Advertisement
Browse Subject Areas
?

Click through the PLOS taxonomy to find articles in your field.

For more information about PLOS Subject Areas, click here.

  • Loading metrics

Open Access

Peer-reviewed

Research Article

Visual cortex cTBS increases mixed percept duration while a-tDCS has no effect on binocular rivalry

  • Dania Abuleil ,

    Roles Data curation, Formal analysis, Investigation, Methodology, Project administration, Writing – original draft

    dania.abuleil@uwaterloo.ca

    Affiliation Department of Optometry and Vision Science, University of Waterloo, Waterloo, ON, Canada

    ⨯
  • Daphne McCulloch,

    Roles Conceptualization, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Software, Supervision, Validation, Visualization, Writing – review & editing

    Affiliations Department of Optometry and Vision Science, University of Waterloo, Waterloo, ON, Canada, Centre for Eye and Vision Research, Hong Kong, China

    ⨯
  • Benjamin Thompson

    Roles Conceptualization, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Software, Supervision, Validation, Visualization, Writing – review & editing

    Affiliations Department of Optometry and Vision Science, University of Waterloo, Waterloo, ON, Canada, Centre for Eye and Vision Research, Hong Kong, China, The Liggins Institute, University of Auckland, Auckland, New Zealand

    ⨯

Abstract

Neuromodulation of the primary visual cortex using anodal transcranial direct current stimulation (a-tDCS) can alter visual perception and enhance neuroplasticity. However, the mechanisms that underpin these effects are currently unknown. When applied to the motor cortex, a-tDCS reduces the concentration of the inhibitory neurotransmitter gamma aminobutyric acid (GABA), an effect that has been linked to increased neuroplasticity. The aim of this study was to assess whether a-tDCS also reduces GABA-mediated inhibition when applied to the human visual cortex. Changes in visual cortex inhibition were measured using the mixed percept duration in binocular rivalry. Binocular rivalry mixed percept duration has recently been advocated as a direct and sensitive measure of visual cortex inhibition whereby GABA agonists decrease mixed percept durations and agonists of the excitatory neurotransmitter acetylcholine (ACH) increase them. Our hypothesis was that visual cortex a-tDCS would increase mixed percept duration by reducing GABA-mediated inhibition and increasing cortical excitation. In addition, we measured the effect of continuous theta-burst transcranial magnetic stimulation (cTBS) of the visual cortex on binocular rivalry dynamics. When applied to the motor or visual cortex, cTBS increases GABA concentration and we therefore hypothesized that visual cortex cTBS would decrease the mixed percept duration. Binocular rivalry dynamics were recorded before and after active and sham a-tDCS (N = 15) or cTBS (N = 15). Contrary to our hypotheses, a-tDCS had no effect, whereas cTBS increased mixed percepts during rivalry. These results suggest that the neurochemical mechanisms of a-tDCS may differ between the motor and visual cortices.

Citation: Abuleil D, McCulloch D, Thompson B (2021) Visual cortex cTBS increases mixed percept duration while a-tDCS has no effect on binocular rivalry. PLoS ONE 16(2): e0239349. https://doi.org/10.1371/journal.pone.0239349

Editor: Lawrence M. Ward, University of British Columbia, CANADA

Received: September 2, 2020; Accepted: December 19, 2020; Published: February 4, 2021

Copyright: © 2021 Abuleil et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability: The data underlying this study are available on Figshare (DOI: https://doi.org/10.6084/m9.figshare.13489245.v1).

Funding: BT received Natural Sciences and Engineering Research Council (NSERC) Grants RPIN-05394 and RGPAS-477166 (https://www.nserc-crsng.gc.ca/index_eng.asp) as well as the Canadian Foundation for Innovation (CFI; https://www.innovation.ca) Grant 34095. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Competing interests: The authors have declared that no competing interests exist.

Introduction

Anodal transcranial direct current stimulation (a-tDCS) is a non-invasive electrical brain stimulation technique that can modulate neural excitability and promote neuroplasticity. When applied to the visual cortex, a-tDCS can increase contrast sensitivity [1–4], improve visual acuity [5,6], and enhance perceptual learning [7,8] in patients with amblyopia, a neurodevelopmental disorder that affects binocular vision, as well as in controls. In addition to perceptual changes, reduced phosphene thresholds [7,9,10] and increased VEP amplitudes [4,7,11] have been reported following visual cortex a-tDCS. Therefore, a-tDCS can induce physiological and neurochemical changes that result in increased visual cortex excitability.

