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Biomedical Optics Express

Biomedical Optics Express

  • Editor: Joseph A. Izatt
  • Vol. 5, Iss. 6 — Jun. 1, 2014
  • pp: 1812–1821
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Hemodynamic responses in rat brain during transcranial direct current stimulation: a functional near-infrared spectroscopy study

Chang-Hee Han, Hyuna Song, Yong-Guk Kang, Beop-Min Kim, and Chang-Hwan Im  »View Author Affiliations


Biomedical Optics Express, Vol. 5, Issue 6, pp. 1812-1821 (2014)
http://dx.doi.org/10.1364/BOE.5.001812


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Abstract

In the present study, we monitored hemodynamic responses in rat brains during transcranial direct current stimulation (tDCS) using functional near-infrared spectroscopy (fNIRS). Seven rats received transcranial anodal stimulation with 200 μA direct current (DC) on their right barrel cortex for 10 min. The concentration changes of oxygenated hemoglobin (oxy-Hb) were continuously monitored during stimulation (10 min) and after stimulation (20 min). The trend of hemodynamic response changes was modeled using linear regression, and the relationship between incremental and decremental rates of oxy-Hb was investigated by correlation analysis. Our results showed that the oxy-Hb concentration was almost linearly increased and decreased during and after stimulation, respectively. In addition, a significant negative correlation (p < 0.05) was found between the rate of increase of oxy-Hb during stimulation and the rate of decrease of oxy-Hb after stimulation, indicating that the recovery time after tDCS may not depend on the total amount of hemodynamic changes in the stimulated brain area. Our results also demonstrated considerable individual variability in the rate of change of hemodynamic responses even with the same direct current dose to identical brain regions. This suggests that individual differences in tDCS after-effects may originate from intrinsic differences in the speed of DC stimulation “uptake” rather than differences in the total capacity of DC uptake, and thus the stimulation parameters may need to be customized for each individual in order to maximize tDCS after-effects.

© 2014 Optical Society of America

1. Introduction

Transcranial direct current stimulation (tDCS) is a noninvasive brain electrical stimulation technique that modulates cortical excitability with a small direct current (DC) flowing between a pair of scalp electrodes [1

1. M. A. Nitsche and W. Paulus, “Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation,” J. Physiol. 527(3), 633–639 (2000). [CrossRef] [PubMed]

]. Since tDCS can effectively facilitate or inhibit cortical excitability of specific brain areas by controlling the direction of stimulating current [2

2. A. Antal, T. Z. Kincses, M. A. Nitsche, O. Bartfai, and W. Paulus, “Excitability changes induced in the human primary visual cortex by transcranial direct current stimulation: direct electrophysiological evidence,” Invest. Ophthalmol. Vis. Sci. 45, 702–707 (2004).

4

4. T. Wagner, A. Valero-Cabre, and A. Pascual-Leone, “Noninvasive human brain stimulation,” Annu. Rev. Biomed. Eng. 9(1), 527–565 (2007). [CrossRef] [PubMed]

], it has recently attracted increased attention from the neuroscience society. tDCS has several advantages over other neuromodulation modalities such as deep brain stimulation (DBS) and transcranial magnetic stimulation (TMS) in that it is cheap, non-invasive, painless, portable, and safe [5

5. M. A. Nitsche, L. G. Cohen, E. M. Wassermann, A. Priori, N. Lang, A. Antal, W. Paulus, F. Hummel, P. S. Boggio, F. Fregni, and A. Pascual-Leone, “Transcranial direct current stimulation: state of the art 2008,” Brain Stimulat. 1(3), 206–223 (2008). [CrossRef] [PubMed]

8

8. P. C. Gandiga, F. C. Hummel, and L. G. Cohen, “Transcranial DC stimulation (tDCS): a tool for double-blind sham-controlled clinical studies in brain stimulation,” Clin. Neurophysiol. 117(4), 845–850 (2006). [CrossRef] [PubMed]

]. Several experimental studies have demonstrated that tDCS can be potentially used for the treatment of various neuropsychiatric diseases and neurological disorders including depression, anxiety, Parkinson’s disease, epilepsy, tinnitus, and chronic pain [9

9. M. A. Nitsche, P. S. Boggio, F. Fregni, and A. Pascual-Leone, “Treatment of depression with transcranial direct current stimulation (tDCS): a review,” Exp. Neurol. 219(1), 14–19 (2009). [CrossRef] [PubMed]

