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Experimental Brain Research

, Volume 238, Issue 1, pp 181–192 | Cite as

Enhancing spatial reasoning by anodal transcranial direct current stimulation over the right posterior parietal cortex

  • Julia WertheimEmail author
  • Lorenza S. Colzato
  • Michael A. Nitsche
  • Marco Ragni
Research Article

Abstract

Spatial reasoning is essential for an agent's navigation and the cognitive processing of abstract arrangements. Meta-analyses of neuroimaging data reveal that both the right posterior parietal cortex and left dorsolateral prefrontal cortex (PPC and DLPFC, respectively) show increased activation during spatial relational reasoning. To investigate whether participants’ reasoning performance can be modified and potentially enhanced, anodal transcranial direct current stimulation (tDCS) was applied over either region. 51 healthy adult participants solved spatial reasoning problems after the application of either anodal tDCS over the right PPC, the left DLPFC or a sham stimulation. We expect anodal stimulation to enhance cortical excitability which would be reflected by enhanced reasoning performance in participants receiving stimulation. The results demonstrate that anodal stimulation applied over the right PPC enhances participants’ performance in indeterminate reasoning problems, compared to sham and anodal stimulation over the left DLPFC. This finding is highly relevant for clarifying the cognitive mechanisms of relational reasoning and for clinical applications, e.g., enhancing or restoring higher cognitive functions for spatial representation and reasoning.

Keywords

Non-invasive brain stimulation Transcranial direct current stimulation Spatial reasoning Relational reasoning Posterior parietal cortex Dorsolateral prefrontal cortex 

Notes

Funding

This work was supported by the BrainLinks-BrainTools Cluster of Excellence, German Research Foundation (DFG, grant number EXC 1086) and the Barbara Wengeler foundation to JW, the DFG grants RA 1934/3-1, RA 1934/2-1, and RA 1934/4-1 to MR and the DFG priority program New Frameworks of Rationality (SPP 1516).

Compliance with ethical standards

Conflict of interest

M.A. Nitsche is a member of the Advisory Board of Neuroelectrics. The other authors declare no conflicts of interest.

Supplementary material

221_2019_5699_MOESM1_ESM.zip (8 kb)
Supplementary material 1 (ZIP 9 kb)

