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Transcranial magnetic stimulation of the occipital pole interferes with verbal processing in blind subjects

Nature Neuroscience volume 7, pages 1266–1270 (2004)Cite this article

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Abstract

Recent neuroimaging studies in blind persons show that the occipital cortex, including the primary visual cortex (V1), is active during language-related and verbal-memory tasks. No studies, however, have identified a causal link between early visual cortex activity and successful performance on such tasks. We show here that repetitive transcranial magnetic stimulation (rTMS) of the occipital pole reduces accuracy on a verb-generation task in blind subjects, but not in sighted controls. An analysis of error types revealed that the most common error produced by rTMS was semantic; phonological errors and interference with motor execution or articulation were rare. Thus, in blind persons, a transient 'virtual lesion' of the left occipital cortex interferes with high-level verbal processing.

*Note: The version of this article that was published online on October 3, 2004, listed incorrect affiliations for one author. Amir Amedi is not affiliated with the Human Cortical Physiology Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD 20892-1428, USA. In addition, the original online version failed to note that the Laboratory for Magnetic Brain Stimulation, Department of Neurology, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA 02215, USA is Amir Amedi's present address. The online version was corrected on 10 October 2004, and the printed version of this article is correct.

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Figure 1: Regions of rTMS stimulation and experimental paradigm.
Figure 2: Verb-generation error rates in the blind and sighted groups as a function of rTMS site.
Figure 3: Semantic errors (as a percentage of all semantic and morphosyntactic errors) for each cortical stimulation site in blind and sighted subjects.

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  • 10 October 2004

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References

  1. Sadato, N. et al. Activation of the primary visual cortex by Braille reading in blind subjects. Nature 380, 526–528 (1996).

    Article  CAS  Google Scholar 

  2. Buchel, C., Price, C., Frackowiak, R.S. & Friston, K. Different activation patterns in the visual cortex of late and congenitally blind subjects. Brain 121, 409–419 (1998).

    Article  Google Scholar 

  3. Burton, H. Visual cortex activity in early and late blind people. J. Neurosci. 23, 4005–4011 (2003).

    Article  CAS  Google Scholar 

  4. Cohen, L.G. et al. Functional relevance of cross-modal plasticity in blind humans. Nature 389, 180–183 (1997).

    Article  CAS  Google Scholar 

  5. Pascual-Leone, A., Wassermann, E.M., Sadato, N. & Hallett, M. The role of reading activity on the modulation of motor cortical outputs to the reading hand in Braille readers. Ann. Neurol. 38, 910–915 (1995).

    Article  CAS  Google Scholar 

  6. Burton, H., Snyder, A.Z., Diamond, J.B. & Raichle, M.E. Adaptive changes in early and late blind: a fMRI study of verb-generation to heard nouns. J. Neurophysiol. 88, 3359–3371 (2002).

    Article  CAS  Google Scholar 

  7. Amedi, A., Raz, N., Pianka, P., Malach, R. & Zohary, E. Early 'visual' cortex activation correlates with superior verbal-memory performance in the blind. Nat. Neurosci. 6, 758–766 (2003).

    Article  CAS  Google Scholar 

  8. Roder, B., Stock, O., Bien, S., Neville, H.J. & Rosler, F. Speech processing activates visual cortex in congenitally blind adults. Eur. J. Neurosci. 16, 930–936 (2002).

    Article  Google Scholar 

  9. Noppeney, U., Friston, K.J. & Price, C.J. Effects of visual deprivation on the organization of the semantic system. Brain 126, 1620–1627 (2003).

    Article  Google Scholar 

  10. Burton, H., Diamond, J.B. & McDermott, K.B. Dissociating cortical regions activated by semantic and phonological tasks: a fMRI study in blind and sighted people. J. Neurophysiol. 90, 1965–1982 (2003).

    Article  CAS  Google Scholar 

  11. Pascual-Leone, A., Walsh, V. & Rothwell, J. Transcranial magnetic stimulation in cognitive neuroscience—virtual lesion, chronometry, and functional connectivity. Curr. Opin. Neurobiol. 10, 232–237 (2000).

