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Induction of visual orientation modules in auditory cortex

Abstract

Modules of neurons sharing a common property are a basic organizational feature of mammalian sensory cortex. Primary visual cortex (V1) is characterized by orientation modules—groups of cells that share a preferred stimulus orientation—which are organized into a highly ordered orientation map. Here we show that in ferrets in which retinal projections are routed into the auditory pathway, visually responsive neurons in ‘rewired’ primary auditory cortex are also organized into orientation modules. The orientation tuning of neurons within these modules is comparable to the tuning of cells in V1 but the orientation map is less orderly. Horizontal connections in rewired cortex are more patchy and periodic than connections in normal auditory cortex, but less so than connections in V1. These data show that afferent activity has a profound influence on diverse components of cortical circuitry, including thalamocortical and local intracortical connections, which are involved in the generation of orientation tuning, and long-range horizontal connections, which are important in creating an orientation map.

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Figure 1: Orientation maps in ‘rewired’ A1 and normal V1.
Figure 2: Optically imaged orientation maps and single cell responses in rewired ferret auditory cortex.
Figure 3: Patterns of long-range horizontal connections in V1, normal A1 and rewired A1.
Figure 4: Correlation of optical imaging maps with intrinsic horizontal connections in normal V1 and rewired A1.
Figure 5: The periodicity of horizontal connections in normal V1, normal A1 and rewired A1.

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Acknowledgements

We thank C. Rao and B. Sheth for participating in early experiments; G. Kalarickal for help in aggregation index calculations; J. Schummers for help with matlab; C. Leamey for an injection case; T. McHugh for technical assistance; R. Marini for veterinary care; and C. Moore, C. Hohnke, A. Lykman, V. Dragoi and C. Rivadulla for comments on the manuscript. We also thank T. Bonhoeffer and S. Lowel for being instrumental in initiating this work. Supported by grants from the NIH (M.S).

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Sharma, J., Angelucci, A. & Sur, M. Induction of visual orientation modules in auditory cortex. Nature 404, 841–847 (2000). https://doi.org/10.1038/35009043

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