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Spatial coding of position and orientation in primary visual cortex

Nature Neuroscience volume 5, pages 874–882 (2002)Cite this article

Abstract

We examined the spatial distribution of population activity in primary visual cortex (V1) of tree shrews with optical imaging and electrophysiology. A line stimulus, thinner than the average V1 receptive field, evoked a broad strip of neural activity of nearly constant size for all stimulus locations tested within the central 10° of visual space. Stimuli in adjacent positions activated highly overlapping populations of neurons; nevertheless, small changes in stimulus position produced orderly changes in the location of the peak of the population response. Statistically significant shifts in the population response were found for stimulus displacements an order of magnitude smaller than receptive field width, down to the limit of optical imaging resolution. Based on the pattern of population activity, we conclude that the map of visual space in V1 is orderly at a fine scale and has uniform coverage of position and orientation without local relationships in the mapping of these features.

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Figure 1: Cortical activity pattern (population response) elicited by presentation of a single bar stimulus.
Figure 2: Population responses and position preference progress in a smooth and continuous fashion across the surface of V1.
Figure 3: Electrophysiological recordings confirm position tuning derived from intrinsic signal imaging.
Figure 4: Orderly progression of population response is unaltered by the presence of an additional line stimulus.
Figure 5: The fine mapping of visual space is independent of the map of orientation preference.
Figure 6: Quantitative analysis confirms the lack of relationship between fine structure of orientation and position maps.
Figure 7: Coverage is uniform for biologically relevant population response sizes and largely invariant with alterations in map relationships.

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References

  1. Tootell, R.B., Switkes, E., Silverman, M.S. & Hamilton, S.L. Functional anatomy of macaque striate cortex. II. Retinotopic organization. J. Neurosci. 8, 1531–1568 (1988).

    Article  CAS  Google Scholar 

  2. Grinvald, A., Lieke, E.E., Frostig, R.D. & Hildesheim, R. Cortical point-spread function and long-range lateral interactions revealed by real-time optical imaging of macaque monkey primary visual cortex. J. Neurosci. 14, 2545–2568 (1994).

    Article  CAS  Google Scholar 

  3. Albus, K. A quantitative study of the projection area of the central and the paracentral visual field in area 17 of the cat. I. The precision of the topography. Exp. Brain Res. 24, 159–179 (1975).

    Article  CAS  Google Scholar 

  4. Hubel, D.H. & Wiesel, T.N. Ferrier lecture. Functional architecture of macaque monkey visual cortex. Proc. R. Soc. Lond. B. Biol. Sci. 198, 1–59 (1977).

    Article  CAS  Google Scholar 

  5. Jancke, D. et al. Parametric population representation of retinal location: neuronal interaction dynamics in cat primary visual cortex. J. Neurosci. 19, 9016–9028 (1999).

    Article  CAS  Google Scholar 

  6. Hinton, G.E., McClelland, J.L. & Rumelhart, D.E. in Parallel Distributed Processing Vol. 1 (eds. Rumelhart, D. E. & McClelland, J. L.) 77–109 (MIT Press, Cambridge, Massachusetts, 1986).

    Google Scholar 

  7. Baldi, P. & Heiligenberg, W. How sensory maps could enhance resolution through ordered arrangements of broadly tuned receivers. Biol. Cybern. 59, 313–318 (1988).

    Article  CAS  Google Scholar 

  8. McIlwain, J.T. Distributed spatial coding in the superior colliculus: a review. Vis. Neurosci. 6, 3–13 (1991).

    Article  CAS  Google Scholar 

  9. McIlwain, J.T. Population coding: a historical sketch. Prog. Brain Res. 130, 3–7 (2001).

    Article  CAS  Google Scholar 

  10. Talbot, S.A. & Marshall, W.H. Physiological studies on neural mechanisms of visual localization and discrimination. Am. J. Ophthalmol. 24, 1255–1264 (1941).

    Article  Google Scholar 

  11. Daniel, P.M. & Whitteridge, D. The representation of the visual field on the cerebral cortex in monkeys. J. Physiol. (Lond.) 159, 203–221 (1961).

    Article  CAS  Google Scholar 

  12. Van Essen, D.C., Newsome, W.T. & Maunsell, J.H. The visual field representation in striate cortex of the macaque monkey: asymmetries, anisotropies, and individual variability. Vision Res. 24, 429–448 (1984).

    Article  CAS  Google Scholar 

  13. Blasdel, G. & Campbell, D. Functional retinotopy of monkey visual cortex. J. Neurosci. 21, 8286–8301 (2001).

    Article  CAS  Google Scholar 

  14. Hubel, D.H. & Wiesel, T.N. Receptive fields, binocular interaction and functional architecture in the cat's visual system. J. Physiol. (Lond.) 160, 106–154 (1962).

    Article  CAS  Google Scholar 

  15. Creutzfeldt, O.D., Kuhnt, U. & Benevento, L.A. An intracellular analysis of visual cortical neurones to moving stimuli: response in a co-operative neuronal network. Exp. Brain Res. 21, 251–274 (1974).

