Modulating Spatial Processes and Navigation via Transcranial Electrical Stimulation: A Mini Review

Tad T Brunyé, Tad T Brunyé

Abstract

Transcranial electrical stimulation (tES) uses low intensity current to alter neuronal activity in superficial cortical regions, and has gained popularity as a tool for modulating several aspects of perception and cognition. This mini-review article provides an overview of tES and its potential for modulating spatial processes underlying successful navigation, including spatial attention, spatial perception, mental rotation and visualization. Also considered are recent advances in empirical research and computational modeling elucidating several stable cortical-subcortical networks with dynamic involvement in spatial processing and navigation. Leveraging these advances may prove valuable for using tES, particularly transcranial direct and alternating current stimulation (tDCS/tACS), to indirectly target subcortical brain regions by altering neuronal activity in distant yet functionally connected cortical areas. We propose future research directions to leverage these advances in human neuroscience.

Keywords: functional connectivity; navigation; spatial cognition; transcranial alternating current stimulation; transcranial direct current stimulation; visualization.

Figures

Figure 1
Figure 1
Transcranial direct current stimulation (tDCS) targeting the right caudal inferior parietal lobule (angular gyrus) with 2.0 mA current intensity. Panel (A) shows electrode montage and current flow in coronal, sagittal and axial views. Panel (B) shows electrical field intensity overlaid onto a standard MNI head model (MNI 152).

References

    1. Alencastro A. S., Borigato E. M., Rios I. B., Santos M. O., Melo R. C. A., Torres R. E., et al. . (2017). Impairment of the visuo-spatial sketch pad by left prefrontal transcranial direct current stimulation. Brain Stimul. 10, 336–337. 10.1016/j.brs.2016.12.010
    1. Ali M. M., Sellers K. K., Fröhlich F. (2013). Transcranial alternating current stimulation modulates large-scale cortical network activity by network resonance. J. Neurosci. 33, 11262–11275. 10.1523/jneurosci.5867-12.2013
    1. Allen G. L. (1999). “Spatial abilities, cognitive maps and wayfinding: bases for individual differences in spatial cognition and behavior,” in Wayfinding Behavior: Cognitive Mapping and Other Spatial Processes, ed. Golledge R. G. (Baltimore, MD: The Johns Hopkins University Press; ), 46–80.
    1. Andersen R. A. (1987). “Inferior parietal lobule function in spatial perception and visuomotor integration,” in Handbook of Physiology Section 1: The Nervous System. Volume V: Higher Functions of the Brain, Part 2, eds Mountcastle V. B., Plum F., Geiger S. R. (Bethesda, MD: American Physiology Association; ), 483–518.
    1. Andersen R. A., Essick G. K., Siegel R. M. (1985). Encoding of spatial location by posterior parietal neurons. Science 230, 456–458. 10.1126/science.4048942
    1. Berlim M. T., Van den Eynde F., Daskalakis Z. J. (2013). Clinical utility of transcranial direct current stimulation (tDCS) for treating major depression: a systematic review and meta-analysis of randomized, double-blind and sham-controlled trials. J. Psychiatr. Res. 47, 1–7. 10.1016/j.jpsychires.2012.09.025
