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Complementary localization and lateralization of orienting and motor attention

Nature Neuroscience volume 4, pages 656–661 (2001)Cite this article

An Erratum to this article was published on 01 September 2001

Abstract

It is widely agreed that the right posterior parietal cortex has a preeminent role in visuospatial and orienting attention. A number of lines of evidence suggest that although orienting and the preparation of oculomotor responses are dissociable from each other, the two are intimately related. If this is true, then it should be possible to identify other attentional mechanisms tied to other response modalities. We used repetitive transcranial magnetic stimulation (rTMS) to demonstrate the existence of a distinct anterior parietal mechanism of motor attention. The critical area for motor attention is anterior to the one concerned with orienting, and it is lateralized to the left hemisphere in humans.

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Figure 1: Experimental design.
Figure 2: TMS sites.
Figure 3: Experimental results.

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References

  1. Colby, C. L. & Goldberg, M. E. Space and attention in parietal cortex. Annu. Rev. Neurosci. 22, 319–349 (1999).

    Article  CAS  Google Scholar 

  2. Corbetta, M., Miezin, F. M., Shulman, G. L. & Petersen, S. E. A PET study of visuospatial attention. J. Neurosci. 13, 1202–1226 (1993).

    Article  CAS  Google Scholar 

  3. Nobre, A. C. et al. Functional localization of the system for visuospatial attention using positron emission tomography. Brain 120, 515–533 (1997).

    Article  Google Scholar 

  4. Gitelman, D. R. et al. A large-scale distributed network for covert spatial attention: further anatomical delineation based on stringent behavioural and cognitive controls. Brain 122, 1093–1106 (1999).

    Article  Google Scholar 

  5. Posner, M. I., Walker, J. A., Friedrich, F. J. & Rafal, R. D. Effects of parietal injury on covert orienting of attention. J. Neurosci. 4, 1863–1874 (1984).

    Article  CAS  Google Scholar 

  6. Posner, M. I., Inhoff, A. W., Friedrich, F. J. & Cohen, A. Isolating attentional systems: a cognitive-anatomical analysis. Psychobiology 1, 107–121 (1987).

    Google Scholar 

  7. Sheliga, B. M., Riggio, L. & Rizzolatti, G. Spatial attention and eye movements. Exp. Brain Res. 105, 261–275 (1995).

    Article  CAS  Google Scholar 

  8. Snyder, L. H., Batista, A. P. & Andersen, R. A. Coding of intention in the posterior parietal cortex. Nature 386, 167–170 (1997).

    Article  CAS  Google Scholar 

  9. Corbetta, M. et al. A common network of functional areas for attention and eye movements. Neuron 21, 761–773 (1998).

    Article  CAS  Google Scholar 

  10. Gottlieb, J. P., Kusonoki, M. & Goldberg, M. E. The representation of visual salience in monkey parietal cortex. Nature 391, 481–484 (1998).

    Article  CAS  Google Scholar 

  11. Gottlieb, J. & Goldberg, M. E. Activity of neurons in the lateral intraparietal area of the monkey during an antisaccade task. Nat. Neurosci. 2, 906–912 (1999).

    Article  CAS  Google Scholar 

  12. Cavada, C. & Goldman-Rakic, P. S. Posterior parietal cortex in rhesus monkey: I. Parcellation of areas based on distinctive limbic and sensory corticocortical connections. J. Comp. Neurol. 287, 393–421 (1989).

    Article  CAS  Google Scholar 

  13. Cavada, C. & Goldman-Rakic, P. S. Posterior parietal cortex in rhesus monkey: II. Evidence for segregated corticocortical networks linking sensory and limbic areas with the frontal lobe. J. Comp. Neurol. 287, 422–445 (1989).

    Article  CAS  Google Scholar 

  14. Paus, T. et al. Transcranial magnetic stimulation during positron emission tomography: a new method for studying connectivity of the human cerebral cortex. J. Neurosci. 17, 3178–3184 (1997).

    Article  CAS  Google Scholar 

  15. Eidelburg, D. & Galaburda, A. M. Inferior parietal lobule: divergent architectonic asymmetries in the human brain. Arch. Neurol. 41, 843–852 (1984).

    Article  Google Scholar 

  16. Von Bonin, G. & Bailey, P. The Neocortex of Macacca Mulatta (Univ. of Illinois Press, Urbana, Illinois, 1947).

    Google Scholar 

  17. Passingham, R. E. in Comparative Neuropsychology (ed. Milner, A. D.) 271–298 (Oxford Univ. Press, Oxford, 1998).

    Book  Google Scholar 

  18. Rushworth, M. F. S., Nixon, P. D. & Passingham, R. E. Parietal cortex and movement. II. Spatial representations. Exp. Brain Res. 117, 311–323 (1997).

