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Spatial updating: how the brain keeps track of changing object locations during observer motion

Abstract

As you move through an environment, the positions of surrounding objects relative to your body constantly change. Updating these locations is a central feature of situational awareness and readiness to act. Here, we used functional magnetic resonance imaging and a virtual environment to test how the human brain uses optic flow to monitor changing object coordinates. Only activation profiles in the precuneus and the dorsal premotor cortex (PMd) were indicative of an updating process operating on a memorized egocentric map of space. A subsequent eye movement study argued against the alternative explanation that activation in PMd could be driven by oculomotor signals. Finally, introducing a verbal response mode revealed a dissociation between the two regions, with the PMd only showing updating-related responses when participants responded by pointing. We conclude that visual spatial updating relies on the construction of updated representations in the precuneus and the context-dependent planning of motor actions in PMd.

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Figure 1: Experimental procedure, variable pointing error and reaction times in Experiment I (mean ± s.e.m.).
Figure 2: Main effect of self motion during the delay phase (Experiment I).
Figure 3: Conjunction analysis: main effect of self motion and a linear activation increase during the delay phase (Experiment I).
Figure 4: Behavioral performance and saccadic eye movements in Experiment II (mean ± s.e.m.).
Figure 5: Slow-phase velocity eye movements during the delay phase of updating trials (Experiment II).
Figure 6: Linear activation increase and interaction with response mode during the delay phase (Experiment III).

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References

  1. Colby, C.L. Action-oriented spatial reference frames in cortex. Neuron 20, 15–24 (1998).

    Article  CAS  Google Scholar 

  2. Byrne, P., Becker, S. & Burgess, N. Remembering the past and imagining the future: a neural model of spatial memory and imagery. Psychol. Rev. 114, 340–375 (2007).

    Article  Google Scholar 

  3. Burgess, N., Maguire, E.A., Spiers, H.J. & O'Keefe, J. A temporoparietal and prefrontal network for retrieving the spatial context of lifelike events. Neuroimage 14, 439–453 (2001).

    Article  CAS  Google Scholar 

  4. Cavanna, A.E. & Trimble, M.R. The precuneus: a review of its functional anatomy and behavioural correlates. Brain 129, 564–583 (2006).

    Article  Google Scholar 

  5. Leichnetz, G.R. Connections of the medial posterior parietal cortex (area 7m) in the monkey. Anat. Rec. 263, 215–236 (2001).

    Article  CAS  Google Scholar 

  6. 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 

  7. Wise, S.P., Boussaoud, D., Johnson, P.B. & Caminiti, R. Premotor and parietal cortex: corticocortical connectivity and combinatorial computations. Annu. Rev. Neurosci. 20, 25–42 (1997).

    Article  CAS  Google Scholar 

  8. Matelli, M. & Luppino, G. Parietofrontal circuits for action and space perception in the macaque monkey. Neuroimage 14, S27–S32 (2001).

    Article  CAS  Google Scholar 

  9. Riecke, B.E., Cunningham, D.W. & Bulthoff, H.H. Spatial updating in virtual reality: the sufficiency of visual information. Psychol. Res. 71, 298–313 (2007).

    Article  Google Scholar 

  10. Bremmer, F., Duhamel, J.R., Ben Hamed, S. & Graf, W. Heading encoding in the macaque ventral intraparietal area (VIP). Eur. J. Neurosci. 16, 1554–1568 (2002).

    Article  Google Scholar 

  11. Peuskens, H., Sunaert, S., Dupont, P., Van Hecke, P. & Orban, G.A. Human brain regions involved in heading estimation. J. Neurosci. 21, 2451–2461 (2001).

    Article  CAS  Google Scholar 

  12. Kovacs, G., Raabe, M. & Greenlee, M.W. Neural correlates of visually induced self-motion illusion in depth. Cereb. Cortex 18, 1779–1787 (2008).

    Article  Google Scholar 

  13. Wolbers, T., Wiener, J.M., Mallot, H.A. & Büchel, C. Differential recruitment of the hippocampus, medial prefrontal cortex and the human motion complex during path integration in humans. J. Neurosci. 27, 9408–9416 (2007).

