Advertisement

Grasping with the eyes: The role of elongation in visual recognition of manipulable objects

  • Jorge AlmeidaEmail author
  • Bradford Z. Mahon
  • Veronica Zapater-Raberov
  • Aleksandra Dziuba
  • Tiago Cabaço
  • J. Frederico Marques
  • Alfonso Caramazza
Article

Abstract

Processing within the dorsal visual stream subserves object-directed action, whereas visual object recognition is mediated by the ventral visual stream. Recent findings suggest that the computations performed by the dorsal stream can nevertheless influence object recognition. Little is known, however, about the type of dorsal stream information that is available to assist in object recognition. Here, we present a series of experiments that explored different psychophysical manipulations known to bias the processing of a stimulus toward the dorsal visual stream in order to isolate its contribution to object recognition. We show that elongated-shaped stimuli, regardless of their semantic category and familiarity, when processed by the dorsal stream, elicit visuomotor grasp-related information that affects how we categorize manipulable objects. Elongated stimuli may reduce ambiguity during grasp preparation by providing a coarse cue to hand shaping and orientation that is sufficient to support action planning. We propose that this dorsal-stream-based analysis of elongation along a principal axis is the basis for how the dorsal visual object processing stream can affect categorization of manipulable objects.

Keywords

Dorsal stream Tools Object recognition Object elongation 

Notes

Acknowledgments

We thank M. Clara Barata and Thomas McKeeff for their comments on earlier versions of the manuscript and Matthew Finkbeiner and Jason Friedman for their help with the analysis of reach trajectories. J.A. was supported by funding from the European Union Seventh Framework Programme (FP7/2007-2013) under grant agreement PCOFUND-GA-2009-246542 and from the Foundation for Science and Technology of Portugal. J.A., A.D., and J.F.M. were sponsored by a Foundation for Science and Technology of Portugal Project Grant PTDC/PSI-PCO/114822/2009. A.C. was supported by National Institute on Deafness and Other Communication Disorders Grant R01 DC006842 and by the Fondazione Cassa di Risparmio di Trento e Rovereto. B.Z.M. was supported in part by R21 NS076176 from NINDS. This research was supported by Foundation for Science and Technology of Portugal Project Grant PTDC/PSI-PCO/114822/2009.

Supplementary material

13415_2013_208_MOESM1_ESM.pdf (1.5 mb)
ESM 1 (PDF 1545 kb)