    1. Blangero A., Menz M. M., McNamara A., Binkofski F. (2009). Parietal modules for reaching. Neuropsychologia 47, 1500–1507. 10.1016/j.neuropsychologia.2008.11.030
    1. Boccia M., Guariglia C., Sabatini U., Nemmi F. (2016). Navigating toward a novel environment from a route or survey perspective: neural correlates and context-dependent connectivity. Brain Struct. Funct. 221, 2005–2021. 10.1007/s00429-015-1021-z
    1. Boccia M., Sulpizio V., Nemmi F., Guariglia C., Galati G. (2017). Direct and indirect parieto-medial temporal pathways for spatial navigation in humans: evidence from resting-state functional connectivity. Brain Struct. Funct. 222, 1945–1957. 10.1007/s00429-016-1318-6
    1. Bolognini N., Olgiati E., Rossetti A., Maravita A. (2010). Enhancing multisensory spatial orienting by brain polarization of the parietal cortex. Eur. J. Neurosci. 31, 1800–1806. 10.1111/j.1460-9568.2010.07211.x
    1. Brotchie P. R., Andersen R. A., Snyder L. H., Goodman S. J. (1995). Head position signals used by parietal neurons to encode locations of visual stimuli. Nature 375, 232–235. 10.1038/375232a0
    1. Brunoni A. R., Vanderhasselt M.-A. (2014). Working memory improvement with non-invasive brain stimulation of the dorsolateral prefrontal cortex: a systematic review and meta-analysis. Brain Cogn. 86, 1–9. 10.1016/j.bandc.2014.01.008
    1. Brunyé T. T., Holmes A., Cantelon J., Eddy M. D., Gardony A. L., Mahoney C. R., et al. . (2014). Direct current brain stimulation enhances navigation efficiency in individuals with low sense of direction. Neuroreport 25, 1175–1179. 10.1097/wnr.0000000000000214
    1. Burgess N. (2008). Spatial cognition and the brain. Ann. N Y Acad. Sci. 1124, 77–97. 10.1196/annals.1440.002
    1. Burgess N., Maguire E. A., O’Keefe J. (2002). The human hippocampus and spatial and episodic memory. Neuron 35, 625–641. 10.1016/s0896-6273(02)00830-9
    1. Burte H., Gardony A. L., Hutton A., Taylor H. A. (2017). Think3d!: improving mathematics learning through embodied spatial training. Cogn. Res. Princ. Implic. 2:13. 10.1186/s41235-017-0052-9
    1. Byrne P., Becker S., Burgess N. (2007). Remembering the past and imagining the future: a neural model of spatial memory and imagery. Psychol. Rev. 114, 340–375. 10.1037/0033-295x.114.2.340
    1. Chafee M. V., Averbeck B. B., Crowe D. A. (2007). Representing spatial relationships in posterior parietal cortex: single neurons code object-referenced position. Cereb. Cortex 17, 2914–2932. 10.1093/cercor/bhm017
    1. Chander B. S., Witkowski M., Braun C., Robinson S. E., Born J., Cohen L. G., et al. . (2016). tACS phase locking of frontal midline theta oscillations disrupts working memory performance. Front. Cell. Neurosci. 10:120. 10.3389/fncel.2016.00120
    1. Chrastil E. R. (2013). Neural evidence supports a novel framework for spatial navigation. Psychon. Bull. Rev. 20, 208–227. 10.3758/s13423-012-0351-6
    1. Cohen M. S., Kosslyn S. M., Breiter H. C., DiGirolamo G. J., Thompson W. L., Anderson A. K., et al. . (1996). Changes in cortical activity during mental rotation A mapping study using functional MRI. Brain 119, 89–100. 10.1093/brain/119.1.89
    1. Constantinidis C., Steinmetz M. A. (1996). Neuronal activity in posterior parietal area 7a during the delay periods of a spatial memory task. J. Neurophysiol. 76, 1352–1355.
