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

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.

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References

  • Abernethy, M., & Coney, J. (1993). Associative priming in the cerebral hemispheres as a function of SOA. Neuropsychologia, 31, 1397–1409.

    PubMed  Article  Google Scholar 

  • 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

  • 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.

    PubMed Central  PubMed  Article  Google Scholar 

  • 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.

    PubMed Central  PubMed  Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Batista, A. P., Buneo, C. A., Snyder, L. H., & Andersen, R. A. (1999). Reach plans in eye-centered coordinates. Science, 285, 257–260.

    PubMed  Article  Google Scholar 

  • Blake, A. (1992). Computational modelling of hand-eye coordination. Philosophical Transactions of the Royal Society: Biological Sciences, 337(1281), 351–360.

    Article  Google Scholar 

  • 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 

  • Brainard, D. H. (1997). The Psychophysics Toolbox. Spatial Vision, 10, 433–436.

    PubMed  Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Bub, D. N., & Lewine, J. (1988). Different modes of word recognition in the left and right visual fields. Brain and Language, 33, 161–188.

    PubMed  Article  Google Scholar 

  • 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.

    PubMed  Article  Google Scholar 

  • 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.

    PubMed  Article  Google Scholar 

  • 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.

    PubMed  Article  Google Scholar 

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

    PubMed  Article  Google Scholar 

  • 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.

    PubMed  Article  Google Scholar 

  • 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.

    PubMed  Article  Google Scholar 

  • 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.

    PubMed  Article  Google Scholar 

  • 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.

    PubMed  Article  Google Scholar 

  • Damasio, H., Tranel, D., Grabowski, T., Adolphs, R., & Damasio, A. (2004). Neural systems behind word and concept retrieval. Cognition, 92, 179–229.

    PubMed  Article  Google Scholar 

  • 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.

  • 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.

    PubMed  Article  Google Scholar 

  • Fang, F., & He, S. (2005). Cortical responses to invisible objects in the human dorsal and ventral pathways. Nature Neuroscience, 8(10), 1380–1385.

    PubMed  Article  Google Scholar 

  • 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.

    PubMed  Article  Google Scholar 

  • 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

    PubMed Central  PubMed  Article  Google Scholar 

  • Forster, K. I., & Forster, J. C. (2003). DMDX: A Windows display program with millisecond accuracy. Behavior Research Methods, Instruments, & Computers, 35(1), 116–124.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Goldenberg, G., & Spatt, J. (2009). The neural basis of tool use. Brain, 132(6), 1645–1655.

    PubMed  Article  Google Scholar 

  • 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.

    PubMed  Article  Google Scholar 

  • 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.

    PubMed  Article  Google Scholar 

  • Goodale, M. A., & Milner, A. D. (1992). Separate visual pathways for perception and action. Trends in Neurosciences, 15(1), 20–25.

    PubMed  Article  Google Scholar 

  • 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.

    PubMed  Article  Google Scholar 

  • 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.

    PubMed  Article  Google Scholar 

  • Haaland, K. Y., Harrington, D. L., & Knight, R. T. (2000). Neural representations of skilled movement. Brain, 123, 2306–2313.

    PubMed  Article  Google Scholar 

  • 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.

    PubMed  Article  Google Scholar 

  • Helbig, H. B., Graf, M., & Kiefer, M. (2006). The role of action representations in visual object recognition. Experimental Brain Research, 174(2), 221–228.

    PubMed  Article  Google Scholar 

  • 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.

    PubMed  Article  Google Scholar 

  • 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.

    PubMed  Article  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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.

    PubMed  Article  Google Scholar 

  • Jiang, Y., & He, S. (2006). Cortical responses to invisible faces: Dissociating subsystems for facial-information processing. Current Biology, 16, 2023–2029.

    PubMed  Article  Google Scholar 

  • Johnson-Frey, S. H. (2004). The neural bases of complex tool use in humans. Trends in Cognitive Sciences, 8(2), 71–78.

    PubMed  Article  Google Scholar 

  • 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.

    PubMed Central  PubMed  Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    PubMed  Article  Google Scholar 

  • Koivisto, M., & Revonsuo, A. (2000). Semantic priming by pictures and words in the cerebral hemispheres. Cognitive Brain Research, 10, 91–98.

