Brain Imaging and Behavior

, Volume 11, Issue 1, pp 17–29 | Cite as

Evoking visual neglect-like deficits in healthy volunteers – an investigation by repetitive navigated transcranial magnetic stimulation

  • Katrin Giglhuber
  • Stefanie Maurer
  • Claus Zimmer
  • Bernhard Meyer
  • Sandro M. Krieg
Original Research

ABSTRACT

In clinical practice, repetitive navigated transcranial magnetic stimulation (rTMS) is of particular interest for non-invasive mapping of cortical language areas. Yet, rTMS studies try to detect further cortical functions. Damage to the underlying network of visuospatial attention function can result in visual neglect—a severe neurological deficit and influencing factor for a significantly reduced functional outcome. This investigation aims to evaluate the use of rTMS for evoking visual neglect in healthy volunteers and the potential of specifically locating cortical areas that can be assigned for the function of visuospatial attention. Ten healthy, right-handed subjects underwent rTMS visual neglect mapping. Repetitive trains of 5 Hz and 10 pulses were applied to 52 pre-defined cortical spots on each hemisphere; each cortical spot was stimulated 10 times. Visuospatial attention was tested time-locked to rTMS pulses by a landmark task. Task pictures were displayed tachistoscopically for 50 ms. The subjects’ performance was analyzed by video, and errors were referenced to cortical spots. We observed visual neglect-like deficits during the stimulation of both hemispheres. Errors were categorized into leftward, rightward, and no response errors. Rightward errors occurred significantly more often during stimulation of the right hemisphere than during stimulation of the left hemisphere (mean rightward error rate (ER) 1.6 ± 1.3 % vs. 1.0 ± 1.0 %, p = 0.0141). Within the left hemisphere, we observed predominantly leftward errors rather than rightward errors (mean leftward ER 2.0 ± 1.3 % vs. rightward ER 1.0 ± 1.0 %; p = 0.0005). Visual neglect can be elicited non-invasively by rTMS, and cortical areas eloquent for visuospatial attention can be detected. Yet, the correlation of this approach with clinical findings has to be shown in upcoming steps.

Keywords

Cortical mapping Landmark task Neuropsychology Tachistoscopic testing Transcranial magnetic stimulation Visual neglect 

Abbreviations

dti

Diffusion tensor imaging

er

Error rate

fef

Frontal eye field

fmri

Functional magnetic resonance imaging

ft

Fiber tracking

ipi

Inter-picture-interval

mri

Magnetic resonance imaging

rmt

Resting motor threshold

ntms

Navigated transcranial magnetic stimulation

rtms

Repetitive navigated transcranial magnetic stimulation

tms

Transcranial magnetic stimulation

tpj

Temporoparietal junction

sd

Standard deviation

vas

Visual analogue scale

3-d

Three-dimensional

Notes

Acknowledgments

The first author gratefully acknowledges the support of the TUM graduate school.

Compliance with ethical standards

Conflict of interest

SK is a consultant for BrainLab AG (Feldkirchen, Germany). Yet, the study was completely financed by institutional grants from the Department of Neurosurgery and the Section of Neuroradiology, and all authors declare to have no conflict of interest affecting this study, nor the materials or methods used, nor the findings specified in this paper.

Informed consent

All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation (institutional and national) and with the Helsinki Declaration of 1975, and the applicable revisions at the time of the investigation. Informed consent was obtained from all patients for being included in the study.

Supplementary material

11682_2016_9506_MOESM1_ESM.docx (114 kb)
Online Resource 1 (DOCX 114 kb)
11682_2016_9506_MOESM2_ESM.docx (112 kb)
Online Resource 2 (DOCX 111 kb)

