Highly ordered arrangement of single neurons in orientation pinwheels


In the visual cortex of higher mammals, neurons are arranged across the cortical surface in an orderly map of preferred stimulus orientations1,2. This map contains ‘orientation pinwheels’, structures that are arranged like the spokes of a wheel such that orientation changes continuously around a centre. Conventional optical imaging3,4 first demonstrated these pinwheels3,5, but the technique lacked the spatial resolution to determine the response properties and arrangement of cells near pinwheel centres. Electrophysiological recordings later demonstrated sharply selective neurons near pinwheel centres6,7, but it remained unclear whether they were arranged randomly or in an orderly fashion. Here we use two-photon calcium imaging in vivo8,9,10,11,12 to determine the microstructure of pinwheel centres in cat visual cortex with single-cell resolution. We find that pinwheel centres are highly ordered: neurons selective to different orientations are clearly segregated even in the very centre. Thus, pinwheel centres truly represent singularities in the cortical map. This highly ordered arrangement at the level of single cells suggests great precision in the development of cortical circuits underlying orientation selectivity.

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Figure 1: Functional maps of orientation pinwheels.
Figure 2: Tuning curves of cells close to a pinwheel centre and in an iso-orientation domain.
Figure 3: Relationship between neurons in the pinwheel centre (less than 65 µm from singularity) and in the periphery (more than 65 µm).


  1. 1

    Hubel, D. H. & Wiesel, T. N. Shape and arrangement of columns in cat's striate cortex. J. Physiol. (Lond.) 165, 559–568 (1963)

    CAS  Article  Google Scholar 

  2. 2

    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)

    CAS  Article  Google Scholar 

  3. 3

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

    ADS  CAS  Article  Google Scholar 

  4. 4

    Grinvald, A., Lieke, E., Frostig, R. D., Gilbert, C. D. & Wiesel, T. N. Functional architecture of cortex revealed by optical imaging of intrinsic signals. Nature 324, 361–364 (1986)

    ADS  CAS  Article  Google Scholar 

  5. 5

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

    ADS  CAS  Article  Google Scholar 

  6. 6

    Maldonado, P. E., Gödecke, I., Gray, C. M. & Bonhoeffer, T. Orientation selectivity in pinwheel centres in cat striate cortex. Science 276, 1551–1555 (1997)

    CAS  Article  Google Scholar 

  7. 7

    Schummers, J., Marino, J. & Sur, M. Synaptic integration by V1 neurons depends on location within the orientation map. Neuron 36, 969–978 (2002)

    CAS  Article  Google Scholar 

  8. 8

    Svoboda, K., Denk, W., Kleinfeld, D. & Tank, D. W. In vivo dendritic calcium dynamics in neocortical pyramidal neurons. Nature 385, 161–165 (1997)

    ADS  CAS  Article  Google Scholar 

  9. 9

    Stosiek, C., Garaschuk, O., Holthoff, K. & Konnerth, A. In vivo two-photon calcium imaging of neuronal networks. Proc. Natl Acad. Sci. USA 100, 7319–7324 (2003)

    ADS  CAS  Article  Google Scholar 

  10. 10

    Ohki, K., Chung, S., Ch'ng, Y. H., Kara, P. & Reid, R. C. Functional imaging with cellular resolution reveals precise micro-architecture in visual cortex. Nature 433, 597–603 (2005)

    ADS  CAS  Article  Google Scholar 

  11. 11

    Sullivan, M. R., Nimmerjahn, A., Sarkisov, D. V., Helmchen, F. & Wang, S. S. In vivo calcium imaging of circuit activity in cerebellar cortex. J. Neurophysiol. 94, 1636–1644 (2005)

    CAS  Article  Google Scholar 

  12. 12

    Kerr, J. N., Greenberg, D. & Helmchen, F. Imaging input and output of neocortical networks in vivo. Proc. Natl Acad. Sci. USA 102, 14063–14068 (2005)

    ADS  CAS  Article  Google Scholar 

  13. 13

    Meister, M. & Bonhoeffer, T. Tuning and topography in an odor map on the rat olfactory bulb. J. Neurosci. 21, 1351–1360 (2001)

    CAS  Article  Google Scholar 

  14. 14

    Gray, C. M., Maldonado, P. E., Wilson, M. & McNaughton, B. Tetrodes markedly improve the reliability and yield of multiple single-unit isolation from multi-unit recordings in cat striate cortex. J. Neurosci. Methods 63, 43–54 (1995)

