Pyramidal cells make specific connections onto smooth (GABAergic) neurons in mouse visual cortex.

Rita Bopp,Morgane M Roth,Kevan A C Martin,Nuno Maçarico Da Costa,Björn M Kampa

doi:10.1371/journal.pbio.1001932

Rita Bopp, Morgane M Roth + Show 3 more

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https://doi.org/10.1371/journal.pbio.1001932

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Abstract

Author SummaryThe mammalian visual cortex, which is part of the cerebral cortex, contains 50 to 100 thousands of neurons per cubic millimetre, most of which are excitatory (85%) and the minority, inhibitory (15%). Unlike neurons in the retina, neurons in the visual cortex are preferentially activated by lines or edges of a particular orientation. This is termed a neuron's “orientation preference.” In the visual cortex of higher mammals like cats and monkeys, neurons that share an orientation preference are clustered in functional columns. However, in rodents like mice, orientation preferences are randomly distributed. In this study, we investigate whether the differences between columnar and non-columnar cortex is correlated with differences in the connectivity patterns between excitatory and inhibitory neurons. Using light and electron microscopy, we mapped the connectivity of pyramidal neurons—the primary excitatory neurons—in the superficial layers of the primary visual cortex (V1) of mice. Our results show that the ratio of excitatory-inhibitory neurons in mouse V1 is similar to that of cat or monkey V1, but in mouse V1 local pyramidal neurons target proportionately many more inhibitory neurons compared to what other studies found in cat or monkey. This difference may indicate the significance of inhibition in maintaining orientation selectivity in the non-columnar visual cortex of rodents like mice and is a distinct difference in the architecture of V1 between mice and higher mammals.

Highlights

The concept of the cortical ‘‘column’’ is one of the few organising principles for cortical circuits that we have, yet the characteristic orientation columns in the primary visual cortex (V1) of the cat and monkey appear to be completely absent in rodent V1
This is termed a neuron’s ‘‘orientation preference.’’ In the visual cortex of higher mammals like cats and monkeys, neurons that share an orientation preference are clustered in functional columns
We investigate whether the differences between columnar and non-columnar cortex is correlated with differences in the connectivity patterns between excitatory and inhibitory neurons

Summary

Introduction

The concept of the cortical ‘‘column’’ is one of the few organising principles for cortical circuits that we have, yet the characteristic orientation columns in the primary visual cortex (V1) of the cat and monkey appear to be completely absent in rodent V1. In place of the ordered maps of orientation seen in cat and monkey, the distribution of orientation preferences in rodent V1 appears to be essentially random [1,2,3]. This ‘‘salt-andpepper’’ arrangement in the rodent must reflect differences in the wiring of superficial layer neurons in rodents compared to cat and monkey. Another striking difference between V1 of mouse and those of cat and monkey is the tuning properties of inhibitory neurons. The large number of excitatory synapses per neuron in the mouse may require a stronger component of recurrent inhibition

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