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Neurons in monkey visual area V2 encode combinations of orientations

Abstract

Contours and textures are important attributes of object surfaces, and are often described by combinations of local orientations in visual images. To elucidate the neural mechanisms underlying contour and texture processing, we examined receptive field (RF) structures of neurons in visual area V2 of the macaque monkey for encoding combinations of orientations. By measuring orientation tuning at several locations within the classical RF, we found that a majority (70%) of V2 neurons have similar orientation tuning throughout the RF. However, many others have RFs containing subregions tuned to different orientations, most commonly about 90° apart. By measuring interactions between two positions within the RF, we found that approximately one-third of neurons show inhibitory interactions that make them selective for combinations of orientations. These results indicate that V2 neurons could play an important role in analyzing contours and textures and could provide useful cues for surface segmentation.

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Figure 1: Examples of space-orientation RF maps for neurons in early visual cortical areas.
Figure 2: Distributions of preferred orientations between pairwise locations within the RF.
Figure 3: Orientation interaction results from an exemplar V2 neuron with a uniform RF.
Figure 4: Orientation interaction results from a V2 neuron with a nonuniform RF.
Figure 5: Further examples of orientation interaction results.
Figure 6: Distributions of TSIs.
Figure 7: Hypothetical neural circuitries underlying orientation selective V2 RFs.

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Acknowledgements

We thank D. Marcus and J. Hegde for their participation in data collection and S. Kumar, E. Reid, M. K. Harmon, and C. Faulkner for their assistance with experiments. We are grateful to E. Kaplan for his advice on propofol, to S. Marron for information on mode testing and to G. DeAngelis for his comments and suggestions on the manuscript. This work was supported by a grant from the US National Eye Institute (EY 02091).

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A.A. conceived the project, designed and performed the experiments and wrote the manuscript; X.P. performed the experiments; D.C.V. supervised and contributed in all phases of the project including data collection.

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Correspondence to Akiyuki Anzai.

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Anzai, A., Peng, X. & Van Essen, D. Neurons in monkey visual area V2 encode combinations of orientations. Nat Neurosci 10, 1313–1321 (2007). https://doi.org/10.1038/nn1975

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