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Journal ArticleDOI

Effects of tDCS on motor learning and memory formation: A consensus and critical position paper

TL;DR: Overall, reproducibility remains to be fully tested, effect sizes with present techniques vary over a wide range, and the basis of observed inter-individual variability in tDCS effects is incompletely understood.
About: This article is published in Clinical Neurophysiology.The article was published on 2017-04-01 and is currently open access. It has received 247 citations till now. The article focuses on the topics: Motor learning.

Summary (2 min read)

1. Introduction

  • Understanding the physics of quantum interacting systems is one of the most challenging problems of condensed matter physics.
  • This is specially true in low dimensions where the interaction effects are usually reinforced by the dimensional confinement and lead to novel physics.
  • And despite remarkable success in realizing and probing one dimensional systems, they still suffer from limitations coming from either the confining potential, that corresponds to a space varying chemical potential and thus blurs the exponents, or limitations of interactions for the systems without the confining potential (see e.g. [9, 10]).
  • Comparison between such calculations and experimental results on the metal-organic spin ladder [15] piperidinium copper bromide (C5H12N)2CuBr4, short (Hpip)2CuBr4, have provided the first quantitative test of the TLL theory [16, 17, 18, 19].

2.1. Compound

  • Recent successes in the synthesis and the growth of single crystals of new metal–organic compounds have opened up exciting new routes for experimental studies of model magnetic materials.
  • In (Hpip)2CuBr4 the magnetic Cu 2+ ions with quantum spin S = 1/2 form one– dimensional ladder–like structural units.
  • Possible interladder exchange (J ′) is very small due to the large organic (C5H12N)+ piperidinium ion effectively separating the ladder units.
  • While only experiments by neutron inelastic scattering are able to unambiguously determine the exchange Hamiltonian of such a spin system [21], also measurements of bulk magnetic properties, such as the uniform magnetization with clear square–root field–dependencies near the critical magnetic fields, may indicate the excellent low– dimensionality of a material [15, 16].
  • Since the Br/Cl–site affects the super–exchange paths, one can thus expect a modification of the value of the exchange parameters.

2.2. Theoretical description

  • The authors thus have two quantum phase transitions.
  • The triplets are of course interacting due to the magnetic exchange.
  • For h > hc2 the whole band of triplets has been filled and the system is gapped again.
  • For the (Hpip)2CuBr4 compound the parameters are indicated in Table 1, and were determined using this technique and NMR measurements of the magnetization [16].

3.1. Theoretical methodology

  • In order to make predictions that can be compared with experiments, the authors need to compute e.g. magnetization and specific heat for the Hamiltonian (1).
  • The theoretical results are obtained using the variants of the density-matrix renormalization group method or also called matrix product state algorithms [32, 33, 34, 35].
  • The numerical method has been proven very powerful in particular describing the ground state or dynamic properties of one-dimensional systems at zero or finite temperature.
  • Here the authors use the auxiliary state variant [36, 37, 38] in order to calculate thermodynamic properties as the magnetization or the specific heat at finite temperature.
  • In the calculations the authors obtained converged results for systems of L = 60 rungs, keeping m = 96 states for the Hilbert space of each block.

3.2. Results and comparisons

  • The slope of the specific heat is directly connected to the speed u of the spin excitation in the TLL by Cm(T ) ∝ T/u [2].
  • As for the high field data the gap is again clearly visible and goes down as the field approaches hc1.
  • The lattice contribution can be subtracted following a procedure that was applied successfully to (Hpip)2CuBr4 [17].
  • It also confirms that the values of the exchange parameters that were determined by an independent method from the critical fields hc1 and hc2 are indeed accurate and more precise than in previous studies [30].

4. Discussion and Conclusion

  • The authors have presented in this paper a determination of the Hamiltonian and of the exchange parameters that describe the compound (Hpip)2CuCl4.
  • The comparison between the measured specific heat in this compound and the calculations, using Density Matrix Renormalization Group calculations, show unambiguously that this compound is very well described by a spin ladder Heisenberg Hamiltonian.
  • The Hamiltonian and general phase diagram of (Hpip)2CuCl4 are similar to the ones of the parent compound (Hpip)2CuBr4, albeit with different exchange constants, and thus different critical fields as shown in Fig.
  • Indeed the substitution of a small concentration of Br– by Cl– will amount to locally change the exchange constants, or in the itinerant particle language to which the triplet excitation can be mapped, to realize a TLL with space dependent hopping and chemical potential.
  • Such a material should thus be a system of choice to tackle the effect of disorder in one dimensional systems, such as the existence and properties of the Bose glass.

