Emergence of Connectivity Motifs in Networks of Model Neurons with Short- and Long-Term Plastic Synapses

Eleni Vasilaki,Michele Giugliano

doi:10.1371/journal.pone.0084626

Eleni Vasilaki, Michele Giugliano

Open Access

https://doi.org/10.1371/journal.pone.0084626

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Journal: PLoS ONE	Publication Date: Jan 15, 2014
Citations: 105	License type: CC BY 4.0

Affiliation: University of Sheffield, University of Antwerp

Abstract

Recent experimental data from the rodent cerebral cortex and olfactory bulb indicate that specific connectivity motifs are correlated with short-term dynamics of excitatory synaptic transmission. It was observed that neurons with short-term facilitating synapses form predominantly reciprocal pairwise connections, while neurons with short-term depressing synapses form predominantly unidirectional pairwise connections. The cause of these structural differences in excitatory synaptic microcircuits is unknown. We show that these connectivity motifs emerge in networks of model neurons, from the interactions between short-term synaptic dynamics (SD) and long-term spike-timing dependent plasticity (STDP). While the impact of STDP on SD was shown in simultaneous neuronal pair recordings in vitro, the mutual interactions between STDP and SD in large networks are still the subject of intense research. Our approach combines an SD phenomenological model with an STDP model that faithfully captures long-term plasticity dependence on both spike times and frequency. As a proof of concept, we first simulate and analyze recurrent networks of spiking neurons with random initial connection efficacies and where synapses are either all short-term facilitating or all depressing. For identical external inputs to the network, and as a direct consequence of internally generated activity, we find that networks with depressing synapses evolve unidirectional connectivity motifs, while networks with facilitating synapses evolve reciprocal connectivity motifs. We then show that the same results hold for heterogeneous networks, including both facilitating and depressing synapses. This does not contradict a recent theory that proposes that motifs are shaped by external inputs, but rather complements it by examining the role of both the external inputs and the internally generated network activity. Our study highlights the conditions under which SD-STDP might explain the correlation between facilitation and reciprocal connectivity motifs, as well as between depression and unidirectional motifs.

Highlights

Our higher cognitive functions and our memories are believed to be encoded in the wiring diagram of the brain
The key mechanisms in this finding are (i) the synaptic dynamics (SD), which results in networks with facilitating synapses to fire at higher rates than networks with depressing synapses, and (ii) the long-lasting potentiation components (LTP) of the spike-timing dependent plasticity (STDP), which above a critical firing frequency threshold prevail over the depression components (LTD), regardless of temporal correlations as observed experimentally by Sjoestrom et al (2001)
As in [14] and [2], we focus on stereotypical motifs of strong synaptic efficacies among weak links between recurrently connected neurons, and study how the values of synaptic coupling become large enough that the internal dynamics of the network dominates over external inputs

Summary

Introduction

Our higher cognitive functions and our memories are believed to be encoded in the wiring diagram of the brain. The technological efforts and the recent initiatives in mapping and understanding the emergence and development of this diagram, the ‘‘connectome’’ [1], undoubtedly represent the cutting edge of research in neuroscience and are confronted with many challenges. Studies at the microcircuit level revealed that connectivity is non-random [2,3] and, in particular, specific cellular connectivity motifs have been found in percentages well above chance level Some of these studies have been able to provide physiological information about the neurons and synapses that are involved in the formation of such motifs [2,3,4,5]. These physiological details are of great significance, as the transmission of information between neurons takes place by means of more than mere ‘‘connectors.’’ For instance, synaptic efficacy undergoes short-term dynamics (SD), quantified as transient and reversible facilitation or depression of postsynaptic responses, upon repeated presynaptic activation [6,12]

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