Fast Recruitment of Recurrent Inhibition in the Cat Visual Cortex

Ora Ohana,Hanspeter Portner,Kevan A C Martin

doi:10.1371/journal.pone.0040601

Abstract

Neurons of the same column in L4 of the cat visual cortex are likely to share the same sensory input from the same region of the visual field. Using visually-guided patch clamp recordings we investigated the biophysical properties of the synapses of neighboring layer 4 neurons. We recorded synaptic connections between all types of excitatory and inhibitory neurons in L4. The E–E, E–I, and I–E connections had moderate CVs and failure rates. However, E–I connections had larger amplitudes, faster rise-times, and shorter latencies. Identification of the sites of putative synaptic contacts together with compartmental simulations on 3D reconstructed cells, suggested that E–I synapses tended to be located on proximal dendritic branches, which would explain their larger EPSP amplitudes and faster kinetics. Excitatory and inhibitory synapses were located at the same distance on distal dendrites of excitatory neurons. We hypothesize that this co-localization and the fast recruitment of local inhibition provides an efficient means of modulating excitation in a precisely timed way.

Highlights

The aim of this study was to describe the statistical and kinetic properties of synaptic connections in layer 4 of the cat’s primary visual cortex
In this experiment a presumed spiny stellate neuron was selected, based on its relatively small and quadratic appearance, while the presumed smooth neuron was selected based on its round shape and the stubby short dendrite emerging from the soma
Measured IPSP reversal potentials in different experiments ranged between – 56 mV and –83 mV with an average at –6969 mV (n = 8), but were not positively correlated with the theoretical Cl2 reversal potential (Correlations Coeff. = 20.37). These results indicate that either the [Cl2] at the dendritic synaptic locations is not well clamped by the pipette ([Cl2]), possibly due to dominant local Cl2 homeostasis at the dendrites, or, the depolarized IPSP reversal potential reflects a mixed flux of Cl2 and hydrocarbonate ([HCO32]i) ions through the GABAA receptor-linked channels [29,30,31,32,33], which are permeable to both anions

Summary

Introduction

The aim of this study was to describe the statistical and kinetic properties of synaptic connections in layer 4 of the cat’s primary visual cortex. Previous studies of the physiological properties of intracortical synapses in layer 4 of the cat visual cortex revealed a network of moderately strong and variable excitatory synapses but highly reliable inhibitory synapses [6,7,8,9,10,11,12,13]. These findings strengthen the hypothesis that the recurrent excitatory connections act to amplify the transient thalamic input, while the recurrent inhibition serves to balance the excitation and prevent runaway excitation [14,15]

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Conclusion