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Spatial invariance of visual receptive fields in parietal cortex neurons

Nature volume 389, pages 845–848 (1997)Cite this article

Abstract

Spatial information is conveyed to the primary visual cortex in retinal coordinates. Movement trajectory programming, however, requires a transformation from this sensory frame of reference into a frame appropriate for the selected part of the body, such as the eye, head or arms1,2,3,4. To achieve this transformation, visual information must be combined with information from other sources: for instance, the location of an object of interest can be defined with respect to the observer's head if the position of the eyes in the orbit is known and is added to the object's retinal coordinates. Here we show that in a subdivision of the monkey parietal lobe, the ventral intraparietal area (VIP), the activity of visual neurons is modulated by eye-position signals, as in many other areas of the cortical visual system5,6,7,8,9,10. We find that individual receptive fields of a population of VIP neurons are organized along a continuum, from eye to head coordinates. In the latter case, neurons encode the azimuth and/or elevation of a visual stimulus, independently of the direction in which the eyes are looking, thus representing spatial locations explicitly in at least a head-centred frame of reference.

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Figure 1: a, Hypothetical retinotopic (left) and spatially invariant (right) receptive fields (RFs).
Figure 2: a, Hypothetical retinotopic (left) and spatially invariant (right) receptive fields (RFs).
Figure 3: Single-neuron data for visual receptive field mappings in which the RF remains in the same spatial location irrespective of eye position.
Figure 4: Single neuron encoding elevation in head-centred coordinates.
Figure 5: Ratio of horizontal and vertical displacement of the RF to horizontal and vertical displacement of the eyes for all VIP neurons studied.

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References

  1. Bernstein, N. The Coordination and Regulation of Movements(Pergamon, Oxford, (1967)).

    Google Scholar 

  2. Georgopoulos, A. P., Schwartz, A. B. & Kettner, R. E. Neuronal population coding of movement direction. Science 233, 1416–1419 (1986).

    Article  ADS  CAS  Google Scholar 

  3. Soechting, J. F. & Flanders, M. Sensorimotor representations for pointing to targets in three-dimensional space. J. Neurophysiol. 62, 582–594 (1989).

    Article  CAS  Google Scholar 

  4. Masino, T. & Knudsen, E. I. Horizontal and vertical components of head movement are controlled by distinct neural circuits in the barn own. Science 345, 434–437 (1990).

    CAS  Google Scholar 

  5. Andersen, R. A., Bracewell, R. M., Barash, S., Gnadt, J. W. & Fogassi, L. Eye position effects on visual, memory, and saccade-related activity in areas LIP and 7a of macaque. J. Neurosci. 10, 1176–1196 (1990).

    Article  CAS  Google Scholar 

  6. Andersen, R. A. & Mountcastle, V. B. The influence of angle of gaze upon the excitability of light-sensitive neurons of posterior parietal cortex. J. Neurosci. 3, 532–548 (1983).

    Article  CAS  Google Scholar 

  7. Bremmer, F., Ilg, U. J., Thiele, A., Distler, C. & Hoffmann, K.-P. Eye position effects in monkey cortex. I: Visual and pursuit related activity in extrastriate areas MT and MST. J. Neurophysiol. 77, 944–956 (1997).

    Article  CAS  Google Scholar 

  8. Galletti, C., Battaglini, P. P. & Fattori, P. Eye position influence on the parieto-occipital area PO(V6) of the macaque monkey. Eur. J. Neurosci. 7, 2486–2501 (1995).

    Article  CAS  Google Scholar 

  9. Boussaoud, D., Barth, T. M. & Wise, S. P. Effect of gaze on apparent visual responses of monkey frontal cortex neurons. Exp. Br. Res. 91, 202–212 (1993).

    Google Scholar 

  10. Galletti, C. & Battaglini, P. P. Gaze-dependent visual neurons in area V3A of monkey prestriate cortex. J. Neurosci. 9, 1112–1125 (1989).

    Article  CAS  Google Scholar 

  11. Hyvrinen, J. Regional distribution of functions in parietal association area 7 of the monkey. Brain Res. 206, 287–303 (1981).

    Article  Google Scholar 

  12. Andersen, R. A., Asanuma, C., Essick, G. & Siegel, R. M. Corticocortical connections of anatomically and physiologically defined subdivisions within the inferior parietal lobule. J. Comp. Neurol. 296, 65–113 (1990).

    Article  CAS  Google Scholar 

  13. Colby, C. L. & Duhamel, J.-R. Heterogeneity of extrastriate visual areas and multiple parietal areas in the macaque monkey. Neuropsychologia 29, 487–515 (1991).

