Effects of tDCS on executive function in Parkinson's disease (2023)

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Neuroscience Letters

Volume 582,

17 October 2014

, Pages 27-31

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https://doi.org/10.1016/j.neulet.2014.08.043Get rights and content

Abstract

Non-motor symptoms in patients with Parkinson's disease (PD) are often poorly recognized, significantly impair quality of life and cause severe disability. Currently, there is limited evidence to guide treatment of associated psychiatric and cognitive problems. Non-invasive brain stimulation techniques have emerged as non-pharmacological alternatives to target cognitive symptoms without worsening motor function. In this context, we conducted a multicenter, sham controlled, double-blinded study to assess the immediate and long-term effects of ten consecutive sessions of transcranial direct current stimulation (tDCS) over the anode on the right dorsolateral prefrontal cortex (DLPFC) (n=5), left DLPFC (n=6) or sham (n=7). We assessed cognitive functions, depressive symptoms and motor functions in 18 PD patients at baseline, at the end of the 2-week stimulation sessions and at 1-month follow-up. Our results showed that active stimulation of both left and right DLPFC resulted in prolonged improvements in Trail Making Test B, an established test to measure executive function, compared to sham tDCS at the 1-month follow-up. These results suggest the existence of a beneficial long-term effect on executive functions in PD patients following active tDCS over the DLPFC. Thus, our findings encourage further investigation exploring tDCS as an adjuvant therapy for cognitive and behavioral treatment in PD.

Introduction

Parkinson's disease (PD) is a neurodegenerative disorder characterized by gradual impairment of affective, cognitive and motor function [1]. Although motor symptoms such as resting tremor, bradykinesia, rigidity and postural instability are the hallmark of this disorder, cognitive and psychiatric non-motor symptoms (NMS) are equally disabling and directly impact the quality of life (QOL) of patients with PD [2]. In fact, recent reports show that even after controlling for duration and severity of motor symptoms, cognitive abilities, such as executive and visuospatial functions, remain positively associated with QOL [3]. Furthermore, psychiatric comorbidities, namely depression, consistently emerge amongst the strongest determinant of health related QOL in this patient cohort [4]. For these reasons, there is growing interest in treating and managing neuropsychiatric symptoms in patients with PD [5].

Cognitive functions are predominantly executed by the cortex, where dopamine is known to play a key role [6]. It has been suggested that impairment of cognitive function is related to a disruption of the dopaminergic system [7], which is also severely affected in PD. In fact, cognitive deficits in Parkinson's disease are similar to a dysexecutive syndrome. Depression, a common co-morbidity in PD, is also suggested to be caused by changes in dopaminergic transmission and alterations in excitability and imbalance between the left DLPFC (L-DLPFC) and right DLPFC (R-DLPFC) [8].

Non-invasive brain stimulation techniques such as transcranial direct current stimulation (tDCS) and transcranial magnetic stimulation (TMS) have shown to be safe and effective methods for improving cognitive and affective functions [9]. TDCS applied with the anode over the L-DLPFC and the cathode over the right supraorbital region, can improve working memory in healthy subjects [10], as well as improve mood in patients with major depression [11], [12]. In this context, several studies have documented the beneficial effects of TMS and tDCS on behavioral and cognitive symptoms in PD [13], [14], [15], [16] without worsening motor symptoms [17].

These results support the idea that active stimulation of the DLPFC with tDCS could have beneficial, lasting effects on both affective and cognitive domains in patients with PD. Therefore, we conducted a two-site, double-blind, sham-controlled, 10-session tDCS study in patients with PD. We hypothesized that tDCS applied over the L-DLPFC would improve cognitive function and affective symptoms without altering motor function when compared to sham stimulation.

Section snippets

Subjects

Eighteen patients (6 women and 12 men) aged between 40 and 71 years (mean age 61±8 years) with idiopathic PD were enrolled in the study. Inclusion criteria included a clinical diagnosis of PD defined by the presence of at least two out of three cardinal motor features of PD (resting tremor, rigidity, and bradykinesia, plus a sustained and significant response to dopaminergic treatment), age of 40 and over, and stable maintenance of their medication at least 30 days prior to enrollment and

Results

Eighteen patients were included in the study: six patients were randomly assigned to the L-DLPFC group, five patients to the R-DLPFC group, and seven patients to the sham tDCS group. The mean baseline MMSE score for all groups was 29.2±0.3 (mean±SEM). There was no significant difference between groups in demographics or in any of the cognitive, affective, or behavioral measures at baseline (all p>0.05). The most common side effects reported were tingling (50%), sleepiness (55%) and mild

Discussion

In this study we assessed the effects of tDCS with the anode over the L-DLPFC or R-DLPFC on a wide range of cognitive, affective and motor functions in patients with PD. We found that anodal tDCS over both L-DLPFC and R-DLPFC showed a significantly lasting improvement specifically in TMT-B performance when compared to sham.