References

  1. Bartolomeo, P., Thiebaut de Schotten, M., Duffau, H., 2007. Mapping of visuospatial functions during brain surgery: A new tool to prevent unilateral spatial neglect. Neurosurgery, 61, e1340.Google Scholar
  2. Bartolomeo, P., de Schotten, M. T., & Chica, A. B. (2012). Brain networks of visuospatial attention and their disruption in visual neglect. Frontiers in Human Neuroscience, 6, 110.PubMedPubMedCentralGoogle Scholar
  3. Bonato, M. (2012). Neglect and extinction depend greatly on task demands: a review. Frontiers in Human Neuroscience, 6, 195.CrossRefPubMedPubMedCentralGoogle Scholar
  4. Brighina, F., Bisiach, E., Oliveri, M., Piazza, A., La Bua, V., Daniele, O., & Fierro, B. (2003). 1 Hz repetitive transcranial magnetic stimulation of the unaffected hemisphere ameliorates contralesional visuospatial neglect in humans. Neuroscience Letters, 336, 131–133.CrossRefPubMedGoogle Scholar
  5. Brighina, F., Bisiach, E., Piazza, A., Oliveri, M., La Bua, V., Daniele, O., & Fierro, B. (2002). Perceptual and response bias in visuospatial neglect due to frontal and parietal repetitive transcranial magnetic stimulation in normal subjects. Neuroreport, 13, 2571–2575.CrossRefPubMedGoogle Scholar
  6. Corbetta, M., & Shulman, G. L. (2002). Control of goal-directed and stimulus-driven attention in the brain. Nature Reviews. Neuroscience, 3, 201–215.CrossRefPubMedGoogle Scholar
  7. Corbetta, M., & Shulman, G. L. (2011). Spatial neglect and attention networks. Annual Review of Neuroscience, 34, 569–599.CrossRefPubMedPubMedCentralGoogle Scholar
  8. Corbetta, M., Kincade, M. J., Lewis, C., Snyder, A. Z., & Sapir, A. (2005). Neural basis and recovery of spatial attention deficits in spatial neglect. Nature Neuroscience, 8, 1603–1610.CrossRefPubMedGoogle Scholar
  9. Corina, D. P., Gibson, E. K., Martin, R., Poliakov, A., Brinkley, J., & Ojemann, G. A. (2005). Dissociation of action and object naming: evidence from cortical stimulation mapping. Human Brain Mapping, 24, 1–10.CrossRefPubMedGoogle Scholar
  10. Duecker, F., Sack, A.T., 2014. The hybrid model of attentional control: New insights into hemispheric asymmetries inferred from TMS research. Neuropsychologia, 74, 21–9.Google Scholar
  11. Epstein, C.M., 1996. Optimum stimulus parameters for lateralized suppression of speech with magnetic brain stimulation. Neurology, 47, 1590–3.Google Scholar
  12. Fierro, B., 2000. Contralateral neglect induced by right posterior parietal rTMS in healthy subjects. Neuroreport, 11, 1519–21.Google Scholar
  13. Fierro, B., Brighina, F., & Bisiach, E. (2006). Improving neglect by TMS. Behavioural Neurology, 17, 169–176.CrossRefPubMedGoogle Scholar
  14. de Haan, B., Karnath, H. O., & Driver, J. (2012). Mechanisms and anatomy of unilateral extinction after brain injury. Neuropsychologia, 50, 1045–1053.CrossRefPubMedGoogle Scholar
  15. Harvey, M., Milner, A. D., & Roberts, R. C. (1995). An investigation of hemispatial neglect using the landmark test. Brain and Cognition, 27, 59–78.CrossRefPubMedGoogle Scholar
  16. Hauck, T., Tanigawa, N., Probst, M., Wohlschlaeger, A., Ille, S., Sollmann, N., Maurer, S., Zimmer, C., Ringel, F., Meyer, B., & Krieg, S. M. (2015a). Stimulation frequency determines the distribution of language positive cortical regions during navigated transcranial magnetic brain stimulation. BMC Neuroscience, 16, 5.Google Scholar