Although the specific mechanisms that underlie the effects of visual cortex a-tDCS are unknown, the effects of motor cortex a-tDCS are attributed in part to a reduction in cortical inhibition mediated by the neurotransmitter gamma amino-butyric acid (GABA). Specifically, magnetic resonance spectroscopy measures indicate that a-tDCS reduces motor cortex GABA concentration [12–18]. We anticipated that a similar reduction in GABA concentration occurs when a-tDCS is applied to the visual cortex based on previous results that are consistent with such an effect. For example, magnetoencephalography measurements made after visual cortex a-tDCS indicated an increase in occipital gamma activity that has been linked with reduced GABA-mediated inhibition [19, but see 20,21]. In addition, visual phenomena that have been associated with neural inhibition such as an attenuated cortical response to inputs from the amblyopic eye in adults with amblyopia [3,4] surround suppression [20] and lateral inhibition [21], can be reduced by a-tDCS.

Cathodal tDCS also reduces GABA concentration within the motor cortex in concert with reduced glutamate concentration [12]. However, continuous theta-burst stimulation (cTBS), a form of transcranial magnetic stimulation that can also alter visual perception [22–25], has been found to increase GABA concentration in both the motor cortex [26] and the visual cortex [23]. cTBS, therefore, would be expected to have the opposite effect to a-tDCS on percepts that are directly influenced by GABA-mediated inhibition.

Binocular rivalry dynamics have recently been advocated as a sensitive measure of GABA-mediated inhibition withing the human visual cortex [27]. Binocular rivalry is a form of bistable perception wherein the brain alternately suppresses one eye over the other stochastically when each eye views a different image [28–31]. Previous studies have found that binocular rivalry dynamics are correlated with visual cortex GABA concentration [32–34]. Specifically, young adults with slower binocular rivalry alternation rates had higher primary visual cortex GABA concentrations [32,34]. In addition, higher GABA concentrations are correlated with longer periods of perceptual dominance, defined as the period of time when either eye dominates perception during rivalry relative to mixed percepts when both eyes contribute to perception [34].

A causal relationship between GABA-mediated inhibition and binocular rivalry dynamics has also been reported. Single doses of clobazam (a GABAa receptor agonist) or arbaclofen (a GABAb receptor agonist) increased perceptual dominance and reduced mixed percept duration during binocular rivalry compared to a placebo [27]. Additionally, reduced inhibition and increased excitation induced by the acetylcholine agonist donepezil was recently found to reduce perceptual dominance and increase mixed percept duration during binocular rivalry [35]. Given this evidence, we used binocular rivalry mixed percept duration as a measure of cortical inhibition.

Whether a-tDCS reduces visual cortex GABA concentration as it does in the motor cortex is not yet known. Our study aimed to address this question. We hypothesized that visual cortex a-tDCS would reduce visual cortex GABA concentration resulting in increased mixed percept durations during binocular rivalry. We further hypothesized that visual cortex cTBS, that has been found to increase visual cortex GABA concentration [23], would have the opposite effect.

Materials and methods

Participants

A total of thirty young adults with normal or corrected-to-normal vision (0.1 LogMAR or better in each eye) participated in one of two within-subject, sham-controlled experiments: an a-tDCS experiment (n = 15, mean participant age 25, median age 24, range 22–30, 11 female) and a cTBS experiment (n = 15, mean participant age 24, median age 24, range 22–29, 7 female). Participants with abnormal binocular vision and those taking psychoactive drugs were excluded. All participants were informed of the nature of the study before participation and provided written informed consent. The project was approved by the University of Waterloo Research Ethics Committee (ORE #30537).

Visual stimuli

Dichoptic, orthogonally oriented (45° and 135°) sinusoidally modulated red/green gratings (0.5 cycles per degree, 6.1 degrees of visual angle) were presented on a 24-inch Asus 3D monitor. Participants wore 120 Hz frame sequential shutter glasses to view the stimuli. The contrast of the gratings was matched using a Chroma Meter CS-100 photometer (mean luminance: red = 8.4 cd/m2; green = 32.9 cd/m2). Stimuli were viewed from 57cm using a chin rest. Participants reported perceiving the 45° grating only, the 135° grating only, or a mixture of both (piecemeal or superimposition percepts) by holding down a computer keyboard key and switching keys as the percept changed.

