Individual Differences and State-Dependent Responses in Transcranial Direct Current Stimulation

Tzu-Yu Hsu, Chi-Hung Juan, Philip Tseng, Tzu-Yu Hsu, Chi-Hung Juan, Philip Tseng

Abstract

Transcranial direct current stimulation (tDCS) has been extensively used to examine whether neural activities can be selectively increased or decreased with manipulations of current polarity. Recently, the field has reevaluated the traditional anodal-increase and cathodal-decrease assumption due to the growing number of mixed findings that report the effects of the opposite directions. Therefore, the directionality of tDCS polarities and how it affects each individual still remain unclear. In this study, we used a visual working memory (VWM) paradigm and systematically manipulated tDCS polarities, types of different independent baseline measures, and task difficulty to investigate how these factors interact to determine the outcome effect of tDCS. We observed that only low-performers, as defined by their no-tDCS corsi block tapping (CBT) performance, persistently showed a decrement in VWM performance after anodal stimulation, whereas no tDCS effect was found when participants were divided by their performance in digit span. In addition, only the optimal level of task difficulty revealed any significant tDCS effect. All these findings were consistent across different blocks, suggesting that the tDCS effect was stable across a short period of time. Lastly, there was a high degree of intra-individual consistency in one's responsiveness to tDCS, namely that participants who showed positive or negative effect to anodal stimulation are also more likely to show the same direction of effects for cathodal stimulation. Together, these findings imply that tDCS effect is interactive and state dependent: task difficulty and consistent individual differences modulate one's responsiveness to tDCS, while researchers' choices of independent behavioral baseline measures can also critically affect how the effect of tDCS is evaluated. These factors together are likely the key contributors to the wide range of "noises" in tDCS effects between individuals, between stimulation protocols, and between different studies in the literature. Future studies using tDCS, and possibly tACS, should take such state-dependent condition in tDCS responsiveness into account.

Keywords: non-invasive brain stimulation; right posterior parietal cortex (rPPC); state-dependence; transcranial direct current stimulation (tDCS); visual working memory (VWM).

Figures

Figure 1
Figure 1
Correlation between change detection performance and different independent measures. corsi block tapping (CBT) scores (orange) showed a significant positive correlation with participants’ change detection performance (X-axis), while digit span (gray) did not, suggesting that CBT and digit span tasks are most likely probing different mechanisms of memory.
Figure 2
Figure 2
Individual differences in the directions of tDCS effects in 18 participants (Anodal-sham and Cathodal-sham contrasts). Even in set size 4 where the level of difficulty is optimal, there is still a wide range of individual differences. Interestingly, although differences exists between different individuals (left chart), the directions of tDCS effect is quite consistent within each individual (lower right pie chart).
Figure 3
Figure 3
Mean K values under manipulations of tDCS and set size. Participants were divided into low and high performers by either digit span (top panel) or CBT (bottom panel) scores, and two separate three-way ANOVAs were conducted for each. A significant interaction between tDCS, set size and group was only observed when participants were divided based on their CBT performance, which was driven by lower K values in the anodal tDCS condition than sham and cathodal conditions under set size 6 and 8 in low performers. Asterisks denote p < 0.05, and error bars denote standard error of the mean.

