Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Neural basis and recovery of spatial attention deficits in spatial neglect

Abstract

The syndrome of spatial neglect is typically associated with focal injury to the temporoparietal or ventral frontal cortex. This syndrome shows spontaneous partial recovery, but the neural basis of both spatial neglect and its recovery is largely unknown. We show that spatial attention deficits in neglect (rightward bias and reorienting) after right frontal damage correlate with abnormal activation of structurally intact dorsal and ventral parietal regions that mediate related attentional operations in the normal brain. Furthermore, recovery of these attention deficits correlates with the restoration and rebalancing of activity within these regions. These results support a model of recovery based on the re-weighting of activity within a distributed neuronal architecture, and they show that behavioral deficits depend not only on structural changes at the locus of injury, but also on physiological changes in distant but functionally related brain areas.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Functional-anatomical model of attention.
Figure 2: Lesion anatomy.
Figure 3: Behavioral results.
Figure 4: Functional maps of the Posner task.
Figure 5: BOLD correlates of rightward bias in parietal cortex.
Figure 6: BOLD correlates of rightward bias in visual cortex.
Figure 7: BOLD correlates of attentional reorienting.

References

  1. Caramazza, A. Some aspects of language processing revealed through the analysis of acquired aphasia: the lexical system. Annu. Rev. Neurosci. 11, 395–421 (1988).

    Article  CAS  Google Scholar 

  2. Jackson, J.H. Evolution and dissolution of the nervous system. Br. Med. J. 1, 591, 660–703 (1884).

    Article  CAS  Google Scholar 

  3. von Monakow, C. Lokalisation der hirnfunktionen [Localization of brain functions]. J. Psychol. Neurol. 17, 185–200 (1911).

    Google Scholar 

  4. Pedersen, P.M., Jorgensen, H.S., Nakayama, H., Raaschou, H.O. & Olsen, T.S. Hemineglect in acute stroke—incidence and prognostic implications. The Copenhagen stroke study. Am. J. Phys. Med. Rehabil. 76, 122–127 (1997).

    Article  CAS  Google Scholar 

  5. Appelros, P., Karlsson, G.M., Seiger, A. & Nydevik, I. Neglect and anosognosia after first-ever stroke: incidence and relationship to disability. J. Rehabil. Med. 34, 215–220 (2002).

    Article  Google Scholar 

  6. Heilman, K.M., Bowers, D., Valenstein, E. & Watson, R.T. in Neurophysiological and Neuropsychological Aspects of Spatial Neglect (ed. Jeannerod, M.) 115–150 (North-Holland, Amsterdam, The Netherlands, 1987).

    Book  Google Scholar 

  7. Halligan, P.W. & Marshall, J.C. Toward a principled explanation of unilateral neglect. Special issue: the cognitive neuropsychology of attention. Cogn. Neuropsychol. 11, 167–206 (1994).

    Article  Google Scholar 

  8. Mesulam, M.M. Spatial attention and neglect: parietal, frontal and cingulate contributions to the mental representation and attentional targeting of salient extrapersonal events. Phil. Trans. R. Soc. Lond. B 354, 1325–1346 (1999).

    Article  CAS  Google Scholar 

  9. Robertson, I.H., Mattingley, J.B., Rorden, C. & Driver, J. Phasic alerting of neglect patients overcomes their spatial deficit in visual awareness. Nature 395, 169–172 (1998).

    Article  CAS  Google Scholar 

  10. Husain, M. & Rorden, C. Non-spatially lateralized mechanisms in hemispatial neglect. Nat. Rev. Neurosci. 4, 26–36 (2003).

    Article  CAS  Google Scholar 

  11. Peers, P.V. et al. Attentional functions of parietal and frontal cortex. Cereb. Cortex (2005).

  12. Vallar, G. & Perani, D. in Neurophysiological and Neuropsychological Aspects of Spatial Neglect (ed Jeannerod, M.) 235–258 (North-Holland, Amsterdam, The Netherlands, 1987).

    Book  Google Scholar 

  13. Mort, D.J. et al. The anatomy of visual neglect. Brain 126, 1986–1997 (2003).

    Article  Google Scholar 

  14. Karnath, H.O., Ferber, S. & Himmelbach, M. Spatial awareness is a function of the temporal not the posterior parietal lobe. Nature 411, 950–953 (2001).

