The Interaction of Intrinsic Dynamics and Network Topology in Determining Network Burst Synchrony

Chris Gaiteri,Jonathan E Rubin

doi:10.3389/fncom.2011.00010

Abstract

The pre-Bötzinger complex (pre-BötC), within the mammalian respiratory brainstem, represents an ideal system for investigating the synchronization properties of complex neuronal circuits via the interaction of cell-type heterogeneity and network connectivity. In isolation, individual respiratory neurons from the pre-BötC may be tonically active, rhythmically bursting, or quiescent. Despite this intrinsic heterogeneity, coupled networks of pre-BötC neurons en bloc engage in synchronized bursting that can drive inspiratory motor neuron activation. The region's connection topology has been recently characterized and features dense clusters of cells with occasional connections between clusters. We investigate how the dynamics of individual neurons (quiescent/bursting/tonic) and the betweenness centrality of neurons’ positions within the network connectivity graph interact to govern network burst synchrony, by simulating heterogeneous networks of computational model pre-BötC neurons. Furthermore, we compare the prevalence and synchrony of bursting across networks constructed with a variety of connection topologies, analyzing the same collection of heterogeneous neurons in small-world, scale-free, random, and regularly structured networks. We find that several measures of network burst synchronization are determined by interactions of network topology with the intrinsic dynamics of neurons at central network positions and by the strengths of synaptic connections between neurons. Surprisingly, despite the functional role of synchronized bursting within the pre-BötC, we find that synchronized network bursting is generally weakest when we use its specific connection topology, which leads to synchrony within clusters but poor coordination across clusters. Overall, our results highlight the relevance of interactions between topology and intrinsic dynamics in shaping the activity of networks and the concerted effects of connectivity patterns and dynamic heterogeneities.

Highlights

Synchronized activity in the pre-Bötzinger complex in the mammalian respiratory brainstem occurs during the inspiratory phase of respiration and drives motoneurons responsible for inspiratory muscle movements (Feldman and Del Negro, 2006)
Our overarching goal was to determine how network topology and intrinsic cell dynamics affect a network’s capacity to generate synchronized bursting activity. To address this broad question, we present results based on which topologies, cell-type hierarchies, and synaptic coupling levels generated network bursts most successfully and how these three main factors interact
The SW concept of low path-length and high clustering, for example, has repeatedly been linked to efficient information transfer and swift network synchronization. How these results relate to the performance of other topologies in networks with realistic cellular dynamics and heterogeneities is rarely explored

Summary

Introduction

Synchronized activity in the pre-Bötzinger complex (pre-BötC) in the mammalian respiratory brainstem occurs during the inspiratory phase of respiration and drives motoneurons responsible for inspiratory muscle movements (Feldman and Del Negro, 2006). Using a combination of neuron-specific staining and calcium imaging, Hartelt et al (2008) identified a highly structured topology of synaptic connections among cells in slice preparations derived from the pre-BötC. In this network, cells were spatially grouped into local clusters with a high prevalence of intra-cluster connections. Cells were spatially grouped into local clusters with a high prevalence of intra-cluster connections These clusters had a defined membership size distribution and were connected via relatively rare inter-cluster links. The main goal of this paper is to computationally explore particular aspects of this hypothesis

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