References

  1. Abernethy, M., & Coney, J. (1993). Associative priming in the cerebral hemispheres as a function of SOA. Neuropsychologia, 31, 1397–1409.PubMedCrossRefGoogle Scholar
  2. Almeida, J., Fintzi, A., & Mahon, B.Z. (2013). Tool Manipulation Knowledge is Retrieved by way of the Ventral Visual Object Processing Pathway. Cortex,  10.1016/j.cortex.2013.05.004 DOI: 10.1016/j.cortex.2013.05.004#doilink
  3. Almeida, J., Mahon, B. Z., & Caramazza, A. (2010). The role of the dorsal visual processing stream in tool identification. Psychological Science, 21(6), 772–778.PubMedCentralPubMedCrossRefGoogle Scholar
  4. Almeida, J., Mahon, B. Z., Nakayama, K., & Caramazza, A. (2008). Unconscious processing dissociates along categorical lines. Proceedings of the National Academy of Sciences of the United States of America, 105(39), 15214–15218.PubMedCentralPubMedCrossRefGoogle Scholar
  5. Almeida, J., Pajtas, P. E., Mahon, B. Z., Nakayama, K., & Caramazza, A. (2013). Affect of the unconscious: Visually suppressed angry faces modulate our decisions. Cognitive, Affective, and Behavioral Neuroscience, 13, 94–101.CrossRefGoogle Scholar
  6. Batista, A. P., Buneo, C. A., Snyder, L. H., & Andersen, R. A. (1999). Reach plans in eye-centered coordinates. Science, 285, 257–260.PubMedCrossRefGoogle Scholar
  7. Blake, A. (1992). Computational modelling of hand-eye coordination. Philosophical Transactions of the Royal Society: Biological Sciences, 337(1281), 351–360.CrossRefGoogle Scholar
  8. Boronat, C. B., Buxbaum, L. J., Coslett, H. B., Tang, K., Saffran, E. M., Kimberg, D. Y., et al. (2005). Distinctions between manipulation and function knowledge of objects: Evidence from functional magnetic resonance imaging. Cognitive Brain Research, 23(2–3), 361–373.Google Scholar
  9. Brainard, D. H. (1997). The Psychophysics Toolbox. Spatial Vision, 10, 433–436.PubMedCrossRefGoogle Scholar
  10. Breitmeyer, B. G., & Ogmen, H. (2000). Recent models and findings in visual backward masking: A comparison, review, and update. Perception & Psychophysics, 62(8), 1572–1595.CrossRefGoogle Scholar
  11. Bub, D. N., & Lewine, J. (1988). Different modes of word recognition in the left and right visual fields. Brain and Language, 33, 161–188.PubMedCrossRefGoogle Scholar
  12. Buxbaum, L. J., Kyle, K. M., Grossman, M., & Coslett, H. B. (2007). Left inferior parietal representations for skilled hand-object interactions: Evidence from stroke and corticobasal degeneration. Cortex, 43(3), 411–23.PubMedCrossRefGoogle Scholar
  13. Cant, J. S., & Goodale, M. A. (2007). Attention to form or surface properties modulates different regions of human occipitotemporal cortex. Cerebral Cortex, 17, 713–731.PubMedCrossRefGoogle Scholar
  14. Carey, D. P., Harvey, M., & Milner, A. D. (1996). Visuomotor sensitivity for shape and orientation in a patient with visual form agnosia. Neuropsychologia, 34(5), 329–337.PubMedCrossRefGoogle Scholar
  15. Chao, L., & Martin, A. (2000). Representation of manipulable man-made objects in the dorsal stream. NeuroImage, 12, 478–484.PubMedCrossRefGoogle Scholar
  16. Chiarello, C., Nuding, S., & Pollock, A. (1988). Lexical decision and naming asymmetries: Influence of response selection and response bias. Brain and Language, 34, 302–314.PubMedCrossRefGoogle Scholar
  17. Connolly, J. D., Andersen, R. A., & Goodale, M. A. (2003). FMRI evidence for a “parietal reach region” in the human brain. Experimental Brain Research, 153, 140–145.PubMedCrossRefGoogle Scholar
  18. Culham, J. C., Cavina-Pratesi, C., & Singhal, A. (2006). The role of parietal cortex in visuomotor control: what have we learned from neuroimaging? Neuropsychologia, 44(13), 2668–84.PubMedCrossRefGoogle Scholar
  19. Culham, J. C., Danckert, S., Souza, J. X. D., Gati, J., Menon, R., & Goodale, M. A. (2003). Visually guided grasping produces fMRI activation in dorsal but not ventral stream brain areas. Experimental Brain Research, 153(2), 180–189.PubMedCrossRefGoogle Scholar