    PubMed  Article  Google Scholar 

  • Lederman, S. J., & Wing, A. M. (2003). Perceptual judgement, grasp point selection and object symmetry. Experimental Brain Research, 152, 156–165.

    PubMed  Article  Google Scholar 

  • Lewis, J. W. (2006). Cortical networks related to human use of tools. The Neuroscientist, 12(3), 211–231.

    PubMed  Article  Google Scholar 

  • Logothetis, N. K., & Schall, J. D. (1989). Neuronal correlates of subjective visual perception. Science, 245(4919), 761–763.

    PubMed  Article  Google Scholar 

  • Lovseth, K., & Atchley, R. A. (2010). Examining lateralized semantic access using pictures. Brain & Cognition, 2, 202–209.

    Article  Google Scholar 

  • Mahon, B. Z., & Caramazza, A. (2005). The orchestration of the sensory-motor systems: Clues from neuropsychology. Cognitive Neuropsychology, 22(3), 480–494.

    PubMed  Article  Google Scholar 

  • 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 

  • 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.

    PubMed Central  PubMed  Article  Google Scholar 

  • Mahon, B. Z., & Wu, W. (in press). Cognitive Penetration of the Dorsal Visual Stream? In J. Zeimbekis & A. Raftopoulos (Eds.), Cognitive Penetration. Oxford University Press

  • Martin, A. (2007). The representation of object concepts in the brain. Annual Review of Psychology, 58, 25–45.

    PubMed  Article  Google Scholar 

  • 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.

    PubMed  Article  Google Scholar 

  • 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.

    PubMed  Article  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Noppeney, U., Price, C., Penny, W., & Friston, K. (2006). Two distinct neural mechanisms for category selective responses. Cerebral Cortex, 16(3), 437–445.

    PubMed  Article  Google Scholar 

  • Pasley, B. N., Mayes, L. C., & Schultz, R. T. (2004). Subcortical discrimination of unperceived objects during binocular rivalry. Neuron, 42, 163–172.

    PubMed  Article  Google Scholar 

  • 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.

    PubMed  Article  Google Scholar 

  • 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.

    PubMed  Article  Google Scholar 

  • 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.

    PubMed  Article  Google Scholar 

  • Rosenthal, R., Rosnow, R. L., & Rubin, D. B. (2000). Contrasts and effect sizes in behavioral research: A correlational approach. Cambridge, England: Cambridge University Press.

  • 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.

    Article  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Sirigu, A., Duhamel, J. R., & Poncet, M. (1991). The role of sensorimotor experience in object recognition. Brain, 114, 2555–2573.

    PubMed  Article  Google Scholar 

  • Song, J., & Nakayama, K. (2008). Numeric comparison in a visually-guided manual reaching task. Cognition, 106, 994–1003.

    PubMed  Article  Google Scholar 

  • 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.

    PubMed  Article  Google Scholar 

  • Tong, F., Nakayama, K., Vaughan, J. T., & Kanwisher, N. (1998). Binocular rivalry and visual awareness in human extrastriate cortex. Neuron, 21, 753–759.

    PubMed  Article  Google Scholar 

  • Tranel, D., Damasio, H., & Damasio, A. R. (1997). A neural basis for the retrieval of conceptual knowledge. Neuropsychologia, 35, 1319–1327.

    PubMed  Article  Google Scholar 

  • Tsuchiya, N., & Koch, C. (2005). Continuous flash suppression reduces negative afterimages. Nature Neuroscience, 8(8), 1096–1101.

    PubMed  Article  Google Scholar 

  • Yang, E., & Blake, R. (2012). Deconstructing continuous flash suppression. Journal of Vision, 12(3), 1–14.

    Article  Google Scholar 

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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.

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Almeida, J., Mahon, B.Z., Zapater-Raberov, V. et al. Grasping with the eyes: The role of elongation in visual recognition of manipulable objects. Cogn Affect Behav Neurosci 14, 319–335 (2014). https://doi.org/10.3758/s13415-013-0208-0

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Keywords

  • Dorsal stream
  • Tools
  • Object recognition
  • Object elongation