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Global visual processing in macaques studied using Kanizsa illusory shapes

Published online by Cambridge University Press:  30 April 2010

KIMBERLY A. FELTNER  and
LYNNE KIORPES
KIMBERLY A. FELTNER*
Affiliation:
Center for Neural Science, New York University, New York, New York, USA
LYNNE KIORPES
Affiliation:
Center for Neural Science, New York University, New York, New York, USA
*
*Address correspondence and reprint requests to: Kimberly A. Feltner, Center for Neural Science, New York University, 4 Washington Place, Room 809, New York, NY 10003. E-mail: [email protected]
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Abstract

The ability to extract form information from a visual scene, for object recognition or figure–ground segregation, is a fundamental visual system function. Many studies of nonhuman primates have addressed the neural mechanisms involved in global form processing, but few have sought to demonstrate this ability behaviorally. In this study, we probed global visual processing in macaque monkeys (Macaca nemestrina) using classical Kanizsa illusory shapes as an assay of global form perception. We trained three monkeys on a “similarity match-to-sample” form discrimination task, first with complete forms embedded in fields of noncontour-inducing “pacman” elements. We then tested them with classic Kanizsa illusory shapes embedded in fields of randomly oriented elements. Two of the three subjects reached our criterion performance level of 80% correct or better on four of five illusory test conditions, demonstrating clear evidence of Kanizsa illusory form perception; the third subject mastered three of five conditions. Performance limits for illusory form discrimination were obtained by manipulating support ratio and by measuring threshold for discriminating “fat” and “thin” illusory squares. Our results indicate that macaque monkeys are capable of global form processing similarly to humans and that the perceptual mechanisms for “filling-in” contour gaps exist in macaques as they do in humans.

Keywords

Kanizsa illusory contoursMacaque monkeyGlobal form perceptionPerceptual completionContour integration
Type
Research Articles
Information
Visual Neuroscience , Volume 27 , Issue 3-4 , July 2010 , pp. 131 - 138
Copyright
Copyright © Cambridge University Press 2010