  20. Damasio, H., Tranel, D., Grabowski, T., Adolphs, R., & Damasio, A. (2004). Neural systems behind word and concept retrieval. Cognition, 92, 179–229.PubMedCrossRefGoogle Scholar
  21. Dehaene, S., Naccache, L., Cohen, L., Le Bihan, D., Mangin, J.-F., Poline, J.-B., & Rivière, D. (2001). Cerebral mechanisms of word masking and unconscious repetition priming. Nature Neuroscience, 4(7), 752–758.Google Scholar
  22. Desmurget, M., Epstein, C. M., Turner, R. S., Prablanc, C., Alexander, G. E., & Grafton, S. T. (1999). Role of the posterior parietal cortex in updating reaching movements to a visual target. Nature Neuroscience, 2, 563–567.PubMedCrossRefGoogle Scholar
  23. Fang, F., & He, S. (2005). Cortical responses to invisible objects in the human dorsal and ventral pathways. Nature Neuroscience, 8(10), 1380–1385.PubMedCrossRefGoogle Scholar
  24. Finkbeiner, M., Almeida, J., & Caramazza, A. (2006). Letter identification processes in reading: Distractor interference reveals a left-lateralized domain-specific mechanism. Cognitive Neuropsychology, 23, 1083–1103.PubMedCrossRefGoogle Scholar
  25. Finkbeiner, M., & Friedman, J. (2011). The flexibility of nonconsciously deployed cognitive processes: Evidence from masked congruence priming. PLoS ONE, 6(2), e17095. doi: 10.1371/journal.pone.0017095 PubMedCentralPubMedCrossRefGoogle Scholar
  26. Forster, K. I., & Forster, J. C. (2003). DMDX: A Windows display program with millisecond accuracy. Behavior Research Methods, Instruments, & Computers, 35(1), 116–124.CrossRefGoogle Scholar
  27. Garcea, F. E., Almeida, J., & Mahon, B. Z. (2012). A right visual field advantage for visual processing of manipulable objects. Cognitive, Affective, and Behavioral Neuroscience, 12(4), 813–25.CrossRefGoogle Scholar
  28. Goldenberg, G., & Spatt, J. (2009). The neural basis of tool use. Brain, 132(6), 1645–1655.PubMedCrossRefGoogle Scholar
  29. Goodale, M. A., Jakobson, L. S., Milner, A. D., & Perrett, D. I. (1994a). The nature and limits of orientation and pattern processing supporting visuomotor control in a visual form agnosic. Journal of Cognitive Neuroscience, 6(1), 46–56.PubMedCrossRefGoogle Scholar
  30. Goodale, M. A., Meenan, J. P., Bülthoff, H. H., Nicolle, D. A., Murphy, K. J., & Racicot, C. I. (1994b). Separate visual pathways for the visual analysis of object shape in perception and prehension. Current Biology, 4, 604–610.PubMedCrossRefGoogle Scholar
  31. Goodale, M. A., & Milner, A. D. (1992). Separate visual pathways for perception and action. Trends in Neurosciences, 15(1), 20–25.PubMedCrossRefGoogle Scholar
  32. Goodale, M. A., Pelisson, D., & Prablanc, C. (1986). Large adjustments in visually guided reaching do not depend on vision of the hand or perception of target displacement. Nature, 320(6064), 748–50.PubMedCrossRefGoogle Scholar
  33. Grill-Spector, K., Kourtzi, Z., & Kanwisher, N. (2001). The lateral occipital complex and its role in object recognition. Vision Research, 41(10–11), 1409–1422.PubMedCrossRefGoogle Scholar
  34. Haaland, K. Y., Harrington, D. L., & Knight, R. T. (2000). Neural representations of skilled movement. Brain, 123, 2306–2313.PubMedCrossRefGoogle Scholar
  35. Handy, T. C., Grafton, S. T., Shroff, N. M., Ketay, S., & Gazzaniga, M. S. (2003). Graspable objects grab attention when the potential for action is recognized. Nature Neuroscience, 6, 421–427.PubMedCrossRefGoogle Scholar
  36. Helbig, H. B., Graf, M., & Kiefer, M. (2006). The role of action representations in visual object recognition. Experimental Brain Research, 174(2), 221–228.PubMedCrossRefGoogle Scholar
  37. Hesselmann, G., & Malach, R. (2011). The link between fMRI-BOLD activation and perceptual awareness is 'stream-invariant' in the human visual system. Cerebral Cortex, 21(12), 2829–37.PubMedCrossRefGoogle Scholar
  38. Hunter, Z. R., & Brysbaert, M. (2008). Visual half-field experiments are a good measure of cerebral language dominance if used properly: Evidence from fMRI. Neuropsychologia, 46, 316–325.PubMedCrossRefGoogle Scholar