    Article  CAS  Google Scholar 

  12. Levelt, W.J. Spoken word production: a theory of lexical access. Proc. Natl Acad. Sci. USA 98, 13464–13471 (2001).

    Article  CAS  Google Scholar 

  13. Hallett, M. Transcranial magnetic stimulation and the human brain. Nature 406, 147–150 (2000).

    Article  CAS  Google Scholar 

  14. Malach, R. et al. Object-related activity revealed by functional magnetic resonance imaging in human occipital cortex. Proc. Natl Acad. Sci. USA 92, 8135–8139 (1995).

    Article  CAS  Google Scholar 

  15. Amedi, A., Malach, R., Hendler, T., Peled, S. & Zohary, E. Visuo-haptic object-related activation in the ventral visual pathway. Nat. Neurosci. 4, 324–330 (2001).

    Article  CAS  Google Scholar 

  16. Lisanby, S.H., Gutman, D., Luber, B., Schroeder, C. & Sackeim, H.A. Sham TMS: intracerebral measurement of the induced electrical field and the induction of motor-evoked potentials. Biol. Psychiatry 49, 460–463 (2001).

    Article  CAS  Google Scholar 

  17. Devlin, J.T., Matthews, P.M. & Rushworth, M.F. Semantic processing in the left inferior prefrontal cortex: a combined functional magnetic resonance imaging and transcranial magnetic stimulation study. J. Cogn. Neurosci. 15, 71–84 (2003).

    Article  Google Scholar 

  18. Gabrieli, J.D.E., Poldrack, R.A. & Desmond, J.E. The role of left prefrontal cortex in language and memory. Proc. Natl Acad. Sci. USA 95, 906–913 (1998).

    Article  CAS  Google Scholar 

  19. Shapiro, K.A., Pascual-Leone, A., Mottaghy, F.M., Gangitano, M. & Caramazza, A. Grammatical distinctions in the left frontal cortex. J. Cogn. Neurosci. 13, 713–720 (2001).

    Article  CAS  Google Scholar 

  20. Floel, A. et al. Prefrontal cortex asymmetry for memory encoding of words and abstract shapes. Cereb. Cortex 14, 404–409 (2004).

    Article  Google Scholar 

  21. Stewart, L., Walsh, V., Frith, U. & Rothwell, J.C. TMS produces two dissociable types of speech disruption. Neuroimage 13, 472–478 (2001).

    Article  CAS  Google Scholar 

  22. Poldrack, R.A. et al. Functional specialization for semantic and phonological processing in the left inferior prefrontal cortex. Neuroimage 10, 15–35 (1999).

    Article  CAS  Google Scholar 

  23. Korpilahti, P., Krause, C.M., Holopainen, I. & Lang, A.H. Early and late mismatch negativity elicited by words and speech-like stimuli in children. Brain Lang. 76, 332–339 (2001).

    Article  CAS  Google Scholar 

  24. Chouinard, P.A., Van Der Werf, Y.D., Leonard, G. & Paus, T. Modulating neural networks with transcranial magnetic stimulation applied over the dorsal premotor and primary motor cortices. J. Neurophysiol. 90, 1071–1083 (2003).

    Article  Google Scholar 

  25. Paus, T. Imaging the brain before, during, and after transcranial magnetic stimulation. Neuropsychologia 37, 219–224 (1999).

    Article  CAS  Google Scholar 

  26. Distler, C., Boussaoud, D., Desimone, R. & Ungerleider, L.G. Cortical connections of inferior temporal area TEO in macaque monkeys. J. Comp. Neurol. 334, 125–150 (1993).

    Article  CAS  Google Scholar 

  27. Rempel-Clower, N.L. & Barbas, H. The laminar pattern of connections between prefrontal and anterior temporal cortices in the Rhesus monkey is related to cortical structure and function. Cereb. Cortex 10, 851–865 (2000).