References

    1. Andrews S. C., Hoy K. E., Enticott P. G., Daskalakis Z. J., Fitzgerald P. B. (2011). Improving working memory: the effect of combining cognitive activity and anodal transcranial direct current stimulation to the left dorsolateral prefrontal cortex. Brain Stimul. 4, 84–89. 10.1016/j.brs.2010.06.004
    1. Antal A., Terney D., Poreisz C., Paulus W. (2007). Towards unravelling task-related modulations of neuroplastic changes induced in the human motor cortex. Eur. J. Neurosci. 26, 2687–2691. 10.1111/j.1460-9568.2007.05896.x
    1. Baker J. M., Rorden C., Fridriksson J. (2010). Using transcranial direct-current stimulation to treat stroke patients with aphasia. Stroke 41, 1229–1236. 10.1161/STROKEAHA.109.576785
    1. Batsikadze G., Paulus W., Kuo M.-F., Nitsche M. A. (2013). Effect of serotonin on paired associative stimulation-induced plasticity in the human motor cortex. Neuropsychopharmacology 38, 2260–2267. 10.1038/npp.2013.127
    1. Benwell C. S. Y., Learmonth G., Miniussi C., Harvey M., Thut G. (2015). Non-linear effects of transcranial direct current stimulation as a function of individual baseline performance: evidence from biparietal tDCS influence on lateralized attention bias. Cortex 69, 152–165. 10.1016/j.cortex.2015.05.007
    1. Berryhill M. E., Jones K. T. (2012). tDCS selectively improves working memory in older adults with more education. Neurosci. Lett. 521, 148–151. 10.1016/j.neulet.2012.05.074
    1. Berryhill M. E., Peterson D. J., Jones K. T., Stephens J. A. (2014). Hits and misses: leveraging tDCS to advance cognitive research. Front. Psychol. 5:800. 10.3389/fpsyg.2014.00800
    1. Berryhill M. E., Wencil E. B., Branch Coslett H., Olson I. R. (2010). A selective working memory impairment after transcranial direct current stimulation to the right parietal lobe. Neurosci. Lett. 479, 312–316. 10.1016/j.neulet.2010.05.087
    1. Bikson M., Rahman A. (2013). Origins of specificity during tDCS: anatomical, activity-selective and input-bias mechanisms. Front. Hum. Neurosci. 7:688. 10.3389/fnhum.2013.00688
    1. Bindman L. J., Lippold O. C., Redfearn J. W. (1964). The action of brief polarizing currents on the cerebral cortex of the rat (1) during current flow and (2) in the production of long-lasting after-effects. J. Physiol. 172, 369–382. 10.1113/jphysiol.1964.sp007425
    1. Bo J., Jennett S., Seidler R. D. (2011). Working memory capacity correlates with implicit serial reaction time task performance. Exp. Brain Res. 214, 73–81. 10.1007/s00221-011-2807-8
    1. Boggio P. S., Castro L. O., Savagim E. A., Braite R., Cruz V. C., Rocha R. R., et al. . (2006a). Enhancement of non-dominant hand motor function by anodal transcranial direct current stimulation. Neurosci. Lett. 404, 232–236. 10.1016/j.neulet.2006.05.051
    1. Boggio P. S., Ferrucci R., Rigonatti S. P., Covre P., Nitsche M., Pascual-Leone A., et al. . (2006b). Effects of transcranial direct current stimulation on working memory in patients with Parkinson’s disease. J. Neurol. Sci. 249, 31–38. 10.1016/j.jns.2006.05.062
    1. Bolognini N., Rossetti A., Casati C., Mancini F., Vallar G. (2011). Neuromodulation of multisensory perception: a tDCS study of the sound-induced flash illusion. Neuropsychologia 49, 231–237. 10.1016/j.neuropsychologia.2010.11.015
    1. Brainard D. H. (1997). The psychophysics toolbox. Spat. Vis. 10, 433–436. 10.1163/156856897x00357
    1. Brunetti R., Del Gatto C., Delogu F. (2014). eCorsi: implementation and testing of the Corsi block-tapping task for digital tablets. Front. Psychol. 5:939. 10.3389/fpsyg.2014.00939
    1. Brunoni A. R., Ferrucci R., Bortolomasi M., Scelzo E., Boggio P. S., Fregni F., et al. . (2013). Interactions between transcranial direct current stimulation (tDCS) and pharmacological interventions in the Major Depressive Episode: findings from a naturalistic study. Eur. Psychiatry 28, 356–361. 10.1016/j.eurpsy.2012.09.001
    1. Brunoni A. R., Ferrucci R., Bortolomasi M., Vergari M., Tadini L., Boggio P. S., et al. . (2011). Transcranial direct current stimulation (tDCS) in unipolar vs. bipolar depressive disorder. Prog. Neuropsychopharmacol. Biol. Psychiatry 35, 96–101. 10.1016/j.pnpbp.2010.09.010
    1. Bueno V. F., Brunoni A. R., Boggio P. S., Bensenor I. M., Fregni F. (2011). Mood and cognitive effects of transcranial direct current stimulation in post-stroke depression. Neurocase 17, 318–322. 10.1080/13554794.2010.509319
    1. Cheeran B., Talelli P., Mori F., Koch G., Suppa A., Edwards M., et al. . (2008). A common polymorphism in the brain-derived neurotrophic factor gene (BDNF) modulates human cortical plasticity and the response to rTMS. J. Physiol. 586, 5717–5725. 10.1113/jphysiol.2008.159905
    1. Chew T., Ho K.-A., Loo C. K. (2015). Inter- and intra-individual variability in response to transcranial direct current stimulation (tDCS) at varying current intensities. Brain Stimul. 8, 1130–1137. 10.1016/j.brs.2015.07.031
    1. Corsi P. M. (1972). Human Memory and the Medial Temporal Region of the Brain. Unpublished Doctoral Dissertation. Montreal, QC: McGill University.