  39. Iberall, T., Bingham, G., & Arbib, M. A. (1986). Opposition Space as a Structuring Concept for the Analysis of Skilled Hand Movements. In H. Heuer & C. Fromm (Eds.), Generation and Modulation of Action Patterns (pp. 158–173). Berlin: Springer-Verlag.CrossRefGoogle Scholar
  40. James, T. W., Humphrey, G. K., Gati, J. S., Menon, R. S., & Goodale, M. A. (2002). Differential effects of viewpoint on object-driven activation in dorsal and ventral streams. Neuron, 35(4), 793–801.PubMedCrossRefGoogle Scholar
  41. Jiang, Y., & He, S. (2006). Cortical responses to invisible faces: Dissociating subsystems for facial-information processing. Current Biology, 16, 2023–2029.PubMedCrossRefGoogle Scholar
  42. Johnson-Frey, S. H. (2004). The neural bases of complex tool use in humans. Trends in Cognitive Sciences, 8(2), 71–78.PubMedCrossRefGoogle Scholar
  43. Johnson-Frey, S., Newman-Norland, R., & Grafton, S. (2005). A distributed left hemisphere network active during planning of everyday tool use skills. Cerebral Cortex, 15, 681–695.PubMedCentralPubMedCrossRefGoogle Scholar
  44. Kellenbach, M. L., Brett, M., & Patterson, K. (2003). Actions speak louder than functions: The importance of manipulability and action in tool representation. Journal of Cognitive Neuroscience, 15, 20–46.CrossRefGoogle Scholar
  45. Klatzky, R. L., McCloskey, B., Doherty, S., Pellegrino, J., & Smith, T. (1987). Knowledge about hand shaping and knowledge about objects. Journal of Motor Behavior, 19, 187–213.PubMedCrossRefGoogle Scholar
  46. Koivisto, M., & Revonsuo, A. (2000). Semantic priming by pictures and words in the cerebral hemispheres. Cognitive Brain Research, 10, 91–98.PubMedCrossRefGoogle Scholar
  47. Lederman, S. J., & Wing, A. M. (2003). Perceptual judgement, grasp point selection and object symmetry. Experimental Brain Research, 152, 156–165.PubMedCrossRefGoogle Scholar
  48. Lewis, J. W. (2006). Cortical networks related to human use of tools. The Neuroscientist, 12(3), 211–231.PubMedCrossRefGoogle Scholar
  49. Logothetis, N. K., & Schall, J. D. (1989). Neuronal correlates of subjective visual perception. Science, 245(4919), 761–763.PubMedCrossRefGoogle Scholar
  50. Lovseth, K., & Atchley, R. A. (2010). Examining lateralized semantic access using pictures. Brain & Cognition, 2, 202–209.CrossRefGoogle Scholar
  51. Mahon, B. Z., & Caramazza, A. (2005). The orchestration of the sensory-motor systems: Clues from neuropsychology. Cognitive Neuropsychology, 22(3), 480–494.PubMedCrossRefGoogle Scholar
  52. Mahon, B., Kumar, N., & Almeida, J. (2013). Spatial frequency tuning reveals visuomotor interactions between the dorsal and ventral visual systems. Journal of Cognitive Neuroscience, 25(6), 862–871. doi: 10.1162/jocn_a_00370 Google Scholar
  53. Mahon, B. Z., Milleville, S., Negri, G. A. L., Rumiati, R. I., Caramazza, A., & Martin, A. (2007). Action-related properties of objects shape object representations in the ventral stream. Neuron, 55(3), 507–520.PubMedCentralPubMedCrossRefGoogle Scholar
  54. Mahon, B. Z., & Wu, W. (in press). Cognitive Penetration of the Dorsal Visual Stream? In J. Zeimbekis & A. Raftopoulos (Eds.), Cognitive Penetration. Oxford University PressGoogle Scholar
  55. Martin, A. (2007). The representation of object concepts in the brain. Annual Review of Psychology, 58, 25–45.PubMedCrossRefGoogle Scholar
  56. Miceli, G., Fouch, E., Capasso, R., Shelton, J. R., Tamaiuolo, F., & Caramazza, A. (2001). The dissociation of color from form and function knowledge. Nature Neuroscience, 4(6), 662–667.PubMedCrossRefGoogle Scholar
  57. Miller, E. K., Nieder, A., Freedman, D. J., & Wallis, J. D. (2003). Neural correlates of categories and concepts. Current Opinion in Neurobiology, 13(2), 198–203.PubMedCrossRefGoogle Scholar
  58. Murata, A., Gallese, V., Luppino, G., Kaseda, M., & Sakata, H. (2000). Selectivity for the shape, size and orientation of objects for grasping in neurons of monkey parietal area AIP. Journal of Neurophysiology, 83(5), 2580–2601.PubMedGoogle Scholar
