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Highly ordered arrangement of single neurons in orientation pinwheels

Abstract

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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Acknowledgements

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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Competing interests

Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

Correspondence to R. Clay Reid.

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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Further reading

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).

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