    Article  Google Scholar 

  14. Colby, C. L. & Duhamel, J.-R. Spatial representations for action in parietal cortex. Cog. Brain Res. 5, 105–115 (1996).

    Article  CAS  Google Scholar 

  15. Maunsell, J. H. R. & Van Essen, D. C. The connections of the middle temporal visual area (MT) and their relationship to a cortical hierarchy in the macaque monkey. J. Neurosci. 3, 2563–2586 (1983).

    Article  CAS  Google Scholar 

  16. Ungerleider, L. G. & Desimone, R. Cortical connection of area MT in the macaque. J. Comp. Neurol. 248, 190–222 (1986).

    Article  CAS  Google Scholar 

  17. Colby, C. L., Duhamel, J. R. & Goldberg, M. E. Ventral Intraparietal area of the macaque monkey: anatomic location and visual response properties. J. Neurophysiol. 69, 902–914 (1993).

    Article  CAS  Google Scholar 

  18. Duhamel, J.-R., Colby, C. L. & Goldberg, M. E. in Brain and Space(ed. Paillard, J.) 223–236 (Oxford Univ. Press, Oxford, (1991)).

    Google Scholar 

  19. Bremmer, F., Duhamel, J.-R., Ben Hamed, S. & Graf, W. in Contribution of the Parietal Lobe to Orientation in Three-Dimensional Space(eds Thier, P. & Karnath, O.) 619–631 (Springer, Berlin and Heidelberg, (1997)).

    Book  Google Scholar 

  20. Duhamel, J.-R., Colby, C. L. & Goldberg, M. E. Ventral intraparietal area of the macaque: congruent visual and somatic response properties. J. Neurophysiol.(in the press).

  21. Matelli, M., Luppino, G., Murata, A. & Sakata, H. Independent anatomical circuits for reaching and grasping linking the inferior parietal sulcus and inferior area 6 in macaque monkey. Soc. Neurosci. Abstr. 20, 404.4 (1994).

    Google Scholar 

  22. Lewis, J. W. & Van Essen, D. C. Connections of visual area VIP with somatosensory and motor areas of the macaque monkey. Soc. Neurosci. Abstr. 22, 160.4 (1996).

    Google Scholar 

  23. 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  ADS  CAS  Google Scholar 

  24. Gnadt, J. W. & Andersen, R. A. Memory related motor planning activity in posterior parietal cortex of macaque. Exp. Br. Res. 70, 216–220 (1988).

    CAS  Google Scholar 

  25. Galletti, C., Battaglini, P. P. & Fattori, P. Parietal neurons encoding spatial locations in craniotopic coordinates. Exp. Brain Res. 96, 221–229 (1993).

    Article  CAS  Google Scholar 

  26. Graziano, M. S. A., Yap, G. S. & Gross, C. G. Coding of visual space by premotor neurons. Science 266, 1054–1056 (1994).

    Article  ADS  CAS  Google Scholar 

  27. Zipser, D. & Andersen, R. A. Aback-propagation programmed network that simulates response properties of a subset of posterior parietal neurons. Nature 331, 679–684 (1988).

    Article  ADS  CAS  Google Scholar 

  28. Fogassi, L. et al. Coding of peripersonal space in inferior premotor cortex (area F4). J. Neurophysiol. 76, 141–157 (1996).

    Article  CAS  Google Scholar 

  29. Tann, J., Boussaoud, D., Boyer-Zeller, N., Moret, V. & Rouiller, E. M. Parietal inputs to dorsal vs. ventral premotor areas in the macaque monkey: a multiple anatomical tracing study. Soc. Neurosci. Abstr., 22, 430.6 (1996).

    Google Scholar 

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Acknowledgements

This research was supported by a HCM network grant from the European Community and by the Human Frontier Science Program.

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Authors and Affiliations

  1. Laboratoire de Physiologie de la Perception et de l'Action, CNRS-Collège de France, 11 Place Marcelin Bertelot, Paris, 75005, France

    Jean-René Duhamel, Frank Bremmer, Suliann Ben Hamed & Werner Graf

  2. Department of Zoology and Neurobiology, Ruhr-University Bochum, Bochum, D-44780, Germany

    Frank Bremmer

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  1. Jean-René Duhamel
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Correspondence to Jean-René Duhamel.

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Duhamel, JR., Bremmer, F., Ben Hamed, S. et al. Spatial invariance of visual receptive fields in parietal cortex neurons. Nature 389, 845–848 (1997). https://doi.org/10.1038/39865

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