    1. Constantinidis C., Steinmetz M. A. (2005). Posterior parietal cortex automatically encodes the location of salient stimuli. J. Neurosci. 25, 233–238. 10.1523/jneurosci.3379-04.2005
    1. Corbetta M. (1998). Frontoparietal cortical networks for directing attention and the eye to visual locations: identical, independent, or overlapping neural systems? Proc. Natl. Acad. Sci. U S A 95, 831–838. 10.1073/pnas.95.3.831
    1. Corbetta M., Shulman G. L., Miezin F. M., Petersen S. E. (1995). Superior parietal cortex activation during spatial attention shifts and visual feature conjunction. Science 270, 802–805. 10.1126/science.270.5237.802
    1. Crowe D. A., Averbeck B. B., Chafee M. V., Georgopoulos A. P. (2005). Dynamics of parietal neural activity during spatial cognitive processing. Neuron 47, 885–891. 10.1016/j.neuron.2005.08.005
    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. de Berker A. O., Bikson M., Bestmann S. (2013). Predicting the behavioral impact of transcranial direct current stimulation: issues and limitations. Front. Hum. Neurosci. 7:613. 10.3389/fnhum.2013.00613
    1. Dedoncker J., Brunoni A. R., Baeken C., Vanderhasselt M.-A. (2016). A systematic review and meta-analysis of the effects of transcranial direct current stimulation (tDCS) over the dorsolateral prefrontal cortex in healthy and neuropsychiatric samples: influence of stimulation parameters. Brain Stimul. 9, 501–517. 10.1016/j.brs.2016.04.006
    1. D’Esposito M., Aguirre G. K., Zarahn E., Ballard D., Shin R. K., Lease J. (1998). Functional MRI studies of spatial and nonspatial working memory. Cogn. Brain Res. 7, 1–13. 10.1016/s0926-6410(98)00004-4
    1. de Tommaso M., Invitto S., Ricci K., Lucchese V., Delussi M., Quattromini P., et al. . (2014). Effects of anodal TDCS stimulation of left parietal cortex on visual spatial attention tasks in men and women across menstrual cycle. Neurosci. Lett. 574, 21–25. 10.1016/j.neulet.2014.05.014
    1. Deutsch G., Bourbon W. T., Papanicolaou A. C., Eisenberg H. M. (1988). Visuospatial tasks compared via activation of regional cerebral blood flow. Neuropsychologia 26, 445–452. 10.1016/0028-3932(88)90097-8
    1. Dudchenko P. A. (2010). Why People Get Lost: The Psychology and Neuroscience of Spatial Cognition. Oxford: Oxford University Press.
    1. Ellison A., Schindler I., Pattison L. L., Milner A. D. (2004). An exploration of the role of the superior temporal gyrus in visual search and spatial perception using TMS. Brain 127, 2307–2315. 10.1093/brain/awh244
    1. Epstein R. A. (2008). Parahippocampal and retrosplenial contributions to human spatial navigation. Trends Cogn. Sci. 12, 388–396. 10.1016/j.tics.2008.07.004
    1. Gauthier I., Hayward W. G., Tarr M. J., Anderson A. W., Skudlarski P., Gore J. C. (2002). BOLD activity during mental rotation and viewpoint-dependent object recognition. Neuron 34, 161–171. 10.1016/s0896-6273(02)00622-0
    1. Hampstead B. M., Brown G. S., Hartley J. F. (2014). Transcranial direct current stimulation modulates activation and effective connectivity during spatial navigation. Brain Stimul. 7, 314–324. 10.1016/j.brs.2013.12.006
    1. Hartley T., Maguire E. A., Spiers H. J., Burgess N. (2003). The well-worn route and the path less traveled: distinct neural bases of route following and wayfinding in humans. Neuron 37, 877–888. 10.1016/S0896-6273(03)00095-3
    1. Harvey C. D., Coen P., Tank D. W. (2012). Choice-specific sequences in parietal cortex during a virtual-navigation decision task. Nature 484, 62–68. 10.1038/nature10918
    1. Hegarty M., Waller D. A. (2005). “Individual differences in spatial abilities,” in The Cambridge Handbook of Visuospatial Thinking, eds Shah P., Miyake A. (New York, NY: Cambridge University Press; ), 121–169.