    1. Creutzfeldt O. D., Fromm G. H., Kapp H. (1962). Influence of transcortical d-c currents on cortical neuronal activity. Exp. Neurol. 5, 436–452. 10.1016/0014-4886(62)90056-0
    1. Datta A., Bansal V., Diaz J., Patel J., Reato D., Bikson M. (2009). Gyri-precise head model of transcranial direct current stimulation: improved spatial focality using a ring electrode versus conventional rectangular pad. Brain Stimul. 2, 201.e1–207.e1. 10.1016/j.brs.2009.03.005
    1. Dockery C. A., Hueckel-Weng R., Birbaumer N., Plewnia C. (2009). Enhancement of planning ability by transcranial direct current stimulation. J. Neurosci. 29, 7271–7277. 10.1523/JNEUROSCI.0065-09.2009
    1. Ellison A., Ball K. L., Moseley P., Dowsett J., Smith D. T., Weis S., et al. . (2014). Functional interaction between right parietal and bilateral frontal cortices during visual search tasks revealed using functional magnetic imaging and transcranial direct current stimulation. PLoS One 9:e93767. 10.1371/journal.pone.0093767
    1. Erdfelder E., Faul F., Buchner A. (1996). GPOWER: a general power analysis program. Behav. Res. Methods Instrum. Comput. 28, 1–11. 10.3758/bf03203630
    1. Faul F., Erdfelder E. (1992). GPOWER: a priori, Posthoc and Compromise Power Analyses for MS-DOS [Computer Software]. Bonn, Germany: Bonn University, Department of Psychology.
    1. Fregni F., Boggio P. S., Nitsche M., Bermpohl F., Antal A., Feredoes E., et al. . (2005). Anodal transcranial direct current stimulation of prefrontal cortex enhances working memory. Exp. Brain Res. 166, 23–30. 10.1007/s00221-005-2334-6
    1. Fregni F., Boggio P. S., Santos M. C., Lima M., Vieira A. L., Rigonatti S. P., et al. . (2006). Noninvasive cortical stimulation with transcranial direct current stimulation in Parkinson’s disease. Mov. Disord. 21, 1693–1702. 10.1002/mds.21012
    1. Gözenman F., Berryhill M. E. (2016). Working memory capacity differentially influences responses to tDCS and HD-tDCS in a retro-cue task. Neurosci. Lett. 629, 105–109. 10.1016/j.neulet.2016.06.056
    1. Heimrath K., Sandmann P., Becke A., Müller N. G., Zaehle T. (2012). Behavioral and electrophysiological effects of transcranial direct current stimulation of the parietal cortex in a visuo-spatial working memory task. Front. Psychiatry 3:56. 10.3389/fpsyt.2012.00056
    1. Heinen K., Sagliano L., Candini M., Husain M., Cappelletti M., Zokaei N. (2016). Cathodal transcranial direct current stimulation over posterior parietal cortex enhances distinct aspects of visual working memory. Neuropsychologia 87, 35–42. 10.1016/j.neuropsychologia.2016.04.028
    1. Horvath J. C., Forte J. D., Carter O. (2015a). Evidence that transcranial direct current stimulation (tDCS) generates little-to-no reliable neurophysiologic effect beyond MEP amplitude modulation in healthy human subjects: a systematic review. Neuropsychologia 66, 213–236. 10.1016/j.neuropsychologia.2014.11.021
