Synaptic polarity of the interneuron circuit controlling C. elegans locomotion

Franciszek Rakowski,Jan Karbowski,Jagan Srinivasan,Paul W Sternberg

doi:10.3389/fncom.2013.00128

Abstract

Caenorhabditis elegans is the only animal for which a detailed neural connectivity diagram has been constructed. However, synaptic polarities in this diagram, and thus, circuit functions are largely unknown. Here, we deciphered the likely polarities of seven pre-motor neurons implicated in the control of worm's locomotion, using a combination of experimental and computational tools. We performed single and multiple laser ablations in the locomotor interneuron circuit and recorded times the worms spent in forward and backward locomotion. We constructed a theoretical model of the locomotor circuit and searched its all possible synaptic polarity combinations and sensory input patterns in order to find the best match to the timing data. The optimal solution is when either all or most of the interneurons are inhibitory and forward interneurons receive the strongest input, which suggests that inhibition governs the dynamics of the locomotor interneuron circuit. From the five pre-motor interneurons, only AVB and AVD are equally likely to be excitatory, i.e., they have probably similar number of inhibitory and excitatory connections to distant targets. The method used here has a general character and thus can be also applied to other neural systems consisting of small functional networks.

Highlights

Caenorhabditis elegans nematode worms possess a very small nervous system composed of only 302 neurons connected by about 5000 chemical synapses and 3000 gap junctions (White et al, 1986)
It was proposed that mammalian cortical networks operate in a dynamic state in which excitation is effectively balanced by inhibition (Haider et al, 2006; Vogels et al, 2011), anatomical number of excitatory connections dominates over inhibitory in the cerebral cortex (DeFelipe et al, 2002)
The strength of the connection between two arbitrary neurons is proportional to the number of anatomical contacts between them determined from the empirical data (Chen et al, 2006)

Summary

Introduction

Caenorhabditis elegans nematode worms possess a very small nervous system composed of only 302 neurons connected by about 5000 chemical synapses and 3000 gap junctions (White et al, 1986). Because of its smallness a precise map of neural connections was possible to construct (White et al, 1986; Chen et al, 2006) This places C. elegans in a unique position among all other animals (Varshney et al, 2011), for which we have at best only rudimentary connectivity data to test various concepts regarding neural wiring and function (Cherniak, 1994; Karbowski, 2001, 2003; Chklovskii, 2004; Chen et al, 2006; Kaiser and Hilgetag, 2006). We think that this topic deserves more attention both theoretical and experimental, if we are to understand the functioning of worm’s circuits (Gray et al, 2005; Sengupta and Samuel, 2009; Ha et al, 2010)

Objectives

Methods

Results

Conclusion