Beneficial effects of tDCS on cognitive function have been shown in healthy subjects and in other neuropsychiatric conditions [9], [10], [11], [12]. However, only a few

Conclusions

Results of this exploratory study suggest that anodal tDCS over the prefrontal cortex might enhance certain executive functions in PD without worsening of motor or mood symptoms. Further studies are needed to determine if there is a topographic specificity to the effects of tDCS on the various symptoms in PD, and whether these effects can be sustained when used as a co-adjuvant to pharmacological treatment.

Conflict of interest

None declared.

Source of funding

This study is sponsored by the RJG Foundation.

Acknowledgments

We would like to acknowledge Huashun Cui, Jean-François Lepage, and Pakorn Wivatvongvana for their technical assistance in this protocol.

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    • Cerebral metabolic rate of oxygen (CMRO<inf>2</inf>) changes measured with simultaneous tDCS-MRI in healthy adults

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      Transcranial direct current stimulation (tDCS) is a safe and well-tolerated noninvasive technique used for cortical excitability modulation. tDCS has been extensively investigated for its clinical applications; however further understanding of its underlying in-vivo physiological mechanisms remains a fundamental focus of current research.

      We investigated the simultaneous effects of tDCS on cerebral blood flow (CBF), venous blood oxygenation (Yv) and cerebral metabolic rate of oxygen (CMRO2) using simultaneous MRI in healthy adults to provide a reference frame for its neurobiological mechanisms.

      Twenty-three healthy participants (age=35.6±15.0years old, 10 males) completed a simultaneous tDCS-MRI session in a 3T scanner fitted with a 64-channels head coil. A MR-compatible tDCS device was used to acquire CBF, Yv and CMRO2 at three time points: pre-, during- and post- 15minutes of 2.0mA tDCS on left anodal dorsolateral prefrontal cortex.

      During tDCS, CBF significantly increased (57.10±8.33mL/100g/min) from baseline (53.67±7.75mL/100g/min; p<0.0001) and remained elevated in post-tDCS (56.79±8.70mL/100g/min). Venous blood oxygenation levels measured in pre-tDCS (60.71±4.12%) did not significantly change across the three timepoints. The resulting CMRO2 significantly increased by 5.9% during-tDCS (175.68±30.78µmol/100g/min) compared to pre-tDCS (165.84±25.32µmol/100g/min; p=0.0015), maintaining increased levels in post-tDCS (176.86±28.58µmol/100g/min).

      tDCS has immediate effects on neuronal excitability, as measured by increased cerebral blood supply and oxygen consumption supporting increased neuronal firing. These findings provide a standard range of CBF and CMRO2 changes due to tDCS in healthy adults that may be incorporated in clinical studies to evaluate its therapeutic potential.

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      Brain plasticity can be defined as the ability of local and extended neural systems to organize either the structure and/or the function of their connectivity patterns to better adapt to changes of our inner/outer environment and optimally respond to new challenging behavioral demands. Plasticity has been traditionally conceived as a spontaneous phenomenon naturally occurring during pre and postnatal development, tied to learning and memory processes, or enabled following neural damage and their rehabilitation. Such effects can be easily observed and measured but remain hard to harness or to tame ‘at will’. Non-invasive brain stimulation (NIBS) technologies offer the possibility to engage plastic phenomena, and use this ability to characterize the relationship between brain regions, networks and their functional connectivity patterns with cognitive process or disease symptoms, to estimate cortical malleability, and ultimately contribute to neuropsychiatric therapy and rehabilitation. NIBS technologies are unique tools in the field of fundamental and clinical research in humans. Nonetheless, their abilities (and also limitations) remain rather unknown and in the hands of a small community of experts, compared to widely established methods such as functional neuroimaging (fMRI) or electrophysiology (EEG, MEG). In the current review, we first introduce the features, mechanisms of action and operational principles of the two most widely used NIBS methods, Transcranial Magnetic Stimulation (TMS) and Transcranial Current Stimulation (tCS), for exploratory or therapeutic purposes, emphasizing their bearings on neural plasticity mechanisms. In a second step, we walk the reader through two examples of recent domains explored by our team to further emphasize the potential and limitations of NIBS to either explore or improve brain function in healthy individuals and neuropsychiatric populations. A final outlook will identify a series of future topics of interest that can foster progress in the field and achieve more effective manipulation of brain plasticity and interventions to explore and improve cognition and treat the symptoms of neuropsychiatric diseases.