    Article  CAS  Google Scholar 

  14. Froehler, M.T. & Duffy, C.J. Cortical neurons encoding path and place: where you go is where you are. Science 295, 2462–2465 (2002).

    Article  CAS  Google Scholar 

  15. Farrell, M.J. & Robertson, I.H. The automatic updating of egocentric spatial relationships and its impairment due to right posterior cortical lesions. Neuropsychologia 38, 585–595 (2000).

    Article  CAS  Google Scholar 

  16. Philbeck, J.W., Behrmann, M., Black, S.E. & Ebert, P. Intact spatial updating during locomotion after right posterior parietal lesions. Neuropsychologia 38, 950–963 (2000).

    Article  CAS  Google Scholar 

  17. Philbeck, J.W., Behrmann, M. & Loomis, J.M. Updating of locations during whole-body rotations in patients with hemispatial neglect. Cogn. Affect. Behav. Neurosci. 1, 330–343 (2001).

    Article  CAS  Google Scholar 

  18. Merriam, E.P. & Colby, C.L. Active vision in parietal and extrastriate cortex. Neuroscientist 11, 484–493 (2005).

    Article  Google Scholar 

  19. Bartels, A. & Zeki, S. The architecture of the colour centre in the human visual brain: new results and a review. Eur. J. Neurosci. 12, 172–193 (2000).

    Article  CAS  Google Scholar 

  20. 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 

  21. Galati, G. et al. The neural basis of egocentric and allocentric coding of space in humans: a functional magnetic resonance study. Exp. Brain Res. 133, 156–164 (2000).

    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. Nichols, T., Brett, M., Andersson, J., Wager, T. & Poline, J.B. Valid conjunction inference with the minimum statistic. Neuroimage 25, 653–660 (2005).

    Article  Google Scholar 

  24. Büttner, U. & Kremmyda, O. Smooth pursuit eye movements and optokinetic nystagmus. Dev. Ophthalmol. 40, 76–89 (2007).

    Article  Google Scholar 

  25. Niemann, T., Lappe, M., Buscher, A. & Hoffmann, K.P. Ocular responses to radial optic flow and single accelerated targets in humans. Vision Res. 39, 1359–1371 (1999).

    Article  CAS  Google Scholar 

  26. Dieterich, M., Bense, S., Stephan, T., Yousry, T.A. & Brandt, T. fMRI signal increases and decreases in cortical areas during small-field optokinetic stimulation and central fixation. Exp. Brain Res. 148, 117–127 (2003).

    Article  Google Scholar 

  27. Koyama, M. et al. Functional magnetic resonance imaging of macaque monkeys performing visually guided saccade tasks: comparison of cortical eye fields with humans. Neuron 41, 795–807 (2004).

    Article  CAS  Google Scholar 

  28. Waller, D. & Hodgson, E. Transient and enduring spatial representations under disorientation and self-rotation. J. Exp. Psychol. Learn. Mem. Cogn. 32, 867–882 (2006).

    Article  Google Scholar 

  29. Wang, R.F. et al. Spatial updating relies on an egocentric representation of space: effects of the number of objects. Psychon. Bull. Rev. 13, 281–286 (2006).

    Article  CAS  Google Scholar 

  30. Krauzlis, R.J. The control of voluntary eye movements: new perspectives. Neuroscientist 11, 124–137 (2005).

    Article  Google Scholar 

  31. Paus, T. Location and function of the human frontal eye-field: a selective review. Neuropsychologia 34, 475–483 (1996).

    Article  CAS  Google Scholar 

  32. Pierrot-Deseilligny, C., Milea, D. & Muri, R.M. Eye movement control by the cerebral cortex. Curr. Opin. Neurol. 17, 17–25 (2004).

    Article  Google Scholar 

  33. Corbetta, M., Kincade, J.M. & Shulman, G.L. Neural systems for visual orienting and their relationships to spatial working memory. J. Cogn. Neurosci. 14, 508–523 (2002).

    Article  Google Scholar 

  34. Brown, M.R., Goltz, H.C., Vilis, T., Ford, K.A. & Everling, S. Inhibition and generation of saccades: rapid event-related fMRI of prosaccades, antisaccades and nogo trials. Neuroimage 33, 644–659 (2006).