  17. Hauck, T., Tanigawa, N., Probst, M., Wohlschlaeger, A., Ille, S., Sollmann, N., Maurer, S., Zimmer, C., Ringel, F., Meyer, B., & Krieg, S. M. (2015b). Task type affects location of language-positive cortical regions by repetitive navigated transcranial magnetic stimulation mapping. PloS One, 10, e0125298.CrossRefPubMedPubMedCentralGoogle Scholar
  18. Heilman, K. M. (1980). Right hemisphere dominance for attention: the mechanism underlying hemispheric asymmetries of inattention (neglect). Neurology, 30, 327.CrossRefPubMedGoogle Scholar
  19. Ille, S., Sollmann, N., Hauck, T., Maurer, S., Tanigawa, N., Obermueller, T., Negwer, C., Droese, D., Zimmer, C., Meyer, B., Ringel, F., & Krieg, S. M. (2015). Combined noninvasive language mapping by navigated transcranial magnetic stimulation and functional MRI and its comparison with direct cortical stimulation. Journal of Neurosurgery, 123, 212–25.Google Scholar
  20. Jehkonen, M., Laihosalo, M., Kettunen, J.E., 2006. Impact of neglect on functional outcome after stroke – a review of methodological issues and recent research findings. Restorative Neurology and Neuroscience, 24, 209–15.Google Scholar
  21. Jehkonen, M., Ahonen, J. P., Dastidar, P., Koivisto, A. M., Laippala, P., Vilkki, J., & Molnar, G. (2000). Visual neglect as a predictor of functional outcome one year after stroke. Acta Neurologica Scandinavica, 101, 195–201.CrossRefPubMedGoogle Scholar
  22. Karnath, H. O., & Rorden, C. (2012). The anatomy of spatial neglect. Neuropsychologia, 50, 1010–1017.CrossRefPubMedGoogle Scholar
  23. Katz, N., Hartman-Maeir, A., Ring, H., Soroker, N., 1999. Functional disability and rehabilitation outcome in right hemisphere damaged patients with and without unilateral spatial neglect. Archives of Physical Medicine and Rehabilitation, 80, 379–84.Google Scholar
  24. Kim, W. J., Min, Y. S., Yang, E. J., & Paik, N.-J. (2014). Neuronavigated vs Conventional Repetitive Transcranial Magnetic Stimulation Method for Virtual Lesioning on the Broca's Area. . Neuromodulation: Technology at the Neural Interface, 17, 16–21.CrossRefGoogle Scholar
  25. Kinsbourne, M. (1977). Hemi-neglect and hemisphere rivalry. Advances in Neurology, 18, 41–49.PubMedGoogle Scholar
  26. Koch, G., Bonni, S., Giacobbe, V., Bucchi, G., Basile, B., Lupo, F., Versace, V., Bozzali, M., & Caltagirone, C. (2012). Theta-burst stimulation of the left hemisphere accelerates recovery of hemispatial neglect. Neurology, 78, 24–30.CrossRefPubMedGoogle Scholar
  27. Krieg, S. M., Shiban, E., Buchmann, N. H., Gempt, J., Foerschler, A., Meyer, B., & Ringel, F. (2012). Utility of presurgical navigated transcranial magnetic brain stimulation for the resection of tumors in eloquent motor areas. Journal of Neurosurgery, 116, 994–1001.CrossRefPubMedGoogle Scholar
  28. Krieg, S. M., Sollmann, N., Hauck, T., Ille, S., Foerschler, A., Meyer, B., & Ringel, F. (2013). Functional language shift to the right hemisphere in patients with language-eloquent brain tumors. PloS One, 8, e75403.CrossRefPubMedPubMedCentralGoogle Scholar
  29. Krieg, S. M., Sollmann, N., Tanigawa, N., Foerschler, A., Meyer, B., & Ringel, F. (2015). Cortical distribution of speech and language errors investigated by visual object naming and navigated transcranial magnetic stimulation. Brain Structure & Function, 38, 1320–1324.Google Scholar
  30. Krieg, S. M., Tarapore, P. E., Picht, T., Tanigawa, N., Houde, J., Sollmann, N., Meyer, B., Vajkoczy, P., Berger, M. S., Ringel, F., & Nagarajan, S. (2014). Optimal timing of pulse onset for language mapping with navigated repetitive transcranial magnetic stimulation. NeuroImage, 100, 219–236.CrossRefPubMedGoogle Scholar