References

  1. Anderson JR (2009) How can the human mind occur in the physical universe? Oxford University Press, New YorkGoogle Scholar
  2. Andrews SC, Hoy KE, Enticott PG, Daskalakis ZJ, Fitzgerald PB (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(2):84–89.  https://doi.org/10.1016/j.brs.2010.06.004 CrossRefPubMedGoogle Scholar
  3. Antal A, Keeser D, Priori A, Padberg F, Nitsche MA (2015) Conceptual and procedural shortcomings of the systematic review “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” by Horvath and co-workers. Brain Stimul 8(4):846–849.  https://doi.org/10.1016/j.brs.2015.05.010 CrossRefPubMedGoogle Scholar
  4. Baddeley AD (2003) Working memory: looking back and looking forward. Nat Rev Neurosci 4(10):829–839.  https://doi.org/10.1038/nrn1201 CrossRefPubMedGoogle Scholar
  5. Baddeley AD (2007) Working memory, thought, and action. Oxford University Press, OxfordCrossRefGoogle Scholar
  6. Baker JM, Rorden C, Fridriksson J (2010) Using transcranial direct-current stimulation to treat stroke patients with aphasia. Stroke 41(6):1229–1236.  https://doi.org/10.1161/STROKEAHA.109.576785 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Boggio PS, Castro LO, Savagim EA, Braite R, Fregni F (2006) Enhancement of non-dominant hand motor function by anodal transcranial direct current stimulation. Neurosci Lett 404(1–2):232–236.  https://doi.org/10.1016/j.neulet.2006.05.051 CrossRefPubMedGoogle Scholar
  8. Coffman BA, Clark VP, Parasuraman R (2014) Battery powered thought: enhancement of attention, learning, and memory in healthy adults using transcranial direct current stimulation. Neuroimage 85:895–908.  https://doi.org/10.1016/j.neuroimage.2013.07.083 CrossRefPubMedGoogle Scholar
  9. Colzato LS, Fagioli S, Erasmus V, Hommel B (2005) Caffeine, but not nicotine, enhances visual feature binding. Eur J Neurosci 21(2):591–595.  https://doi.org/10.1111/j.1460-9568.2005.03868.x CrossRefPubMedGoogle Scholar
  10. Colzato LS, Kool W, Hommel B (2008) Stress modulation of visuomotor binding. Neuropsychologia 46(5):1542–1548.  https://doi.org/10.1016/j.neuropsychologia.2008.01.006 CrossRefPubMedGoogle Scholar
  11. Corsi PM (1972) Human memory and the medial temporal region of the brain. Diss Abstr Int 34:819BGoogle Scholar
  12. Dockery CA, Hueckel-Weng R, Birbaumer N, Plewnia C (2009) Enhancement of planning ability by transcranial direct current stimulation. J Neurosci 29(22):7271–7277.  https://doi.org/10.1523/JNEUROSCI.0065-09.2009 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Elsner B, Kugler J, Pohl M, Mehrholz J (2013) Transcranial direct current stimulation (tDCS) for improving function and activities of daily living in patients after stroke. Cochrane Database Syst Rev.  https://doi.org/10.1002/14651858.CD009645.pub3 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Eslinger PJ, Blair C, Wang J (2009) Developmental shifts in fMRI activations during visuospatial relational reasoning. Brain Cogn 69(1):1–10.  https://doi.org/10.1016/j.bandc.2008.04.010 CrossRefPubMedGoogle Scholar
  15. Fangmeier T, Knauff M, Ruff CC, Sloutsky V (2006) fMRI evidence for a three-stage model of deductive reasoning. J Cogn Neurosci 18(3):320–334.  https://doi.org/10.1162/jocn.2006.18.3.320 CrossRefPubMedGoogle Scholar
  16. Fiori V, Coccia M, Marinelli CV, Vecchi V, Bonifazi S, Ceravolo MG, Provinciali L, Tomaiuolo F, Marangolo P (2011) Transcranial direct current stimulation improves word retrieval in healthy and nonfluent aphasic subjects. J Cogn Neurosci 23(9):2309–2323.  https://doi.org/10.1162/jocn.2010.21579 CrossRefPubMedGoogle Scholar
  17. Flöel A (2014) tDCS-enhanced motor and cognitive function in neurological diseases. Neuroimage 85:934–947.  https://doi.org/10.1016/j.neuroimage.2013.05.098 CrossRefPubMedGoogle Scholar
