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Sparse short-distance connections enhance calcium wave propagation in a 3D model of astrocyte networks.

ABSTRACT: Traditionally, astrocytes have been considered to couple via gap-junctions into a syncytium with only rudimentary spatial organization. However, this view is challenged by growing experimental evidence that astrocytes organize as a proper gap-junction mediated network with more complex region-dependent properties. On the other hand, the propagation range of intercellular calcium waves (ICW) within astrocyte populations is as well highly variable, depending on the brain region considered. This suggests that the variability of the topology of gap-junction couplings could play a role in the variability of the ICW propagation range. Since this hypothesis is very difficult to investigate with current experimental approaches, we explore it here using a biophysically realistic model of three-dimensional astrocyte networks in which we varied the topology of the astrocyte network, while keeping intracellular properties and spatial cell distribution and density constant. Computer simulations of the model suggest that changing the topology of the network is indeed sufficient to reproduce the distinct ranges of ICW propagation reported experimentally. Unexpectedly, our simulations also predict that sparse connectivity and restriction of gap-junction couplings to short distances should favor propagation while long-distance or dense connectivity should impair it. Altogether, our results provide support to recent experimental findings that point toward a significant functional role of the organization of gap-junction couplings into proper astroglial networks. Dynamic control of this topology by neurons and signaling molecules could thus constitute a new type of regulation of neuron-glia and glia-glia interactions.

SUBMITTER: Lallouette J

PROVIDER: S-EPMC3997029 | biostudies-literature | 2014

REPOSITORIES: biostudies-literature

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Sparse short-distance connections enhance calcium wave propagation in a 3D model of astrocyte networks.

Lallouette Jules J De Pittà Maurizio M Ben-Jacob Eshel E Berry Hugues H

Frontiers in computational neuroscience 20140416

Traditionally, astrocytes have been considered to couple via gap-junctions into a syncytium with only rudimentary spatial organization. However, this view is challenged by growing experimental evidence that astrocytes organize as a proper gap-junction mediated network with more complex region-dependent properties. On the other hand, the propagation range of intercellular calcium waves (ICW) within astrocyte populations is as well highly variable, depending on the brain region considered. This su ...[more]

PMID: 24795613

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Project description: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.

Project description:ObjectiveTo determine whether there is a "dose-dependent" relationship between coronary atherosclerosis and the burden of exercise.BackgroundRecent data have suggested there may be negative consequences related to strenuous exercise. Previous studies evaluating the presence of coronary atherosclerosis as assessed by coronary calcium scores have been confounded by the presence of other cardiovascular risk factors. We aimed to assess whether there was a relationship between the burden of coronary calcium and the amount of running in a local cohort.Patients and methodsEighty-five runners were screened on the basis of an exercise questionnaire that was later used to determine the experimental groups from January 2016 through October 2016. Twenty-nine individuals were excluded from the study because of the presence of preexisting cardiovascular risk factors. Runners were divided into 3 categories: Group A comprised runners who had competed in at least 10 ultramarathons and/or Ironman competitions in 10 years. Group B included runners who had participated in more than 9 marathons over 10 years. Group C comprised runners who had competed in more than 9 shorter races over 10 years. Coronary artery calcium (CAC) scores were assessed by computed tomography. Statistical analysis was performed using chi-square analyses. Logistic regression models were used to assess the relationship between runner groups and calcium score greater than 100, calcium score percentile, and calcium score greater than 0.ResultsThere were no differences between groups A and B for CAC scores greater than 0 or greater than 100, and a similar percentage of group A and B athletes had scores greater than the 50th percentile. Groups A and B were combined for further analysis. Among those runners participating in extreme distance running (groups A and B), 73% of runners had CAC scores greater than 0 whereas only 21% of group C runners had CAC scores greater than 0 (P=.0002). Moreover, 70% of group A + B athletes ranked above the 50th percentile of their age and sex as assessed by a national database (Hoff JA, Chomka EV, Krainik AJ, Daviglus M, Rich S, Kondos GT. Age and gender distributions of coronary artery calcium detected by electron beam tomography in 35,246 adults. Am J Cardiol. 2001;87(12):1335-1339), whereas only 19% of group C runners were ranked above the 50th percentile (P=.0001). One-third of runners in group A + B had CAC scores greater than 100 as compared with only 12% of runners in group C (P=.05). When controlling for age, sex, and number of years running, the study group was not a significant predictor of CAC greater than 100 (P=.12). In contrast, group A + B was 10 times more likely than group C to have CAC scores in the 50th percentile or greater (P=.02) and 8.8 times more likely to have a abnormal calcium score when controlling for covariates (P=.03).ConclusionA significantly higher rate of coronary artery calcification existed in long-term marathon, ultramarathon, and extreme runners than in submarathon runners. Marathoners and ultramarathoners also had a higher incidence of calcification, as well as higher average plaque burden, as compared to a standard database. Marathoners and ultramarathoners also had above-average coronary calcium scores as compared to a national database.

Dataset Information

Sparse short-distance connections enhance calcium wave propagation in a 3D model of astrocyte networks.

Publications

Sparse short-distance connections enhance calcium wave propagation in a 3D model of astrocyte networks.

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