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      Over the last 15-years, transcranial direct current stimulation (tDCS), a relatively novel form of neuromodulation, has seen a surge of popularity in both clinical and academic settings. Despite numerous claims suggesting that a single session of tDCS can modulate cognition in healthy adult populations (especially working memory and language production), the paradigms utilized and results reported in the literature are extremely variable. To address this, we conduct the largest quantitative review of the cognitive data to date.

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      Transcranial direct current stimulation (tDCS) is increasingly used in research and clinical settings, and the dorsolateral prefrontal cortex (DLPFC) is often chosen as a target for stimulation. While numerous studies report modulation of cognitive abilities following DLPFC stimulation, the wide array of cognitive functions that can be modulated makes it difficult to predict its precise outcome.

      The present review aims at identifying and characterizing the various cognitive domains affected by tDCS over DLPFC.

      Articles using tDCS over DLPFC indexed in PubMed and published between January 2000 and January 2014 were included in the present review.

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      We aimed to investigate the effects and safety of repetitive transcranial direct current stimulation (tDCS) on apathy in moderate AD patients.

      Forty patients were randomized to receive either active or sham-tDCS over the left dorsolateral prefrontal cortex (DLPFC). Patients received six sessions of intervention during 2 weeks and were evaluated at baseline, at week 1 and 2, and after 1 week without intervention. Clinical raters, patients, and caregivers were blinded. The primary outcome was apathy. Global cognition and neuropsychiatric symptoms were examined as secondary outcomes.

      The mean MMSE score at baseline was 15.2±2.9 and the mean Apathy Scale score was 27.7±6.7. Changes on apathy scores over time were not different between active and sham tDCS (P=0.552 for repeated measures). Further analyses confirm that changes from baseline did not differ between groups after the sixth session (active tDCS−1.95 (95%CI−3.49,−0.41); sham-tDCS−2.05 (95%CI−3.68,−0.42); P=0.989]. Similarly, tDCS had no effect on secondary outcomes (P>0.40). tDCS was well tolerated and not associated with significant adverse effects.

      In this adequately powered study for minimal clinically significant difference, our findings show that using the parameters we chose for this study, repeated anodal tDCS over the left DLPFC had no effect on apathy in elderly patients with moderate AD.

    • Research article

      Testing the limits: Investigating the effect of tDCS dose on working memory enhancement in healthy controls

      Neuropsychologia, Volume 51, Issue 9, 2013, pp. 1777-1784

      Transcranial Direct Current Stimulation (tDCS) is a non-invasive form of brain stimulation which has been shown to induce changes in brain activity and subsequent functioning. In particular, there is a rapidly growing evidence base showing that anodal tDCS applied to the left prefrontal cortex (PFC) is able to enhance aspects of cognitive functioning, in particular working memory (WM). This has led to both excitement and concerns regarding the possibility of ‘electrodoping’ in order to greatly improve one's cognitive performance. We investigated the behavioural and neurophysiological effects of increasing the current (or ‘dose’) of tDCS on the degree of WM improvement in healthy controls. Single sessions of 1mA, 2mA and sham anodal tDCS to the left PFC were undertaken over a period of three weeks. Participants underwent a WM task at three time points post-stimulation (0, 20 and 40min) with concurrent electrophysiological (EEG) recordings. Our results showed that while active tDCS can enhance behavioural performance, with neurophysiological findings indicating improve efficiency of cognitive processing; we showed that 1mA produced the most significant effects. These findings are somewhat unexpected as tDCS dose effects in cognitive enhancement have been shown previously in patient populations. Our results provide valuable information regarding the potential limits of tDCS induced cognitive enhancement in healthy controls, as well as providing additional insights into the possible mechanisms of action of tDCS.

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