    1. Herrmann C. S., Rach S., Neuling T., Strüber D. (2013). Transcranial alternating current stimulation: a review of the underlying mechanisms and modulation of cognitive processes. Front. Hum. Neurosci. 7:279. 10.3389/fnhum.2013.00279
    1. Iaria G., Chen J. K., Guariglia C., Ptito A., Petrides M. (2007). Retrosplenial and hippocampal brain regions in human navigation: complementary functional contributions to the formation and use of cognitive maps. Eur. J. Neurosci. 25, 890–899. 10.1111/j.1460-9568.2007.05371.x
    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. Jaušovec N., Jaušovec K., Pahor A. (2014). The influence of theta transcranial alternating current stimulation (tACS) on working memory storage and processing functions. Acta Psychol. 146, 1–6. 10.1016/j.actpsy.2013.11.011
    1. Jordan K., Wüstenberg T., Heinze H. J., Peters M., Jäncke L. (2002). Women and men exhibit different cortical activation patterns during mental rotation tasks. Neuropsychologia 40, 2397–2408. 10.1016/s0028-3932(02)00076-3
    1. Kasten F. H., Herrmann C. S. (2017). Transcranial alternating current stimulation (tACS) enhances mental rotation performance during and after stimulation. Front. Hum. Neurosci. 11:2. 10.3389/fnhum.2017.00002
    1. Keeser D., Meindl T., Bor J., Palm U., Pogarell O., Mulert C., et al. . (2011). Prefrontal transcranial direct current stimulation changes connectivity of resting-state networks during fMRI. J. Neurosci. 31, 15284–15293. 10.1523/JNEUROSCI.0542-11.2011
    1. Klippel A. (2003). “Wayfinding choremes,” in Spatial Information Theory: Foundations of Geographic Information Science. Conference on Spatial Information Theory (COSIT) 2003, eds Kuhn W., Worboys M. F., Timpf S. (Berlin: Springer; ), 320–334.
    1. Kozhevnikov M., Motes M. A., Hegarty M. (2007). Spatial visualization in physics problem solving. Cogn. Sci. 31, 549–579. 10.1080/15326900701399897
    1. Krause B., Márquez-Ruiz J., Cohen Kadosh R. (2013). The effect of transcranial direct current stimulation: a role for cortical excitation/inhibition balance? Front. Hum. Neurosci. 7:602. 10.3389/fnhum.2013.00602
    1. Kravitz D., Saleem K., Baker C., Mishkin M. (2011). A new neural framework for visuospatial processing. J. Vis. 11:319 10.1167/11.11.923
    1. Krishnamurthy V., Gopinath K., Brown G. S., Hampstead B. M. (2015). Resting-state fMRI reveals enhanced functional connectivity in spatial navigation networks after transcranial direct current stimulation. Neurosci. Lett. 604, 80–85. 10.1016/j.neulet.2015.07.042
    1. Laczó B., Antal A., Niebergall R., Treue S., Paulus W. (2012). Transcranial alternating stimulation in a high γ frequency range applied over V1 improves contrast perception but does not modulate spatial attention. Brain Stimul. 5, 484–491. 10.1016/j.brs.2011.08.008
    1. Linn M. C., Petersen A. C. (1985). Emergence and characterization of sex differences in spatial ability: a meta-analysis. Child Dev. 56, 1479–1498. 10.1111/j.1467-8624.1985.tb00213.x
    1. Loomis J. M., Philbeck J. W. (2008). “Measuring perception with spatial updating and action,” in Embodiment, Ego-Space, and Action, eds Klatzky R. L., Behrmann M., MacWhinney B. (Mahwah, NJ: Erlbaum; ), 1–43.
    1. Maguire E. A., Burgess N., O’Keefe J. (1999). Human spatial navigation: cognitive maps, sexual dimorphism, and neural substrates. Curr. Opin. Neurobiol. 9, 171–177. 10.1016/s0959-4388(99)80023-3
    1. Marshall L., Binder S. (2013). Contribution of transcranial oscillatory stimulation to research on neural networks: an emphasis on hippocampo-neocortical rhythms. Front. Hum. Neurosci. 7:614. 10.3389/fnhum.2013.00614
    1. Martin D. M., Liu R., Alonzo A., Green M., Loo C. K. (2014). Use of transcranial direct current stimulation (tDCS) to enhance cognitive training: effect of timing of stimulation. Exp. Brain Res. 232, 3345–3351. 10.1007/s00221-014-4022-x
    1. Molaee-Ardekani B., Márquez-Ruiz J., Merlet I., Leal-Campanario R., Gruart A., Sánchez-Campusano R., et al. . (2013). Effects of transcranial direct current stimulation (tDCS) on cortical activity: a computational modeling study. Brain Stimul. 6, 25–39. 10.1016/j.brs.2011.12.006
    1. Montello D. R. (2005). “Navigation,” in The Cambridge Handbook of Visuospatial Thinking, eds Shah P., Miyake A. (New York, NY: Cambridge University Press; ), 257–294.