  18. Flöel A, Rösser N, Michka O, Knecht S, Breitenstein C (2008) Noninvasive brain stimulation improves language learning. J Cogn Neurosci 20(8):1415–1422.  https://doi.org/10.1162/jocn.2008.20098 CrossRefPubMedGoogle Scholar
  19. Frank AU (1996) Qualitative spatial reasoning: cardinal directions as an example. Int J Geogr Inf Sci 10(3):269–290.  https://doi.org/10.1080/02693799608902079 CrossRefGoogle Scholar
  20. Frederick S (2005) Cognitive reflection and decision making. J Econ Perspect 19(4):25–42.  https://doi.org/10.1257/089533005775196732 CrossRefGoogle Scholar
  21. Fregni F, Boggio PS, Nitsche M, Bermpohl F, Antal A, Feredoes E, Marcolin MA, Rigonatti SP, Silva MTA, Paulus W, Pascual-Leone A (2005) Anodal transcranial direct current stimulation of prefrontal cortex enhances working memory. Exp Brain Res 166(1):23–30.  https://doi.org/10.1007/s00221-005-2334-6 CrossRefPubMedGoogle Scholar
  22. Gauthier I, Hayward WG, Tarr MJ, Anderson AW, Skudlarski P, Gore JC (2006) BOLD activity during mental rotation and viewpoint-dependent object recognition. Neuron 34(1):161–171.  https://doi.org/10.1016/S0896-6273(02)00622-0 CrossRefGoogle Scholar
  23. Giglia G, Brighina F, Rizzo S et al (2014) Anodal transcranial direct current stimulation of the right dorsolateral prefrontal cortex enhances memory-guided responses in a visuospatial working memory task. Funct Neurol 29(3):189–193PubMedPubMedCentralGoogle Scholar
  24. Goel V, Dolan RJ (2004) Differential involvement of left prefrontal cortex in inductive and deductive reasoning. Cognition 93(3):B109–B121.  https://doi.org/10.1016/j.cognition.2004.03.001 CrossRefPubMedGoogle Scholar
  25. Goel V, Tierney M, Sheesley L, Bartolo A, Vartanian O, Grafman J (2007) Hemispheric specialization in human prefrontal cortex for resolving certain and uncertain inferences. Cereb Cortex 17(10):2245–2250.  https://doi.org/10.1093/cercor/bhl132 CrossRefPubMedGoogle Scholar
  26. Gruber O, von Cramon DY (2001) Domain-specific distribution of working memory processes along human prefrontal and parietal cortices: a functional magnetic resonance imaging study. Neurosci Lett 297(1):29–32.  https://doi.org/10.1016/S0304-3940(00)01665-7 CrossRefPubMedGoogle Scholar
  27. Hecht D, Walsh V, Lavidor M (2010) Transcranial direct current stimulation facilitates decision making in a probabilistic guessing task. J Neurosci 30(12):4241–4245.  https://doi.org/10.1523/JNEUROSCI.2924-09.2010 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Heimrath K, Sandmann P, Becke A, Müller NG, 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.  https://doi.org/10.3389/fpsyt.2012.00056 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Hobeika L, Diard-Detoeuf C, Garcin B, Levy R, Volle E (2016) General and specialized brain correlates for analogical reasoning: a meta-analysis of functional imaging studies. Hum Brain Mapp 37(5):1953–1969.  https://doi.org/10.1002/hbm.23149 CrossRefPubMedGoogle Scholar
  30. Hogeveen J, Obhi SS, Banissy MJ, Santiesteban I, Press C, Catmur C, Bird G (2014) Task-dependent and distinct roles of the temporoparietal junction and inferior frontal cortex in the control of imitation. Soc Cogn Affect Neurosci 10(7):1003–1009.  https://doi.org/10.1093/scan/nsu148 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Horvath JC, Forte JD, Carter O (2015) Quantitative review finds no evidence of cognitive effects in healthy populations from single-session transcranial direct current stimulation (tDCS). Brain Stimul 8(3):535–550.  https://doi.org/10.1016/j.brs.2015.01.400 CrossRefPubMedGoogle Scholar
  32. Jeon SY, Han SJ (2012) Improvement of the working memory and naming by transcranial direct current stimulation. Ann Rehabil Med 36(5):585–595.  https://doi.org/10.5535/arm.2012.36.5.585 CrossRefPubMedPubMedCentralGoogle Scholar