    CAS  PubMed  Google Scholar 

  16. Hubel, D.H. & Wiesel, T.N. Uniformity of monkey striate cortex: a parallel relationship between field size, scatter, and magnification factor. J. Comp. Neurol. 158, 295–305 (1974).

    Article  CAS  Google Scholar 

  17. Das, A. & Gilbert, C.D. Distortions of visuotopic map match orientation singularities in primary visual cortex. Nature 387, 594–598 (1997).

    Article  CAS  Google Scholar 

  18. Das, A. & Gilbert, C.D. Topography of contextual modulations mediated by short-range interactions in primary visual cortex. Nature 399, 655–661 (1999).

    Article  CAS  Google Scholar 

  19. Hubel, D.H. & Wiesel, T.N. Sequence regularity and geometry of orientation columns in the monkey striate cortex. J. Comp. Neurol. 158, 267–293 (1974).

    Article  CAS  Google Scholar 

  20. Swindale, N.V. Coverage and the design of striate cortex. Biol. Cybern. 65, 415–424 (1991).

    Article  CAS  Google Scholar 

  21. Swindale, N.V., Shoham, D., Grinvald, A., Bonhoeffer, T. & Hubener, M. Visual cortex maps are optimized for uniform coverage. Nat. Neurosci. 3, 822–826 (2000).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  24. Blasdel, G.G. Orientation selectivity, preference, and continuity in monkey striate cortex. J. Neurosci. 12, 3139–3161 (1992).

    Article  CAS  Google Scholar 

  25. Bonhoeffer, T. & Grinvald, A. 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 (1993).

    Article  CAS  Google Scholar 

  26. Durbin, R. & Mitchison, G. A dimension reduction framework for understanding cortical maps. Nature 343, 644–647 (1990).

    Article  CAS  Google Scholar 

  27. Obermayer, K., Ritter, H. & Schulten, K. A principle for the formation of the spatial structure of cortical feature maps. Proc. Natl. Acad. Sci. USA 87, 8345–8349 (1990).

    Article  CAS  Google Scholar 

  28. Grinvald, A., Frostig, R.D., Lieke, E. & Hildesheim, R. Optical imaging of neuronal activity. Physiol. Rev. 68, 1285–1366 (1988).

    Article  CAS  Google Scholar 

  29. Blasdel, G.G. Differential imaging of ocular dominance and orientation selectivity in monkey striate cortex. J. Neurosci. 12, 3115–3138 (1992).

    Article  CAS  Google Scholar 

  30. Bonhoeffer, T. & Grinvald, A. in Brain Mapping: the Methods (eds. Toga, A. W. & Mazziotta, J. C.) 55–97 (Academic, New York, 1996).

    Google Scholar 

  31. Grinvald, A. et al. in Modern Techniques in Neuroscience Research (eds. Windhorst, U. & Johansson, H.) 893–969 (Springer, Berlin, 1999).

    Book  Google Scholar 

  32. Blasdel, G.G. & Fitzpatrick, D. Physiological organization of layer 4 in macaque striate cortex. J. Neurosci. 4, 880–895 (1984).

    Article  CAS  Google Scholar 

  33. Hetherington, P.A. & Swindale, N.V. Receptive field and orientation scatter studied by tetrode recordings in cat area 17. Vis. Neurosci. 16, 637–652 (1999).

    Article  CAS  Google Scholar 

  34. Obermayer, K. & Blasdel, G.G. Geometry of orientation and ocular dominance columns in monkey striate cortex. J. Neurosci. 13, 4114–4129 (1993).

    Article  CAS  Google Scholar 

  35. Hubener, M., Shoham, D., Grinvald, A. & Bonhoeffer, T. Spatial relationships among three columnar systems in cat area 17. J. Neurosci. 17, 9270–9284 (1997).

    Article  CAS  Google Scholar 

  36. Crair, M.C., Ruthazer, E.S., Gillespie, D.C. & Stryker, M.P. Ocular dominance peaks at pinwheel center singularities of the orientation map in cat visual cortex. J. Neurophysiol. 77, 3381–3385 (1997).

    Article  CAS  Google Scholar 

  37. Crair, M.C., Ruthazer, E.S., Gillespie, D.C. & Stryker, M.P. Relationship between the ocular dominance and orientation maps in visual cortex of monocularly deprived cats. Neuron 19, 307–318 (1997).

    Article  CAS  Google Scholar 

  38. Kim, D.S., Matsuda, Y., Ohki, K., Ajima, A. & Tanaka, S. Geometrical and topological relationships between multiple functional maps in cat primary visual cortex. NeuroReport 10, 2515–2522 (1999).

    Article  CAS  Google Scholar 

  39. Shmuel, A. & Grinvald, A. Functional organization for direction of motion and its relationship to orientation maps in cat area 18. J. Neurosci. 16, 6945–6964 (1996).

    Article  CAS  Google Scholar 

  40. Weliky, M., Bosking, W.H. & Fitzpatrick, D. A systematic map of direction preference in primary visual cortex. Nature 379, 725–728 (1996).

    Article  CAS  Google Scholar 

  41. Sparks, D.L., Holland, R. & Guthrie, B.L. Size and distribution of movement fields in the monkey superior colliculus. Brain Res. 113, 21–34 (1976).