    Article  Google Scholar 

  35. Curtis, C.E. Prefrontal and parietal contributions to spatial working memory. Neuroscience 139, 173–180 (2006).

    Article  CAS  Google Scholar 

  36. Schmidt, D. et al. Visuospatial working memory and changes of the point of view in 3D space. Neuroimage 36, 955–968 (2007).

    Article  CAS  Google Scholar 

  37. Angelaki, D.E. & Hess, B.J. Self-motion-induced eye movements: effects on visual acuity and navigation. Nat. Rev. Neurosci. 6, 966–976 (2005).

    Article  CAS  Google Scholar 

  38. Hagler, D.J., Jr, Riecke, L. & Sereno, M.I. Parietal and superior frontal visuospatial maps activated by pointing and saccades. Neuroimage 35, 1562–1577 (2007).

    Article  Google Scholar 

  39. Wiest, G. et al. Vestibular processing in human paramedian precuneus as shown by electrical cortical stimulation. Neurology 62, 473–475 (2004).

    Article  CAS  Google Scholar 

  40. Connolly, J.D., Andersen, R.A. & Goodale, M.A. FMRI evidence for a 'parietal reach region' in the human brain. Exp. Brain Res. 153, 140–145 (2003).

    Article  Google Scholar 

  41. Fernandez-Ruiz, J., Goltz, H.C., DeSouza, J.F., Vilis, T. & Crawford, J.D. Human parietal “reach region” primarily encodes intrinsic visual direction, not extrinsic movement direction, in a visual motor dissociation task. Cereb. Cortex 17, 2283–2292 (2007).

    Article  Google Scholar 

  42. Wallentin, M., Roepstorff, A., Glover, R. & Burgess, N. Parallel memory systems for talking about location and age in precuneus, caudate and Broca's region. Neuroimage 32, 1850–1864 (2006).

    Article  Google Scholar 

  43. Churchland, M.M., Yu, B.M., Ryu, S.I., Santhanam, G. & Shenoy, K.V. Neural variability in premotor cortex provides a signature of motor preparation. J. Neurosci. 26, 3697–3712 (2006).

    Article  CAS  Google Scholar 

  44. Cisek, P. & Kalaska, J.F. Neural correlates of reaching decisions in dorsal premotor cortex: specification of multiple direction choices and final selection of action. Neuron 45, 801–814 (2005).

    Article  CAS  Google Scholar 

  45. Hoshi, E. & Tanji, J. Distinctions between dorsal and ventral premotor areas: anatomical connectivity and functional properties. Curr. Opin. Neurobiol. 17, 234–242 (2007).

    Article  CAS  Google Scholar 

  46. Picard, N. & Strick, P.L. Imaging the premotor areas. Curr. Opin. Neurobiol. 11, 663–672 (2001).

    Article  CAS  Google Scholar 

  47. Simon, S.R. et al. Spatial attention and memory versus motor preparation: premotor cortex involvement as revealed by fMRI. J. Neurophysiol. 88, 2047–2057 (2002).

    Article  Google Scholar 

  48. Parvizi, J., Van Hoesen, G.W., Buckwalter, J. & Damasio, A. Neural connections of the posteromedial cortex in the macaque. Proc. Natl. Acad. Sci. USA 103, 1563–1568 (2006).

    Article  CAS  Google Scholar 

  49. Barborica, A. & Ferrera, V.P. Modification of saccades evoked by stimulation of frontal eye field during invisible target tracking. J. Neurosci. 24, 3260–3267 (2004).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank T. Sommer for helpful comments on an earlier draft of this manuscript and S. Glasauer for help with the eye-movement analysis. This work was supported by the European Commission (Marie Curie Outgoing International Fellowship 022072 awarded to T.W.), the Volkswagenstiftung and the German Ministry of Education and Research (BMBF).

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Contributions

T.W. designed the experiments, conducted data acquisition and analyses, and wrote the manuscript. M.H. and J.M.L. designed the experiments and wrote the manuscript. C.B. wrote the manuscript.

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Correspondence to Thomas Wolbers.

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Wolbers, T., Hegarty, M., Büchel, C. et al. Spatial updating: how the brain keeps track of changing object locations during observer motion. Nat Neurosci 11, 1223–1230 (2008). https://doi.org/10.1038/nn.2189

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