    1. Horvath J. C., Forte J. D., Carter O. (2015b). Quantitative review finds no evidence of cognitive effects in healthy populations from single-session transcranial direct current stimulation (tDCS). Brain Stimul. 8, 535–550. 10.1016/j.brs.2015.01.400
    1. Hoy K. E., Emonson M. R., Arnold S. L., Thomson R. H., Daskalakis Z. J., Fitzgerald P. B. (2013). Testing the limits: investigating the effect of tDCS dose on working memory enhancement in healthy controls. Neuropsychologia 51, 1777–1784. 10.1016/j.neuropsychologia.2013.05.018
    1. Hsu T. Y., Tseng P., Liang W. K., Cheng S. K., Juan C. H. (2014). Transcranial direct current stimulation over right posterior parietal cortex changes prestimulus alpha oscillation in visual short-term memory task. Neuroimage 98, 306–313. 10.1016/j.neuroimage.2014.04.069
    1. Jacobson L., Koslowsky M., Lavidor M. (2012). tDCS polarity effects in motor and cognitive domains: a meta-analytical review. Exp. Brain Res. 216, 1–10. 10.1007/s00221-011-2891-9
    1. Jo J. M., Kim Y.-H., Ko M.-H., Ohn S. H., Joen B., Lee K. H. (2009). Enhancing the working memory of stroke patients using tDCS. Am. J. Phys. Med. Rehabil. 88, 404–409. 10.1097/PHM.0b013e3181a0e4cb
    1. Jones K. T., Berryhill M. E. (2012). Parietal contributions to visual working memory depend on task difficulty. Front. Psychiatry 3:81. 10.3389/fpsyt.2012.00081
    1. Juan C. H., Tseng P., Hsu T. Y. (in press). Elucidating and modulating the neural correlates of visuospatial working memory via noninvasive brain stimulation. Curr. Dir. Psychol. Sci.
    1. Kang E. K., Baek M. J., Kim S., Paik N. J. (2009). Non-invasive cortical stimulation improves post-stroke attention decline. Restor. Neurol. Neurosci. 27, 645–650. 10.3233/RNN-2009-0514
    1. Kang E. K., Paik N.-J. (2011). Effect of a tDCS electrode montage on implicit motor sequence learning in healthy subjects. Exp. Transl. Stroke Med. 3:4. 10.1186/2040-7378-3-4
    1. Kessels R. P., van Zandvoort M. J., Postma A., Kappelle L. J., de Haan E. H. (2000). The corsi block-tapping task: standardization and normative data. Appl. Neuropsychol. 7, 252–258. 10.1207/s15324826an0704_8
    1. Krause B., Cohen Kadosh R. (2014). Not all brains are created equal: the relevance of individual differences in responsiveness to transcranial electrical stimulation. Front. Syst. Neurosci. 8:25. 10.3389/fnsys.2014.00025
    1. Learmonth G., Thut G., Benwell C. S. Y., Harvey M. (2015). The implications of state-dependent tDCS effects in aging: behavioural response is determined by baseline performance. Neuropsychologia 74, 108–119. 10.1016/j.neuropsychologia.2015.01.037
    1. Looi C. Y., Duta M., Brem A.-K., Huber S., Nuerk H.-C., Cohen Kadosh R. (2016). Combining brain stimulation and video game to promote long-term transfer of learning and cognitive enhancement. Sci. Rep. 6:22003. 10.1038/srep22003