    CAS  Article  Google Scholar 

  15. 15

    Gödecke, I., Kim, D. S., Bonhoeffer, T. & Singer, W. Development of orientation preference maps in area 18 of kitten visual cortex. Eur. J. Neurosci. 9, 1754–1762 (1997)

    Article  Google Scholar 

  16. 16

    Crair, M. C., Gillespie, D. C. & Stryker, M. P. The role of visual experience in the development of columns in cat visual cortex. Science 279, 566–570 (1998)

    ADS  CAS  Article  Google Scholar 

  17. 17

    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)

    CAS  Article  Google Scholar 

  18. 18

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

    ADS  CAS  Article  Google Scholar 

  19. 19

    Swindale, N. V., Matsubara, J. A. & Cynader, M. S. Surface organization of orientation and direction selectivity in cat area 18. J. Neurosci. 7, 1414–1427 (1987)

    CAS  Article  Google Scholar 

  20. 20

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

    ADS  CAS  Article  Google Scholar 

  21. 21

    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)

    CAS  Article  Google Scholar 

  22. 22

    Marino, J. et al. Invariant computations in local cortical networks with balanced excitation and inhibition. Nature Neurosci. 8, 194–201 (2005)

    ADS  CAS  Article  Google Scholar 

  23. 23

    Chapman, B., Stryker, M. P. & Bonhoeffer, T. Development of orientation preference maps in ferret primary visual cortex. J. Neurosci. 16, 6443–6453 (1996)

    CAS  Article  Google Scholar 

  24. 24

    Gilbert, C. D. & Wiesel, T. N. Columnar specificity of intrinsic horizontal and corticocortical connections in cat visual cortex. J. Neurosci. 9, 2432–2442 (1989)

    CAS  Article  Google Scholar 

  25. 25

    Mooser, F., Bosking, W. H. & Fitzpatrick, D. A morphological basis for orientation tuning in primary visual cortex. Nature Neurosci. 7, 872–879 (2004)

    CAS  Article  Google Scholar 

  26. 26

    Katz, L. C., Gilbert, C. D. & Wiesel, T. N. Local circuits and ocular dominance columns in monkey striate cortex. J. Neurosci. 9, 1389–1399 (1989)

    CAS  Article  Google Scholar 

  27. 27

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

    Article  Google Scholar 

  28. 28

    Kossel, A., Löwel, S. & Bolz, J. Relationships between dendritic fields and functional architecture in striate cortex of normal and visually deprived cats. J. Neurosci. 15, 3913–3926 (1995)

    CAS  Article  Google Scholar 

  29. 29

    Hickmott, P. W. & Merzenich, M. M. Dendritic bias of neurons in rat somatosensory cortex associated with a functional boundary. J. Comp. Neurol. 409, 385–399 (1999)

    CAS  Article  Google Scholar 

  30. 30

    Swindale, N. V., Grinvald, A. & Shmuel, A. The spatial pattern of response magnitude and selectivity for orientation and direction in cat visual cortex. Cereb. Cortex 13, 225–238 (2003)

    Article  Google Scholar 

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We thank S. Yurgenson for technical support and programming, A. Kerlin for programming, and A. Vagodny for surgical assistance. This work was supported by grants from the NIH, the Lefler Fund, the Goldenson/Berenberg Fund, and the Max Planck Society.

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Correspondence to R. Clay Reid.

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Supplementary information

Supplementary Methods and Figures

This file contains Supplementary Methods, ten Supplementary Figures and their Legends. (PDF 2081 kb)

Supplementary Video 1

Three dimensional reconstruction of an orientation map from nine different depths (130-290 µm; shown in Figure 1c). Selective cells are coloured according to their preferred orientation. (MOV 3272 kb)

Supplementary Video 2

A time-lapse movie of fluorescence signal change (µF/F) of cells and neuropil to eight different orientations of stimuli (see top-right corner of the movie). Unlike for the data presented in the paper, in this example the stimuli were drifted back and forth in both directions orthogonal to the orientation. The brightest change represents 20% signal increase. (MOV 8150 kb)

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Ohki, K., Chung, S., Kara, P. et al. Highly ordered arrangement of single neurons in orientation pinwheels. Nature 442, 925–928 (2006). https://doi.org/10.1038/nature05019

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