12

12. P. S. Boggio, A. Nunes, S. P. Rigonatti, M. A. Nitsche, A. Pascual-Leone, and F. Fregni, “Repeated sessions of noninvasive brain DC stimulation is associated with motor function improvement in stroke patients,” Restor. Neurol. Neurosci. 25(2), 123–129 (2007). [PubMed]

]. Furthermore, some recent studies have shown that tDCS could temporarily enhance cognitive functions such as working memory, performance of mental calculation, and attention in both patients and healthy people [13

13. P. S. Boggio, R. Ferrucci, S. P. Rigonatti, P. Covre, M. Nitsche, A. Pascual-Leone, and F. Fregni, “Effects of transcranial direct current stimulation on working memory in patients with Parkinson’s disease,” J. Neurol. Sci. 249(1), 31–38 (2006). [CrossRef] [PubMed]

15

15. T. U. Hauser, S. Rotzer, R. H. Grabner, S. Mérillat, and L. Jäncke, “Enhancing performance in numerical magnitude processing and mental arithmetic using transcranial Direct Current Stimulation (tDCS),” Front Hum. Neurosci. 7, 244 (2013). [CrossRef] [PubMed]

].

The aim of this study was to observe temporal changes of hemodynamic responses during and after tDCS. Seven rats received transcranial anodal stimulation with 200 μA direct current on their right barrel cortex for 10 min, and the concentration of oxy-Hb was continuously recorded using fNIRS. We also conducted linear regression analysis to model changes in oxy-Hb during and after tDCS. Then we performed correlation analysis to investigate the relationship between the rates of increase and decrease of oxy-Hb.

2. Materials and methods

2.1 Animal preparation

Twelve adult male Sprague-Dawley (SD) rats (body weight 300~350 g, see Fig. 1
Fig. 1 Configuration of tDCS electrodes and NIRS probes. Left and middle pictures show the experimental environments. Red circles in the rightmost figure indicate positions of detectors and sources of NIRS, and a blue circle indicates the position of the tDCS anodal electrode.
) were used for the experiment. However, five of them were excluded in the data processing due to gross systemic noises/artifacts in the signal or unexpected death during the experiment (see Fig. 2
Fig. 2 Examples of NIRS data excluded from our post-analyses due to gross systemic noises/artifacts. Both data were acquired from the stimulation side (ipsilateral hemisphere). A figure on the left panel shows an example NIRS signal excluded due to the large unexpected baseline contamination (marked with gray), while a figure on the right panel shows that excluded due to large variation in the baseline NIRS signal.
for examples of NIRS signals recorded from the excluded rats). All animals were anesthetized with inhalation of isoflurane mixed with oxygen under spontaneous respiration and fixed to a stereotaxic apparatus to minimize motion artifacts. Body temperature was maintained and monitored at 37 ± 5 °C using a heating pad. Respiratory activity and oxygen saturation (SpO2) were also monitored using a commercial pulse oximetry device (CANL-425SV-A, Med Associates, Inc., VT, USA). After each rat was anesthetized, the scalp was removed until the skull was exposed. All animals were cared for in accordance with the guidelines established by the Institutional Animal Care and Use Committee (IACUC) of Korea University, and they were sacrificed after the experiment.

2.2 Transcranial direct current stimulation (tDCS) setup

The tDCS system used for the experiment was developed by the Computational Neuroengineering Laboratory of Hanyang University. The system was originally designed for a 4-channel anodal tDCS system, but only a single anodal channel was used for this experiment. This system shares the same basic design concept of our recent array-type tDCS system with 16-channel anodes, of which the detailed information can be found in the literature [20

20. Y.-J. Jung, J.-H. Kim, D. Kim, and C.-H. Im, “An image-guided transcranial direct current stimulation system: a pilot phantom study,” Physiol. Meas. 34(8), 937–950 (2013). [CrossRef] [PubMed]

]. An anodal electrode made of a copper plate was placed onto the right barrel cortex areas (2 mm posterior from bregma and 5 mm lateral from the medial point) with a defined contact area (3.5 mm2) (see Fig. 1). A reference electrode was placed onto the ventral thorax of the restrained animal using a hammock. In our experiment, an Ag/AgCl electrode was used as the reference electrode. The anodal DC stimulation was applied at a current intensity of 200 μA for 10 min. The stimulation protocols and the electrode design were based on Liebetanz et al.’s study [21