    Article  CAS  Google Scholar 

  19. Rushworth, M. F. S., Johansen-Berg, H. & Young, S. A. Parietal cortex and spatial-postural transformation during arm movements. J. Neurophysiol. 79, 478–482 (1998).

    Article  CAS  Google Scholar 

  20. Colby C. L., Duhamel, J. R. & Goldberg, M. E. Oculocentric spatial representation in parietal cortex. Cereb. Cortex 5, 470–481 (1995).

    Article  CAS  Google Scholar 

  21. Duhamel, J. R., Bremmer, F., BenHamed, S. & Graf, W. Spatial invariance of visual receptive fields in parietal cortex neurons. Nature 389, 845–848 (1997).

    Article  CAS  Google Scholar 

  22. Cracco, R. Q., Cracco, J. B., Maccabee, P. J. & Amassian, V. E. Cerebral function revealed by transcranial magnetic stimulation. J. Neurosci. Methods 86, 209–219 (1999).

    Article  CAS  Google Scholar 

  23. Edgley, S. A., Eyre, J. A., Lemon, R. N. & Miller, S. Comparison of activation of corticospinal neurons and spinal motor neurons by magnetic and electrical stimulation in the lumbosacral cord of the anaesthetized monkey. Brain 120, 839–853 (1997).

    Article  Google Scholar 

  24. Paus, T. et al. Dose-dependent reduction of cerebral blood flow during rapid-rate transcranial magnetic stimulation of the human sensorimotor cortex. J. Neurophysiol. 79, 1102–1107 (1998).

    Article  CAS  Google Scholar 

  25. Walsh, V. & Cowey, A. Magnetic stimulation studies of visual cognition. Trends Cogn. Sci. 2, 103–110 (1998).

    Article  CAS  Google Scholar 

  26. Walsh, V. & Rushworth, M. F. S. The use of transcranial magnetic stimulation in neuropsychological testing. Neuropsychologia 37, 125–135 (1999).

    CAS  PubMed  Google Scholar 

  27. Pascual-Leone, A. et al. Induction of visual extinction by rapid-rate transcranial magnetic stimulation of parietal lobe. Neurology 44, 494–498 (1994).

    Article  CAS  Google Scholar 

  28. Ashbridge, E., Walsh, V. & Cowey, A. Temporal aspects of visual search studied by transcranial magnetic stimulation. Neuropsychologia 35, 1121–1131 (1997).

    Article  CAS  Google Scholar 

  29. Marzi, C. A. et al. Transcranial magnetic stimulation selectively impairs interhemispheric transfer of visuo-motor information in humans. Exp. Brain Res. 118, 435–438 (1998).

    Article  CAS  Google Scholar 

  30. Walsh, V., Ellison, A., Battelli, L. & Cowey, A. Task-specific impairments and enhancements induced by magnetic stimulation of human visual area V5. Proc. R. Soc. Lond. B Biol. Sci. 265, 537–543 (1998).

    Article  CAS  Google Scholar 

  31. Oliveri, M. et al. Left frontal transcranial magnetic stimulation reduces contralesional extinction in patients with unilateral right brain damage. Brain 122, 1731–1739 (1999).

    Article  Google Scholar 

  32. Talairach, J. & Tournoux, P. Co-Planar Stereotaxic Atlas of the Human Brain (Thieme, Stuttgart, 1988).

    Google Scholar 

  33. Evans, A. C., Collins, D. L. & Holmes, C. J. in Brain Mapping: The Methods (eds. Toga, A. W. & Mazziotta, J. C.) 343–361 (Academic, San Diego, 1996).

    Google Scholar 

  34. Desmurget, M. et al. Role of the posterior parietal cortex in updating reaching movements to a visual target. Nat. Neurosci. 2, 563–567 (1999).

    Article  CAS  Google Scholar 

  35. Pisella, L. et al. An 'automatic pilot' for the hand in human posterior parietal cortex: toward reinterpreting optic ataxia. Nat. Neurosci. 3, 729–736 (2000).

    Article  CAS  Google Scholar 

  36. Corbetta, M., Kincade, J. M., Ollinger, J. M., McAvoy, M. P. & Shulman, G. L. Voluntary orienting is dissociated from target detection in human posterior parietal cortex. Nat. Neurosci. 3, 292–297 (2000).

