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An explanation of contextual modulation by short-range isotropic connections and orientation map geometry in the primary visual cortex

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Abstract.

Recent experimental studies on the primary visual cortex have revealed complicated nonclassical neuronal activities. Contextual modulation on orientation-contrast is one typical example of nonclassical neuronal behavior. This modulation by surrounding stimuli in a nonclassical receptive field is mainly thought to be mediated by short- and long-range horizontal connections within the primary visual cortex. Short-range connections are circularly symmetrical and relatively independent of orientation preferences, while long-range connections are patchy, asymmetrical, and orientation specific. Although this modulation can be explained by long-range specific connections qualitatively, recent studies suggest that long-range connections alone may be insufficient with respect to the balance between two types of connections. Here, in order to clarify the role of short-range connections in the process of contextual modulation, we propose a model of the primary visual cortex with isotropic short-range connections and a geometric orientation map. Computational simulations using the model have demonstrated that contextual modulation can be explained by short-range connections alone. This is due to the interaction between the spatial periodicity of orientation domains and the excitatory-inhibitory regions arising from the propagation of activities.

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References

  1. Anderson J, Lampl I, Reichova I, Carandini M, Ferster D (2000) Stimulus dependence of two-state fluctuations of membrane potential in cat visual cortex. Nat Neurosci 3:617–621

    Google Scholar 

  2. Bartfeld E, Grinvald A (1992) Relationships between orientation-preference pinwheels cytochrome oxidase blobs and ocular-dominance columns in primate striate cortex. Proc Natl Acad Sci USA 89:11905–11909

    Google Scholar 

  3. Blasdel GG (1992) Orientation selectivity preference and continuity in monkey striate cortex. J Neurosci 12:3139–3161

    Google Scholar 

  4. Blasdel GG, Salama G (1986) Voltage-sensitive dyes reveal a modular organization in monkey striate cortex. Nature 321:579–585

    Google Scholar 

  5. Bonhoeffer T, Grinvald A (1991) Iso-orientation domains in cat visual cortex are arranged in pinwheel-like patterns. Nature 353:429–431

    Google Scholar 

  6. Bonhoeffer T, Grinvald A (1993) The layout of iso-orientation domains in area 18 of cat visual cortex: optical imaging reveals a pinwheel-like organization. J Neurosci 13:4157–4180

    Google Scholar 

  7. Bosking WH, Zhang Y, Schofield B, Fitzpatrick D (1997) Orientation selectivity and the arrangement of horizontal connections in tree shrew striate cortex. J Neurosci 17:2112–2127

    Google Scholar 

  8. Carandini M, Ferster D (1997) A tonic hyperpolarization underlying contrast adaptation in cat visual cortex. Science 276:949–952

    Google Scholar 

  9. Crair MC, Ruthazer ES, Gillespie DC, Stryker MP (1997) Ocular dominance peaks at pinwheel center singularities of the orientation map in cat visual cortex. J Neurophysiol 77:3381–3385

    Google Scholar 

  10. Das A, Gilbert CD (1999) Topography of contextual modulations mediated by short-range interactions in primary visual cortex. Nature 399:655–661

    Google Scholar 

  11. DeAngelis GC, Freeman RD, Ohzawa I (1994) Length and width tuning of neurons in the cat’s primary visual cortex. J Neurophysiol 71:347–374

    Google Scholar 

  12. Gilbert CD, Wiesel TN (1989) Columnar specificity of intrinsic horizontal and corticocortical connections in cat visual cortex. J Neurosci 9:2432–2442

    Google Scholar 

  13. Hubel DH, Wiesel TN (1977) Ferrier lecture: functional architecture of macaque monkey visual cortex. Proc R Soc Lond B 198:1–59

    Google Scholar 

  14. Hübener M, Bolz J (1992) Relationships between dendritic morphology and cytochrome oxidase compartments in monkey striate cortex. J Comp Neurol 324:67–80

    Google Scholar 

  15. Kapadia MK, Ito M, Gilbert CD, Westheimer G (1995) Improvement in visual sensitivity by changes in local context: parallel studies in human observers and in V1 of alert monkeys. Neuron 15:843–856

    Google Scholar 

  16. Kastner S, Nothdurft HC, Pigarev IN (1997) Neuronal correlates of pop-out in cat striate cortex. Vis Res 37:371–376

    Google Scholar 

  17. Katz LC, Gilbert CD, Wiesel TN (1989) Local circuits and ocular dominance columns in monkey striate cortex. J Neurosci 9:1389–1399

    Google Scholar 

  18. Kisvárday ZF, Tóth É, Rausch M, Eysel UT (1997) Orientation-specific relationship between populations of excitatory and inhibitory lateral connections in the visual cortex of the cat. Cereb Cortex 7:605–618

    Google Scholar 

  19. Knierim JJ, Van Essen DC (1992) Neuronal responses to static texture patterns in area V1 of the alert macaque monkey. J Neurophysiol 67:961–980

    Google Scholar 

  20. Kuroiwa J, Inawashiro S, Miyake S, Aso H (2000) Self-organization of orientation maps in a formal neuron model using a cluster learning rule. Neural Netw 13:31–40

    Google Scholar 

  21. Lamme VAF (1995) The neurophysiology of figure-ground segregation in primary visual cortex. J Neurosci 15:1605–1615

    Google Scholar 

  22. Li CY, Li W (1994) Extensive integration field beyond the classical receptive field of cat’s striate cortical neurons—classification and tuning properties. Vis Res 34:2337–2355

    Google Scholar 

  23. Linsker R (1986) From basic network principles to neural architecture (series). Proc Natl Acad Sci USA 83:7508–7512, 8390–8394, 8779–8783