    Article  CAS  Google Scholar 

  15. Karnath, H.O., Fruhmann Berger, M., Kuker, W. & Rorden, C. The anatomy of spatial neglect based on voxelwise statistical analysis: a study of 140 patients. Cereb. Cortex 14, 1164–1172 (2004).

    Article  Google Scholar 

  16. Friedrich, F.J., Egly, R., Rafal, R.D. & Beck, D. Spatial attention deficits in humans: a comparison of superior parietal and temporal-parietal junction lesions. Neuropsychology 12, 193–207 (1998).

    Article  CAS  Google Scholar 

  17. Hillis, A.E. et al. Anatomy of spatial attention: insights from perfusion imaging and hemispatial neglect in acute stroke. J. Neurosci. 25, 3161–3167 (2005).

    Article  CAS  Google Scholar 

  18. 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 

  19. Connolly, J.D., Goodale, M.A., Menon, R.S. & Munoz, D.P. Human fMRI evidence for the neural correlates of preparatory set. Nat. Neurosci. 5, 1345–1352 (2002).

    Article  CAS  Google Scholar 

  20. Astafiev, S.V. et al. Functional organization of human intraparietal and frontal cortex for attending, looking, and pointing. J. Neurosci. 23, 4689–4699 (2003).

    Article  CAS  Google Scholar 

  21. Kincade, J.M., Abrams, R.A., Astafiev, S.V., Shulman, G.L. & Corbetta, M. An event-related functional magnetic resonance imaging study of voluntary and stimulus-driven orienting of attention. J. Neurosci. 25, 4593–4604 (2005).

    Article  CAS  Google Scholar 

  22. Sereno, M.I., Pitzalis, S. & Martinez, A. Mapping of contralateral space in retinotopic coordinates by a parietal cortical area in humans. Science 294, 1350–1354 (2001).

    Article  CAS  Google Scholar 

  23. Silver, M.A., Ress, D. & Heeger, D.J. Topographic maps of visual spatial attention in human parietal cortex. J. Neurophysiol. 94, 1358–1371 (2005).

    Article  Google Scholar 

  24. Corbetta, M. & Shulman, G.L. Control of goal-directed and stimulus-driven attention in the brain. Nat. Rev. Neurosci. 3, 201–215 (2002).

    Article  CAS  Google Scholar 

  25. Downar, J., Crawley, A.P., Mikulis, D.J. & Davis, K.D. A multimodal cortical network for the detection of changes in the sensory environment. Nat. Neurosci. 3, 277–283 (2000).

    Article  CAS  Google Scholar 

  26. Macaluso, E., Frith, C.D. & Driver, J. Supramodal effects of covert spatial orienting triggered by visual or tactile events. J. Cogn. Neurosci. 14, 389–401 (2002).

    Article  Google Scholar 

  27. Deuel, R.K. & Collins, R.C. The functional anatomy of frontal lobe neglect in the monkey: behavioral and quantitative 2-deoxyglucose studies. Ann. Neurol. 15, 521–529 (1984).

    Article  CAS  Google Scholar 

  28. Vallar, G. et al. Recovery from aphasia and neglect after subcortical stroke: neuropsychological and cerebral perfusion study. J. Neurol. Neurosurg. Psychiatry 51, 1269–1276 (1988).

    Article  CAS  Google Scholar 

  29. Pizzamiglio, L. Recovery of neglect after right hemispheric damage: H215O positron emission tomographic activation study. Arch. Neurol. 55, 561–568 (1998).

    Article  CAS  Google Scholar 

  30. 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 

  31. Morrow, L.A. & Ratcliff, G. The disengagement of covert attention and the neglect syndrome. Psychobiology 16, 261–269 (1988).

    Google Scholar 

  32. Kinsbourne, M. in Hemi-inattention and Hemispheric Specialization (eds. Weinstein, E. A. & Friedland, R. L.) 41–52 (Raven Press, New York, 1977).