  33. Jia X, Liang P, Lu J, Yang Y, Zhong N, Li K (2011) Common and dissociable neural correlates associated with component processes of inductive reasoning. Neuroimage 56(4):2292–2299.  https://doi.org/10.1016/j.neuroimage.2011.03.020 CrossRefPubMedGoogle Scholar
  34. Johnson-Laird PN (1983) A computational analysis of consciousness. Cognition & Brain Theory 6:499–508Google Scholar
  35. Just MA, Carpenter PA, Keller TA, Emery L, Zajac H, Thulborn KR (2001a) Interdependence of nonoverlapping cortical systems in dual cognitive tasks. Neuroimage 14(2):417–426.  https://doi.org/10.1006/nimg.2001.0826 CrossRefPubMedGoogle Scholar
  36. Just MA, Carpenter PA, Maguire M, Diwadkar V, McMains S (2001b) Mental rotation of objects retrieved from memory: a functional MRI study of spatial processing. J Exp Psychol Gen 130(3):493–503.  https://doi.org/10.1037/0096-3445.130.3.493 CrossRefPubMedGoogle Scholar
  37. Kincses TZ, Antal A, Nitsche MA, Bártfai O, Paulus W (2004) Facilitation of probabilistic classification learning by transcranial direct current stimulation of the prefrontal cortex in the human. Neuropsychologia 42(1):113–117.  https://doi.org/10.1016/S0028-3932(03)00124-6 CrossRefPubMedGoogle Scholar
  38. Klem GH, Lüders HO, Jasper HH, Elger C (1999) The ten-twenty electrode system of the International Federation. Electroencephalogr Clin Neurophysiol 52(3):3–6Google Scholar
  39. Knauff M, Rauh R, Schlieder C (1995) Preferred mental models in qualitative spatial reasoning: A cognitive assessment of Allen’s calculus. In: Moore JD, Lehmann JF (eds) Proceedings of the Seventeenth Annual Conference of the Cognitive Science Society. Lawrence Erlbaum Associates, Pittsburgh, pp 200–205Google Scholar
  40. Koenigs M, Barbey AK, Postle BR, Grafman J (2009) Superior parietal cortex is critical for the manipulation of information in working memory. J Neurosci 29(47):14980–14986.  https://doi.org/10.1523/JNEUROSCI.3706-09.2009 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Krawczyk DC, McClelland MM, Donovan CM (2011) A hierarchy for relational reasoning in the prefrontal cortex. Cortex 47(5):588–597.  https://doi.org/10.1016/j.cortex.2010.04.008 CrossRefPubMedGoogle Scholar
  42. Kuehne M, Heimrath K, Heinze HJ, Zaehle T (2015) Transcranial direct current stimulation of the left dorsolateral prefrontal cortex shifts preference of moral judgments. PLoS One 10(5):e0127061.  https://doi.org/10.1371/journal.pone.0127061 CrossRefPubMedPubMedCentralGoogle Scholar
  43. Lecrubier Y, Sheehan DV, Weiller E, Amorim P, Bonora I, Sheehan KH, Janavs J, Dunbar GC (1997) The Mini International Neuropsychiatric Interview (MINI). A short diagnostic structured interview: reliability and validity according to the CIDI. Eur Psychiatry 12(5):224–231.  https://doi.org/10.1016/S0924-9338(97)83296-8 CrossRefGoogle Scholar
  44. Lee KH, Choi YY, Gray JR, Cho SH, Chae JH, Lee S, Kim K (2006) Neural correlates of superior intelligence: stronger recruitment of posterior parietal cortex. Neuroimage 29(2):578–586.  https://doi.org/10.1016/j.neuroimage.2005.07.036 CrossRefPubMedGoogle Scholar
  45. Martin DM, Liu R, Alonzo A, Green M, Player MJ, Sachdev P, Loo CK (2013) Can transcranial direct current stimulation enhance outcomes from cognitive training? A randomized controlled trial in healthy participants. Int J Neuropsychopharmacol 16:1927–1936CrossRefGoogle Scholar
  46. Miranda PC, Lomarev M, Hallett M (2006) Modeling the current distribution during transcranial direct current stimulation. Clin Neurophysiol 117(7):1623–1629.  https://doi.org/10.1016/j.clinph.2006.04.009 CrossRefPubMedGoogle Scholar
  47. Molero-Chamizo A, Bailén JRA, Béjar TG, López MG, Rodríguez IJ, Lérida CG, Panal SP, Ángel GG, Corchero LL, Vega MJR, Nitsche MA, Rivera-Urbina GN (2018) Poststimulation time interval-dependent effects of motor cortex anodal tDCS on reaction-time task performance. Cogn Affect Behav Neurosci 18(1):167–175.  https://doi.org/10.3758/s13415-018-0561-0 CrossRefPubMedGoogle Scholar