    1. Macmillan N. A., Creelman C. D. (1991). Detection Theory: A User’s Guide. Cambridge: Cambridge University Press.
    1. Mattay V. S., Goldberg T. E., Fera F., Hariri A. R., Tessitore A., Egan M. F., et al. . (2003). Catechol O-methyltransferase val158-met genotype and individual variation in the brain response to amphetamine. Proc. Natl. Acad. Sci. U S A 100, 6186–6191. 10.1073/pnas.0931309100
    1. Miniussi C., Cappa S. F., Cohen L. G., Floel A., Fregni F., Nitsche M. A., et al. . (2008). Efficacy of repetitive transcranial magnetic stimulation/transcranial direct current stimulation in cognitive neurorehabilitation. Brain Stimul. 1, 326–336. 10.1016/j.brs.2008.07.002
    1. Miniussi C., Harris J. A., Ruzzoli M. (2013). Modelling non-invasive brain stimulation in cognitive neuroscience. Neurosci. Biobehav. Rev. 37, 1702–1712. 10.1016/j.neubiorev.2013.06.014
    1. Miniussi C., Ruzzoli M., Walsh V. (2010). The mechanism of transcranial magnetic stimulation in cognition. Cortex 46, 128–130. 10.1016/j.cortex.2009.03.004
    1. Miyaguchi S., Onishi H., Kojima S., Sugawara K., Tsubaki A., Kirimoto H., et al. . (2013). Corticomotor excitability induced by anodal transcranial direct current stimulation with and without non-exhaustive movement. Brain Res. 1529, 83–91. 10.1016/j.brainres.2013.07.026
    1. Monte-Silva K., Kuo M.-F., Liebetanz D., Paulus W., Nitsche M. A. (2010). Shaping the optimal repetition interval for cathodal transcranial direct current stimulation (tDCS). J. Neurophysiol. 103, 1735–1740. 10.1152/jn.00924.2009
    1. Mulquiney P. G., Hoy K. E., Daskalakis Z. J., Fitzgerald P. B. (2011). Improving working memory: exploring the effect of transcranial random noise stimulation and transcranial direct current stimulation on the dorsolateral prefrontal cortex. Clin. Neurophysiol. 122, 2384–2389. 10.1016/j.clinph.2011.05.009
    1. Nitsche M. A., Paulus W. (2000). Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. J. Physiol. 527, 633–639. 10.1111/j.1469-7793.2000.t01-1-00633.x
    1. Ohn S. H., Park C.-I., Yoo W.-K., Ko M.-H., Choi K. P., Kim G.-M., et al. . (2008). Time-dependent effect of transcranial direct current stimulation on the enhancement of working memory. Neuroreport 19, 43–47. 10.1097/WNR.0b013e3282f2adfd
    1. Pashler H. (1988). Familiarity and visual change detection. Percept. Psychophys. 44, 369–378. 10.3758/bf03210419
    1. Paulus W. (2011). Transcranial electrical stimulation (tES–tDCS; tRNS, tACS) methods. Neuropsychol. Rehabil. 21, 602–617. 10.1080/09602011.2011.557292
    1. Pelli D. G. (1997). The VideoToolbox software for visual psychophysics: transforming numbers into movies. Spat. Vis. 10, 437–442. 10.1163/156856897x00366
    1. Pellicciari M. C., Brignani D., Miniussi C. (2013). Excitability modulation of the motor system induced by transcranial direct current stimulation: a multimodal approach. Neuroimage 83, 569–580. 10.1016/j.neuroimage.2013.06.076
    1. Peterchev A. V., Wagner T. A., Miranda P. C., Nitsche M. A., Paulus W., Lisanby S. H., et al. . (2012). Fundamentals of transcranial electric and magnetic stimulation dose: definition, selection and reporting practices. Brain Stimul. 5, 435–453. 10.1016/j.brs.2011.10.001
    1. Purpura D. P., McMurtry J. G. (1965). Intracellular activities and evoked potential changes during polarization of motor cortex. J. Neurophysiol. 28, 166–185.