    1. Neuling T., Rach S., Herrmann C. S. (2013). Orchestrating neuronal networks: sustained after-effects of transcranial alternating current stimulation depend upon brain states. Front. Hum. Neurosci. 7:161. 10.3389/fnhum.2013.00161
    1. Nitsche M. A., Cohen L. G., Wassermann E. M., Priori A., Lang N., Antal A., et al. . (2008). Transcranial direct current stimulation: state of the art 2008. Brain Stimul. 1, 206–223. 10.1016/j.brs.2008.06.004
    1. Oldrati V., Colombo B., Antonietti A. (2018). Combination of a short cognitive training and tDCS to enhance visuospatial skills: a comparison between online and offline neuromodulation. Brain Res. 1678, 32–39. 10.1016/j.brainres.2017.10.002
    1. Paulus W. (2011). Transcranial electrical stimulation (tES’tDCS; tRNS, tACS) methods. Neuropsychol. Rehabil. 21, 602–617. 10.1080/09602011.2011.557292
    1. Peña-Gómez C., Sala-Lonch R., Junqué C., Clemente I. C., Vidal D., Bargalló N., et al. . (2012). Modulation of large-scale brain networks by transcranial direct current stimulation evidenced by resting-state functional MRI. Brain Stimul. 5, 252–263. 10.1016/j.brs.2011.08.006
    1. Posner M. I. (1980). Orienting of attention. Q. J. Exp. Psychol. 32, 3–25. 10.1080/00335558008248231
    1. Radman T., Ramos R. L., Brumberg J. C., Bikson M. (2009). Role of cortical cell type and morphology in subthreshold and suprathreshold uniform electric field stimulation in vitro. Brain Stimul. 2, 215.e3–228.e3. 10.1016/j.brs.2009.03.007
    1. Rafal R. D., Posner M. I. (1987). Deficits in human visual spatial attention following thalamic lesions. Proc. Natl. Acad. Sci. U S A 84, 7349–7353. 10.1073/pnas.84.20.7349
    1. Rahman A., Reato D., Arlotti M., Gasca F., Datta A., Parra L. C., et al. . (2013). Cellular effects of acute direct current stimulation: somatic and synaptic terminal effects. J. Physiol. 591, 2563–2578. 10.1113/jphysiol.2012.247171
    1. Ratcliff G. (1979). Spatial thought, mental rotation and the right cerebral hemisphere. Neuropsychologia 17, 49–54. 10.1016/0028-3932(79)90021-6
    1. Reichenbach A., Thielscher A., Peer A., Bülthoff H. H., Bresciani J. P. (2014). A key region in the human parietal cortex for processing proprioceptive hand feedback during reaching movements. Neuroimage 84, 615–625. 10.1016/j.neuroimage.2013.09.024
    1. Richter W., Ugurbil K., Georgopoulos A., Kim S.-G. (1997). Time-resolved fMRI of mental rotation. Neuroreport 8, 3697–3702. 10.1097/00001756-199712010-00008
    1. Roy L. B., Sparing R., Fink G. R., Hesse M. D. (2015). Modulation of attention functions by anodal tDCS on right PPC. Neuropsychologia 74, 96–107. 10.1016/j.neuropsychologia.2015.02.028
    1. Ruffini G., Fox M. D., Ripolles O., Miranda P. C., Pascual-Leone A. (2014). Optimization of multifocal transcranial current stimulation for weighted cortical pattern targeting from realistic modeling of electric fields. Neuroimage 89, 216–225. 10.1016/j.neuroimage.2013.12.002
    1. Ruohonen J., Karhu J. (2012). TDCS possibly stimulates glial cells. Clin. Neurophysiol. 123, 2006–2009. 10.1016/j.clinph.2012.02.082
    1. Rushworth M. F. S., Behrens T. E. J., Johansen-Berg H. (2006). Connection patterns distinguish 3 regions of human parietal cortex. Cereb. Cortex 16, 1418–1430. 10.1093/cercor/bhj079