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Journal ArticleDOI
TL;DR: The state of non-invasive brain stimulation research in humans is summarized, some current debates about properties and limitations of these methods are discussed, and recommendations for how these challenges may be addressed are given.
Abstract: In the past three decades, our understanding of brain–behavior relationships has been significantly shaped by research using non-invasive brain stimulation (NIBS) techniques. These methods allow non-invasive and safe modulation of neural processes in the healthy brain, enabling researchers to directly study how experimentally altered neural activity causally affects behavior. This unique property of NIBS methods has, on the one hand, led to groundbreaking findings on the brain basis of various aspects of behavior and has raised interest in possible clinical and practical applications of these methods. On the other hand, it has also triggered increasingly critical debates about the properties and possible limitations of these methods. In this review, we discuss these issues, clarify the challenges associated with the use of currently available NIBS techniques for basic research and practical applications, and provide recommendations for studies using NIBS techniques to establish brain–behavior relationships.

544 citations

Journal ArticleDOI
TL;DR: An overview of the current knowledge available regarding physiological mechanisms of tDCS, spanning from acute regional effects, over neuroplastic effects to its impact on cerebral networks is given.
Abstract: Direct current stimulation is a neuromodulatory noninvasive brain stimulation tool, which was first introduced in animal and human experiments in the 1950s, and added to the standard arsenal of methods to alter brain physiology as well as psychological, motor, and behavioral processes and clinical symptoms in neurological and psychiatric diseases about 20 years ago. In contrast to other noninvasive brain stimulation tools, such as transcranial magnetic stimulation, it does not directly induce cerebral activity, but rather alters spontaneous brain activity and excitability by subthreshold modulation of neuronal membranes. Beyond acute effects on brain functions, specific protocols are suited to induce long-lasting alterations of cortical excitability and activity, which share features with long-term potentiation and depression. These neuroplastic processes are important foundations for various cognitive functions such as learning and memory formation and are pathologically altered in numerous neurological and psychiatric diseases. This explains the increasing interest to investigate transcranial direct current stimulation (tDCS) as a therapeutic tool. However, for tDCS to be used effectively, it is crucial to be informed about physiological mechanisms of action. These have been increasingly elucidated during the last years. This review gives an overview of the current knowledge available regarding physiological mechanisms of tDCS, spanning from acute regional effects, over neuroplastic effects to its impact on cerebral networks. Although knowledge about the physiological effects of tDCS is still not complete, this might help to guide applications on a scientifically sound foundation.