Anodal transcranial direct current stimulation

Two 5x7 cm electrode sponges were placed on the scalp, the anode at 2 cm above the inion over the visual cortex and the cathode at the vertex. Each tDCS electrode was placed inside a saline-soaked sponge. The electrodes were secured using a head mount. A-tDCS was delivered at 2mA for 15 minutes in addition to a 30-second ramp-up and 30-second ramp-down period using a NeuroConn DC-Stimulator MC-8. Electrode impedance levels were below 5 k Ohms throughout each session and were continuously monitored during the experiment. The intensity and duration of a-tDCS were matched to those of studies providing evidence for a-tDCS effects on visual cortex function [4,21]. The sham condition consisted only of the ramp-up and ramp-down periods. Participants were masked to the stimulation condition. The experimenter could not be masked due to resource limitations; however, session order (active first or sham first) was randomly sequenced prior to the start of data collection. For both active and sham conditions, six 60-second trials of binocular rivalry were completed before, during, 5 minutes, and 30 minutes post stimulation (Fig 1A).

thumbnail
Download:
Fig 1.

a-tDCS (A) and cTBS (B) experiment protocols. Binocular rivalry dynamics were recorded for 6 minutes at baseline (pre), during, 5 minutes post and 30 minutes post a-tDCS. A-tDCS electrodes were placed on the head following the baseline measure. Similarly, for cTBS, binocular rivalry dynamics were recorded pre, 5 minutes post and 30 minutes post stimulation. Motor thresholding was completed on the first visit following the baseline measure.

https://doi.org/10.1371/journal.pone.0239349.g001

Continuous theta burst stimulation

cTBS was delivered using a MagVenture MagPro X100 stimulator (MagVenture Farum, Denmark) with BrainSight frameless neuro-navigation software (Rogue Research Inc., Montreal, Canada). Active motor thresholds (AMTs) were used to calibrate visual cortex cTBS intensity [36]. We chose to use AMT rather than phosphene threshold to calibrate cTBS intensity because AMT is objective, not everyone perceives TMS induced phosphenes and AMT is positively correlated with phosphene threshold [37]. The procedure for determining AMT involved placing a surface electrode on the belly of the first dorsal interosseous muscle tendon (left or right based on hand dominance) and a second electrode on the lateral bone of the wrist. The electromyographic (EMG) response was monitored using BrainSight software as the participant was asked to steadily press their pointer finger against the arm of their chair to generate a motor evoked potential (MEP) of 100μV. A single pulse of TMS was systematically delivered to different points of a contralateral motor cortex stimulation grid (3 by 3 cm) beginning at 40% of the maximum stimulator output (MSO) until the region hotspot—defined as the stimulation location corresponding to the maximum TMS-induced MEP amplitude—was located [38,39]. Using the Rossini-Rothwell algorithm for determining AMT, single pulses were then delivered to this region while increasing the intensity by 1% until a peak-to-peak amplitude of 200μV was generated for 5 out of 10 pulses (50%) [40].

For visual cortex cTBS, the TMS coil was centered 2 cm above the inion, on the sagittal midline. Stimulation involved five bursts of three 50Hz pulses delivered every second for 40 seconds at 100% of the participant’s AMT [36]. The control condition used the same protocol with a sham coil. Both the participant and experimenter were masked to the stimulation condition (active and sham condition codes were given to the experimenter by another researcher). Binocular rivalry dynamics were recorded for six 60-second trials before, 5 minutes post, and 30 minutes post stimulation (Fig 1B).

Analysis

The duration of mixed perception during binocular rivalry was calculated in seconds per 60-second trial. We also analysed binocular rivalry ocular dominance index ((time viewing the dominant eye percept–time viewing the non-dominant eye percept)/total time excluding mixed percepts) and alternation rates (any change in perception). Measures were averaged across all six trials for each time point separately for each participant. The dominant eye was defined as the eye with the longest pre-stimulation viewing time at the initial visit.

A repeated measures ANOVA with factors of Condition (active vs. sham) and Time (a-tDCS: pre vs. during vs. 5min post vs. 30min post; cTBS: pre vs. 5min post vs. 30min post) was conducted separately for mixed percept duration, ocular dominance index and alternation rate for each stimulation type. Post-hoc testing of significant interactions was conducted using t-tests. Effect sizes were calculated as either partial eta squared (ηp2) or Cohen’s d based on the analysis.