  31. Kwon, J. C., Ahn, S., Kim, S., & Heilman, K. M. (2011). Ipsilesional ‘where’ with contralesional ‘what’ neglect. Neurocase, 18, 415–423.CrossRefPubMedGoogle Scholar
  32. Lioumis, P., Zhdanov, A., Makela, N., Lehtinen, H., Wilenius, J., Neuvonen, T., Hannula, H., Deletis, V., Picht, T., & Makela, J. P. (2012). A novel approach for documenting naming errors induced by navigated transcranial magnetic stimulation. Journal of Neuroscience Methods, 204, 349–354.CrossRefPubMedGoogle Scholar
  33. Lunven, M., Thiebaut De Schotten, M., Bourlon, C., Duret, C., Migliaccio, R., Rode, G., & Bartolomeo, P. (2015). White matter lesional predictors of chronic visual neglect: a longitudinal study. Brain, 138, 746–760.CrossRefPubMedPubMedCentralGoogle Scholar
  34. Maurer, S., Tanigawa, N., Sollmann, N., Hauck, T., Ille, S., Boeckh-Behrens, T., Meyer, B., & Krieg, S. (2015a). Non-invasive mapping of calculation function by repetitive navigated transcranial magnetic stimulation. Brain Structure and Function, 28(4), 1–21.Google Scholar
  35. Miranda, P. C. (2013). Physics of effects of transcranial brain stimulation. Handbook of Clinical Neurology, 116, 353–366.CrossRefPubMedGoogle Scholar
  36. Pascual-Leone, A., Gates, J. R., & Dhuna, A. (1991). Induction of speech arrest and counting errors with rapid-rate transcranial magnetic stimulation. Neurology, 41, 697–702.CrossRefPubMedGoogle Scholar
  37. Picht, T., Krieg, S. M., Sollmann, N., Rosler, J., Niraula, B., Neuvonen, T., Savolainen, P., Lioumis, P., Makela, J. P., Deletis, V., Meyer, B., Vajkoczy, P., & Ringel, F. (2013). A comparison of language mapping by preoperative navigated transcranial magnetic stimulation and direct cortical stimulation during awake surgery. Neurosurgery, 72, 808–819.CrossRefPubMedGoogle Scholar
  38. Ricci, R., Salatino, A., Li, X., Funk, A. P., Logan, S. L., Mu, Q., Johnson, K. A., Bohning, D. E., & George, M. S. (2012). Imaging the neural mechanisms of TMS neglect-like bias in healthy volunteers with the interleaved TMS/fMRI technique: preliminary evidence. Frontiers in Human Neuroscience, 6, 326.CrossRefPubMedPubMedCentralGoogle Scholar
  39. Rossi, S., Hallett, M., Rossini, P. M., & Pascual-Leone, A. (2009). Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clinical Neurophysiology, 120, 2008–2039.CrossRefPubMedPubMedCentralGoogle Scholar
  40. Roux, F. E., Dufor, O., Lauwers-Cances, V., Boukhatem, L., Brauge, D., Draper, L., Lotterie, J. A., Demonet, J. F. (2011). Electrostimulation mapping of spatial neglect. Neurosurgery, 69, 1218–31.Google Scholar
  41. Ruff, C. C., Bestmann, S., Blankenburg, F., Bjoertomt, O., Josephs, O., Weiskopf, N., Deichmann, R., & Driver, J. (2008). Distinct causal influences of parietal versus frontal areas on human visual cortex: evidence from concurrent TMS-fMRI. Cerebral Cortex, 18, 817–827.CrossRefPubMedGoogle Scholar
  42. Ruohonen, J., & Karhu, J. (2010). Navigated transcranial magnetic stimulation. Neurophysiologie Clinique, 40, 7–17.CrossRefPubMedGoogle Scholar
  43. Sacchetti, D. L., Goedert, K. M., Foundas, A. L., & Barrett, A. M. (2015). Ipsilesional neglect: behavioral and anatomical correlates. Neuropsychology, 29, 183–190.CrossRefPubMedGoogle Scholar
  44. Sack, A.T., 2010. Using non-invasive brain interference as a tool for mimicking spatial neglect in healthy volunteers. Restorative Neurology and Neuroscience, 28(4), 485–497.Google Scholar
