Superficial layer pyramidal cells communicate heterogeneously between multiple functional domains of cat primary visual cortex.

Kevan A C Martin,Stephan Roth,Elisha S Rusch

doi:10.1038/ncomms6252

Kevan A C Martin, Stephan Roth + Show 1 more

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https://doi.org/10.1038/ncomms6252

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Abstract

The axons of pyramidal neurons in the superficial layers of the neocortex of higher mammals form lateral networks of discrete clusters of synaptic boutons. In primary visual cortex the clusters are reported to link domains that share the same orientation preferences, but how individual neurons contribute to this network is unknown. Here we performed optical imaging to record the intrinsic signal, which is an indirect measure of neuronal firing, and determined the global map of orientation preferences in the cat primary visual system. In the same experiment, single cells were recorded and labelled intracellularly. We found that individual axons arborise within the retinotopic representation of the classical receptive field, but their bouton clusters were not aligned along their preferred axis of orientation along the retinotopic map. Axon clusters formed in a variety of different orientation domains, not just the like-orientation domains. This topography and heterogeneity of single-cell connectivity provides circuits for normalization and context-dependent feature processing of visual scenes.

Highlights

The axons of pyramidal neurons in the superficial layers of the neocortex of higher mammals form lateral networks of discrete clusters of synaptic boutons
After fine-grained three-dimensional (3D) reconstruction of 33 neurons, we found that all neurons formed anisotropic lateral projections that covered only a few degrees of visual field representation on the cortex, matching the size of the classical receptive field (RF)
Of 153 impaled neurons 50 were ‘bestfills’, but after excluding neurons associated with indifferent optical imaging maps, we arrived at a final data set of neurons

Summary

Introduction

The axons of pyramidal neurons in the superficial layers of the neocortex of higher mammals form lateral networks of discrete clusters of synaptic boutons. In primary visual cortex the clusters are reported to link domains that share the same orientation preferences, but how individual neurons contribute to this network is unknown. Axon clusters formed in a variety of different orientation domains, not just the likeorientation domains This topography and heterogeneity of single-cell connectivity provides circuits for normalization and context-dependent feature processing of visual scenes. T he neocortex is thought to be constructed of a system of radial ‘columns’ that form the functional units of cortex[1] In higher mammals these columns are interlinked by lateral excitatory connections that form a patchy network known as the cortical ‘daisy’[2,3]. The pyramidal cells in the superficial layers of cat V1 are more richly recurrently connected with each other than neurons in any other layer[8], and so ‘like-to-like’ would generate a hazardous positive feedback unless it were balanced with strong inhibition[9], which seems not to be present

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