For one tDCS participant, the 5 minutes post stimulation data for the sham condition was irretrievably lost. For one TMS participant, baseline data and 5 minutes post stimulation data for the sham condition were irretrievably lost. The missing data points were imputed using the mean value of the other 14 participants [41].

Results

Anodal transcranial direct current stimulation

No significant effects of a-tDCS were observed for any measure of binocular rivalry dynamics (ηp2 range 0.03 to 0.09, p > 0.05). Fig 2 illustrates mixed percept duration, ocular dominance index and alternation rate for the active a-tDCS and sham conditions.

thumbnail
Download:
Fig 2.

Average time spent in mixed percept (A), ocular dominance indices (B), and alternation rates (C) for 15 participants pre, during, 5 minutes and 30 minutes post a-tDCS. Error bars = SEM. No statistically significant effects were observed.

https://doi.org/10.1371/journal.pone.0239349.g002

Continuous theta burst stimulation

cTBS significantly increased the duration of mixed percepts relative to sham stimulation (significant interaction between Condition and Time, F28 = 3.53, ηp2 = 0.20, p = 0.043; Fig 3A). Post hoc t-tests revealed a significant increase in mixed percept duration with active cTBS from pre to 5min post (t14 = -3.065, Cohen’s d = -0.80, p = 0.008) and from pre to 30min post (t14 = -2.31, Cohen’s d = -0.60, p = 0.037; Fig 3A). There were no significant differences between the active cTBS and sham conditions at any timepoint (pre cTBS and pre sham, t = -1.333, Cohen’s d = -0.344, p = 0.204; post-5 cTBS and post-5 sham; t = 1.065, Cohen’s d = 0.287, p = 0.305; post-30 cTBS and post-30 sham, t = 0.621, Cohen’s d = 0.160, p = 0.545). There were no effects of cTBS on ocular dominance index or alternation rate (Fig 3B & 3C).

thumbnail
Download:
Fig 3.

Average time spent in mixed percept (A), ocular dominance indices (B), and alternation rates (C) for 15 participants pre-stimulation, 5 minutes and 30 minutes post cTBS. Error bars = SEM. * p<0.05.

https://doi.org/10.1371/journal.pone.0239349.g003

Discussion

We tested the hypothesis that visual cortex a-tDCS, which has been observed to reduce regional GABA concentration [13,17], acts to reduce GABA-mediated inhibition within visual cortex as evidenced by increased binocular rivalry mixed percept duration [27]. Mixed percept duration during binocular rivalry has been causally linked to visual cortex GABA concentration through pharmacological antagonism of GABAa and GABAb receptors [27]. We hypothesized that visual cortex cTBS would have the opposite effect to a-tDCS and reduce mixed percept duration because cTBS applied to the motor cortex [26] or visual cortex [23] increases GABA concentration.

Contrary to our hypotheses, visual cortex a-tDCS had no effect on mixed percept duration and visual cortex cTBS increased mixed percept duration, a result that was opposite to the anticipated effect. As expected, neither form of non-invasive brain stimulation altered ocular dominance index or alternation rate during binocular rivalry.

No effect of a-tDCS on mixed percept duration

The most obvious explanation for the lack of an a-tDCS effect on mixed percept duration is that a-tDCS simply had no effect on the visual cortex at all. Although we certainly cannot rule out this possibility, the vast majority of published studies using the same or similar stimulation parameters over visual cortex have reported a-tDCS effects, including effects that are consistent with reduced GABA-mediated inhibition such as reduced surround suppression [20], reduced lateral inhibition [21] (with a moderate to large effect size) and an equalization of the cortical response to each eye in adults with amblyopia [3,4]. Therefore, we also propose possible alternative explanations.

One explanation is that a-tDCS does reduce visual cortex GABA concentration, but that the primary visual cortex is not the appropriate region to target because binocular rivalry is associated with a broad network of brain areas that includes the LGN [42], V1 [43], and the prefrontal cortex [44,45]. We chose V1 as our brain stimulation target because of the reported association between GABA concentration and binocular rivalry dynamics in this region [27,33,46]. However, the relatively large rivalry stimuli with strongly competing features that we used may have primarily recruited higher-level regions of the rivalry network. It is conceivable that a-tDCS may alter binocular rivalry dynamics for smaller rivalrous stimuli that do not contain strongly competing features.