237 citations

Journal ArticleDOI
TL;DR: This update broadened the inclusion criteria to compare any kind of active tDCS for improving ADLs, function, muscle strength and cognitive abilities (including spatial neglect) versus anykind of placebo or control intervention.
Abstract: Background Stroke is one of the leading causes of disability worldwide. Functional impairment, resulting in poor performance in activities of daily living (ADLs) among stroke survivors is common. Current rehabilitation approaches have limited effectiveness in improving ADL performance, function, muscle strength and cognitive abilities (including spatial neglect) after stroke, but a possible adjunct to stroke rehabilitation might be non-invasive brain stimulation by transcranial direct current stimulation (tDCS) to modulate cortical excitability, and hence to improve ADL performance, arm and leg function, muscle strength and cognitive abilities (including spatial neglect), dropouts and adverse events in people after stroke. Objectives To assess the effects of tDCS on ADLs, arm and leg function, muscle strength and cognitive abilities (including spatial neglect), dropouts and adverse events in people after stroke. Search methods We searched the Cochrane Stroke Group Trials Register (February 2015), the Cochrane Central Register of Controlled Trials (CENTRAL; the Cochrane Library; 2015, Issue 2), MEDLINE (1948 to February 2015), EMBASE (1980 to February 2015), CINAHL (1982 to February 2015), AMED (1985 to February 2015), Science Citation Index (1899 to February 2015) and four additional databases. In an effort to identify further published, unpublished and ongoing trials, we searched trials registers and reference lists, handsearched conference proceedings and contacted authors and equipment manufacturers. Selection criteria This is the update of an existing review. In the previous version of this review we focused on the effects of tDCS on ADLs and function. In this update, we broadened our inclusion criteria to compare any kind of active tDCS for improving ADLs, function, muscle strength and cognitive abilities (including spatial neglect) versus any kind of placebo or control intervention. Data collection and analysis Two review authors independently assessed trial quality and risk of bias (JM and MP) and extracted data (BE and JM). If necessary, we contacted study authors to ask for additional information. We collected information on dropouts and adverse events from the trial reports. Main results We included 32 studies involving a total of 748 participants aged above 18 with acute, postacute or chronic ischaemic or haemorrhagic stroke. We also identified 55 ongoing studies. The risk of bias did not differ substantially for different comparisons and outcomes. We found nine studies with 396 participants examining the effects of tDCS versus sham tDCS (or any other passive intervention) on our primary outcome measure, ADLs after stroke. We found evidence of effect regarding ADL performance at the end of the intervention period (standardised mean difference (SMD) 0.24, 95% confidence interval (CI) 0.03 to 0.44; inverse variance method with random-effects model; moderate quality evidence). Six studies with 269 participants assessed the effects of tDCS on ADLs at the end of follow-up, and found improved ADL performance (SMD 0.31, 95% CI 0.01 to 0.62; inverse variance method with random-effects model; moderate quality evidence). However, the results did not persist in a sensitivity analysis including only trials of good methodological quality. One of our secondary outcome measures was upper extremity function: 12 trials with a total of 431 participants measured upper extremity function at the end of the intervention period, revealing no evidence of an effect in favour of tDCS (SMD 0.01, 95% CI -0.48 to 0.50 for studies presenting absolute values (low quality evidence) and SMD 0.32, 95% CI -0.51 to 1.15 (low quality evidence) for studies presenting change values; inverse variance method with random-effects model). Regarding the effects of tDCS on upper extremity function at the end of follow-up, we identified four studies with a total of 187 participants (absolute values) that showed no evidence of an effect (SMD 0.01, 95% CI -0.48 to 0.50; inverse variance method with random-effects model; low quality evidence). Ten studies with 313 participants reported outcome data for muscle strength at the end of the intervention period, but in the corresponding meta-analysis there was no evidence of an effect. Three studies with 156 participants reported outcome data on muscle strength at follow-up, but there was no evidence of an effect. In six of 23 studies (26%), dropouts, adverse events or deaths that occurred during the intervention period were reported, and the proportions of dropouts and adverse events were comparable between groups (risk difference (RD) 0.01, 95% CI -0.02 to 0.03; Mantel-Haenszel method with random-effects model; low quality evidence; analysis based only on studies that reported either on dropouts, or on adverse events, or on both). However, this effect may be underestimated due to reporting bias. Authors' conclusions At the moment, evidence of very low to moderate quality is available on the effectiveness of tDCS (anodal/cathodal/dual) versus control (sham/any other intervention) for improving ADL performance after stroke. However, there are many ongoing randomised trials that could change the quality of evidence in the future. Future studies should particularly engage those who may benefit most from tDCS after stroke and in the effects of tDCS on upper and lower limb function, muscle strength and cognitive abilities (including spatial neglect). Dropouts and adverse events should be routinely monitored and presented as secondary outcomes. They should also address methodological issues by adhering to the Consolidated Standards of Reporting Trials (CONSORT) statement.

177 citations

Journal ArticleDOI
TL;DR: Understanding dose- response in human applications of tDCS is needed for protocol optimization including individualized dose to reduce outcome variability, which requires intelligent design of dose-response studies.

131 citations

References
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TL;DR: An Explanation and Elaboration of the PRISMA Statement is presented and updated guidelines for the reporting of systematic reviews and meta-analyses are presented.
Abstract: Systematic reviews and meta-analyses are essential to summarize evidence relating to efficacy and safety of health care interventions accurately and reliably. The clarity and transparency of these reports, however, is not optimal. Poor reporting of systematic reviews diminishes their value to clinicians, policy makers, and other users. Since the development of the QUOROM (QUality Of Reporting Of Meta-analysis) Statement—a reporting guideline published in 1999—there have been several conceptual, methodological, and practical advances regarding the conduct and reporting of systematic reviews and meta-analyses. Also, reviews of published systematic reviews have found that key information about these studies is often poorly reported. Realizing these issues, an international group that included experienced authors and methodologists developed PRISMA (Preferred Reporting Items for Systematic reviews and Meta-Analyses) as an evolution of the original QUOROM guideline for systematic reviews and meta-analyses of evaluations of health care interventions. The PRISMA Statement consists of a 27-item checklist and a four-phase flow diagram. The checklist includes items deemed essential for transparent reporting of a systematic review. In this Explanation and Elaboration document, we explain the meaning and rationale for each checklist item. For each item, we include an example of good reporting and, where possible, references to relevant empirical studies and methodological literature. The PRISMA Statement, this document, and the associated Web site (http://www.prisma-statement.org/) should be helpful resources to improve reporting of systematic reviews and meta-analyses.

