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.

  • Article
  • Published:

Graspable objects grab attention when the potential for action is recognized

Nature Neuroscience volume 6, pages 421–427 (2003)Cite this article

Abstract

Visually guided grasping movements require a rapid transformation of visual representations into object-specific motor programs. Here we report that graspable objects may facilitate these visuomotor transformations by automatically grabbing visual spatial attention. Human subjects viewed two task-irrelevant objects—one was a 'tool', the other a 'non-tool'—while waiting for a target to be presented in one of the two object locations. Using event-related potentials (ERPs), we found that spatial attention was systematically drawn to tools in the right and lower visual fields, the hemifields that are dominant for visuomotor processing. Using event-related fMRI, we confirmed that tools grabbed spatial attention only when they also activated dorsal regions of premotor and prefrontal cortices, regions associated with visually guided actions and their planning. Although it is widely accepted that visual sensory gain aids perception, our results suggest that it may also have consequences for object-directed actions.

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

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

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

Figure 1: Display and trial types.
Figure 2: The lateral occipital P1 by condition from experiment 1, averaged across participants.
Figure 3: The lateral occipital P1 by condition from experiment 2, averaged across participants.
Figure 4: fMRI BOLD response as a function of trial type, averaged across participants.
Figure 5: fMRI BOLD response as a function of contrast, averaged across participants.

Similar content being viewed by others

References

  1. Craighero, L., Fadiga, L., Umilta, C.A. & Rizzolatti, G. Evidence for visuomotor priming effect. Neuroreport 8, 347–349 (1996).

    Article  CAS  Google Scholar 

  2. Jeannerod, M., Arbib, M.A., Rizzolatti, G. & Sakata, H. Grasping objects: the cortical mechanisms of visuomotor transformation. Trends Neurosci. 18, 314–320 (1995).

    Article  CAS  Google Scholar 

  3. Tucker, M. & Ellis, R. On the relations between seen objects and components of potential actions. J. Exp. Psychol. Hum. Percept. Perform. 24, 830–846 (1998).

    Article  CAS  Google Scholar 

  4. Chao, L.L. & Martin, A. Representation of manipulable man-made objects in the dorsal stream. Neuroimage 12, 478–484 (2000).

    Article  CAS  Google Scholar 

  5. Grafton, S.T., Fadiga, L., Arbib, M.A. & Rizzolatti, G. Premotor cortex activation during observation and naming of familiar tools. Neuroimage 6, 231–236 (1997).

    Article  CAS  Google Scholar 

  6. Martin, A., Haxby, J.V., Lalonde, F.M., Wiggs, C.L. & Ungerleider, L.G. Discrete cortical regions associated with knowledge of color and knowledge of action. Science 270, 102–105 (1995).

    Article  CAS  Google Scholar 

  7. Martin, A., Wiggs, C.L., Ungerleider, L.G., & Haxby, J.V. Neural correlates of category-specific knowledge. Nature 379, 649–652 (1996).

    Article  CAS  Google Scholar 

  8. Bonfiglioli, C., Duncan, J., Rorden, C. & Kennett, S. Action and perception: evidence against converging selection processes. Vis. Cognit. 9, 458–476 (2002).

    Article  Google Scholar 

  9. Craighero, L., Fadiga, L., Rizzolatti, G. & Umiltà, C. Action for perception: a motor-visual attentional effect. J. Exp. Psychol. Hum. Percept. Perform. 25, 1673–1692 (1999).

    Article  CAS  Google Scholar 

  10. Desimone, R. & Duncan, J. Neural mechanisms of selective visual attention. Annu. Rev. Neurosci. 18, 193–222 (1995).

    Article  CAS  Google Scholar 

  11. Duncan, J., Humphreys, G. & Ward, R. Competitive brain activity in visual attention. Curr. Opin. Neurobiol. 7, 255–261 (1997).

    Article  CAS  Google Scholar 

  12. Snodgrass, J.G. & Vanderwart, M. A standardized set of 260 pictures: norms for name agreement, image agreement, familiarity and visual complexity. J. Exp. Psychol. Hum. Learn. Mem. 6, 174–215 (1980).

    Article  CAS  Google Scholar 

  13. Ward, R. Interaction between perception and action systems: a model for selective action. in Attention, Space and Action: Studies in Cognitive Neuroscience (eds. Humphreys, G.W., Duncan, J. and Treisman, A.) 311–332 (Oxford Univ. Press, New York, 1999).

