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.

Maintaining internal representations: the role of the human superior parietal lobe

Abstract

In sensorimotor integration, sensory input and motor output signals are combined to provide an internal estimate of the state of both the world and one's own body. Although a single perceptual and motor snapshot can provide information about the current state, computational models show that the state can be optimally estimated by a recursive process in which an internal estimate is maintained and updated by the current sensory and motor signals. These models predict that an internal state estimate is maintained or stored in the brain. Here we report a patient with a lesion of the superior parietal lobe who shows both sensory and motor deficits consistent with an inability to maintain such an internal representation between updates. Our findings suggest that the superior parietal lobe is critical for sensorimotor integration, by maintaining an internal representation of the body's state.

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: A schematic of the sensorimotor integration process.
Figure 2: The lesion found in the patient P.
Figure 3: Mean time to fade (with standard error bars) against the mass of the object placed on PJ's right hand.
Figure 4: Grip force against time when trying to maintain a constant force level with and without visual feedback of performance.
Figure 5: Perceived drift of right arm.
Figure 6

References

  1. Bálint, R. Seelenlähmung des 'schauens', optische ataxie, raümliche störung der aufmerksam. Monatschr. Psychiat. Neurol. 25, 51–81 (1909).

    Article  Google Scholar 

  2. Holmes, G. Disorders of visual orientation. Br. J. Ophthalmol. 2, 449–468 (1918).

    Article  CAS  Google Scholar 

  3. McFie, J., Piercy, F. J. & Zangwill, O. L. Visual-spatial agnosia associated with lesions of the right cerebral hemisphere. Brain 73, 167–170 (1950).

    Article  CAS  Google Scholar 

  4. DeRenzi, E. Disorders of Space Exploration and Cognition (John Wiley, Chichester, 1982).

    Google Scholar 

  5. 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 

  6. Corbetta, M., Shulman, G. L., Miezin, F. M. & Petersen, S. E. Superior parietal cortex activation during spatial attention shifts and visual feature conjunction. Science 270, 802– 805 (1995).

    Article  CAS  Google Scholar 

  7. Grafton, S. T., Fagg, A. H., Woods, R. P. & Arbib, M. A. Functional-anatomy of pointing and grasping in humans. Cereb. Cortex 6, 226–237 (1996).

    Article  CAS  Google Scholar 

  8. Clower, D. M. et al. Role of posterior parietal cortex in the recalibration of visually guided reaching. Nature 383, 618 –621 (1996).

    Article  CAS  Google Scholar 

  9. Andersen, R. in Handbook of Physiology vol. V Part II (eds Plum, F. & Mountcastle, V. B.) 483–518 (American Physiological Society, Rockville, Maryland, 1987).

    Google Scholar 

  10. Milner, A. D. & Goodale, M. The Visual Brain in Action (Oxford Univ. Press, Oxford, 1995).

    Google Scholar 

  11. Jeannerod, M. The Cognitive Neuroscience of Action (Blackwell, Oxford, 1997).

    Google Scholar 

  12. Husain, M. in Vision and Visual Dysfunction vol. 13 (ed. Stein, J. F.) 12 –43 (Macmillan, Basingstoke, UK, 1991 ).

    Google Scholar 

  13. Mountcastle, V. B., Lynch, J. C., Georgopoulos, A. P., Sakata, H. & Acuna, C. Posterior parietal association cortex of the monkey: command function for operations within extrapersonal space . J. Neurophysiol. 38, 871– 907 (1975).

    Article  CAS  Google Scholar 

  14. Bushnell, M. C., Goldberg, M. E. & Robinson, D. L. Behavioural enhancement of visual responses in monkey cerebral cortex. I. modulation in posterior parietal cortex related to selective visual attention. J. Neurophysiol. 46, 755 –772 (1981).

    Article  CAS  Google Scholar 

  15. 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 

  16. Andersen, R. A., Snyder, L. H., Bradley, D. C. & Xing, J. Multimodal representation of space in the posterior parietal cortex and its use in planning movements. Annu. Rev. Neurosci. 20, 303–330 (1997).