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TL;DR: This Explanation and Elaboration document explains the meaning and rationale for each checklist item and includes an example of good reporting and, where possible, references to relevant empirical studies and methodological literature.

8,021 citations


"Effects of tDCS on motor learning a..." refers background in this paper

  • ...A concerted effort by investigators in clinical research to address these issues has culminated in the PRISMA statement (Liberati et al., 2009), which included guidelines and a checklist for best practices (see http:// www.prisma-statement.org/ for more information)....

    [...]

  • ...A concerted effort by investigators in clinical research to address these issues has culminated in the PRISMA statement (Liberati et al., 2009), which included guidelines and a checklist for best practices (see http:// www....

    [...]

Journal ArticleDOI
TL;DR: An overview of the state of the art for transcranial direct current stimulation (tDCS) is offered, which suggests that it can induce beneficial effects in brain disorders and facilitate and standardize future tDCS studies.

2,539 citations


"Effects of tDCS on motor learning a..." refers methods in this paper

  • ...…the glia in tDCS-mediated effects represents a new area of investigation (Gellner et al., 2016). tDCS has also been used as a tool to gain insight into possible causal relationships between altered activity in relatively large regions of the brain and particular behaviors (Nitsche et al., 2008)....

    [...]

Journal ArticleDOI
TL;DR: The authors show that in the human transcranial direct current stimulation is able to induce sustained cortical excitability elevations, and this technique is a potentially valuable tool in neuroplasticity modulation.
Abstract: The authors show that in the human transcranial direct current stimulation is able to induce sustained cortical excitability elevations. As revealed by transcranial magnetic stimulation, motor cortical excitability increased approximately 150% above baseline for up to 90 minutes after the end of stimulation. The feasibility of inducing long-lasting excitability modulations in a noninvasive, painless, and reversible way makes this technique a potentially valuable tool in neuroplasticity modulation.

2,289 citations


"Effects of tDCS on motor learning a..." refers background in this paper

  • ..., 2015b) but the nature and magnitude of these effects are variable across individuals (Nitsche and Paulus, 2001; Hamada et al., 2013; Wiethoff et al., 2014; Nettekoven et al., 2015)....

    [...]

  • ...…tDCS on motor cortical excitability appear to be relatively stable over prolonged time courses (Lopez-Alonso et al., 2015b) but the nature and magnitude of these effects are variable across individuals (Nitsche and Paulus, 2001; Hamada et al., 2013; Wiethoff et al., 2014; Nettekoven et al., 2015)....

    [...]

Journal ArticleDOI
TL;DR: Spread of excitation, which may be a warning sign for seizures, occurred in one subject and was not accompanied by increased MEP amplitude, suggesting that spread ofexcitation and amplitude changes are different phenomena and also indicating the need for adequate monitoring even with stimulations at low frequencies.
Abstract: We studied the effects of low-frequency transcranial magnetic stimulation (TMS) on motor cortex excitability in humans. TMS at 0.1 Hz for 1 hour did not change cortical excitability. Stimulation at 0.9 Hz for 15 minutes (810 pulses), similar to the parameters used to induce long-term depression (LTD) in cortical slice preparations and in vivo animal studies, led to a mean decrease in motor evoked potential (MEP) amplitude of 19.5%. The decrease in cortical excitability lasted for at least 15 minutes after the end of the 0.9 Hz stimulation. The mechanism underlying this decrease in excitability may be similar to LTD. TMS-induced reduction of cortical excitability has potential clinical applications in diseases such as epilepsy and myoclonus. Spread of excitation, which may be a warning sign for seizures, occurred in one subject and was not accompanied by increased MEP amplitude, suggesting that spread of excitation and amplitude changes are different phenomena and also indicating the need for adequate monitoring even with stimulations at low frequencies.