    1. Sack A. T., Kohler A., Bestmann S., Linden D. E. J., Dechent P., Goebel R., et al. . (2007). Imaging the brain activity changes underlying impaired visuospatial judgments: simultaneous fMRI, TMS, and behavioral studies. Cereb. Cortex 17, 2841–2852. 10.1093/cercor/bhm013
    1. Santiesteban I., Banissy M. J., Catmur C., Bird G. (2012). Enhancing social ability by stimulating right temporoparietal junction. Curr. Biol. 22, 2274–2277. 10.1016/j.cub.2012.10.018
    1. Schinazi V. R., Epstein R. A. (2010). Neural correlates of real-world route learning. Neuroimage 53, 725–735. 10.1016/j.neuroimage.2010.06.065
    1. Sejnowski T. J., Paulsen O. (2006). Network oscillations: emerging computational principles. J. Neurosci. 26, 1673–1676. 10.1523/JNEUROSCI.3737-05d.2006
    1. Shelton A. L., Gabrieli J. D. E. (2002). Neural correlates of encoding space from route and survey perspectives. J. Neurosci. 22, 2711–2717.
    1. Shepard R. N., Metzler J. (1971). Mental rotation of three-dimensional objects. Science 171, 701–703. 10.1126/science.171.3972.701
    1. Sherrill K. R., Chrastil E. R., Ross R. S., Erdem U. M., Hasselmo M. E., Stern C. E. (2015). Functional connections between optic flow areas and navigationally responsive brain regions during goal-directed navigation. Neuroimage 118, 386–396. 10.1016/j.neuroimage.2015.06.009
    1. Siegel A. W., White S. H. (1975). The development of spatial representations of large-scale environments. Adv. Child Dev. Behav. 10, 9–55. 10.1016/s0065-2407(08)60007-5
    1. Silva S., Basser P. J., Miranda P. C. (2008). Elucidating the mechanisms and loci of neuronal excitation by transcranial magnetic stimulation using a finite element model of a cortical sulcus. Clin. Neurophysiol. 119, 2405–2413. 10.1016/j.clinph.2008.07.248
    1. Sorby S. A. (1999). Developing 3-D spatial visualization skills. Eng. Des. Graph. J. 63, 21–32.
    1. Sparing R., Thimm M., Hesse M. D., Küst J., Karbe H., Fink G. R. (2009). Bidirectional alterations of interhemispheric parietal balance by non-invasive cortical stimulation. Brain 132, 3011–3020. 10.1093/brain/awp154
    1. Spiers H. J., Maguire E. A. (2006). Thoughts, behaviour, and brain dynamics during navigation in the real world. Neuroimage 31, 1826–1840. 10.1016/j.neuroimage.2006.01.037
    1. Straube B., Chatterjee A. (2010). Space and time in perceptual causality. Front. Hum. Neurosci. 4:28. 10.3389/fnhum.2010.00028
    1. Straube B., Wolk D., Chatterjee A. (2011). The role of the right parietal lobe in the perception of causality: a tDCS study. Exp. Brain Res. 215, 315–325. 10.1007/s00221-011-2899-1
    1. Tagaris G. A., Kim S.-G., Strupp J. P., Andersen P., Uğurbil K., Georgopoulos A. P. (1996). Quantitative relations between parietal activation and performance in mental rotation. Neuroreport 7, 773–776. 10.1097/00001756-199602290-00022
    1. Tagaris G. A., Kim S.-G., Strupp J. P., Andersen P., Uğurbil K., Georgopoulos A. P. (1997). Mental rotation studied by functional magnetic resonance imaging at high field (4 tesla): performance and cortical activation. J. Cogn. Neurosci. 9, 419–432. 10.1162/jocn.1997.9.4.419
    1. Taylor H. A., Hutton A. (2013). Think3d!: training spatial thinking fundamental to stem education. Cogn. Instr. 31, 434–455. 10.1080/07370008.2013.828727
    1. Thiebaut de Schotten M. T., Dell’Acqua F., Forkel S. J., Simmons A., Vergani F., Murphy D. G. M., et al. . (2011). A lateralized brain network for visuospatial attention. Nat. Neurosci. 14, 1245–1246. 10.1038/nn.2905