  48. Moliadze V, Antal A, Paulus W (2010) Electrode-distance dependent after-effects of transcranial direct and random noise stimulation with extracephalic reference electrodes. Clin Neurophysiol 121(12):2165–2171.  https://doi.org/10.1016/j.clinph.2010.04.033 CrossRefPubMedGoogle Scholar
  49. Nitsche MA, Paulus W (2000) Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. J Physiol 527(3):633–639.  https://doi.org/10.1111/j.1469-7793.2000.t01-1-00633.x CrossRefPubMedPubMedCentralGoogle Scholar
  50. Nitsche MA, Paulus W (2001) Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans. Neurology 57(10):1899–1901.  https://doi.org/10.1212/WNL.57.10.1899 CrossRefPubMedGoogle Scholar
  51. Nitsche MA, Liebetanz D, Antal A, Lang N, Tergau F, Paulus W (2003a) Modulation of cortical excitability by weak direct current stimulation–technical, safety and functional aspects. Suppl Clin Neurophysiol 56:255–276.  https://doi.org/10.1016/S1567-424X(09)70230-2 CrossRefPubMedGoogle Scholar
  52. Nitsche MA, Nitsche MS, Klein CC, Tergau F, Rothwell JC, Paulus W (2003b) Level of action of cathodal DC polarisation induced inhibition of the human motor cortex. Clin Neurophysiol 114(4):600–604.  https://doi.org/10.1016/S1388-2457(02)00412-1 CrossRefPubMedGoogle Scholar
  53. Nitsche MA, Cohen LG, Wassermann EM, Priori A, Lang N, Antal A, Paulus W, Hummel F, Boggio PS, Fregni F, Pascual-Leone A (2008) Transcranial direct current stimulation: state of the art 2008. Brain Stimul 1(3):206–223.  https://doi.org/10.1016/j.brs.2008.06.004 CrossRefPubMedGoogle Scholar
  54. Oldrati V, Patricelli J, Colombo B, Antonietti A (2016) The role of dorsolateral prefrontal cortex in inhibition mechanism: a study on cognitive reflection test and similar tasks through neuromodulation. Neuropsychologia 91:499–508.  https://doi.org/10.1016/j.neuropsychologia.2016.09.010 CrossRefPubMedGoogle Scholar
  55. Olson IR, Berryhill M (2009) Some surprising findings on the involvement of the parietal lobe in human memory. Neurobiol Learn Mem 91(2):155–165.  https://doi.org/10.1016/j.nlm.2008.09.006 CrossRefPubMedGoogle Scholar
  56. Opitz A, Paulus W, Will S, Antunes A, Thielscher A (2015) Determinants of the electric field during transcranial direct current stimulation. Neuroimage 109:140–150.  https://doi.org/10.1016/j.neuroimage.2015.01.033 CrossRefPubMedGoogle Scholar
  57. Park SH, Seo JH, Kim YH, Ko MH (2014) Long-term effects of transcranial direct current stimulation combined with computer-assisted cognitive training in healthy older adults. NeuroReport 25(2):122–126.  https://doi.org/10.1097/WNR.0000000000000080 CrossRefPubMedGoogle Scholar
  58. Parsons LM, Osherson D (2001) New evidence for distinct right and left brain systems for deductive versus probabilistic reasoning. Cerebr Cortex 11(10):954–965.  https://doi.org/10.1093/cercor/11.10.954 CrossRefGoogle Scholar
  59. Poreisz C, Boros K, Antal A, Paulus W (2007) Safety aspects of transcranial direct current stimulation concerning healthy subjects and patients. Brain Res Bull 72(4–6):208–214.  https://doi.org/10.1016/j.brainresbull.2007.01.004 CrossRefPubMedGoogle Scholar
  60. Preusse F, van der Meer E, Ullwer D, Brucks M, Krueger F, Wartenburger I (2010) Long-term characteristics of analogical processing in high-school students with high fluid intelligence: an fMRI study. ZDM 42(6):635–647.  https://doi.org/10.1007/s11858-010-0259-4 CrossRefGoogle Scholar
  61. Qiu J, Li H, Jou J, Liu J, Luo Y, Feng T, Wu Z, Zhang Q (2010) Neural correlates of the “Aha” experiences: evidence from an fMRI study of insight problem solving. Cortex 46(3):397–403.  https://doi.org/10.1016/j.cortex.2009.06.006 CrossRefPubMedGoogle Scholar
