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Volume 17, Number 6, Issue of March 15, 1997 pp. 2112-2127
Copyright ©1997 Society for NeuroscienceOrientation Selectivity and the Arrangement of Horizontal Connections in Tree Shrew Striate Cortex
Received Aug. 5, 1996; revised Dec. 9, 1996; accepted Dec. 12, 1996.
William H. Bosking, Ying Zhang, Brett Schofield, and David Fitzpatrick Department of Neurobiology, Duke University Medical Center, Durham, North Carolina 27710
Horizontal connections, formed primarily by the axon collaterals of pyramidal neurons in layer 2/3 of visual cortex, extend for millimeters parallel to the cortical surface and form patchy terminations. Previous studies have provided evidence that the patches formed by horizontal connections exhibit modular specificity, preferentially linking columns of neurons with similar response characteristics, such as preferred orientation. The issue of how these connections are distributed with respect to the topographic map of visual space, however, has not been resolved. Here we combine optical imaging of intrinsic signals with small extracellular injections of biocytin to assess quantitatively the specificity of horizontal connections with respect to both the map of orientation preference and the map of visual space in tree shrew V1. Our results indicate that horizontal connections outside a radius of 500 µm from the injection site exhibit not only modular specificity, but also specificity for axis of projection. Labeled axons extend for longer distances, and give off more terminal boutons, along an axis in the map of visual space that corresponds to the preferred orientation of the injection site. Inside of 500 µm, the pattern of connections is much less specific, with boutons found along every axis, contacting sites with a wide range of preferred orientations. The system of long-range horizontal connections can be summarized as preferentially linking neurons with co-oriented, co-axially aligned receptive fields. These observations suggest specific ways that horizontal circuits contribute to the response properties of layer 2/3 neurons and to mechanisms of visual perception.
Key words: orientation selectivity; topography; optical imaging; visual cortex; surround effects; tree shrew; biocytin; horizontal connections
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