were not provided, we pooled the data of seven studies in a meta-analysis.
In recent years, there has been a heightened interest in the effect of non-invasive brain stimulation on executive functioning. However, there is no comprehensive overview of its effects on different executive functioning domains in healthy individuals. Here, we assessed the state of the field by conducting a systematic review and meta-analysis on the effectiveness of non-invasive brain stimulation (i.e. repetitive transcranial magnetic stimulation and transcranial direct current stimulation) over prefrontal regions on tasks assessing working memory, inhibition, flexibility, planning and initiation performance. Our search yielded 63 studies (n = 1537), and the effectiveness of excitatory and inhibitory non-invasive brain stimulation were assessed per executive functioning task. Our analyses showed that excitatory non-invasive brain stimulation had a small but positive effect on Stop Signal Task and Go/No-Go Task performance, and that inhibitory stimulation had a small negative effect on Flanker Task performance. Non-invasive brain stimulation did not affect performance on working memory and flexibility tasks, and effects on planning tasks were inconclusive.
The effect of bilateral high frequency repetitive transcranial magnetic stimulation on cognitive functions in schizophrenia
2020, Schizophrenia Research: Cognition
Citation Excerpt :
In a neuroimaging study with perfusion SPECT on healthy people, 20 Hz rTMS targeted the left DLPFC region has been resulted in increased blood flow in dorsolateral prefrontal, anterior cingulate and orbitofrontal cortices (George et al., 1999). With high frequency rTMS on DLPFC, although, some studies reported an improvement in selective attention (Martis et al., 2003; Rektorova et al., 2005), some found no difference of cognitive functions (Boggio et al., 2005; Huang et al., 2004; Zhuo et al., 2019). In another study, Barr et al. have shown a significant improvement in working memory by applying bilateral 20 Hz rTMS on DLPFC sequentially (Barr et al., 2013).
Cognitive functioning before and after repetitive transcranial magnetic stimulation (rTMS): A quantitative meta-analysis in healthy adults
2020, Neuropsychologia
Repetitive transcranial magnetic stimulation (rTMS) is thought to modulate brain function through methods of electromagnetic induction. Over the last few decades, a large body of studies have investigated the clinical applications of rTMS in a variety of patient populations for a diverse range of symptoms from depressive symptomology to post-stroke motor functioning. There is still no clear consensus, however, on how rTMS influences cognitive functioning in the healthy brain. We conducted a quantitative meta-analysis in order to evaluate whether offline rTMS (the delivery of rTMS when not actively engaged in a cognitive task) influences cognition in healthy adults. More specifically, we examined studies that applied rTMS to the dorsal lateral prefrontal cortex (DLFPC) and that tracked cognitive outcomes both before and after a prescribed period of rTMS. Fifteen studies met our inclusion criteria. Cognitive performance was pooled and examined across studies for four cognitive domains (working memory, executive functioning, episodic memory, and visual perception) and under two types of stimulation conditions (excitatory and inhibitory rTMS). Whereas excitatory rTMS was associated with statistically reliable effects for improving executive functioning, inhibitory rTMS was associated with statistically reliable effects for improving episodic memory and visual perception. However, the magnitude of these effects was small and no other significant effects were observed. Though future studies are still needed, our findings suggest that offline forms of rTMS may have limited utility in affecting cognitive functioning when applied to the DLPFC in healthy adults, irrespective of cognitive domain or stimulation type.
Transcranial magnetic stimulation: Neurophysiological and clinical applications
2019, Handbook of Clinical Neurology
Citation Excerpt :
The authors observed that 10-Hz rTMS to the left DLPFC improved reaction times on the Stroop task for both congruent and incongruent trials (Vanderhasselt et al., 2006a, 2007), while targeting the right DLPFC improved reaction times for cued trials on a task-switching paradigm (Vanderhasselt et al., 2006b). By comparison, Huang et al. (2004) found no change in go–no go task performance following 5-Hz rTMS to the left DLPFC. Smirni et al. (2017) used 1-Hz rTMS to both the right and left DLPFC and reported decreased verbal fluency after 1 Hz to the left but increased after 1 Hz to the right.