  62. Ragni M, Knauff M (2013) A theory and a computational model of spatial reasoning with preferred mental models. Psychol Rev 120(3):561–588.  https://doi.org/10.1037/a0032460 CrossRefPubMedGoogle Scholar
  63. Ragni M, Franzmeier I, Maier S, Knauff M (2016) Uncertain relational reasoning in the parietal cortex. Brain Cogn 104:72–81.  https://doi.org/10.1016/j.bandc.2016.02.006 CrossRefPubMedGoogle Scholar
  64. Rauh R, Hagen C, Knauff M, Kuss T, Schlieder C, Strube G (2005) Preferred and alternative mental models in spatial reasoning. Spat Cogn Comput 5(2–3):239–269.  https://doi.org/10.1080/13875868.2005.9683805 CrossRefGoogle Scholar
  65. Rêgo GG, Lapenta OM, Marques LM, Costa TL, Leite J, Carvalho S, Boggio PS (2015) Hemispheric dorsolateral prefrontal cortex lateralization in the regulation of empathy for pain. Neurosci Lett 594:12–16.  https://doi.org/10.1016/j.neulet.2015.03.042 CrossRefPubMedGoogle Scholar
  66. Ruff CC, Knauff M, Fangmeier T, Spreer J (2003) Reasoning and working memory: common and distinct neuronal processes. Neuropsychologia 41(9):1241–1253.  https://doi.org/10.1016/S0028-3932(03)00016-2 CrossRefPubMedGoogle Scholar
  67. Santiesteban I, Banissy MJ, Catmur C, Bird G (2015) Functional lateralization of temporoparietal junction–imitation inhibition, visual perspective-taking and theory of mind. Eur J Neurosci 42(8):2527–2533.  https://doi.org/10.1111/ejn.13036 CrossRefPubMedGoogle Scholar
  68. Sellaro R, Güroǧlu B, Nitsche MA, van den Wildenberg WPM, Massaro V, Durieux J, Hommel B, Colzato L (2015) Increasing the role of belief information in moral judgments by stimulating the right temporoparietal junction. Neuropsychologia 77:400–408.  https://doi.org/10.1016/j.neuropsychologia.2015.09.016 CrossRefPubMedGoogle Scholar
  69. Sellaro R, Nitsche MA, Colzato LS (2016) The stimulated social brain: effects of transcranial direct current stimulation on social cognition. Ann N Y Acad Sci 1369(1):218–239.  https://doi.org/10.1111/nyas.13098 CrossRefPubMedGoogle Scholar
  70. Shafi MM, Westover MB, Fox MD, Pascual-Leone A (2012) Exploration and modulation of brain network interactions with noninvasive brain stimulation in combination with neuroimaging. Eur J Neurosci 35(6):805–825.  https://doi.org/10.1111/j.1460-9568.2012.08035.x CrossRefPubMedPubMedCentralGoogle Scholar
  71. Shepard RN, Metzler J (1971) Mental rotation of three-dimensional objects Science 171(3972):701–703.  https://doi.org/10.1126/science.171.3972.701 CrossRefPubMedGoogle Scholar
  72. Tsujii T, Sakatani K, Masuda S, Akiyama T, Watanabe S (2011) Evaluating the roles of the inferior frontal gyrus and superior parietal lobule in deductive reasoning: an rTMS study. NeuroImage 58(2):640–646.  https://doi.org/10.1016/j.neuroimage.2011.06.076 CrossRefPubMedGoogle Scholar
  73. van Asselen M, Kessels RP, Neggers SF, Kappelle LJ, Frijns CJ, Postma A (2006) Brain areas involved in spatial working memory. Neuropsychologia 44(7):1185–1194.  https://doi.org/10.1016/j.neuropsychologia.2005.10.005 CrossRefGoogle Scholar
  74. Vandierendonck A, Vooght AVGD (1997) Working memory constraints on linear reasoning with spatial and temporal contents. Q J Exp Psychol 50A(4):803–820.  https://doi.org/10.1080/713755735 CrossRefGoogle Scholar
  75. Volle E, Gilbert SJ, Benoit RG, Burgess PW (2010) Specialization of the rostral prefrontal cortex for distinct analogy processes. Cereb Cortex 20(11):2647–2659.  https://doi.org/10.1093/cercor/bhq012 CrossRefPubMedPubMedCentralGoogle Scholar
  76. Wager TD, Smith EE (2003) Neuroimaging studies of working memory. Cogn Affect Behav Ne 3(4):255–274.  https://doi.org/10.3758/CABN.3.4.255 CrossRefGoogle Scholar