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References

Banton, T. & Levi, D.M. (1992). The perceived strength of illusory contours. Perception & Psychophysics 52, 676–684.CrossRefGoogle ScholarPubMed
Baumann, R., van der Zwan, R. & Peterhans, E. (1997). Figure-ground segregation at contours: A neural mechanism in the visual cortex of the alert monkey. The European Journal of Neuroscience 9, 1290–1303.CrossRefGoogle ScholarPubMed
Danilova, M.V. & Kojo, I. (2001). Detection of a gabor patch superimposed on an illusory contour. Spatial Vision 15, 1–23.CrossRefGoogle Scholar
De Weerd, P., Desimone, R. & Ungerleider, L.G. (1996). Cue-dependent deficits in grating orientation discrimination after V4 lesions in macaques. Visual Neuroscience 13, 529–538.CrossRefGoogle ScholarPubMed
Fagot, J. & Tomanaga, M. (2001). Effects of element separation on perceptual grouping by humans (Homo sapiens) and chimpanzees (Pan troglodytes): Perception of Kanizsa illusory figures. Animal Cognition 4, 171–177.CrossRefGoogle ScholarPubMed
Feltner, K. & Kiorpes, L. (2009). Developmental onset of illusory form perception in pigtailed macaque monkeys [Abstract] Journal of Vision, 9(8), 908a. doi:10.1167/9.8.908. Presented at the VSS Spring Meeting, 2009, Naples, FL.Google Scholar
Ffytche, D.H. & Zeki, S. (1996). Brain activity related to the perception of illusory contours. NeuroImage 3, 104–108.CrossRefGoogle Scholar
Finney, D.J. (1971). Probit analysis. New York: Cambridge University.Google Scholar
Fujita, K. (2001). Perceptual completion in rhesus monkeys (Macaca mulatta) and pigeons (Columbia livia). Perception & Psychophysics 63, 115–125.CrossRefGoogle ScholarPubMed
Fujita, K. & Giersch, A. (2005). What perceptual rules do capuchin monkeys (Cebus apella) follow in completing partly occluded figures? Journal of Experimental Psychology. Animal Behavior Processes 31, 387–398.CrossRefGoogle ScholarPubMed
Gillam, B. & Nakayama, K. (2002). Subjective contours at line terminations depend on scene layout analysis, not image processing. Journal of Experimental Psychology. Human Perception and Performance 28, 43–53.CrossRefGoogle Scholar
Gold, J.M., Murray, R.F., Bennett, P.J. & Sekuler, A.B. (2000). Deriving behavioural receptive fields for visually completed contours. Current Biology 10, 663–666.CrossRefGoogle ScholarPubMed
Grosof, D.H., Shapley, R.M. & Hawken, M.J. (1993). Macaque V1 neurons can signal ‘illusory’ contours. Nature 365, 550–552.CrossRefGoogle ScholarPubMed
Hadad, B., Maurer, D. & Lewis, T. (2009). Filling in the gaps: The development of contour interpolation [Abstract] Journal of Vision, 9(8), 909a. doi:10.1167/9.8.909. Presented at the VSS Spring Meeting, 2009, Naples, FL.Google Scholar
Halgren, E., Mendola, J., Chong, C.D. & Dale, A.M. (2003). Cortical activation to illusory shapes as measured with magnetoencephalography. NeuroImage 18, 1001–1009.CrossRefGoogle ScholarPubMed
Halko, M.A., Mingolla, E. & Somers, D.C. (2008). Multiple mechanisms of illusory contour perception. Journal of Vision 8, 17, 11–17.CrossRefGoogle ScholarPubMed
Heider, B., Meskenaite, V. & Peterhans, E. (2000). Anatomy and physiology of a neural mechanism defining depth order and contrast polarity at illusory contours. The European Journal of Neuroscience 12, 4117–4130.CrossRefGoogle ScholarPubMed
Hirsch, J., DeLaPaz, R.L., Relkin, N.R., Victor, J., Kim, K., Li, T., Borden, P., Rubin, N. & Shapley, R. (1995). Illusory contours activate specific regions in human visual cortex: Evidence from functional magnetic resonance imaging. Proceedings of the National Academy of Sciences of the United States of America 92, 6469–6473.CrossRefGoogle ScholarPubMed
Huxlin, K.R., Saunders, R.C., Marchionini, D., Pham, H.A. & Merigan, W.H. (2000). Perceptual deficits after lesions of inferotemporal cortex in macaques. Cereberal Cortex 10, 671–683.CrossRefGoogle ScholarPubMed
Kanizsa, G. (1979). Organization in Vision: Essays on Gestalt Perception. New York: Praeger.Google Scholar
Kellman, P.J., Yin, C. & Shipley, T.F. (1998). A common mechanism for illusory and occluded object completion. Journal of Experimental Psychology. Human Perception and Performance 24, 859–869.CrossRefGoogle ScholarPubMed
Kiorpes, L. (2006). Visual processing in amblyopia: Animal studies. Strabismus 14, 3–10.CrossRefGoogle ScholarPubMed
Kiorpes, L. & Bassin, S.A. (2003). Development of contour integration in macaque monkeys. Visual Neuroscience 20, 567–575.CrossRefGoogle ScholarPubMed
Kiorpes, L., Tang, C., Hawken, M.J. & Movshon, J.A. (2003). Ideal observer analysis of the development of spatial contrast sensitivity in macaque monkeys. Journal of Vision 3, 630–641.CrossRefGoogle ScholarPubMed
Kojo, I., Liinasuo, M. & Rovamo, J. (1993). Spatial and temporal properties of illusory figures. Vision Research 33, 897–901.CrossRefGoogle ScholarPubMed
Kovacs, G., Vogels, R. & Orban, G.A. (1995). Selectivity of macaque inferior temporal neurons for partially occluded shapes. The Journal of Neuroscience 15, 1984–1997.CrossRefGoogle ScholarPubMed
Larsson, J., Amunts, K., Gulyas, B., Malikovic, A., Zilles, K. & Roland, P.E. (1999). Neuronal correlates of real and illusory contour perception: Functional anatomy with PET. The European Journal of Neuroscience 11, 4024–4036.CrossRefGoogle ScholarPubMed
Lee, T.S. & Nguyen, M. (2001). Dynamics of subjective contour formation in the early visual cortex. Proceedings of the National Academy of Sciences of the United States of America 98, 1907–1911.CrossRefGoogle ScholarPubMed