An alternative explanation is that a-tDCS does not act to modulate GABA concentration in visual cortex. In non-visual areas, usually motor cortex, most studies using magnetic resonance spectroscopy (MRS) to quantify neurotransmitters have reported reduced GABA concentration following a-tDCS; however, not all studies have observed this effect [18,47–49]. It is possible that a-tDCS modulation of GABA concentration is highly dependent on stimulation parameters [see citation 50 for a comprehensive review] and/or the distribution of male and female participants within the study population [51–53], all of which differ among previous studies and our own. In addition, it is possible that a-tDCS mechanisms differ between brain regions. For example, Dwyer et al. [54] recently reported no change in GABA or GLX concentration following temporal lobe a-tDCS. A detailed study of repetitive TMS (rTMS) effects over different brain regions using functional connectivity and computational modeling has recently revealed that the effects of a fixed 1 Hz stimulation protocol differ significantly when the stimulation is applied to different brain regions [55]. In particular, occipital 1Hz rTMS induced opposite functional connectivity effects when compared to frontal 1 Hz rTMS. We posit that similar phenomenon occurs for a-tDCS such that visual cortex a-tDCS may not influence local GABA concentration in the same way as a-tDCS of motor cortex. An MRS study of visual cortex a-tDCS is required to directly address this question.

Increased mixed percept duration following visual cortex cTBS

MRS measurements made after visual and motor cortex cTBS have indicated increased visual cortex GABA concentration [23,26], an effect that would be expected to reduce mixed percept duration [27,56]. However, we observed the opposite effect; an increase in mixed percept duration following cTBS. The interaction effect that we observed for mixed percept duration had only a moderate effect size, raising the possibility of a type 2 error, although the within-condition pairwise comparisons indicating changes from the pre-cTBS baseline had moderate to strong effect sizes.

Previous studies have reported counter intuitive improvements in visual perception following inhibitory cTBS of the visual cortex [25,26]. These results were explained in the context of changes in the signal to noise ratio within visual cortex. However, it is not immediately apparent how such changes may influence binocular rivalry mixed percept duration. Previous work identifying a causal relationship between GABA-mediated inhibition and mixed percept duration used a systemic pharmacological intervention, whereas we targeted only the primary visual cortex with cTBS. Further studies are required to more fully understand how visual cortex cTBS affects the larger network of brain areas that contribute to binocular rivalry.

Measures of binocular rivalry dynamics

There are differences in binocular rivalry dynamics calculations across previous studies, and subtle differences in definitions. For instance, some studies calculate the proportion of perceptual dominance to mixed percept perception (referred to as perceptual suppression) [27,34], while mean dominance durations calculated as the average duration that a dominant percept lasts in seconds is used by others [32]. Our measures were designed to capture any changes in dominance and mixed percepts.

We also measured alternation rates because previous studies have suggested that visual cortex GABA concentration is correlated with alternation rate in young adults [32,34]. We did not observe an association between alternation rate and visual cortex a-tDCS or cTBS. Notably, GABA agonists do increase perceptual suppression (i.e. reduce mixed percept duration), but do not consistently influence alternation rate suggesting that different mechanisms may gate alternation rate [27,32].

Overall, our results suggest that the effects of a-tDCS on GABA concentration may differ between the visual cortex and the motor cortex and bring into question the mechanism for reported visual perception changes following a-tDCS. Further investigation of this question using techniques such as MRS is required to elucidate the mechanisms of visual cortex a-tDCS and help guide the continued development of visual rehabilitation strategies that involve a-tDCS or other forms on non-invasive brain stimulation.