2,013 citations


"Effects of tDCS on motor learning a..." refers background in this paper

  • ...It has been argued that rTMS and tDCS can either enhance or decrease excitability in targeted cortical regions depending on the parameters of stimulation employed (Chen et al., 1997; Galea et al., 2009; Labruna et al., 2016; Woods et al., 2016) and the underlying intrinsic state of the stimulated brain networks (Silvanto et al....

    [...]

  • ...…that rTMS and tDCS can either enhance or decrease excitability in targeted cortical regions depending on the parameters of stimulation employed (Chen et al., 1997; Galea et al., 2009; Labruna et al., 2016; Woods et al., 2016) and the underlying intrinsic state of the stimulated brain networks…...

    [...]

Frequently Asked Questions (14)
Q1. What have the authors contributed in "Effects of tdcs on motor learning and memory formation: a consensus and critical position paper" ?

A growing body of work continues to support the use of non-invasive brain stimulation as a tool for neuromodulation of motor learning this paper. 

Furthermore, under-reporting of negative effects ( Horvath et al., 2015b ) due to publication bias ( Mancuso, Ilieva, Hamilton, & Farah, 2016 ; Shiozawa et al., 2014 ; Vannorsdall et al., 2016 ) represents another important scientific caveat that must be addressed in order to facilitate future research progress. As nuanced understanding of the possibilities and limitations of a given experimental technique matures, critical evaluation amongst experts leads to the progressive refinement of standards associated with its use. These circumstances limit the information that can be drawn from the effects of tDCS on those tasks. Therefore, better understanding of motor learning processes and the tasks used to assess them will be critical to determine whether NIBS can or can not manipulate behaviors that are potentially impactful to daily life. 

Following three days of training in each task with concurrent application of sham or anodal tDCS applied over M1, they observed that anodal stimulation improved online sequence learning, but only skill retention for the pinch force task. 

A growing body of work continues to support the use of noninvasive brain stimulation as a tool for neuromodulation of motor learning. 

Concurrent application of anodal tDCS with training also appears crucial for these effects to emerge as stimulation applied post-training only did not induce offline skill gains, consistent with the finding that tDCS alone does not elicit LTP unless it is associated with a second input delivered to the motor cortex in rodents (Fritsch et al., 2010). 

in a force-field reaching task that assesses adaptation to perturbed upper limb dynamics, anodal tDCS applied to the cerebellum increased error-dependent learning and facilitated adaptation, while M1 stimulation had no effect (Herzfeld et al., 2014). 

In a follow-up study, effects mediated by consolidation processes were further supported as offline skill gains induced by anodal tDCS were found to be dependent upon the passage of time, as opposed to requiring overnight sleep (Reis et al., 2015). 

replicability is best tested for stochastic data using Bayesian paradigms of accumulating evidence more than binary criteria of successful or unsuccessful replication (Goodman et al., 2016). 

Over longer periods of time, such as over several hours, days or training sessions, motor memories may transition to a consolidation phase (Gais et al., 2007; Marshall & Born, 2007; Stickgold, 2005; Walker, Brakefield, Hobson, & Stickgold, 2003). 

Each time a given skill is executed, retrieval of these previously consolidated motor memories may initiate a cascade of plasticity mechanisms that enable their composition to be modified in order to maintain skill performance optimization over the long term (Censor, Buch, Nader, & Cohen, 2015; Censor, Dayan, & Cohen, 2014; Censor, Dimyan, & Cohen, 2010; Censor, Horovitz, & Cohen, 2014; Dayan, Laor-Maayany, & Censor, 2016; Wymbs et al., 2016). 

The applied perturbations can be designed to affect either limb kinematics or dynamics, and typically involve rotating visual feedback representations of the movement (Krakauer, Ghilardi, & Ghez, 1999) or applying external forces to the moving limb via a robotic manipulandum (Smith, Brandt, & Shadmehr, 2000), respectively. 

Since published findings using rTMS, TBS, tACS and tRNS for enhancing motor learning remain particularly sparse (Figure 1) the primary focus of the review will be on tDCSbased interventions. 

An interesting approach to address the issue of heterogeneity of stimulation protocols and tasks could be to directly account for the heterogeneity within statistical models through inclusion of stimulation parameters, electrode montages and task variants as covariates. 

(Goodman et al., 2016)A unique concern that has emerged with transcranial electrical stimulation techniques, isthat the simplicity, low-cost nature of, and public access to the technology has lead to the emergence of a popular do-it-yourself movement where individuals participate in selfexperimentation without oversight.