    Google Scholar 

  14. Van Voorhis, S. & Hillyard, S.A. Visual evoked potentials and selective attention to points in space. Percept. Psychophys. 23, 146–160 (1977).

    Google Scholar 

  15. Hillyard, S.A., Vogel, E.K. & Luck, S.J. Sensory gain control (amplification) as a mechanism of selective attention: electrophysiological and neuroimaging evidence. in Attention, Space and Action: Studies in Cognitive Neuroscience (eds. Humphreys, G.W., Duncan, J. and Treisman, A.) 311–332 (Oxford Univ. Press, New York, 1999).

    Google Scholar 

  16. Handy, T.C. & Mangun, G.R. Attention and spatial selection: electrophysiological evidence for modulation by perceptual load. Percept. Psychophys. 62, 175–186 (2000).

    Article  CAS  Google Scholar 

  17. Mangun, G.R. & Hillyard, S.A. Spatial gradients of visual attention: behavioral and electrophysiological evidence. Electroencephal. Clin. Neurophysiol. 70, 417–428 (1988).

    Article  CAS  Google Scholar 

  18. Haaland, K.Y. & Harrington, D.L. Hemispheric asymmetry of movement. Curr. Opin. Neurobiol. 6, 796–800 (1996).

    Article  CAS  Google Scholar 

  19. 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. 13, 698–710 (2001).

    Article  CAS  Google Scholar 

  20. Boles, D.B. An experimental comparison of stimulus type, display type and input variable contributions to visual field asymmetry. Brain Cogn. 24, 184–197 (1994).

    Article  CAS  Google Scholar 

  21. Danckert, J. & Goodale, M.A. Superior performance for visually guided pointing in the lower visual field. Exp. Brain Res. 137, 303–308 (2001).

    Article  CAS  Google Scholar 

  22. Kenemans, J.L., Baas, J.M.P., Mangun, G.R., Lijffijt, M. & Verbaten, M.N. On the processing of spatial frequencies as revealed by evoked-potential source modeling. Clin. Neurophysiol. 111, 1113–1123 (2000).

    Article  CAS  Google Scholar 

  23. Zani, A. & Proverbio, A.M. Attention modulation of short latency ERPs by selective attention to conjunction of spatial frequency and location. J. Psychophysiol. 11, 21–32 (1997).

    Google Scholar 

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

    Article  CAS  Google Scholar 

  25. Marconi, B. et al. Eye-hand coordination during reaching. I. Anatomical relationships between parietal and frontal cortex. Cereb. Cortex 11, 513–527 (2001).

    Article  CAS  Google Scholar 

  26. Battaglia-Mayer, A. et al. Eye-hand coordination during reaching. II. An analysis of the relationships between visuomanual signals in parietal cortex and parieto-frontal association projections. Cereb. Cortex 11, 528–544 (2001).

    Article  CAS  Google Scholar 

  27. 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 

  28. Hopfinger, J.B., Buonocore, M.H. & Mangun, G.R. The neural mechanisms of top-down attentional control. Nat. Neurosci. 3, 284–291 (2000).

    Article  CAS  Google Scholar 

  29. Luck, S.J. et al. Effects of spatial cuing on luminance detectability: psychophysical and electrophysiological evidence for early selection. J. Exp. Psychol. Hum. Percept. Perform. 20, 887–904 (1994).

    Article  CAS  Google Scholar 

  30. Hopfinger, J.B. & Mangun, G.R. Reflexive attention modulates processing of visual stimuli in human extrastriate cortex. Psychol. Sci. 9, 441–446 (1998).

    Article  Google Scholar 

  31. Handy, T.C., Soltani, M. & Mangun, G.R. Perceptual load and visuocortical processing: ERP evidence of sensory-level selection. Psychol. Sci. 12, 213–218 (2001).

    Article  CAS  Google Scholar 

  32. Ivry, R.B. & Robertson, L.C. The Two Sides of Perception (MIT Press, Cambridge, Massachusetts, 1998).

    Google Scholar 

  33. Posner, M.I. Orienting of attention. Q. J. Exp. Psychol. 32, 3–25 (1980).

    Article  CAS  Google Scholar 

  34. Handy, T.C., Green, V., Klein, R. & Mangun, G.R. Combined expectancies: ERPs reveal the early benefits of spatial attention that are obscured by reaction time measures. J. Exp. Psychol. Hum. Percept. Perform. 27, 303–317 (2001).

    Article  CAS  Google Scholar 

  35. Rushworth, M.F.S., Ellison, A. & Walsh, V. Complementary localization and lateralization of orienting and motor attention. Nat. Neurosci. 4, 656–661 (2001).

