Synaptic connections formed by patchy projections of pyramidal cells in the superficial layers of cat visual cortex

German Koestinger,Elisha S Rusch,Kevan A C Martin,Stephan Roth

doi:10.1007/s00429-017-1384-4

German Koestinger, Elisha S Rusch + Show 2 more

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https://doi.org/10.1007/s00429-017-1384-4

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Abstract

The present study is the first to describe quantitatively the patterns of synaptic connections made by the patchy network of pyramidal cell axons in the superficial layers of cat V1 in relation to the orientation map. Intrinsic signal imaging of the orientation map was combined with 3D morphological reconstructions of physiologically-characterized neurons at light and electron microscope levels. A Similarity Index (SI) expressed the similarity of the orientation domain of a given bouton cluster to that of its parent dendritic tree. Six pyramidal cells whose axons had a wide range of SIs were examined. Boutons were sampled from five local and five distal clusters, and from the linear segments that link the clusters. The synaptic targets were reconstructed by serial section electron microscopy. Of the 233 synapses examined, 182 synapses were formed with spiny neurons, the remainder with smooth neurons. The proportion of smooth neurons that were synaptic targets varied greatly (from 0 to 50%) between the cluster samples, but was not correlated with the SI. The postsynaptic density sizes were similar for synapses in local and distal clusters, regardless of their SI. This heterogeneity in the synaptic targets of single cells within the superficial layers is a network feature well-suited for context-dependent processing.

Highlights

For Hubel and Wiesel (Hubel and Wiesel 1962), the radial cortical column is the ‘functional unit of cortex’ that most economically achieves the highly specific wiring needed to generate simple and complex cells in different layers
To reduce potential ambiguities in interpretation, we selected Similarity Index (SI) that represented the extremes of the index—i.e., clusters that were located in orientation domains that were very similar to the dendritic tree (SI > 0.65) or those located in very different domains (SI < 0.35) and not those with intermediate indices (0.35 < SI < 0.65)
While it is known that almost all axons in the white matter below V1 in adult cats are myelinated (Anderson et al 1992), little is currently known of the degree of myelination of axons that form the lateral pathways within a cortical area

Summary

Introduction

For Hubel and Wiesel (Hubel and Wiesel 1962), the radial cortical column is the ‘functional unit of cortex’ that most economically achieves the highly specific wiring needed to generate simple and complex cells in different layers. A common view is that the lateral connections link patches of common orientation preference, expressing a ‘like-to-like’ connection rule, achieved by means of a ‘fire-together-wire together’ mechanism (Gilbert and Wiesel 1989; Malach et al 1994; Bosking et al 1997; Sincich and Blasdel 2001) Given this consensus, we were surprised to discover that individual pyramidal cells in the superficial layers of the cat’s visual cortex form lateral clusters in a variety of orientation domains, including domains that were orthogonal to the parent cell’s preferred orientation (Martin et al 2014a). All of these receptive field properties require that pyramidal cells lying some distance apart in the

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