Liinasuo, M., Rovamo, J. & Kojo, I. (1997). Effects of spatial configuration and number of fixations on Kanizsa triangle detection. Investigative Ophthalmology & Visual Science 38, 2554–2565.Google ScholarPubMed
Logothetis, N.K. & Sheinberg, D.L. (1996). Visual object recognition. Annual Review of Neuroscience 19, 577–621.CrossRefGoogle ScholarPubMed
Maertens, M. & Pollmann, S. (2005). fMRI reveals a common neural substrate of illusory and real contours in V1 after perceptual learning. Journal of Cognitive Neuroscience 17, 1553–1564.CrossRefGoogle ScholarPubMed
Matsuno, T. & Fujita, K. (2009). A comparative psychophysical approach to visual perception in primates. Primates 50, 121–130.CrossRefGoogle ScholarPubMed
Mendola, J.D., Dale, A.M., Fischl, B., Liu, A.K. & Tootell, R.B. (1999). The representation of illusory and real contours in human cortical visual areas revealed by functional magnetic resonance imaging. The Journal of Neuroscience 19, 8560–8572.CrossRefGoogle ScholarPubMed
Nieder, A. (2002). Seeing more than meets the eye: Processing of illusory contours in animals. Journal of Comparative Physiology Review 188, 249–260.CrossRefGoogle ScholarPubMed
Nieder, A. & Wagner, H. (1999). Perception and neuronal coding of subjective contours in the owl. Nature Neuroscience 2, 660–663.CrossRefGoogle ScholarPubMed
Otsuka, Y., Kanazawa, S. & Yamaguchi, M.K. (2004). The effect of support ratio on infants’ perception of illusory contours. Perception 33, 807–816.CrossRefGoogle ScholarPubMed
Peterhans, E. & von der Heydt, R. (1989). Mechanisms of contour perception in monkey visual cortex. II. Contours bridging gaps. The Journal of Neuroscience 9, 1749–1763.CrossRefGoogle ScholarPubMed
Peterhans, E. & von der Heydt, R. (1991). Subjective contours—Bridging the gap between psychophysics and physiology. Trends in Neurosciences 14, 112–119.CrossRefGoogle Scholar
Ramsden, B.M., Hung, C.P. & Roe, A.W. (2001). Real and illusory contour processing in area V1 of the primate: A cortical balancing act. Cerebral Cortex 11, 648–665.CrossRefGoogle ScholarPubMed
Ringach, D.L. & Shapley, R. (1996). Spatial and temporal properties of illusory contours and amodal boundary completion. Vision Research 36, 3037–3050.CrossRefGoogle ScholarPubMed
Rubin, N., Nakayama, K. & Shapley, R. (1997). Abrupt learning and retinal size specificity in illusory-contour perception. Current Biology 7, 461–467.CrossRefGoogle ScholarPubMed
Sáry, G., Chadaide, Z., Tompa, T., Koteles, K., Kovacs, G. & Benedek, G. (2007). Illusory shape representation in the monkey inferior temporal cortex. The European Journal of Neuroscience 25, 2558–2564.CrossRefGoogle ScholarPubMed
Sáry, G., Koteles, K., Kaposvari, P., Lenti, L., Csifcsak, G., Franko, E., Benedek, G. & Tompa, T. (2008). The representation of Kanizsa illusory contours in the monkey inferior temporal cortex. The European Journal of Neuroscience 28, 2137–2146.CrossRefGoogle ScholarPubMed
Sato, A., Kanazawa, S. & Fujita, K. (1997). Perception of object unity in a chimpanzee (Pan troglodytes). Japanese Psychological Research 39, 191–199.CrossRefGoogle Scholar
Schiller, P.H. (1995). Effect of lesions in visual cortical area V4 on the recognition of transformed objects. Nature 376, 342–344.CrossRefGoogle ScholarPubMed
Shipley, T.F. & Kellman, P.J. (1992). Strength of visual interpolation depends on the ratio of physically specified to total edge length. Perception & Psychophysics 52, 97–106.CrossRefGoogle ScholarPubMed
Sigala, N., Gabbiani, F. & Logothetis, N.K. (2002). Visual categorization and object representation in monkeys and humans. Journal of Cognitive Neuroscience 14, 187–198.CrossRefGoogle ScholarPubMed
Sigala, N. & Logothetis, N.K. (2002). Visual categorization shapes feature selectivity in the primate temporal cortex. Nature 415, 318–320.CrossRefGoogle ScholarPubMed
Singh, M., Hoffman, D. & Albert, M. (1999). Contour completion and relative depth: Petter’s rule and support ratio. Psychological Science 10, 423–428.CrossRefGoogle Scholar
Soriano, M., Spillmann, L. & Bach, M. (1996). The abutting grating illusion. Vision Research 36, 109–116.CrossRefGoogle ScholarPubMed
Spillmann, L. & Dresp, B. (1995). Phenomena of illusory form: Can we bridge the gap between levels of explanation? Perception 24, 1333–1364.CrossRefGoogle Scholar
Stanley, D.A. & Rubin, N. (2003). fMRI activation in response to illusory contours and salient regions in the human lateral occipital complex. Neuron 37, 323–331.CrossRefGoogle ScholarPubMed
von der Heydt, R., Peterhans, E. & Baumgartner, G. (1984). Illusory contours and cortical neuron responses. Science 224, 1260–1262.CrossRefGoogle ScholarPubMed
Williams, R.A., Boothe, R.G., Kiorpes, L. & Teller, D.Y. (1981). Oblique effects in normally reared monkeys (Macaca nemestrina): Meridional variations in contrast sensitivity measured with operant techniques. Vision Research 21, 1253–1266.CrossRefGoogle ScholarPubMed
Wright, A.A., Cook, R.G., Rivera, J.J., Sands, S.F. & Delius, J.D. (1998). Concept Learning by Pigeons: Matching-to-Sample with Trial unique video picture stimuli. Animal Learning and Behavior, 16, 436–444.CrossRefGoogle Scholar
Wright, A.A., Rivera, J.J., Katz, J.S. & Bachevalier, J. (2003). Abstract-concept learning and list-memory processing by capuchin and rhesus monkeys. Journal of Experimental Psychology. Animal Behavior Processes 29, 184–198.CrossRefGoogle ScholarPubMed
Zhou, J., Tjan, B.S., Zhou, Y. & Liu, Z. (2008). Better discrimination for illusory than for occluded perceptual completions. Journal of Vision 8, 26, 1–17.CrossRefGoogle ScholarPubMed