  77. Wagner T, Fregni F, Fecteau S, Grodzinsky A, Zahn M, Pascual-Leone A (2007) Transcranial direct current stimulation: a computer-based human model study. Neuroimage 35(3):1113–1124.  https://doi.org/10.1016/j.neuroimage.2007.01.027 CrossRefPubMedGoogle Scholar
  78. Wang J, Wang Y, Hu Z, Li X (2014) Transcranial direct current stimulation of the dorsolateral prefrontal cortex increased pain empathy. Neuroscience 281:202–207.  https://doi.org/10.1016/j.neuroscience.2014.09.044 CrossRefPubMedGoogle Scholar
  79. Wassermann EM, Grafman J (2005) Recharging cognition with DC brain polarization. Trends Cogn Sci 9(11):503–505.  https://doi.org/10.1212/01.WNL.0000152986.07469.E9 CrossRefPubMedGoogle Scholar
  80. Wendelken C, Bunge SA (2010) Transitive inference: distinct contributions of rostrolateral prefrontal cortex and the hippocampus. J Cogn Neurosci 22(5):837–847.  https://doi.org/10.1016/j.bandc.2008.04.010 CrossRefPubMedPubMedCentralGoogle Scholar
  81. Wertheim J, Ragni M (2018) The neural correlates of relational reasoning: a meta-analysis of 47 functional magnetic resonance studies. J Cogn Neurosci 30(11):1734–1748.  https://doi.org/10.1162/jocn_a_01311 CrossRefPubMedGoogle Scholar
  82. Wraga M, Thompson WL, Alpert NM, Kosslyn SM (2003) Implicit transfer of motor strategies in mental rotation. Brain Cogn 52(2):135–143.  https://doi.org/10.1016/S0278-2626(03)00033-2 CrossRefPubMedGoogle Scholar
  83. Wraga M, Shephard JM, Church JA, Inati S, Kosslyn SM (2005) Imagined rotations of self versus objects: an fMRI study. Neuropsychologia 43(9):1351–1361.  https://doi.org/10.1016/j.neuropsychologia.2004.11.028 CrossRefPubMedGoogle Scholar
  84. Wu YJ, Tseng P, Chang CF, Pai MC, Hsu KS, Lin CC, Juan CH (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.  https://doi.org/10.1016/j.bandc.2014.09.002 CrossRefPubMedGoogle Scholar
  85. Zaehle T, Sandmann P, Thorne JD, Jäncke L, Herrmann CS (2011) Transcranial direct current stimulation of the prefrontal cortex modulates working memory performance: combined behavioural and electrophysiological evidence. BMC Neurosci 12(1):2.  https://doi.org/10.1186/1471-2202-12-2 CrossRefPubMedPubMedCentralGoogle Scholar
  86. Zimmermann K, Freksa C (1996) Qualitative spatial reasoning using orientation, distance, and path knowledge. Appl Artif Intell 6(1):49–58.  https://doi.org/10.1007/BF00117601 CrossRefGoogle Scholar
  87. Zmigrod S, Colzato LS, Hommel B (2014) Evidence for a role of the right dorsolateral prefrontal cortex in controlling stimulus-response integration: a transcranial direct current stimulation (tDCS) study. Brain Stimul 7(4):516–520.  https://doi.org/10.1016/j.brs.2014.03.004 CrossRefPubMedGoogle Scholar
  88. Zmigrod S, Colzato LS, Hommel B (2015) Stimulating creativity: modulation of convergent and divergent thinking by transcranial direct current stimulation (tDCS). Creat Res J 27(4):353–360.  https://doi.org/10.1080/10400419.2015.1087280 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Julia Wertheim
    • 1
    Email author
  • Lorenza S. Colzato
    • 2
    • 3
    • 4
    • 5
  • Michael A. Nitsche
    • 6
    • 7
  • Marco Ragni
    • 1
  1. 1.Cognitive Computation LabAlbert-Ludwigs-Universität FreiburgFreiburgGermany
  2. 2.Cognitive Neurophysiology, Department of Child and Adolescent Psychiatry, Faculty of MedicineTechnical University DresdenDresdenGermany
  3. 3.Department of Cognitive Psychology Institute of Cognitive Neuroscience Faculty of PsychologyRuhr University BochumBochumGermany
  4. 4.Institute for Sports and Sport Science, University of KasselKasselGermany
  5. 5.Institute for Psychological Research & Leiden Institute for Brain and CognitionLeiden UniversityLeidenThe Netherlands
  6. 6.Leibniz Research Center for Working Environment and Human FactorsDortmundGermany
  7. 7.Department of NeurologyUniversity Medical Hospital BergmannsheilBochumGermany

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