21. D. Liebetanz, R. Koch, S. Mayenfels, F. König, W. Paulus, and M. A. Nitsche, “Safety limits of cathodal transcranial direct current stimulation in rats,” Clin. Neurophysiol. 120(6), 1161–1167 (2009). [CrossRef] [PubMed]

], which reported safe stimulation of rat brains without generation of lesions. They reported that brain lesions were not generated at a current density smaller than 142.9 A/m2 when rats were stimulated for less than 10 minutes. We determined the stimulation current intensity (200 μA) considering the contact area of an anodal electrode (3.5 mm2) and the stimulation duration (10-min). We set the average current density to be about a third of the safety limit considering the edge effect on the electrode [22

22. P. Minhas, A. Datta, and M. Bikson, “Cutaneous perception during tDCS: role of electrode shape and sponge salinity,” Clin. Neurophysiol. 122(4), 637–638 (2011). [CrossRef] [PubMed]

]. To consistently flow a constant direct current, we continuously monitored whether the stimulating current was normally flowing using a multimeter connected between a pair of tDCS electrodes. We confirmed that our tDCS system transmitted the designated amount of direct current consistently during the entire experiment.

2.3 Near-infrared spectroscopy (NIRS) setup

Changes in hemoglobin concentration were measured using a commercial multi-channel frequency domain NIRS system (Imagent, ISS, IL, USA). Each channel consists of a pair of light sources which use two different wavelengths, 690 and 830 nm, and one detector. Two of these channels, one per each hemisphere, were placed onto a rat skull using 400 μm core diameter optical fibers (FT-400EMT, Thorlabs, NJ, USA) as shown in Fig. 1. The distance between the source and detector was 1 cm, which was sufficient to detect neural responses under the tDCS electrode [23

23. G. Paxinos and C. Watson, The Rat Brain in Stereotaxic Coordinates: Hard Cover Edition (Access Online via Elsevier, 2006).

]. In this way, neural responses between stimulated and normal brain regions could be compared. NIRS signals were acquired at a sampling rate of 31.25 Hz. This NIRS system could detect changes in cortical concentration levels of oxygenated hemoglobin (oxy-Hb), deoxygenated hemoglobin (deoxy-Hb), and total hemoglobin (total-Hb) by applying the modified Beer-Lambert law (see Section 2.4) [24

24. G. Strangman, M. A. Franceschini, and D. A. Boas, “Factors affecting the accuracy of near-infrared spectroscopy concentration calculations for focal changes in oxygenation parameters,” Neuroimage 18(4), 865–879 (2003). [CrossRef] [PubMed]

].

2.4 NIRS data processing

We divided oxy-Hb data measured in each rat into two segments acquired during and after tDCS, then each segment was fitted with a first-order polynomial using a curve fitting toolbox implemented in MATLAB 2009a (Mathworks Inc., MA, USA). In this procedure, only concentration changes of oxy-Hb were used because the concentration of deoxy-Hb showed much smaller changes than that of oxy-Hb. After the curve fitting, the slope values of incremental (during tDCS) and decremental (after tDCS) periods were evaluated for each rat. We then performed a correlation analysis to investigate the relationship between the rates of increase and decrease of oxy-Hb. Pearson correlation coefficient and p-value were evaluated using a software package for statistics, SPSS 18.0 (IBM Inc., NY, USA). In this analysis, a significance level was set at less than 0.05.

3. Results

Figure 4
Fig. 4 Concentration changes of oxy-Hb during and after tDCS in each rat. A blue vertical line in each panel indicates the end of tDCS. Red solid lines in each graph present the first-order polynomial obtained from linear regression of the data.
shows the individual concentration changes of oxy-Hb in seven rats. Similar to the grand averaged waveforms shown in Fig. 3, the oxy-Hb in each rat almost linearly increased during tDCS and linearly decreased immediately after the termination of tDCS. Each of the increasing and decreasing periods of oxy-Hb signals was fitted with a first-order polynomial (red lines in Fig. 4). As seen in the figure, the incremental and decremental periods could be modeled well with first-order polynomials. However, regardless of identical experimental conditions, the degrees of change were remarkably different in each rat. Interestingly, the concentration of oxy-Hb after tDCS showed a decreasing trend in proportion to the increasing slope during DC stimulation; that is to say, when oxy-Hb increased rapidly during tDCS, it also decreased rapidly after tDCS. Likewise, when oxy-Hb increased slowly during tDCS, it also decreased slowly after tDCS. Rats 1, 2, 3, and 4 showed a relatively rapid increase and decrease of oxy-Hb, while rats 5, 6, and 7 showed a relatively slower increase and decrease.

To confirm this visual inspection, a correlation between the rates of increase and decrease of oxy-Hb was evaluated. The slope values of incremental and decremental periods for each rat are plotted in Fig. 5
Fig. 5 Relationship between slope values in incremental and decremental phases
. The correlation analysis showed a statistically significant negative correlation between the two variables (Pearson correlation coefficient = −0.769, p = 0.043). Our findings suggest that each individual may have intrinsic differences in the speed of “uptake” (and restoration) of DC currents rather than uptake capacity, which implies that stimulation parameters such as stimulation duration and current strength need to be customized individually to facilitate improved tDCS after-effects.

4. Discussion

In most practical applications of tDCS, stimulation parameters such as stimulation duration and DC current strength are identically applied to all individuals participating in the tDCS experiments [31

31. C. K. Loo, A. Alonzo, D. Martin, P. B. Mitchell, V. Galvez, and P. Sachdev, “Transcranial direct current stimulation for depression: 3-week, randomised, sham-controlled trial,” Br. J. Psychiatry 200(1), 52–59 (2012). [CrossRef] [PubMed]

, 33

33. Á. Foerster, S. Rocha, C. Wiesiolek, A. P. Chagas, G. Machado, E. Silva, F. Fregni, and K. Monte-Silva, “Site-specific effects of mental practice combined with transcranial direct current stimulation on motor learning,” Eur. J. Neurosci. 37(5), 786–794 (2013). [CrossRef] [PubMed]

, 34

34. U. Palm, C. Schiller, Z. Fintescu, M. Obermeier, D. Keeser, E. Reisinger, O. Pogarell, M. A. Nitsche, H.-J. Möller, and F. Padberg, “Transcranial direct current stimulation in treatment resistant depression: a randomized double-blind, placebo-controlled study,” Brain Stimulat. 5(3), 242–251 (2012). [CrossRef] [PubMed]

]. According to our findings, these parameters need to be customized for each individual in order to maximize tDCS after-effects and reduce individual variability. It is expected that the customized stimulation strategy may enhance the efficacy of clinical tDCS applications. For example, some side-effects of tDCS such as mild headache and dizziness might be reduced by decreasing stimulation duration for individuals whose neural excitability is modulated rapidly. On the other hands, enhanced tDCS after-effects can be expected by increasing the stimulation duration for individuals whose neural excitability is modulated relatively slowly. Our results also suggest that fNIRS might be a useful tool for predicting the tDCS after-effects of individuals as well as designing individual-specific stimulation protocols when recorded simultaneously during tDCS. Importantly, this area of research needs to be investigated further in future studies with human subjects.

Acknowledgments

This research was supported in part by the National Research Foundation of Korea (NRF) grant funded by the Korean government (MSIP) (No. NRF-2012R1A2A2A03045395) and a grant of the Korea Health Technology R&D Project through the Korea Health Industry Development Institute (KHIDI), funded by the Ministry of Health & Welfare, Republic of Korea (No: HI13C1501).

References and links

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M. A. Nitsche and W. Paulus, “Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation,” J. Physiol. 527(3), 633–639 (2000). [CrossRef] [PubMed]

2.

A. Antal, T. Z. Kincses, M. A. Nitsche, O. Bartfai, and W. Paulus, “Excitability changes induced in the human primary visual cortex by transcranial direct current stimulation: direct electrophysiological evidence,” Invest. Ophthalmol. Vis. Sci. 45, 702–707 (2004).

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F. Fregni, P. S. Boggio, M. Nitsche, and A. Pascual-Leone, “Transcranial direct current stimulation,” Br. J. Psychiatry 186(5), 446–447 (2005). [CrossRef] [PubMed]

4.

T. Wagner, A. Valero-Cabre, and A. Pascual-Leone, “Noninvasive human brain stimulation,” Annu. Rev. Biomed. Eng. 9(1), 527–565 (2007). [CrossRef] [PubMed]

5.

M. A. Nitsche, L. G. Cohen, E. M. Wassermann, A. Priori, N. Lang, A. Antal, W. Paulus, F. Hummel, P. S. Boggio, F. Fregni, and A. Pascual-Leone, “Transcranial direct current stimulation: state of the art 2008,” Brain Stimulat. 1(3), 206–223 (2008). [CrossRef] [PubMed]

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A. Priori, “Brain polarization in humans: a reappraisal of an old tool for prolonged non-invasive modulation of brain excitability,” Clin. Neurophysiol. 114(4), 589–595 (2003). [CrossRef] [PubMed]

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J. A. Williams, M. Imamura, and F. Fregni, “Updates on the use of non-invasive brain stimulation in physical and rehabilitation medicine,” J. Rehabil. Med. 41(5), 305–311 (2009). [CrossRef] [PubMed]

8.

P. C. Gandiga, F. C. Hummel, and L. G. Cohen, “Transcranial DC stimulation (tDCS): a tool for double-blind sham-controlled clinical studies in brain stimulation,” Clin. Neurophysiol. 117(4), 845–850 (2006). [CrossRef] [PubMed]

9.

M. A. Nitsche, P. S. Boggio, F. Fregni, and A. Pascual-Leone, “Treatment of depression with transcranial direct current stimulation (tDCS): a review,” Exp. Neurol. 219(1), 14–19 (2009). [CrossRef] [PubMed]

10.

F. Fregni, S. Freedman, and A. Pascual-Leone, “Recent advances in the treatment of chronic pain with non-invasive brain stimulation techniques,” Lancet Neurol. 6(2), 188–191 (2007). [CrossRef] [PubMed]

11.

A. Mignon, V. Laudenbach, F. Guischard, A. Limoge, J.-M. Desmonts, and J. Mantz, “Transcutaneous cranial electrical stimulation (Limoge’s currents) decreases early buprenorphine analgesic requirements after abdominal surgery,” Anesth. Analg. 83(4), 771–775 (1996). [PubMed]

12.

P. S. Boggio, A. Nunes, S. P. Rigonatti, M. A. Nitsche, A. Pascual-Leone, and F. Fregni, “Repeated sessions of noninvasive brain DC stimulation is associated with motor function improvement in stroke patients,” Restor. Neurol. Neurosci. 25(2), 123–129 (2007). [PubMed]

13.

P. S. Boggio, R. Ferrucci, S. P. Rigonatti, P. Covre, M. Nitsche, A. Pascual-Leone, and F. Fregni, “Effects of transcranial direct current stimulation on working memory in patients with Parkinson’s disease,” J. Neurol. Sci. 249(1), 31–38 (2006). [CrossRef] [PubMed]

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B. A. Coffman, M. C. Trumbo, and V. P. Clark, “Enhancement of object detection with transcranial direct current stimulation is associated with increased attention,” BMC Neurosci. 13(1), 108 (2012). [CrossRef] [PubMed]

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T. U. Hauser, S. Rotzer, R. H. Grabner, S. Mérillat, and L. Jäncke, “Enhancing performance in numerical magnitude processing and mental arithmetic using transcranial Direct Current Stimulation (tDCS),” Front Hum. Neurosci. 7, 244 (2013). [CrossRef] [PubMed]

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Y.-J. Jung, J.-H. Kim, D. Kim, and C.-H. Im, “An image-guided transcranial direct current stimulation system: a pilot phantom study,” Physiol. Meas. 34(8), 937–950 (2013). [CrossRef] [PubMed]

21.

D. Liebetanz, R. Koch, S. Mayenfels, F. König, W. Paulus, and M. A. Nitsche, “Safety limits of cathodal transcranial direct current stimulation in rats,” Clin. Neurophysiol. 120(6), 1161–1167 (2009). [CrossRef] [PubMed]

22.

P. Minhas, A. Datta, and M. Bikson, “Cutaneous perception during tDCS: role of electrode shape and sponge salinity,” Clin. Neurophysiol. 122(4), 637–638 (2011). [CrossRef] [PubMed]

23.

G. Paxinos and C. Watson, The Rat Brain in Stereotaxic Coordinates: Hard Cover Edition (Access Online via Elsevier, 2006).

24.

G. Strangman, M. A. Franceschini, and D. A. Boas, “Factors affecting the accuracy of near-infrared spectroscopy concentration calculations for focal changes in oxygenation parameters,” Neuroimage 18(4), 865–879 (2003). [CrossRef] [PubMed]

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K. Weltman and M. Lavidor, “Modulating lexical and semantic processing by transcranial direct current stimulation,” Exp. Brain Res. 226(1), 121–135 (2013). [CrossRef] [PubMed]

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Á. Foerster, S. Rocha, C. Wiesiolek, A. P. Chagas, G. Machado, E. Silva, F. Fregni, and K. Monte-Silva, “Site-specific effects of mental practice combined with transcranial direct current stimulation on motor learning,” Eur. J. Neurosci. 37(5), 786–794 (2013). [CrossRef] [PubMed]

34.

U. Palm, C. Schiller, Z. Fintescu, M. Obermeier, D. Keeser, E. Reisinger, O. Pogarell, M. A. Nitsche, H.-J. Möller, and F. Padberg, “Transcranial direct current stimulation in treatment resistant depression: a randomized double-blind, placebo-controlled study,” Brain Stimulat. 5(3), 242–251 (2012). [CrossRef] [PubMed]

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M. E. Mendonca, M. B. Santana, A. F. Baptista, A. Datta, M. Bikson, F. Fregni, and C. P. Araujo, “Transcranial DC stimulation in fibromyalgia: optimized cortical target supported by high-resolution computational models,” J. Pain 12(5), 610–617 (2011). [CrossRef] [PubMed]

OCIS Codes
(170.0170) Medical optics and biotechnology : Medical optics and biotechnology
(170.6510) Medical optics and biotechnology : Spectroscopy, tissue diagnostics
(170.2655) Medical optics and biotechnology : Functional monitoring and imaging

ToC Category:
Neuroscience and Brain Imaging

History
Original Manuscript: March 5, 2014
Revised Manuscript: April 18, 2014
Manuscript Accepted: April 21, 2014
Published: May 13, 2014

Citation
Chang-Hee Han, Hyuna Song, Yong-Guk Kang, Beop-Min Kim, and Chang-Hwan Im, "Hemodynamic responses in rat brain during transcranial direct current stimulation: a functional near-infrared spectroscopy study," Biomed. Opt. Express 5, 1812-1821 (2014)
http://www.opticsinfobase.org/boe/abstract.cfm?URI=boe-5-6-1812


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References

  1. M. A. Nitsche and W. Paulus, “Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation,” J. Physiol.527(3), 633–639 (2000). [CrossRef] [PubMed]
  2. A. Antal, T. Z. Kincses, M. A. Nitsche, O. Bartfai, and W. Paulus, “Excitability changes induced in the human primary visual cortex by transcranial direct current stimulation: direct electrophysiological evidence,” Invest. Ophthalmol. Vis. Sci.45, 702–707 (2004).
  3. F. Fregni, P. S. Boggio, M. Nitsche, and A. Pascual-Leone, “Transcranial direct current stimulation,” Br. J. Psychiatry186(5), 446–447 (2005). [CrossRef] [PubMed]
  4. T. Wagner, A. Valero-Cabre, and A. Pascual-Leone, “Noninvasive human brain stimulation,” Annu. Rev. Biomed. Eng.9(1), 527–565 (2007). [CrossRef] [PubMed]
  5. M. A. Nitsche, L. G. Cohen, E. M. Wassermann, A. Priori, N. Lang, A. Antal, W. Paulus, F. Hummel, P. S. Boggio, F. Fregni, and A. Pascual-Leone, “Transcranial direct current stimulation: state of the art 2008,” Brain Stimulat.1(3), 206–223 (2008). [CrossRef] [PubMed]
  6. A. Priori, “Brain polarization in humans: a reappraisal of an old tool for prolonged non-invasive modulation of brain excitability,” Clin. Neurophysiol.114(4), 589–595 (2003). [CrossRef] [PubMed]
  7. J. A. Williams, M. Imamura, and F. Fregni, “Updates on the use of non-invasive brain stimulation in physical and rehabilitation medicine,” J. Rehabil. Med.41(5), 305–311 (2009). [CrossRef] [PubMed]
  8. P. C. Gandiga, F. C. Hummel, and L. G. Cohen, “Transcranial DC stimulation (tDCS): a tool for double-blind sham-controlled clinical studies in brain stimulation,” Clin. Neurophysiol.117(4), 845–850 (2006). [CrossRef] [PubMed]
  9. M. A. Nitsche, P. S. Boggio, F. Fregni, and A. Pascual-Leone, “Treatment of depression with transcranial direct current stimulation (tDCS): a review,” Exp. Neurol.219(1), 14–19 (2009). [CrossRef] [PubMed]
  10. F. Fregni, S. Freedman, and A. Pascual-Leone, “Recent advances in the treatment of chronic pain with non-invasive brain stimulation techniques,” Lancet Neurol.6(2), 188–191 (2007). [CrossRef] [PubMed]
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