Learning excitatory-inhibitory neuronal assemblies in recurrent networks.

Owen Mackwood,Henning Sprekeler,Laura B Naumann

doi:10.7554/elife.59715

Abstract

Understanding the connectivity observed in the brain and how it emerges from local plasticity rules is a grand challenge in modern neuroscience. In the primary visual cortex (V1) of mice, synapses between excitatory pyramidal neurons and inhibitory parvalbumin-expressing (PV) interneurons tend to be stronger for neurons that respond to similar stimulus features, although these neurons are not topographically arranged according to their stimulus preference. The presence of such excitatory-inhibitory (E/I) neuronal assemblies indicates a stimulus-specific form of feedback inhibition. Here, we show that activity-dependent synaptic plasticity on input and output synapses of PV interneurons generates a circuit structure that is consistent with mouse V1. Computational modeling reveals that both forms of plasticity must act in synergy to form the observed E/I assemblies. Once established, these assemblies produce a stimulus-specific competition between pyramidal neurons. Our model suggests that activity-dependent plasticity can refine inhibitory circuits to actively shape cortical computations.

Highlights

With the advent of modern optogenetics, the functional role of inhibitory interneurons has developed into one of the central topics of systems neuroscience (Fishell and Kepecs, 2020)
To understand which activity-dependent mechanisms can generate specific feedback inhibition in circuits without feature topography—such as mouse V1 (Figure 1a), we studied a rate-based network model consisting of NE 1⁄4 512 excitatory Pyr neurons and NI 1⁄4 64 inhibitory PV neurons
To endow the excitatory neurons with a stimulus tuning similar to Pyr cells in layer 2/3 of mouse V1 (Znamenskiy et al, 2018), each excitatory neuron receives external excitatory input that is tuned to orientation, temporal frequency and spatial frequency (Figure 1b)

Summary

Introduction

With the advent of modern optogenetics, the functional role of inhibitory interneurons has developed into one of the central topics of systems neuroscience (Fishell and Kepecs, 2020). Excitatory and inhibitory currents are often highly correlated in their response to stimuli (Wehr and Zador, 2003; Froemke et al, 2007; Tan et al, 2011; Bhatia et al, 2019), in time (Okun and Lampl, 2008; Dipoppa et al, 2018) and across neurons (Xue et al, 2014). These mutual preferences in synaptic organisation suggest that feedback inhibition may be more stimulus-specific than previously thought and that Pyr and PV neurons form specialised—albeit potentially overlapping—excitatory-inhibitory (E/I) assemblies (Chenkov et al, 2017; Yoshimura et al, 2005; Litwin-Kumar and Doiron, 2012; LitwinKumar and Doiron, 2014). Synergistic plasticity of the incoming and outgoing synapses of PV interneurons can drive the development of stimulusspecific feedback inhibition, resulting in a competition between Pyr neurons with similar stimulus preference

Results

Discussion

Materials and methods

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