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.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Anderson JR (2009) How can the human mind occur in the physical universe? Oxford University Press, New York
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
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
Baddeley AD (2003) Working memory: looking back and looking forward. Nat Rev Neurosci 4(10):829–839. https://doi.org/10.1038/nrn1201
Baddeley AD (2007) Working memory, thought, and action. Oxford University Press, Oxford
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
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
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
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
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
Corsi PM (1972) Human memory and the medial temporal region of the brain. Diss Abstr Int 34:819B
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
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
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
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
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
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
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
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
Frederick S (2005) Cognitive reflection and decision making. J Econ Perspect 19(4):25–42. https://doi.org/10.1257/089533005775196732
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
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
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):189–193
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
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
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
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
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
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
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
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
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
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
Johnson-Laird PN (1983) A computational analysis of consciousness. Cognition & Brain Theory 6:499–508
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
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
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
Klem GH, Lüders HO, Jasper HH, Elger C (1999) The ten-twenty electrode system of the International Federation. Electroencephalogr Clin Neurophysiol 52(3):3–6
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 200–205
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
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
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
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
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
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 16:1927–1936
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
M.A. Nitsche is a member of the Advisory Board of Neuroelectrics. The other authors declare no conflicts of interest.
Additional information
Communicated by Winston D Byblow.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Wertheim, J., Colzato, L.S., Nitsche, M.A. et al. Enhancing spatial reasoning by anodal transcranial direct current stimulation over the right posterior parietal cortex. Exp Brain Res 238, 181–192 (2020). https://doi.org/10.1007/s00221-019-05699-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-019-05699-5