    Article  CAS  Google Scholar 

  42. Groh, J.M., Born, R.T. & Newsome, W.T. How is a sensory map read out? Effects of microstimulation in visual area MT on saccades and smooth pursuit eye movements. J. Neurosci. 17, 4312–4330 (1997).

    Article  CAS  Google Scholar 

  43. Treue, S., Hol, K. & Rauber, H.J. Seeing multiple directions of motion—physiology and psychophysics. Nat. Neurosci. 3, 270–276 (2000).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  45. Bosking, W.H., Kretz, R., Pucak, M.L. & Fitzpatrick, D. Functional specificity of callosal connections in tree shrew striate cortex. J. Neurosci. 20, 2346–2359 (2000).

    Article  CAS  Google Scholar 

  46. Kaas, J.H., Hall, W.C., Killackey, H. & Diamond, I.T. Visual cortex of the tree shrew (Tupaia glis): architectonic subdivisions and representations of the visual field. Brain Res. 42, 491–496 (1972).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank A. Basole, H. Chisum, M. Pucak, T. Tucker and L. White for discussions and D. Katz for advice with data analysis. This research was supported by a grant from the National Institutes of Health (EY06821) and by The McKnight Foundation (to D.F.).

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Authors and Affiliations

  1. Dept. of Neurobiology, Box 3209, Duke University Medical Center, Durham, 27710, North Carolina, USA

    William H. Bosking, Justin C. Crowley & David Fitzpatrick

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Correspondence to David Fitzpatrick.

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Supplementary information

Supplementary Fig. 1.

Statistical analysis of the minimum stimulus separation that produced significant changes in population response. Using imaging results from three animals (illustrated in a, b and c), chi-square tests were used to evaluate whether the population response profiles obtained for pairs of individually presented stimuli separated by a given distance were significantly different. The chi-square value for each stimulus pair is plotted as a function of separation distance in degrees (blue and red circles). The blue circles indicate separation distances that yielded significant differences in the population response (p < 0.05), while the red circles denote separation distances that did not reach significance. Solid lines indicate regression for chi-square values versus stimulus separation. Dashed lines indicate the chi-square value corresponding to a significant difference (p < 0.05) between the two population responses. The intersection between these lines provides an estimate of the minimum stimulus separation that would lead to significantly different population responses. For each animal, the full data set is plotted on the left, and values for separation distances less than 2° are reproduced at a larger scale on the right. Estimates for the minimum separation distance for each animal: TS9758 = 0.49° TS9764 = 0.55°; TS9737 = 0.63°. Average minimum separation distance = 0.56°. Assuming a mapping of visual space at a rate of 200 μm/°, this minimal separation distance would yield a separation in V1 of approximately 100 μm. (JPG 33 kb)

Supplementary Fig. 2.

High-resolution optical imaging demonstrates the lack of relationship between the map of visual space and the map of orientation preference. (a) Population responses obtained with the vertical bar stimulus located at 9 different positions from 1° left to 7° right of the vertical meridian. The optical imaging window for this experiment is rotated by 90° relative to the optical imaging window used in all other figures; therefore, iso-azimuth lines in visual space run vertically across the imaging window. (b) Position preference map generated from the population responses shown in (a). Position preference for each site is color-coded according to the key shown beneath the panel. Locations in cortex that have a position preference of < 1° or > 6° in azimuth are coded in gray because of the limited sampling available for these regions. Black lines indicate iso-azimuth lines spaced at 1° intervals, black squares and corresponding letters (b, c) indicate the location of 14 radial electrode penetrations spaced at approximately 50 μm intervals used to obtain multi-unit electrophysiological recordings of position preference (see Fig. 5d). (c) Orientation preference map for the same region of cortex. Note that the smooth progression of position preference is unaffected by non-linearities in the map of orientation preference. Orientation preference is color-coded according to the key beneath the panel. Scale bars, 200 μm; bar in (c) also applies to (b). (JPG 20 kb)

Supplementary Fig. 3.

Artificially generated position preference maps used for coverage analysis. In each panel, iso-azimuth contours spaced at 1° intervals (black lines) are shown over the map of orientation preference for the same region (color coded according to the key at the bottom of the figure). Artificial maps of position preference were generated so as to have uniform rate of change in position preference (not shown), positive correlation between rate of change in position preference and rate of change in orientation preference (a), or inverse correlation between rate of change in position preference and rate of change in orientation preference (b). The same procedure was used to generate artificial position preference maps for the elevation axis; however, contours from these maps have been omitted for clarity. See Supplementary Methods for details. The star in each panel indicates the location of a high rate of change area in the orientation preference map. Iso-azimuth contour lines tend to cluster at this location in (a), and tend to avoid this region in (b). Scale bar, 1 mm, applies to both panels. (JPG 28 kb)

Supplementary Methods (PDF 34 kb)

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Bosking, W., Crowley, J. & Fitzpatrick, D. Spatial coding of position and orientation in primary visual cortex. Nat Neurosci 5, 874–882 (2002). https://doi.org/10.1038/nn908

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