  59. Noppeney, U., Price, C., Penny, W., & Friston, K. (2006). Two distinct neural mechanisms for category selective responses. Cerebral Cortex, 16(3), 437–445.PubMedCrossRefGoogle Scholar
  60. Pasley, B. N., Mayes, L. C., & Schultz, R. T. (2004). Subcortical discrimination of unperceived objects during binocular rivalry. Neuron, 42, 163–172.PubMedCrossRefGoogle Scholar
  61. Perenin, M. T., & Vighetto, A. (1988). Optic ataxia: a specific disruption in visuomotor mechanisms i. Different aspects of the deficit in reaching for objects. Brain, 111(3), 643–674.PubMedCrossRefGoogle Scholar
  62. Prado, J., Clavagnier, S., Otzenberger, H., Scheiber, C., Kennedy, H., & Perenin, M. T. (2005). Two cortical systems for reaching in central and peripheral vision. Neuron, 48(5), 849–58.PubMedCrossRefGoogle Scholar
  63. Rolls, E. T., & Tovee, M. J. (1994). Processing speed in the cerebral-cortex and the neurophysiology of visual masking. Proceedings of the Royal Society B: Biological Sciences, 257(1348), 9–15.PubMedCrossRefGoogle Scholar
  64. Rosenthal, R., Rosnow, R. L., & Rubin, D. B. (2000). Contrasts and effect sizes in behavioral research: A correlational approach. Cambridge, England: Cambridge University Press.Google Scholar
  65. Sakata, H., Taira, M., Kusunoki, M., Murata, A., Tanaka, Y., & Tsutsui, K. (1998). Neural coding of 3D features of objects for hand action in the parietal cortex of the monkey. Philosophical Transactions of the Royal Society B: Biological Sciences, 353(1373), 1363–1373.CrossRefGoogle Scholar
  66. Shikata, E., Hamzei, F., Glauche, V., Knab, R., Dettmers, C., Weiller, C., & Buchel, C. (2001). Surface orientation discrimination activates caudal and anterior intraparietal sulcus in humans: An event-related fMRI study. Journal of Neurophysiology, 85, 1309–1314.PubMedGoogle Scholar
  67. Sirigu, A., Duhamel, J. R., & Poncet, M. (1991). The role of sensorimotor experience in object recognition. Brain, 114, 2555–2573.PubMedCrossRefGoogle Scholar
  68. Song, J., & Nakayama, K. (2008). Numeric comparison in a visually-guided manual reaching task. Cognition, 106, 994–1003.PubMedCrossRefGoogle Scholar
  69. Sterzer, P., Haynes, J. D., & Rees, G. (2008). Fine-scale activity patterns within high-level ventral visual areas encode the category of invisible objects. Journal of Vision, 8(15), 1–12.PubMedCrossRefGoogle Scholar
  70. Tong, F., Nakayama, K., Vaughan, J. T., & Kanwisher, N. (1998). Binocular rivalry and visual awareness in human extrastriate cortex. Neuron, 21, 753–759.PubMedCrossRefGoogle Scholar
  71. Tranel, D., Damasio, H., & Damasio, A. R. (1997). A neural basis for the retrieval of conceptual knowledge. Neuropsychologia, 35, 1319–1327.PubMedCrossRefGoogle Scholar
  72. Tsuchiya, N., & Koch, C. (2005). Continuous flash suppression reduces negative afterimages. Nature Neuroscience, 8(8), 1096–1101.PubMedCrossRefGoogle Scholar
  73. Yang, E., & Blake, R. (2012). Deconstructing continuous flash suppression. Journal of Vision, 12(3), 1–14.CrossRefGoogle Scholar

Copyright information

© Psychonomic Society, Inc. 2013

Authors and Affiliations

  • Jorge Almeida
    • 1
    • 2
    • 3
    Email author
  • Bradford Z. Mahon
    • 4
    • 5
  • Veronica Zapater-Raberov
    • 6
  • Aleksandra Dziuba
    • 2
  • Tiago Cabaço
    • 2
  • J. Frederico Marques
    • 2
  • Alfonso Caramazza
    • 6
    • 7
  1. 1.Faculty of Psychology and Education SciencesUniversity of CoimbraCoimbraPortugal
  2. 2.Faculty of PsychologyUniversity of LisbonLisbonPortugal
  3. 3.School of PsychologyUniversity of MinhoMinhoPortugal
  4. 4.Department of NeurosurgeryUniversity of Rochester Medical SchoolRochesterUSA
  5. 5.Department of Brain and Cognitive SciencesUniversity of RochesterRochesterUSA
  6. 6.Department of PsychologyHarvard UniversityCambridgeUSA
  7. 7.Center for Mind/Brain SciencesUniversità degli Studi di TrentoPolo di RoveretoItaly

Personalised recommendations