    1. Rouder J. N., Morey R. D., Morey C. C., Cowan N. (2011). How to measure working memory capacity in the change detection paradigm. Psychon. Bull. Rev. 18, 324–330. 10.3758/s13423-011-0055-3
    1. Ruzzoli M., Marzi C. A., Miniussi C. (2010). The neural mechanisms of the effects of transcranial magnetic stimulation on perception. J. Neurophysiol. 103, 2982–2989. 10.1152/jn.01096.2009
    1. Silvanto J., Cattaneo Z., Battelli L., Pascual-Leone A. (2008). Baseline cortical excitability determines whether TMS disrupts or facilitates behavior. J. Neurophysiol. 99, 2725–2730. 10.1152/jn.01392.2007
    1. Silvanto J., Muggleton N. G., Cowey A., Walsh V. (2007). Neural adaptation reveals state-dependent effects of transcranial magnetic stimulation. Eur. J. Neurosci. 25, 1874–1881. 10.1111/j.1460-9568.2007.05440.x
    1. Stagg C. J., Nitsche M. A. (2011). Physiological basis of transcranial direct current stimulation. Neuroscientist 17, 37–53. 10.1177/1073858410386614
    1. Teo F., Hoy K. E., Daskalakis Z. J., Fitzgerald P. B. (2011). Investigating the role of current strength in tdcs modulation of working memory performance in healthy controls. Front. Psychiatry 2:45. 10.3389/fpsyt.2011.00045
    1. Todd J., Marois R. (2004). Capacity limit of visual short-term memory in human posterior parietal cortex. Nature 428, 751–754. 10.1038/nature02466
    1. Tseng P., Bridgeman B. (2011). Improved change detection with nearby hands. Exp. Brain Res. 209, 257–269. 10.1007/s00221-011-2544-z
    1. Tseng P., Chang Y. T., Liang W. K., Chang C. F., Juan C. H. (2016). The critical role of phase difference in gamma oscillation within the temporoparietal network for binding visual working memory. Sci. Rep. 6:32138. 10.1038/srep32138
    1. Tseng P., Hsu T. Y., Chang C. F., Tzeng O. J., Hung D. L., Muggleton N. G., et al. . (2012). Unleashing potential: transcranial direct current stimulation over the right posterior parietal cortex improves change detection in low-performing individuals. J. Neurosci. 32, 10554–10561. 10.1523/JNEUROSCI.0362-12.2012
    1. Vallar G., Bolognini N. (2011). Behavioural facilitation following brain stimulation: implications for neurorehabilitation. Neuropsychol. Rehabil. 21, 618–649. 10.1080/09602011.2011.574050
    1. Veniero D., Struber D., Thut G., Herrmann C. S. (2016). Noninvasive brain stimulation techniques can modulate cognitive processing. Organ. Res. Methods 10.1177/1094428116658960
    1. Vogel E. K., Machizawa M. G. (2004). Neural activity predicts individual differences in visual working memory capacity. Nature 428, 748–751. 10.1038/nature02447
    1. Vogel E. K., McCollough A. W., Machizawa M. G. (2005). Neural measures reveal individual differences in controlling access to working memory. Nature 438, 500–503. 10.1038/nature04171
    1. Wu Y.-J., Tseng P., Chang C. F., Pai M.-C., Hsu K. S., Lin C.-C., et al. . (2014). Modulating the interference effect on spatial working memory by applying transcranial direct current stimulation over the right dorsolateral prefrontal cortex. Brain Cogn. 91, 87–94. 10.1016/j.bandc.2014.09.002
    1. Wu Y.-J., Tseng P., Huang H.-W., Hu J.-F., Juan C.-H., Hsu K.-S., et al. . (2016). The facilitative effect of transcranial direct current stimulation on visuospatial working memory in patients with diabetic polyneuropathy: a pre-post sham-controlled study. Front. Hum. Neurosci. 10:479. 10.3389/fnhum.2016.00479
    1. Xu Y., Chun M. M. (2006). Dissociable neural mechanisms supporting visual short-term memory for objects. Nature 440, 91–95. 10.1038/nature04262
    1. You D. S., Kim D. Y., Chun M. H., Jung S. E., Park S. J. (2011). Cathodal transcranial direct current stimulation of the right Wernicke’s area improves comprehension in subacute stroke patients. Brain Lang. 119, 1–5. 10.1016/j.bandl.2011.05.002
    1. Zaehle T., Sandmann P., Thorne J. D., Jäncke L., Herrmann C. S. (2011). Transcranial direct current stimulation of the prefrontal cortex modulates working memory performance: combined behavioural and electrophysiological evidence. BMC Neurosci. 12:2. 10.1186/1471-2202-12-2

Source: PubMed

3
구독하다