  45. Salatino, A., Poncini, M., George, M. S., & Ricci, R. (2014). Hunting for right and left parietal hot spots using single-pulse TMS: modulation of visuospatial perception during line bisection judgment in the healthy brain. Frontiers in Psychology, 5, 1238.CrossRefPubMedPubMedCentralGoogle Scholar
  46. Sanai, N., Martino, J., & Berger, M. S. (2012). Morbidity profile following aggressive resection of parietal lobe gliomas. Journal of Neurosurgery, 116, 1182–1186.CrossRefPubMedGoogle Scholar
  47. Shinoura, N., Suzuki, Y., Yamada, R., Tabei, Y., Saito, K., & Yagi, K. (2009). Damage to the right superior longitudinal fasciculus in the inferior parietal lobe plays a role in spatial neglect. Neuropsychologia, 47, 2600–2603.CrossRefPubMedGoogle Scholar
  48. Sollmann, N., Giglhuber, K., Tussis, L., Meyer, B., Ringel, F., & Krieg, S. M. (2015b). NTMS-based DTI fiber tracking for language pathways correlates with language function and aphasia – a case report. Clinical Neurology and Neurosurgery, 136, 25–28.CrossRefPubMedGoogle Scholar
  49. Sollmann, N., Ille, S., Obermueller, T., Negwer, C., Ringel, F., Meyer, B., & Krieg, S. M. (2015a). The impact of repetitive navigated transcranial magnetic stimulation coil positioning and stimulation parameters on human language function. European Journal of Medical Research, 20, 47.CrossRefPubMedPubMedCentralGoogle Scholar
  50. Sollmann, N., Tanigawa, N., Ringel, F., Zimmer, C., Meyer, B., & Krieg, S. M. (2014). Language and its right-hemispheric distribution in healthy brains: An investigation by repetitive transcranial magnetic stimulation. NeuroImage, 102(Part 2), 776–788.CrossRefPubMedGoogle Scholar
  51. Sollmann, N., Tanigawa, N., Tussis, L., Hauck, T., Ille, S., Maurer, S., Negwer, C., Zimmer, C., Ringel, F., Meyer, B., & Krieg, S. M. (2015c). Cortical regions involved in semantic processing investigated by repetitive navigated transcranial magnetic stimulation and object naming. Neuropsychologia, 70, 185–195.CrossRefPubMedGoogle Scholar
  52. Suchan, J., Rorden, C., & Karnath, H. O. (2012). Neglect severity after left and right brain damage. Neuropsychologia, 50, 1136–1141.CrossRefPubMedPubMedCentralGoogle Scholar
  53. Suchan, J., Umarova, R., Schnell, S., Himmelbach, M., Weiller, C., Karnath, H. O., & Saur, D. (2014). Fiber pathways connecting cortical areas relevant for spatial orienting and exploration. Human Brain Mapping, 35, 1031–1043.CrossRefPubMedGoogle Scholar
  54. Tarapore, P. E., Findlay, A. M., Honma, S. M., Mizuiri, D., Houde, J. F., Berger, M. S., & Nagarajan, S. S. (2013). Language mapping with navigated repetitive TMS: proof of technique and validation. NeuroImage, 82, 260–272.CrossRefPubMedGoogle Scholar
  55. Umarova, R. M., Reisert, M., Beier, T. U., Kiselev, V. G., Kloppel, S., Kaller, C. P., Glauche, V., Mader, I., Beume, L., Hennig, J., & Weiller, C. (2014). Attention-network specific alterations of structural connectivity in the undamaged white matter in acute neglect. Human Brain Mapping, 35, 4678–4692.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  1. 1.Department of Neurosurgery, Klinikum rechts der IsarTechnische Universität MünchenMunichGermany
  2. 2.TUM-Neuroimaging Center, Klinikum rechts der IsarTechnische Universität MünchenMunichGermany
  3. 3.Section of Neuroradiology, Department of Radiology, Klinikum rechts der IsarTechnische Universität MünchenMunichGermany

Personalised recommendations