References

  1. 1. Antal A, Nitsche MA, Paulus W. External modulation of visual perception in humans. Acta Ophthalmol. 2001;12(16):3553–5. pmid:11733710
  2. 2. Behrens JR, Kraft A, Irlbacher K, Gerhardt H, Olma MC, Brandt SA. Long-Lasting Enhancement of Visual Perception with Repetitive Noninvasive Transcranial Direct Current Stimulation. Front Cell Neurosci. 2017;11(August):1–10. pmid:28860969
  3. 3. Spiegel DP, Byblow WD, Hess RF, Thompson B. Anodal transcranial direct current stimulation transiently improves contrast sensitivity and normalizes visual cortex activation in individuals with amblyopia. Neurorehabil Neural Repair. 2013;27(8):760–9. pmid:23774122
  4. 4. Ding Z, Li J, Spiegel DP, Chen Z, Chan L, Luo G, et al. The effect of transcranial direct current stimulation on contrast sensitivity and visual evoked potential amplitude in adults with amblyopia. Sci Rep. 2016;6(July 2015):1–11. pmid:28442746
  5. 5. Reinhart RMGG, Xiao W, McClenahan LJ, Woodman GF. Electrical Stimulation of Visual Cortex Can Immediately Improve Spatial Vision. Curr Biol. 2016;26(14):1867–72. pmid:27374337
  6. 6. Bocci T, Nasini F, Caleo M, Restani L, Barloscio D, Ardolino G, et al. Unilateral Application of Cathodal tDCS Reduces Transcallosal Inhibition and Improves Visual Acuity in Amblyopic Patients. 2018;12(May):1–9.
  7. 7. Sczesny-Kaiser M, Beckhaus K, Dinse HR, Schwenkreis P, Tegenthoff M, Höffken O. Repetitive transcranial direct current stimulation induced excitability changes of primary visual cortex and visual learning effects—A pilot study. Front Behav Neurosci. 2016;10(JUN):1–11. pmid:27375452
  8. 8. Spiegel DP, Li J, Hess RF, Byblow WD, Deng D, Yu M, et al. Transcranial direct current stimulation enhances recovery of stereopsis in adults with amblyopia. Neurotherapeutics. 2013;10(4):831–9. pmid:23857313
  9. 9. Antal A, Kincses TZ, Nitsche MA, Paulus W. Manipulation of phosphene thresholds by transcranial direct current stimulation in man. Exp Brain Res. 2003;150(3):375–8. pmid:12698316
  10. 10. Antal A, Kincses TZ, Nitsche MA, Paulus W. Modulation of moving phosphene thresholds by transcranial direct current stimulation of V1 in human. Neuropsychologia. 2003;41(13):1802–7. pmid:14527543
  11. 11. Strigaro G, Mayer I, Chen JC, Cantello R, Rothwell JC. Transcranial direct current stimulation effects on single and paired flash visual evoked potentials. Clin EEG Neurosci. 2015;46(3):208–13. pmid:25253432
  12. 12. Stagg CJ, Best JG, Stephenson MC, Shea JO, Wylezinska M, Kincses TZ, et al. Polarity-Sensitive Modulation of Cortical Neurotransmitters by Transcranial Stimulation. J Neurosci. 2009;29(16):5202–6. pmid:19386916
  13. 13. Patel HJ, Romanzetti S, Pellicano A, Reetz K, Binkofski F. Sustained GABA reduction induced by anodal Transcranial direct current stimulation (tDCS) in motor cortex–a proton magnetic resonance spectroscopy study. Clin Neurophysiol. 2017;128(10):e308—e309.
  14. 14. Patel HJ, Romanzetti S, Pellicano A, Nitsche MA, Reetz K, Binkofski F. Proton magnetic resonance spectroscopy of the motor cortex reveals long term GABA change following anodal transcranial direct current stimulation. Sci Rep. 2019;9(1):1–8. pmid:30626917
  15. 15. Bachtiar V, Near J, Johansen-Berg H, Stagg CJ. Modulation of GABA and resting state functional connectivity by transcranial direct current stimulation. Elife. 2015;4(September 2015):1–9. pmid:26381352
  16. 16. Kim S, Stephenson MC, Morris PG, Jackson SR. TDCS-induced alterations in GABA concentration within primary motor cortex predict motor learning and motor memory: A 7T magnetic resonance spectroscopy study. Neuroimage. 2014;99:237–43. pmid:24904994
  17. 17. Antonenko D, Schubert F, Bohm F, Ittermann B, Aydin S, Hayek D, et al. tDCS-Induced Modulation of GABA Levels and Resting-State Functional Connectivity in Older Adults. J Neurosci. 2017;37(15):4065–73. pmid:28314813
