Abstract
Orientation and spatial frequency tuning are highly salient properties of neurons in primary visual cortex (V1). The combined organization of these particular tuning properties in the cortical space will strongly shape the V1 population response to different visual inputs, yet it is poorly understood. In this study, we used two-photon imaging in macaque monkey V1 to demonstrate the three-dimensional cell-by-cell layout of both spatial frequency and orientation tuning. We first found that spatial frequency tuning was organized into highly structured maps that remained consistent across the depth of layer II/III, similarly to orientation tuning. Next, we found that orientation and spatial frequency maps were intimately related at the fine spatial scale observed with two-photon imaging. Not only did the map gradients tend notably toward orthogonality, but they also co-varied negatively from cell to cell at the spatial scale of cortical columns.
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Change history
03 December 2012
In the version of this article initially published, the scale bar length for Figure 1e was misstated as 500 μm. The correct length is 50 μm. The error has been corrected in the HTML and PDF versions of the article.
09 January 2013
In the version of this article initially published, the computation performed to yield the values on the x axis of Figure 6c was incorrectly defined in the text and on the axis label as the absolute difference between Aθ and Aϕ (mod 90°). The correct computation is 90° − || Aθ − Aϕ | − 90°|, which yields values near 0° for parallel gradients and values near 90° for perpendicular gradients. The error has been corrected in the HTML and PDF versions of the article.
11 January 2013
In the version of this article initially published, in the equation for Aθ on p. 5, the subscript to the variable f was given as an e. The correct character is θ. The error has been corrected in the HTML and PDF versions of the article.
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Acknowledgements
We are grateful to S. Chatterjee, K. Ohki and C. Reid for preliminary designs of the imaging chamber and for graciously helping us to get started with monkey two-photon imaging. We also thank D. Ringach for comments on an earlier version of the manuscript. Finally, we thank M. De La Parra for technical assistance with the experiments. This work was supported by US National Eye Institute grants EY-010742 to E.M.C., EY-019821 to I.N and MH093567 to A.A.D.
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I.N., K.J.N. and E.M.C. designed the research. I.N., K.J.N., A.A.D. and E.M.C. performed experiments. I.N. analyzed the data. I.N., K.J.N. and E.M.C. wrote the paper.
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Supplementary information
Supplementary Text and Figures
Supplementary Figures 1–8 (PDF 860 kb)
Supplementary Video 1
The acquired images during a flashed grating stimulus, played at 2x the actual speed, are shown on the left. The movie begins about 8 sec after the start of the trial, as depicted by the "progress bar" along the x-axis in each of the two panels on the right. The stimulus begins 2 s after the start of the timecourse, and lasts for 60 s. The right panels also contain the measured (black) and predicted (blue/red) response of the two circled neurons in the movie. The red and blue circles move with the measured location of each neuron as determined by the movement correction algorithm. The dominant movement in this trial is coupled to the animal's breathing. The heartbeat can be seen as well, but is more subtle. This difference between the two motion sources was typical, although this is not always the case, as demonstrated by the trial from Supp. Fig. 6b. (AVI 34564 kb)
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Nauhaus, I., Nielsen, K., Disney, A. et al. Orthogonal micro-organization of orientation and spatial frequency in primate primary visual cortex. Nat Neurosci 15, 1683–1690 (2012). https://doi.org/10.1038/nn.3255
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DOI: https://doi.org/10.1038/nn.3255
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