Transcranial magnetic stimulation (TMS) is a safe and noninvasive means of electrically stimulating the brain by electromagnetic induction. TMS is capable of probing intracortical circuits and modulating cortical activity in humans; as such it has been instrumental to studying the neurophysiology and functional neuroanatomy of the frontal lobes. For example, using TMS to induce “virtual lesions”—transient disruption of function in the targeted brain region—has yielded important insights into the functional organization of the prefrontal cortex (PFC) with respect to working memory, language, and other core cognitive functions. Whereas neuroimaging is typically limited to observing correlations between brain function and behavior, TMS, by interacting with neural circuits, can lead to causal inferences that bridge human, nonhuman primate, and other model system studies. Applied repetitively in trains of stimuli, TMS is also capable of normalizing aberrant patterns of cortical activity in the treatment of neurologic and psychiatric disorders. The earliest and most well-established clinical use of repetitive TMS is in the treatment of medication-resistant depression with high-frequency stimulation of the left dorsolateral PFC. Research efforts to identify other promising clinical applications—such as for stroke and Alzheimer's disease—are rapidly expanding; however, the majority of these indications have yet to have devices cleared by the FDA for on-label use.
High frequency repetitive transcranial magnetic stimulation treatment for major depression: Dissociated effects on psychopathology and neurocognition
2017, Journal of Affective Disorders
This open-label pilot study explored the effects of a course of accelerated high-frequency repetitive transcranial magnetic stimulation (HF-rTMS) on two neurocognitive domains (decision-making and impulse control) in patients with major depressive disorder (MDD).
Participants with MDD and a treatment resistant major depressive episode (n=24) underwent twice-daily HF-rTMS targeted at the left dorsolateral prefrontal cortex (lDLPFC) over two weeks. Psychopathology was assessed by clinician-administered and self-reported measures of depression and anxiety; decision-making was assessed by the Iowa Gambling Task, the Balloon Analog Risk Task and the Game of Dice Task; impulse control was assessed by the Stroop Color-Word Task, the Continuous Performance Task and the Stop-Signal Task.
Depression and anxiety scores significantly improved from pre-post HF-rTMS treatment. However, none of the decision-making or impulse control variables of interest changed significantly from pre-post HF-rTMS. Moreover, there was no correlation between changes in psychopathological symptoms and in neurocognition.
This is a moderately sized open label trial, and the confounds of ongoing psychotropics and illness chronicity can not be excluded in this treatment resistant sample.
There is dissociation between acute symptomatic benefit after a course of accelerated HF-rTMS applied to the lDLPFC in treatment resistant MDD and performance on tests of decision making and impulse control. Though rTMS appears cognitively safe, additional research is warranted to understand this potential dissociation and its putative clinical implications.

View all citing articles on Scopus

View full text

Effect of 5 Hz repetitive transcranial magnetic stimulation on cognition during a Go/NoGo task

Abstract

Introduction

Section snippets

Subjects

Results

Discussion

Conclusion

Acknowledgements

Neuroscience Letters

Psychiatry Research

Biological Psychiatry

Brain Research

Neuroscience Letters

Journal of Psychiatric Research

Brain Research and Cognitive Brain Research

Clinical Neurophysiology

Electroencephalography and Clinical Neurophysiology

Electroencephalography and Clinical Neurophysiology

Enhancing analogic reasoning with rTMS over the left prefrontal cortex

Neurology

Transcranial magnetic stimulation: an assessment of cognitive and other cerebral effects

Neurology

The role of the left frontal lobe in action naming: rTMS evidence

Neurology

The impact of transcranial magnetic stimulation on cognitive processing: an event-related potential study

Neuroreport

The use of rapid-rate transcranial magnetic stimulation (rTMS) in refractory depressed patients

Journal of Neuropsychiatry and Clinical Neuroscience

Linguistic processing during repetitive transcranial magnetic stimulation

Neurology