  24. Livingstone MS, Hubel DH (1984) Anatomy and physiology of a color system in the primate visual cortex. J Neurosci 4:309–356

    Google Scholar 

  25. Malach R (1992) Dendritic sampling across processing streams in monkey striate cortex. J Comp Neurol 315:303–312

    Google Scholar 

  26. Malach R (1994) Cortical colomns as devices for maximizing neuronal diversity. Trends Neurosci 17:101–104

    Google Scholar 

  27. Malach R, Amir Y, Harel M, Grinvald A (1993) Relationship between intrinsic connections and functional architecture revealed by optical imaging and in vivo targeted biocytin injections in primate striate cortex. Proc Natl Acad Sci USA 90:10469–10473

    Google Scholar 

  28. McGuire BA, Gilbert CD, Rivlin PK, Wiesel TN (1991) Targets of horizontal connections in macaque primary visual cortex. J Comp Neurol 305:370–392

    Google Scholar 

  29. Miller KD (1994) A model for the development of simple cell receptive fields and the ordered arrangement of orientation columns through activity-dependent competition between ON- and OFF-center inputs. J Neurosci 14:409–441

    Google Scholar 

  30. Obermayer K, Blasdel GG (1997) Singularities in primate orientation maps. Neural Comput 9:555–575

    Google Scholar 

  31. Obermayer K, Blasdel GG, Schulten K (1992) Statistical-mechanical analysis of self-organization and pattern formation during the development of visual maps. Phys Rev A 45:7568–7589

    Google Scholar 

  32. Pei X, Vidyasagar TR, Voigushev M, Creutzfeldt OD (1994) Receptive field analysis and orientation selectivity of postsynaptic potentials of simple cells in cat visual cortex. J Neurosci 14:7130–7140

    Google Scholar 

  33. Rossi AF, Rittenhouse CD, Paradiso MA (1996) The representation of brightness in primary visual cortex. Science 273:1104–1107

    Google Scholar 

  34. Schwartz O, Simoncelli P (2001) Natural signal statistics and sensory gain control. Nat Neurosci 4:819–825

    Google Scholar 

  35. Sengpiel F, Sen A, Blakemore C (1997) Characteristics of surround inhibition in cat area 17. Exp Brain Res 116:216–228

    Google Scholar 

  36. Sillito AM, Grieve KL, Jones HE, Cudeiro J, Davis J (1995) Visual cortical mechanisms detecting focal orientation discontinuities. Nature 378:492–496

    Google Scholar 

  37. Tanaka S (1990) Theory of self-organization of cortical maps: mathematical framework. Neural Netw 3:625–640

    Google Scholar 

  38. Ts’o DY, Frostig RD, Lieke EE, Grinvald A (1990) Functional organization of primate visual cortex revealed by high resolution optical imaging. Science 249:417–420

    Google Scholar 

  39. Varela JA, Song S, Turrigiano GG, Nelson SB (1999) Differential depression at excitatory and inhibitory synapses in visual cortex. J Neurosci 19:4293–4304

    Google Scholar 

  40. Weliky M, Kandler K, Fitzpatrick D, Katz LC (1995) Patterns of excitation and inhibition evoked by horizontal connections in visual cortex share a common relationship to orientation columns. Neuron 15:541–552

    Google Scholar 

  41. Yoshimura Y, Sato H, Imamura K, Watanabe Y (2000) Properties of hirizontal and vertical inputs to pyramidal cells in the superficial layers of the cat visual cortex. J Neurosci 20:1931–1940

    Google Scholar 

  42. Zetzsche C, Barth E (1990) Fundamental limits of linear filters in the visual processing of two-dimensional signals. Vis Res 30:1111–1117

    Google Scholar 

  43. Zipser K, Lamme VAF, Schiller PH (1996) Contextual modulation in primary visual cortex. J Neurosci 16:7376–7389

    Google Scholar 

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Authors and Affiliations

  1. Department of Quantum Engineering and Systems Science, University of Tokyo Graduate School of Engineering, 7-3-1 Hongo, Bunkyo-ku, Tokyo, 113-8654, Japan

    Tsuyoshi Okamoto, Masataka Watanabe & Shunsuke Kondo

  2. Department of Complexity Science and Engineering, The University of Tokyo Graduate School of Frontier Sciences, 7-3-1 Hongo, Bunkyo-ku, Tokyo, 113-8654, Japan

    Kazuyuki Aihara

  3. Core Research for Evolutional Science and Technology, Japan Science and Technology Corporation, 4-1-8 Hon-cho, Kawaguchi, Saitama, 332-0012, Japan

    Kazuyuki Aihara

  4. Aihara Complexity Modelling Project, ERATO, JST, 45-18 Oyama, Shibuya-ku, Tokyo, 151-0065, Japan

    Tsuyoshi Okamoto & Kazuyuki Aihara

Authors
  1. Tsuyoshi Okamoto
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  2. Masataka Watanabe
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  3. Kazuyuki Aihara
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  4. Shunsuke Kondo
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Correspondence to Tsuyoshi Okamoto.

Additional information

Acknowledgement We gratefully acknowledge useful conversations with Hiromichi, Sato. The present work was partly supported by Grant-in-Aid for Scientific Research on Priority Areas (C) Advanced Brain Science Project from the Japanese Ministry of Education, Science, Sports, and Culture.

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Okamoto, T., Watanabe, M., Aihara, K. et al. An explanation of contextual modulation by short-range isotropic connections and orientation map geometry in the primary visual cortex. Biol. Cybern. 91, 396–407 (2004). https://doi.org/10.1007/s00422-004-0528-9

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  • DOI: https://doi.org/10.1007/s00422-004-0528-9

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