    1. Titus S., Horsman E. (2009). Characterizing and improving spatial visualization skills. J. Geosci. Edu. 57, 242–254. 10.5408/1.3559671
    1. Tremblay S., Lepage J. F., Latulipe-Loiselle A., Fregni F., Pascual-Leone A., Théoret H. (2014). The uncertain outcome of prefrontal tDCS. Brain Stimul. 7, 773–783. 10.1016/j.brs.2014.10.003
    1. Tseng P., Chang Y. T., Chang C. F., Liang W. K., Juan C. H. (2016). The critical role of phase difference in γ 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. L., 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. Uttal D. H., Meadow N. G., Tipton E., Hand L. L., Alden A. R., Warren C., et al. . (2013). The malleability of spatial skills: a meta-analysis of training studies. Psychol. Bull. 139, 352–402. 10.1037/a0028446
    1. Vogt B. A., Finch D. M., Olson C. R. (1992). Functional heterogeneity in cingulate cortex: the anterior executive and posterior evaluative regions. Cereb. Cortex 2, 435–443. 10.1093/cercor/2.6.435-a
    1. Vossen A., Gross J., Thut G. (2015). α power increase after transcranial alternating current stimulation at α frequency (a-tACS) reflects plastic changes rather than entrainment. Brain Stimul. 8, 499–508. 10.1016/j.brs.2014.12.004
    1. Watson C. E., Chatterjee A. (2012). A bilateral frontoparietal network underlies visuospatial analogical reasoning. Neuroimage 59, 2831–2838. 10.1016/j.neuroimage.2011.09.030
    1. Weber M. J., Messing S. B., Rao H., Detre J. A., Thompson-Schill S. L. (2014). Prefrontal transcranial direct current stimulation alters activation and connectivity in cortical and subcortical reward systems: a tDCS-fMRI study. Hum. Brain Mapp. 35, 3673–3686. 10.1002/hbm.22429
    1. Whitlock J. R., Sutherland R. J., Witter M. P., Moser M.-B., Moser E. I. (2008). Navigating from hippocampus to parietal cortex. Proc. Natl. Acad. Sci. U S A 105, 14755–14762. 10.1073/pnas.0804216105
    1. Wiener J. M., Büchner S. J., Hölscher C. (2009). Taxonomy of human wayfinding tasks: a knowledge-based approach. Spat. Cogn. Comput. 9, 152–165. 10.1080/13875860902906496
    1. Wiener M., Michaelis K., Thompson J. C. (2016). Functional correlates of likelihood and prior representations in a virtual distance task. Hum. Brain Mapp. 37, 3172–3187. 10.1002/hbm.23232
    1. Woldorff M. G., Tempelmann C., Fell J., Tegeler C., Gaschler-Markefski B., Hinrichs H., et al. . (1999). Lateralized auditory spatial perception and the contralaterality of cortical processing as studied with functional magnetic resonance imaging and magnetoencephalography. Hum. Brain Mapp. 7, 49–66. 10.1002/(sici)1097-0193(1999)7:1<49::aid-hbm5>;2-j
    1. Woods A. J., Antal A., Bikson M., Boggio P. S., Brunoni A. R., Celnik P., et al. . (2016). A technical guide to tDCS, and related non-invasive brain stimulation tools. Clin. Neurophysiol. 127, 1031–1104. 10.1016/j.clinph.2015.11.012
    1. Wright J. M. J. M., Krekelberg B. (2014). Transcranial direct current stimulation over posterior parietal cortex modulates visuospatial localization. J. Vis. 14:5. 10.1167/14.9.5
    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. Zacks J. M., Gilliam F., Ojemann J. G. (2003). Selective disturbance of mental rotation by cortical stimulation. Neuropsychologia 41, 1659–1667. 10.1016/s0028-3932(03)00099-x

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