    Google Scholar 

  33. Kastner, S. & Ungerleider, L.G. Mechanisms of visual attention in the human cortex. Annu. Rev. Neurosci. 23, 315–341 (2000).

    Article  CAS  Google Scholar 

  34. Rossini, P.M. et al. Does cerebrovascular disease affect the coupling between neuronal activity and local haemodynamics? Brain 127, 99–110 (2004).

    Article  CAS  Google Scholar 

  35. Pineiro, R., Pendlebury, S., Johansen-Berg, H. & Matthews, P.M. Altered hemodynamic responses in patients after subcortical stroke measured by functional MRI. Stroke 33, 103–109 (2002).

    Article  CAS  Google Scholar 

  36. Binkofski, F. & Seitz, R.J. Modulation of the BOLD-response in early recovery from sensorimotor stroke. Neurology 63, 1223–1229 (2004).

    Article  Google Scholar 

  37. Luck, S.J., Hillyard, S.A., Mangun, G.R. & Gazzaniga, M.S. Independent hemispheric attentional systems mediate visual search in split-brain patients. Nature 342, 543–545 (1989).

    Article  CAS  Google Scholar 

  38. Hornak, J. Ocular exploration in the dark by patients with visual neglect. Neuropsychologia 30, 547–552 (1992).

    Article  CAS  Google Scholar 

  39. Lynch, J.C. & McLaren, J.W. Deficits of visual attention and saccadic eye movements after lesions of parietooccipital cortex in monkeys. J. Neurophysiol. 61, 74–90 (1989).

    Article  CAS  Google Scholar 

  40. Perenin, M.T. & Vighetto, A. Optic ataxia: a specific disruption in visuomotor mechanisms. I. Different aspects of the deficit in reaching for objects. Brain 111, 643–674 (1988).

    Article  Google Scholar 

  41. Pouget, A. & Driver, J. Relating unilateral neglect to the neural coding of space. Curr. Opin. Neurobiol. 10, 242–249 (2000).

    Article  CAS  Google Scholar 

  42. Murase, N., Duque, J., Mazzocchio, R. & Cohen, L.G. Influence of interhemispheric interactions on motor function in chronic stroke. Ann. Neurol. 55, 400–409 (2004).

    Article  Google Scholar 

  43. Heiss, W.D., Kessler, J., Thiel, A., Ghaemi, M. & Karbe, H. Differential capacity of left and right hemispheric areas for compensation of post-stroke aphasia. Ann. Neurol. 45, 430–438 (1999).

    Article  CAS  Google Scholar 

  44. Naeser, M.A. et al. Improved picture naming in chronic aphasia after TMS to part of right Broca's area: an open-protocol study. Brain Lang. 93, 95–105 (2005).

    Article  Google Scholar 

  45. Brighina, F. et al. 1 Hz repetitive transcranial magnetic stimulation of the unaffected hemisphere ameliorates contralesional visuospatial neglect in humans. Neurosci. Lett. 336, 131–133 (2003).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank G.L. Shulman for discussions and comments. Supported by the J. S. McDonnell Foundation, the J. S. McDonnell Center for Higher Brain Function and the National Institute of Neurological Disorders.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Maurizio Corbetta.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Fig. 1

Push-pull pattern in dorsal parietal cortex, not in frontal cortex. (PDF 135 kb)

Supplementary Fig. 2

Correlation between left SPL signal magnitude and rightward bias in chronic patients (r2=0.36, P = 0.051). (PDF 44 kb)

Supplementary Fig. 3

Reactivation of TPJ as function of anatomical damage. (PDF 145 kb)

Supplementary Table 1

Demographics and neuropsychological scores neglect group. (PDF 44 kb)

Supplementary Table 2

Regions showing greater activity at acute than chronic stage. (PDF 60 kb)

Supplementary Table 3

Regions differentially responding to invalidly vs. validly cued targets at acute and chronic stage. (PDF 51 kb)

Supplementary Methods (PDF 115 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Corbetta, M., Kincade, M., Lewis, C. et al. Neural basis and recovery of spatial attention deficits in spatial neglect. Nat Neurosci 8, 1603–1610 (2005). https://doi.org/10.1038/nn1574

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn1574

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing