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Differential human brain activation by vertical and horizontal global visual textures

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Abstract

Mid-level visual processes which integrate local orientation information for the detection of global structure can be investigated using global form stimuli of varying complexity. Several lines of evidence suggest that the identification of concentric and parallel organisations relies on different underlying neural substrates. The current study measured brain activation by concentric, horizontal parallel, and vertical parallel arrays of short line segments, compared to arrays of randomly oriented segments. Six subjects were scanned in a blocked design functional magnetic resonance imaging experiment. We compared percentage BOLD signal change during the concentric, horizontal and vertical blocks within early retinotopic areas, the fusiform face area and the lateral occipital complex. Unexpectedly, we found that vertical and horizontal parallel forms differentially activated visual cortical areas beyond V1, but in general, activations to concentric and parallel forms did not differ. Vertical patterns produced the highest percentage signal change overall and only area V3A showed a significant difference between concentric and parallel (horizontal) stimuli, with the former better activating this area. These data suggest that the difference in brain activation to vertical and horizontal forms arises at intermediate or global levels of visual representation since the differential activity was found in mid-level retinotopic areas V2 and V3 but not in V1. This may explain why earlier studies—using methods that emphasised responses to local orientation—did not discover this vertical–horizontal anisotropy.

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References

  • Achtman RL, Hess RF, Wang Y-Z (2003) Sensitivity for global shape detection. J Vis 3:616–624

    Article  PubMed  Google Scholar 

  • Allman J, Miezin F, McGuinness E (1985) Stimulus specific responses from beyond the classical receptive field: neurophysiological mechanisms for local-global comparisons in visual neurons. Annu Rev Neurosci 8:407–430

    Article  CAS  PubMed  Google Scholar 

  • Appelle S (1972) Perception and discrimination as a function of stimulus orientation—oblique effect in man and animals. Psychol Bull 78:266

    Article  CAS  PubMed  Google Scholar 

  • Aspell JE, Tanskanen T, Hurlbert AC (2005) Neuromagnetic correlates of visual motion coherence. Eur J Neurosci 22:2937–2945

    Article  CAS  PubMed  Google Scholar 

  • Aspell JE, Wattam-Bell J, Braddick O (2006) Interaction of spatial and temporal integration in global form processing. Vis Res 46:2834–2841

    Article  PubMed  Google Scholar 

  • Badcock D, Clifford C (2006) The inputs to global form. In: Jenkins M, Harris R (eds) Seeing spatial form. Oxford University Press, Oxford, pp 37–50

    Google Scholar 

  • Bell J, Badcock DR, Wilson H, Wilkinson F (2007) Detection of shape in radial frequency contours: independence of local and global form information. Vis Res 47:1518–1522

    Article  PubMed  Google Scholar 

  • Braddick OJ, Lin MH, Atkinson J, O’Brien J, Wattam-Bell J, Turner R (1999) Form coherence: a measure of extrastriate pattern processing. Perception 28:59

    Google Scholar 

  • Braddick OJ, O’Brien JMD, Wattam-Bell J, Atkinson J, Turner R (2000) Form and motion coherence activate independent, but not dorsal/ventral segregated, networks in the human brain. Curr Biol 10:731–734

    Article  CAS  PubMed  Google Scholar 

  • Chapman B, Bonhoeffer T (1998) Overrepresentation of horizontal and vertical orientation preferences in developing ferret area 17. Proc Natl Acad Sci USA 95:2609–2614

    Article  CAS  PubMed  Google Scholar 

  • Coppola DM, White LE, Fitzpatrick D, Purves D (1998) Unequal representation of cardinal and oblique contours in ferret visual cortex. Proc Natl Acad Sci USA 95:2621–2623

    Article  CAS  PubMed  Google Scholar 

  • Cumming BG (2002) An unexpected specialization for horizontal disparity in primate primary visual cortex. Nature 418:633–636

    Article  CAS  PubMed  Google Scholar 

  • Dakin SC (1997a) The detection of structure in glass patterns: Psychophysics and computational models. Vis Res 37:2227–2246

    Article  CAS  PubMed  Google Scholar 

  • Dakin SC (1997b) Glass patterns: some contrast effects re-evaluated. Perception 26:253–268

    Article  CAS  PubMed  Google Scholar 

  • Dakin SC (1999) Orientation variance as a quantifier of structure in texture. Spat Vis 12:1–30

    Article  CAS  PubMed  Google Scholar 

  • Dale AM, Fischl B, Sereno MI (1999) Cortical surface-based analysis I: segmentation and surface reconstruction. NeuroImage 9:179–194

    Article  CAS  PubMed  Google Scholar 

  • Dumoulin SO, Hess RF (2007) Cortical specialization for concentric shape processing. Vis Res 47:1608–1613

    Article  PubMed  Google Scholar 

  • Essock EA, DeFord JK, Hansen BC, Sinai MJ (2003) Oblique stimuli are seen best (not worst!) in naturalistic broad-band stimuli: a horizontal effect. Vis Res 43:1329–1335

    Article  PubMed  Google Scholar 

  • Felleman DJ, Van Essen DC (1991) Distributed hierarchical processing in the primate cerebral cortex. Cereb Cortex 1:1-a-47

    Google Scholar 

  • Fischl B, Sereno MI, Dale AM (1999) Cortical surface-based analysis II: inflation, flattening, and a surface-based coordinate system. NeuroImage 9:195–207

    Article  CAS  PubMed  Google Scholar 

  • Furmanski CS, Engel SA (2000) An oblique effect in human primary visual cortex. Nat Neurosci 3:535–536

    Article  CAS  PubMed  Google Scholar 

  • Gallant JL, Braun J, Van Essen DC (1993) Selectivity for polar, hyperbolic, and cartesian gratings in macaque visual cortex. Science 259:100–103

    Article  CAS  PubMed  Google Scholar 

  • Gallant JL, Shoup RE, Mazer JA (2000) A human extrastriate area functionally homologous to macaque V4. Neuron 27:227–235

    Article  CAS  PubMed  Google Scholar 

  • Grill-Spector K, Malach R (2004) The Human Visual Cortex. Annu Rev Neurosci 27:649–677

    Article  CAS  PubMed  Google Scholar 

  • Grill-Spector K, Kushnir T, Edelman S, Avidan G, Itzchak Y, Malach R (1999) Differential processing of objects under various viewing conditions in the human lateral occipital complex. Neuron 24:187–203

    Article  CAS  PubMed  Google Scholar 

  • Hansen BC, Essock EA (2004) A horizontal bias in human visual processing of orientation and its correspondence to the structural components of natural scenes. J Vis 4(12):5, 1044–1060

    Google Scholar 

  • Hubel DH, Wiesel TN (1968) Receptive fields and functional architecture of monkey striate cortex. J Physiol 195:215–243

    CAS  PubMed  Google Scholar 

  • Humphreys GW, Forde EM (2001) Hierarchies, similarity, and interactivity in object recognition: “category-specific” neuropsychological deficits. Behav Brain Sci 24:453–476

    CAS  PubMed  Google Scholar 

  • Ierusalimschy R (2003) Programming in Lua. Lua.org, Rio de Janerio

  • Jenkinson M, Smith SM (2001) A global optimisation method for robust affine registration of brain images. Med Image Anal 5:143–156

    Article  CAS  PubMed  Google Scholar 

  • Jenkinson M, Bannister P, Brady M, Smith S (2002) Improved optimisation for the robust and accurate linear registration and motion correction of brain images. NeuroImage 17:825–841

    Article  PubMed  Google Scholar 

  • Kanwisher N, McDermott J, Chun MM (1997) The fusiform face area: a module in human extrastriate cortex specialized for face perception. J Neurosci 17:4302–4311

    CAS  PubMed  Google Scholar 

  • Keil MS, Cristóbal G (2000) Separating the chaff from the wheat: possible origins of the oblique effect. J Opt Soc Am A 17:697–710

    Article  CAS  Google Scholar 

  • Kobatake E, Tanaka K (1994) Neuronal selectivities to complex object features in the ventral visual pathway of the macaque cerebral cortex. J Neurophysiol 71:856–867

    CAS  PubMed  Google Scholar 

  • Kofka K (1935) Principles of Gestalt psychology. Harcourt, New York

    Google Scholar 

  • Kourtzi Z, Tolias AS, Altmann CF, Augath M, Logothetis NK (2003) Integration of local features into global shapes: monkey and human fMRI studies. Neuron 37:333–346

    Article  CAS  PubMed  Google Scholar 

  • Kovacs I, Julesz B (1993) A closed curve is much more than an incomplete one: Effect of closure in figure-ground segmentation. Proc Natl Acad Sci USA 90:7495–7497

    Article  CAS  PubMed  Google Scholar 

  • Koyama S, Sasaki Y, Andersen GJ, Tootell RBH, Matsuura M, Watanabe T (2005) Separate processing of different global-motion structures in visual cortex is revealed by fMRI. Curr Biol 15:2027–2032

    Article  CAS  PubMed  Google Scholar 

  • Kurki I, Saarinen J (2004) Shape perception in human vision: specialized detectors for concentric spatial structures? Neurosci Lett 360:100–102

    Article  CAS  PubMed  Google Scholar 

  • Lamme VAF, Supèr H, Spekreijse H (1998) Feedforward, horizontal, and feedback processing in the visual cortex. Curr Opin Neurobiol 8:529–535

    Article  CAS  PubMed  Google Scholar 

  • Lewis TL, Ellemberg D, Maurer D, Dirks M, Wilkinson F, Wilson HR (2004) A window on the normal development of sensitivity to global form in glass patterns. Perception 33:409–418

    Article  PubMed  Google Scholar 

  • Li B, Peterson MR, Freeman RD (2003) Oblique effect: a neural basis in the visual cortex. J Neurophysiol 90:204–217

    Article  PubMed  Google Scholar 

  • Liu T, Slotnick SD, Yantis S (2004) Human MT+ mediates perceptual filling-in during apparent motion. NeuroImage 21:1772–1780

    Article  PubMed  Google Scholar 

  • Mahon LE, De Valois RL (2001) Cartesian and non-Cartesian responses in LGN, V1, and V2 cells. Vis Neurosci 18:973–981

    CAS  PubMed  Google Scholar 

  • Malach R, Reppas JB, Benson RR, Kwong KK, Jiang H, Kennedy WA, Ledden PJ, Brady TJ, Rosen BR, Tootell RB (1995) Object-related activity revealed by functional magnetic resonance imaging in human occipital cortex. Proc Natl Acad Sci USA 92:8135–8139

    Article  CAS  PubMed  Google Scholar 

  • Maloney RK, Mitchison GJ, Barlow HB (1987) Limit to the detection of glass patterns in the presence of noise. J Opt Soc Am Opt Image Sci Vis 4:2336–2341

    Article  CAS  Google Scholar 

  • Maunsell JHR, Newsome WT (1987) Visual processing in monkey extrastriate cortex. Annu Rev Neurosci 10:363–401

    Article  CAS  PubMed  Google Scholar 

  • Murray SO, Kersten D, Olshausen BA, Schrater P, Woods DL (2002) Shape perception reduces activity in human primary visual cortex. Proc Natl Acad Sci USA 99:15164–15169

    Article  CAS  PubMed  Google Scholar 

  • Ostwald D, Lam JM, Li S, Kourtzi Z (2008) Neural coding of global form in the human visual cortex. J Neurophysiol 99:2456–2469

    Article  PubMed  Google Scholar 

  • Pei F, Pettet MW, Vildavski VY, Norcia AM (2005) Event-related potentials show configural specificity of global form processing. Neuroreport 16:1427–1430

    Article  PubMed  Google Scholar 

  • Romani A, Callieco R, Tavazzi E, Cosi V (2003) The effects of collinearity and orientation on texture visual evoked potentials. Clin Neurophysiol 114:1021–1026

    Article  PubMed  Google Scholar 

  • Sasaki Y, Rajimehr R, Kim BW, Ekstrom LB, Vanduffel W, Tootell RBH (2006) The radial bias: a different slant on visual orientation sensitivity in human and nonhuman primates. Neuron 51:661–670

    Article  CAS  PubMed  Google Scholar 

  • Schira MM, Fahle M, Donner TH, Kraft A, Brandt SA (2004) Differential contribution of early visual areas to the perceptual process of contour processing. J Neurophysiol 91:1716–1721

    Article  PubMed  Google Scholar 

  • Sereno MI, Dale AM, Reppas JB (1993) Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging. Science 268:889–893

    Article  Google Scholar 

  • Smith S (2002) Fast robust automated brain extraction. Hum Brain Mapp 17:143–155

    Article  PubMed  Google Scholar 

  • Smith MA, Bair W, Movshon JA (2002) Signals in macaque striate cortical neurons that support the perception of glass patterns. J Neurosci 22:8334–8345

    CAS  PubMed  Google Scholar 

  • Switkes E, Mayer MJ, Sloan JA (1978) Spatial frequency analysis of the visual environment: Anisotropy and the carpentered environment hypothesis. Vis Res 18:1393–1399

    Article  CAS  PubMed  Google Scholar 

  • Tootell RBH, Mendola JD, Hadjikhani NK, Ledden PJ, Liu AK, Reppas JB (1997) Functional analysis of V3A and related areas in human visual cortex. J Neurosci 17:7060–7078

    CAS  PubMed  Google Scholar 

  • Vanduffel W, Fize D, Mandeville JB, Nelissen K, Van Hecke P, Rosen BR, Tootell RBH, Orban GA (2001) Visual motion processing investigated using contrast agent-enhanced fMRI in awake behaving monkeys. Neuron 32:565–577

    Article  CAS  PubMed  Google Scholar 

  • Wang G, Ding S, Yunokuchi K (2003) Representation of cardinal contour overlaps less with representation of nearby angles in cat visual cortex. J Neurophysiol 90:3912–3920

    Article  PubMed  Google Scholar 

  • Warnking J, Dojat M, Guérin-Dugué A, Delon-Martin C, Olympieff S, Richard N, Chéhikian A, Segebarth C (2002) fMRI retinotopic mapping—step by step. NeuroImage 17:1665–1683

    Article  CAS  PubMed  Google Scholar 

  • Wilkinson F, James TW, Wilson HR, Gati JS, Menon RS, Goodale MA (2000) An fMRI study of the selective activation of human extrastriate form vision areas by radial and concentric gratings. Curr Biol 10:1455–1458

    Article  CAS  PubMed  Google Scholar 

  • Wilson HR, Wilkinson F (1998) Detection of global structure in Glass patterns: implications for form vision. Vis Res 38:2933–2947

    Article  CAS  PubMed  Google Scholar 

  • Wilson HR, Wilkinson F (2003) Further evidence for global orientation processing in circular Glass patterns. Vis Res 43:563–564

    Article  PubMed  Google Scholar 

  • Wilson HR, Wilkinson F, Asaad W (1997) Concentric orientation summation in human form vision. Vis Res 37:2325–2330

    Article  CAS  PubMed  Google Scholar 

  • Woolrich MW, Ripley BD, Brady JM, Smith SM (2001) Temporal autocorrelation in univariate linear modelling of FMRI data. NeuroImage 14:1370–1386

    Article  CAS  PubMed  Google Scholar 

  • Worsley KJ, Evans AC, Marrett S, Neelin P (1992) A three-dimensional statistical analysis for CBF activation studies in human brain. J Cereb Blood Flow Metab 12:900–918

    CAS  PubMed  Google Scholar 

  • Xu X, Collins CE, Khaytin I, Kaas JH, Casagrande VA (2006) Unequal representation of cardinal vs. oblique orientations in the middle temporal visual area. Proc Natl Acad Sci USA 103:17490–17495

    Article  CAS  PubMed  Google Scholar 

  • Yacoub E, Harel N, Km UÄŸurbil (2008) High-field fMRI unveils orientation columns in humans. Proc Natl Acad Sci USA 105:10607–10612

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by Medical Research Council (UK) Programme Grant # G7908507. Thanks to H. Bridge for her help with the retinotopy analyses.

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Correspondence to Jane E. Aspell.

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Aspell, J.E., Wattam-Bell, J., Atkinson, J. et al. Differential human brain activation by vertical and horizontal global visual textures. Exp Brain Res 202, 669–679 (2010). https://doi.org/10.1007/s00221-010-2173-y

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