    Article  CAS  Google Scholar 

  37. Rushworth, M. F. S., Krams, M. & Passingham, R. E. The attentional role of the left parietal cortex: the distinct lateralization and localization of motor attention in the human brain. J. Cogn. Neurosci. (in press).

  38. Deiber, M.-P., Ibanez, V., Sadato, N. & Hallet, M. Cerebral structures participating in motor preparation in humans: a positron emission tomography study. J. Neurophysiol. 75, 233–247 (1996).

    Article  CAS  Google Scholar 

  39. Steinmetz, M. A. & Constantinidis, C. Neurophysiological evidence for a role of posterior parietal cortex in redirecting visual attention. Cereb. Cortex 5, 448–456 (1995).

    Article  CAS  Google Scholar 

  40. Robinson, C. J. & Burton, H. Organization of somatosensory receptive fields in cortical areas 7b, retroinsula, postauditory and granular insula of M. fascicularis. J. Comp. Neurol. 192, 69–92 (1980).

    Article  CAS  Google Scholar 

  41. Sakata, H. et al. Neural representation of three-dimensional features of manipulation objects with stereopsis. Exp. Brain Res. 128, 160–169 (1999).

    Article  CAS  Google Scholar 

  42. Ferraina, S. et al. Combination of hand and gaze signals during reaching: activity in parietal area 7m of the monkey. J. Neurophysiol. 77, 1034–1038 (1997).

    Article  CAS  Google Scholar 

  43. Walsh, V., Ellison, A., Ashbridge, E. & Cowey, A. The role of the parietal cortex in visual attention–hemispheric asymmetries and the effects of learning: a magnetic stimulation study. Neuropsychologia 37, 245–251 (1999).

    Article  CAS  Google Scholar 

  44. Wittelson, S. F. & Kigar, D. L. Sylvian fissure morphology and asymmetry in men and women: bilateral differences in relation to handedness in men. J. Comp. Neurol. 323, 326–340 (1992).

    Article  Google Scholar 

  45. Rushworth, M. F. S., Nixon, P. D., Renowden S., Wade, D. T. & Passingham, R. E. The left parietal cortex and attention to action. Neuropsychologia 35, 1261–1273 (1997).

    Article  CAS  Google Scholar 

  46. Duhamel, J. R., Colby, C. L. & Goldberg, M. E. The updating of the representation of visual space in parietal cortex by intended eye movements. Science 255, 90–92 (1992).

    Article  CAS  Google Scholar 

  47. Duhamel, J. R., Goldberg, M. E., Fitzgibbon, E. J., Sirigu, A. & Grafman, J. Saccadic dysmetria in a patient with a right frontoparietal lesion. The importance of corollary discharge for accurate spatial behaviour. Brain 115, 1387–1402 (1992).

    Article  Google Scholar 

  48. Wassermann E. M. Risk and safety of repetitive transcranial magnetic stimulation: report and suggested guidelines from the international workshop on the safety of repetitive transcranial magnetic stimulation, June 5–7, 1996. Electroenceph. Clin. Neurophysiol. 198, 1–16 (1998).

    Article  Google Scholar 

  49. Schluter, N., Rushworth, M. F. S., Nixon, P. D., Mills, K. & Passingham, R. E. Temporary inteference in human lateral premotor cortex suggests dominance for the selection of movements: a study using transcranial magnetic stimulation. Brain 121, 785–799 (1998).

    Article  Google Scholar 

  50. Ruohonen, J. R. & Ilmoniemi, J. Modelling of the stimulating field generation in TMS. Electroenceph. Clin. Neurophysiol. Suppl. 51, 30–40 (1999).

    CAS  Google Scholar 

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Acknowledgements

Supported by the Royal Society, the Dr. Hadwen Trust, and the Medical Research Council.

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Authors and Affiliations

  1. Department of Experimental Psychology, University of Oxford, South Parks Road, Oxford, OX1 3UD, UK

    Matthew F. S. Rushworth, Amanda Ellison & Vincent Walsh

  2. Department of Clinical Neurology, Oxford Centre for Functional Magnetic Resonance Imaging of the Brain, University of Oxford, John Radcliffe Hospital, Headley Way, OX3 9DU, Oxford, UK

    Matthew F. S. Rushworth

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Correspondence to Matthew F. S. Rushworth.

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Rushworth, M., Ellison, A. & Walsh, V. Complementary localization and lateralization of orienting and motor attention. Nat Neurosci 4, 656–661 (2001). https://doi.org/10.1038/88492

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