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Nonlinear Gap Junctions Enable Long-Distance Propagation of Pulsating Calcium Waves in Astrocyte Networks

2010/08/26 by Mati Goldberg, Maurizio De Pittà, Vladislav Volman +3 · 113 citations
Biochemistry, Genetics and Molecular Biology · Neuroscience · Physics and Astronomy · #Astrocyte #Biology #Calcium signaling #Cell #Cell biology #Central nervous system #Connexins and lens biology #Coupling (piping) #Gap junction #Inositol #Inositol trisphosphate #Intracellular #Materials science #Neural dynamics and brain function #Neuroscience #Nonlinear system #Photoreceptor and optogenetics research #Physics #Receptor #Syncytium #nlin.CD #q-bio.CB #q-bio.NC

paper · pdf · doi:10.1371/journal.pcbi.1000909

published in PLoS Computational Biology 6(8), e1000909 (Public Library of Science) · Article: 30 pages, 7 figures. Supplementary Material: 11 pages, 6 figures

openalex publication_date 2010/08/26 · arxiv created 2010/09/12 · arxiv updated 2010/09/14 · openalex created_date 2025/10/10 · openalex updated_date 2026/08/06

Abstract

A new paradigm has recently emerged in brain science whereby communications between glial cells and neuron-glia interactions should be considered together with neurons and their networks to understand higher brain functions. In particular, astrocytes, the main type of glial cells in the cortex, have been shown to communicate with neurons and with each other. They are thought to form a gap-junction-coupled syncytium supporting cell-cell communication via propagating Ca(2+) waves. An identified mode of propagation is based on cytoplasm-to-cytoplasm transport of inositol trisphosphate (IP(3)) through gap junctions that locally trigger Ca(2+) pulses via IP(3)-dependent Ca(2+)-induced Ca(2+) release. It is, however, currently unknown whether this intracellular route is able to support the propagation of long-distance regenerative Ca(2+) waves or is restricted to short-distance signaling. Furthermore, the influence of the intracellular signaling dynamics on intercellular propagation remains to be understood. In this work, we propose a model of the gap-junctional route for intercellular Ca(2+) wave propagation in astrocytes. Our model yields two major predictions. First, we show that long-distance regenerative signaling requires nonlinear coupling in the gap junctions. Second, we show that even with nonlinear gap junctions, long-distance regenerative signaling is favored when the internal Ca(2+) dynamics implements frequency modulation-encoding oscillations with pulsating dynamics, while amplitude modulation-encoding dynamics tends to restrict the propagation range. As a result, spatially heterogeneous molecular properties and/or weak couplings are shown to give rise to rich spatiotemporal dynamics that support complex propagation behaviors. These results shed new light on the mechanisms implicated in the propagation of Ca(2+) waves across astrocytes and the precise conditions under which glial cells may participate in information processing in the brain.

Citations