    Article  CAS  Google Scholar 

  17. Rizzolatti, G., Fogassi, L. & Gallese, V. Parietal cortex: from sight to action. Curr. Opin. Neurobiol. 7, 562–567 (1997).

    Article  CAS  Google Scholar 

  18. Wolpert, D. M., Ghahramani, Z. & Jordan, M. I. Are arm trajectories planned in kinematic or dynamic coordinates? An adaptation study. Exp. Brain Res. 103 , 460–470 (1995).

    Article  CAS  Google Scholar 

  19. Wolpert, D. M. Computational approaches to motor control. Trends Cogn. Sci. 1, 209–216 (1997).

    Article  CAS  Google Scholar 

  20. Goodwin, G. C. & Sin, K. S. Adaptive Filtering Prediction and Control (Prentice-Hall, Englewood Cliffs, New Jersey, 1984).

    Google Scholar 

  21. Wolpert, D. M., Ghahramani, Z. & Jordan, M. I. An internal model for sensorimotor integration. Science 269, 1880–1882 (1995).

    Article  CAS  Google Scholar 

  22. Mesulam, M. M. Principles of Behavioural Neurology: Tests of Directed Attention and Memory (Davis FA, Philadelphia, 1985).

    Google Scholar 

  23. Jeannerod, M., Michel, F. & Prablanc, C. The control of hand movements in a case of hemianaesthesia following a parietal lesion. Brain 107, 899–920 (1984).

    Article  Google Scholar 

  24. Rothwell, J. C. et al. Manual motor performance in a deafferented man. Brain 105, 515–542 (1982).

    Article  Google Scholar 

  25. Wann, J. P. & Ibrahim, S. F. Does limb proprioception drift . Exp. Brain Res. 91, 162– 166 (1992).

    Article  CAS  Google Scholar 

  26. 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 

  27. Critchley, M. The Parietal Lobes (Edward Arnold, London, 1953 ).

    Google Scholar 

  28. Mennemeier, M. S. et al. Contributions of the parietal and frontal lobes to sustained attention and habituation. Neuropsychologia 32, 703–716 (1994).

    Article  CAS  Google Scholar 

  29. Holliday, I. E., Kennard, C. & Ruddock, K. H. Rapid fading of visual sensations in a subject with a parietal occipital tumor. Ophthalmic Physiol. Opt. 5, 149–156 (1985).

    CAS  PubMed  Google Scholar 

  30. Head, H. & Holmes, G. Sensory disturbances from cerebral lesions. Brain 34, 102– 213 (1912).

    Article  Google Scholar 

  31. Vallar, G. & Perani, D. The anatomy of unilateral neglect after right-hemisphere stroke lesions. A clinical/CT-scan correlation study in man. Neuropsychologia 24, 609– 622 (1986).

    Article  CAS  Google Scholar 

  32. Mattingley, J. B., Husain, M., Rorden, C., Kennard, C. & Driver, J. Motor role of human inferior parietal lobe revealed in unilateral neglect patients. Nature 392, 179–182 (1998).

    Article  CAS  Google Scholar 

  33. 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 

  34. Pardo, J. V., Fox, P. T. & Raichle, M. E. Localization of a human system for sustained attention by positron emission tomography. Nature 349, 61–64 (1991).

    Article  CAS  Google Scholar 

  35. Coull, J. T., Frith, C. D., Frackowiak, R. S. J. & Grasby, P. M. A frontoparietal network for rapid visual information-processing: a PET study of sustained attention and working-memory. Neuropsychologia 34, 1085–1095 (1996).

    Article  CAS  Google Scholar 

  36. 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 

  37. Milner, A. D. in Parietal Lobe Contributions to Orientation in 3D Space (eds Thier, P. & Karnath, H. O.) 3–22 (Springer-Verlag, Heidelberg, 1997).

    Book  Google Scholar 

Download references

Acknowledgements

We thank PJ for participating in the study and Jon Driver and Tobe Freeman for helpful discussions. This work was supported by a grant from the Wellcome Trust and the Royal Society.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Daniel M. Wolpert.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wolpert, D., Goodbody, S. & Husain, M. Maintaining internal representations: the role of the human superior parietal lobe. Nat Neurosci 1, 529–533 (1998). https://doi.org/10.1038/2245

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/2245

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