  18. 18. Heise KF, Niehoff M, Feldheim J-F, Liuzzi G, Gerloff C, Hummel FC. Differential behavioral and physiological effects of anodal transcranial direct current stimulation in healthy adults of younger and older age. Front Aging Neurosci. 2014;6(July):146. pmid:25071555
  19. 19. Wilson TW, McDermott TJ, Mills MS, Coolidge NM, Heinrichs-Graham E. tDCS Modulates Visual Gamma Oscillations and Basal Alpha Activity in Occipital Cortices: Evidence from MEG. Cereb Cortex. 2018;28(5):1597–609. pmid:28334214
  20. 20. Spiegel DP, Hansen BC, Byblow WD, Thompson B. Anodal Transcranial Direct Current Stimulation Reduces Psychophysically Measured Surround Suppression in the Human Visual Cortex. PLoS One. 2012;7(5):1–9. pmid:22563485
  21. 21. Raveendran RN, Tsang K, Tiwana D, Chow A, Thompson B. Anodal transcranial direct current stimulation reduces collinear lateral inhibition in normal peripheral vision. PLoS One. 2020;15(5):1–11. pmid:32374787
  22. 22. Clavagnier S, Thompson B, Hess RF. Long lasting effects of daily theta burst rTMS sessions in the human amblyopic cortex. Brain Stimul. 2013;6(6):860–7. pmid:23664756
  23. 23. Allen CPG, Dunkley BT, Muthukumaraswamy SD, Edden R, Evans CJ, Sumner P, et al. Enhanced awareness followed reversible inhibition of human visual cortex: A combined TMS, MRS and MEG study. PLoS One. 2014;9(6). pmid:24956195
  24. 24. Waterston ML, Pack CC. Improved discrimination of visual stimuli following repetitive transcranial magnetic stimulation. PLoS One. 2010;5(4). pmid:20442776
  25. 25. Rahnev D, Kok P, Munneke M, Bahdo L, de Lange FP, Lau H. Continuous theta burst transcranial magnetic stimulation reduces resting state connectivity between visual areas. J Neurophysiol. 2013;110(8):1811–21. pmid:23883858
  26. 26. Stagg CJ, Wylezinska M, Matthews PM, Johansen-Berg H, Jezzard P, Rothwell JC, et al. Neurochemical effects of theta burst stimulation as assessed by magnetic resonance spectroscopy. J Neurophysiol. 2009;101(6):2872–7. pmid:19339458
  27. 27. Mentch J, Spiegel A, Ricciardi C, Robertson CE. GABAergic Inhibition Gates Perceptual Awareness During Binocular. J Neurosci. 2019;39(42):8398–407. pmid:31451579
  28. 28. Blake R, Logothetis NK. Visual competition. Nat Rev Neurosci. 2002;3(1):13–21. pmid:11823801
  29. 29. Kovács I, Papathomas TV, Yang M, Feher A. When the brain changes its mind: Interocular grouping. Proc Natl Acad Sci. 1996;93(December):15508–11. pmid:8986842
  30. 30. Tong F, Nakayama K, Vaughan JT, Kanwisher N. Binocular rivalry and visual awareness in human extrastriate cortex. Neuron. 1998;21(4):753–9. pmid:9808462
  31. 31. Tong F, Meng M, Blake R. Neural bases of binocular rivalry. Trends Cogn Sci. 2006;10(11). pmid:16997612
  32. 32. van Loon AM, Knapen T, Scholte HS, St. John-Saaltink E, Donner T, Lamme VAF. GABA shapes the dynamics of bistable perception. Curr Biol. 2013;23(9):823–7. pmid:23602476
  33. 33. Pitchaimuthu K, Wu QZ, Carter OL, Nguyen BN, Ahn S, Egan GF, et al. Occipital GABA levels in older adults and their relationship to visual perceptual suppression. Sci Rep. 2017;7(1):14231. pmid:29079815
  34. 34. Robertson CE, Ratai EM, Kanwisher N. Reduced GABAergic Action in the Autistic Brain. Curr Biol. 2016;26(1):80–5. pmid:26711497
  35. 35. Sheynin Y, Rosa-Neto P, Hess RF, Vaucher E. Cholinergic modulation of binocular vision. J Neurosci. 2020;00(00):JN-RM-2484-19. pmid:32457075
  36. 36. Cai P, Chen N, Zhou T, Thompson B, Fang F. Global versus local: double dissociation between MT+ and V3A in motion processing revealed using continuous theta burst transcranial magnetic stimulation. Exp Brain Res. 2014;232(12):4035–41. pmid:25200175
  37. 37. Deblieck C, Thompson B, Iacoboni M, Wu AD. Correlation between motor and phosphene thresholds: A transcranial magnetic stimulation study. Hum Brain Mapp. 2008;29(6):662–70. pmid:17598167