    Article  CAS  Google Scholar 

  36. Hodges, J.R., Spatt, J. & Patterson, K. “What” and “how”: evidence for the dissociation of object knowledge and mechanical problem-solving skills in the human brain. Proc. Natl. Acad. Sci. USA 96, 9444–9448 (1999).

    Article  CAS  Google Scholar 

  37. Humphreys, G.W. & Riddoch, M.J. Knowing what you need but not what you want: affordances and action-defined templates in neglect. Behav. Neurol. 13, 75–87 (2001).

    Article  Google Scholar 

  38. Riddoch, M.J., Humphreys, G.W., Edwards, S., Baker, T. & Willson, K. Seeing the action: neuropsychological evidence for action-based effects on object selection. Nat. Neurosci. 6, 82–89 (2003).

    Article  CAS  Google Scholar 

  39. Humphreys, G.W. & Riddoch, M.J. Detection by action: neuropsychological evidence for action-defined templates in search. Nat. Neurosci. 4, 84–88 (2001).

    Article  CAS  Google Scholar 

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

    Google Scholar 

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

    Article  CAS  Google Scholar 

  42. Marotta, J.J. & Goodale, M.A. The role of familiar size in the control of grasping. J. Cogn. Neurosci. 13, 8–17 (2001).

    Article  CAS  Google Scholar 

  43. Murata, A., Gallese, V., Luppino, G., Kaseda, M. & Sakata, H. Selectivity for the shape, size and orientation of objects for grasping in neurons of monkey parietal area AIP. J. Neurophysiol. 83, 2580–2601 (2000).

    Article  CAS  Google Scholar 

  44. Batista, A.P. & Andersen, R.A. The parietal reach region codes the next planned movement in a sequential reach task. J. Neurophysiol. 85, 539–544 (2001).

    Article  CAS  Google Scholar 

  45. Carey, D.P. Eye-hand coordination: eye to hand or hand to eye? Curr. Biol. 10, 416–419 (2000).

    Article  Google Scholar 

  46. Graziano, M.S.A. Where is my arm? The relative role of vision and proprioception in the neuronal representation of limb position. Proc. Natl. Acad. Sci. USA 96, 10418–10421 (1999).

    Article  CAS  Google Scholar 

  47. Friston, K.J. et al. Spatial registration and normalization of images. Hum. Brain Mapp. 2 165–189 (1995).

    Article  Google Scholar 

  48. Friston, K.J., Holmes, A.P., Worsley, K.J., Poline, J.-P., Frith, C.D. & Frackowiak, R.S.J. statistical parametric maps in functional imaging: a general linear approach. Human Brain Mapp. 2, 189–210 (1995b).

    Article  Google Scholar 

  49. Friston, K.J., Williams, S., Howard, R., Frackowiak, R.S. & Turner, R. Movement-related effects in fMRI time-series. Magn. Reson. Med. 35, 346–355 (1996).

    Article  CAS  Google Scholar 

  50. Talairach, J. & Tournoux, P. Co-planar Stereotaxic Atlas of the Human Brain (Thieme, New York, 1988).

    Google Scholar 

Download references

Acknowledgements

This study was supported by funding from the National Institute of Health and Dartmouth College. We thank D. Turk, W. Kelley, E. R. Matheney and S. Mann for technical assistance.

Author information

Authors and Affiliations

  1. Center for Cognitive Neuroscience, 6162 Moore Hall, Dartmouth College, Hanover, 03755, New Hampshire, USA

    Todd C. Handy, Scott T. Grafton, Neha M. Shroff, Sarah Ketay & Michael S. Gazzaniga

  2. Department of Psychological and Brain Sciences, 6162 Moore Hall, Dartmouth College, Hanover, 03755, New Hampshire, USA

    Todd C. Handy, Scott T. Grafton, Neha M. Shroff, Sarah Ketay & Michael S. Gazzaniga

  3. Dartmouth Brain Imaging Center, 6162 Moore Hall, Dartmouth College, Hanover, 03755, New Hampshire, USA

    Scott T. Grafton

Authors
  1. Todd C. Handy
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Scott T. Grafton
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Neha M. Shroff
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sarah Ketay
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Michael S. Gazzaniga
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Todd C. Handy.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Handy, T., Grafton, S., Shroff, N. et al. Graspable objects grab attention when the potential for action is recognized. Nat Neurosci 6, 421–427 (2003). https://doi.org/10.1038/nn1031

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn1031

This article is cited by

Search

Advanced 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