    Article  CAS  Google Scholar 

  28. Dehay, C., Bullier, J. & Kennedy, H. Transient projections from the fronto-parietal and temporal cortex to areas 17, 18 and 19 in the kitten. Exp. Brain Res. 57, 208–212 (1984).

    Article  CAS  Google Scholar 

  29. Buckner, R.L., Kelley, W.M. & Petersen, S.E. Frontal cortex contributes to human memory formation. Nat. Neurosci. 2, 311–314 (1999).

    Article  CAS  Google Scholar 

  30. Buchel, C. Cortical hierarchy turned on its head. Nat. Neurosci. 6, 657–658 (2003).

    Article  Google Scholar 

  31. Pascual-Leone, A. & Hamilton, R. The metamodal organization of the brain. Progr. Brain Res. 134, 427–445 (2001).

    Article  CAS  Google Scholar 

  32. Boroojerdi, B. et al. Enhanced excitability of the human visual cortex induced by short-term light deprivation. Cereb. Cortex 10, 529–534 (2000).

    Article  CAS  Google Scholar 

  33. Oldfield, R.C. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9, 97–113 (1971).

    Article  CAS  Google Scholar 

  34. Kucera, W.N. & Francis, H. Computational Analysis of Present-Day American English (Brown University Press, Providence, 1967).

    Google Scholar 

  35. Rossini, P.M. et al. Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an I.F.C.N. committee. Electroencephalogr. Clin. Neurophysiol. 91, 79–92 (1994).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank C. Wu for help with MRI acquisition; C. Poletto for help and advice on the recording and auditory equipment; D. Glasser, A. Dorsch and M. Skupinsky for research assistance; and our dedicated blind and sighted subjects. A.F. is supported by a grant (Fl 379/1-1) from the Deutsche Forschungsgemeinschaft, Bonn. E.Z. was supported by McDonnell—Pew Foundation grant JSMF#220020046 and A.A. by a Horowitz fellowship.

Author information

Author notes

  1. Amir Amedi

    Present address: Laboratory for Magnetic Brain Stimulation, Department of Neurology, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Massachusetts, 02215, USA

  2. Amir Amedi and Agnes Floel: These authors contributed equally to this work.

Authors and Affiliations

  1. Neurobiology Department, Life Science Institute and Interdisciplinary Center for Neural Computation, Hebrew University, Jerusalem, 91904, Israel

    Amir Amedi & Ehud Zohary

  2. Human Cortical Physiology Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, 20892-1428, Maryland, USA

    Agnes Floel & Leonardo G Cohen

  3. University of Muenster, Albert-Schweitzer-Str. 33, Muenster, 48148, Germany

    Agnes Floel & Stefan Knecht

Authors
  1. Amir Amedi
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  3. Stefan Knecht
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  4. Ehud Zohary
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  5. Leonardo G Cohen
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Corresponding authors

Correspondence to Ehud Zohary or Leonardo G Cohen.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Fig. 1

Scatter plot of the change in error rate (delta ER) versus the change in reaction time (from rTMS onset, delta RT) for each subject and cortical stimulation site in blind and sighted subjects. The absence of points scattered in the second and fourth quadrants of the graph indicate that a speed–accuracy trade-off, which would depend on the occurrence of more errors (delta ER>0) with shorter reaction times (delta RT<0) and vice versa, cannot account for the increase in error rates for either the blind or the sighted subjects. (PDF 186 kb)

Supplementary Table 1

Verb-generation performance: normalized accuracy score ([condition–sham]/sham) for percentage of correct responses. (PDF 19 kb)

Supplementary Table 2

Verb-generation performance. (PDF 19 kb)

Supplementary Results (PDF 25 kb)

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Amedi, A., Floel, A., Knecht, S. et al. Transcranial magnetic stimulation of the occipital pole interferes with verbal processing in blind subjects. Nat Neurosci 7, 1266–1270 (2004). https://doi.org/10.1038/nn1328

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