  38. 38. Groppa S, Oliviero A, Eisen A, Quartarone A, Cohen LG, Mall V, et al. A practical guide to diagnostic transcranial magnetic stimulation: Report of an IFCN committee. Clin Neurophysiol. 2016;30(4):873–82.
  39. 39. Tranulis C, Guéguen B, Pham-Scottez A, Vacheron MN, Cabelguen G, Costantini A, et al. Motor threshold in transcranial magnetic stimulation: Comparison of three estimation methods. Neurophysiol Clin. 2006;36(1):1–7. pmid:16530137
  40. 40. Rothwell JC, Hallet M, Berardelli A, Eisen A, Rossini PM, Paulus W. Magnetic stimulation: motor evoked potentials. Elsevier Sci. 1999;52:97–103. pmid:10590980
  41. 41. Kang H. The prevention and handling of the missing data. Korean J Anesthesiol. 2013;64(5):402–6. pmid:23741561
  42. 42. Haynes JD, Deichmann R, Rees G. Eye-specific suppression in human LGN reflects perceptual dominance during binocular rivalry. Nature. 2006;438(7067):496–9.
  43. 43. Tong F, Engel SA. Interocular rivalry revealed in the human cortical blind-spot representation. J Vis. 2001;1(3):195–9. pmid:11346796
  44. 44. Carmel D, Walsh V, Lavie N, Rees G. Right parietal TMS shortens dominance durations in binocular rivalry. Curr Biol. 2010;20(18):799–800. pmid:20869603
  45. 45. Zaretskaya N, Thielscher A, Logothetis NK, Bartels A. Disrupting parietal function prolongs dominance durations in binocular rivalry. Curr Biol. 2010;20(23):2106–11. pmid:21093263
  46. 46. van Loon AM, Knapen T, Scholte HS, St. John-Saaltink E, Donner TH, Lamme VAF. GABA Shapes the Dynamics of Bistable Perception. Curr Biol. 2013;23(9):823–7. pmid:23602476
  47. 47. Nwaroh C, Giuffre A, Cole L, Bell T, Carlson HL, MacMaster FP, et al. Effects of transcranial direct current stimulation on GABA and Glx in children: A pilot study. PLoS One. 2020;15(1):1–18. pmid:31910218
  48. 48. Amadi U, Allman C, Johansen-Berg H, Stagg CJ. The homeostatic interaction between anodal transcranial direct current stimulation and motor learning in humans is related to GABAA activity. Brain Stimul. 2015;8(5):898–905. pmid:26279408
  49. 49. Wilke S, List J, Mekle R, Lindenberg R, Bukowski M, Ott S, et al. No Effect of Anodal Transcranial Direct Current Stimulation on Gamma-Aminobutyric Acid Levels in Patients with Recurrent Mild Traumatic Brain Injury. J Neurotrauma. 2017;34(2):281–90. pmid:27393381
  50. 50. Grasso PA, Tonolli E, Miniussi C. Effects of different transcranial direct current stimulation protocols on visuo-spatial contextual learning formation: evidence of homeostatic regulatory mechanisms. Sci Rep. 2020;1–14. pmid:31913322
  51. 51. Chaieb L, Antal A, Paulus W. Gender-specific modulation of short-term neuroplasticity in the visual cortex induced by transcranial direct current stimulation. Vis Neurosci. 2008;25(1):77–81. pmid:18282312
  52. 52. Epperson CN, O’Malley S, Czarkowski KA, Gueorguieva R, Jatlow P, Sanacora G, et al. Sex, GABA, and nicotine: The impact of smoking on cortical GABA levels across the menstrual cycle as measured with proton magnetic resonance spectroscopy. Biol Psychiatry. 2005;57(1):44–8. pmid:15607299
  53. 53. Hsu TY, Juan CH, Tseng P. Individual differences and state-dependent responses in transcranial direct current stimulation. Front Hum Neurosci. 2016;10(DEC2016):1–12. pmid:26858619
  54. 54. Dwyer GE, Craven AR, Hirnstein M, Kompus K, Assmus J, Ersland L, et al. No effects of anodal tDCS on local GABA and GLx levels in the left posterior superior temporal gyrus. Front Neurol. 2019;10(JAN):1–10. pmid:30671014
  55. 55. Castrillon G, Sollmann N, Kurcyus K, Razi A, Krieg SM, Riedl V. The physiological effects of noninvasive brain stimulation fundamentally differ across the human cortex. Sci Adv. 2020;6(5). pmid:32064344
  56. 56. Sheynin Y, Chamoun M, Baldwin AS, Rosa-Neto P, Hess RF, Vaucher E. Cholinergic potentiation alters perceptual eye dominance plasticity induced by a few hours of monocular patching in adults. Front Neurosci. 2019;13(JAN):1–12. pmid:30766471