Origins of the Embryo: Self-organization through cybernetic regulation

Stone, Robert B.; Portegys, Tom; Mikhailovsky, George; Alicea, Bradly

doi:10.1016/j.biosystems.2018.08.005

“…A first-mover model is meant to capture the process of growth, differentiation, and associated interactions defining the transition from emerging structure to organized function ( Vogelstein et al, 2019 ). The first-mover model of Stackelberg competition was first applied to developmental systems in Stone et al (2018) , and is used here to represent the evolution of interactions between the emergence of newly born neurons, asymmetric ion channel expression amongst bilateral pairs, and the formation of neural circuits.…”

Section: Introductionmentioning

confidence: 99%

Raising the Connectome: The Emergence of Neuronal Activity and Behavior in Caenorhabditis elegans

Alicea

¹

2020

Front. Cell. Neurosci.

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The differentiation of neurons and formation of connections between cells is the basis of both the adult phenotype and behaviors tied to cognition, perception, reproduction, and survival. Such behaviors are associated with local (circuits) and global (connectome) brain networks. A solid understanding of how these networks emerge is critical. This opinion piece features a guided tour of early developmental events in the emerging connectome, which is crucial to a new view on the connectogenetic process. Connectogenesis includes associating cell identities with broader functional and developmental relationships. During this process, the transition from developmental cells to terminally differentiated cells is defined by an accumulation of traits that ultimately results in neuronal-driven behavior. The well-characterized developmental and cell biology of Caenorhabditis elegans will be used to build a synthesis of developmental events that result in a functioning connectome. Specifically, our view of connectogenesis enables a first-mover model of synaptic connectivity to be demonstrated using data representing larval synaptogenesis. In a first-mover model of Stackelberg competition, potential pre- and postsynaptic relationships are shown to yield various strategies for establishing various types of synaptic connections. By comparing these results to what is known regarding principles for establishing complex network connectivity, these strategies are generalizable to other species and developmental systems. In conclusion, we will discuss the broader implications of this approach, as what is presented here informs an understanding of behavioral emergence and the ability to simulate related biological phenomena.

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“…By contrast, a few long-distance movements in a background of shorter migrations suggests that there are regulative mechanisms at work, particularly as they are related to sublineage-specific function (Wiegner & Schierenberg, 1999). Such superdiffusive processes (Deterich et al, 2008) have been shown in other cellular systems to be the signature of non-Brownian noise, which in turn contributes to spatial order through selective positioning (Stone et al, 2018). Diffusion in the early embryo can be informative in terms of how cells move and ultimately position themselves during embryogenesis (Woods et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

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Supplemental Information 1: Supplemental File 1: Circular Network Topologies Comparing Connections Among Subtrees and Tree Leve

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One overarching principle of eukaroytic development is the generative spatial emergence and self-organization of cell populations. As cells divide and differentiate, they and their descendants form a spatiotemporally explicit and increasingly compartmentalized complex system. Yet despite this compartmentalization, there is selective functional overlap between these structural components. While contemporary tools such as lineage trees and molecular signaling networks provide a window into this complexity, they do not characterize embryogenesis as a global process. Using a four-dimensional spatial representation, major features of the developmental process are revealed. To establish the role of developmental mechanisms that turn a spherical embryo into a highly asymmetrical adult phenotype, we can map the outcomes of the cell division process to a complex network model. This type of representational model provides information about the top-down mechanisms relevant to the differentiation process. In a complementary manner, looking for phenomena such as superdiffusive positioning and sublineage-based anatomical clustering incorporates dynamic information to our parallel view of embryogenesis. Characterizing the spatial organization and geometry of embryos in this way allows for novel indicators of developmental patterns both within and between organisms.PeerJ Preprints | https://doi.org/10.7287/peerj.preprints.26587v2 | CC BY 4.0 Open Access | rec: ABSTRACTOne overarching principle of eukaroytic development is the generative spatial emergence and self-organization of cell populations. As cells divide and differentiate, they and their descendants form a spatiotemporally explicit and increasingly compartmentalized complex system. Yet despite this compartmentalization, there is selective functional overlap between these structural components. While contemporary tools such as lineage trees and molecular signaling networks provide a window into this complexity, they do not characterize embryogenesis as a global process. Using a four-dimensional spatial representation, major features of the developmental process are revealed. To establish the role of developmental mechanisms that turn a spherical embryo into a highly asymmetrical adult phenotype, we can map the outcomes of the cell division process to a complex network model. This type of representational model provides information about the top-down mechanisms relevant to the differentiation process. In a complementary manner, looking for phenomena such as superdiffusive positioning and sublineage-based anatomical clustering incorporates dynamic information to our parallel view of embryogenesis. Characterizing the spatial organization and geometry of embryos in this way allows for novel indicators of developmental patterns both within and between organisms.

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“…By contrast, a few long-distance movements in a background of shorter migrations suggests that there are regulative mechanisms at work, particularly as they are related to sublineage-specific function (Wiegner & Schierenberg, 1999). Such superdiffusive processes (Deterich et al, 2008) have been shown in other cellular systems to be the signature of non-Brownian noise, which in turn contributes to spatial order through selective positioning (Stone et al, 2018). Diffusion in the early embryo can be informative in terms of how cells move and ultimately position themselves during embryogenesis (Woods et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

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Supplemental Information 3: Supplemental File 3

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One overarching principle of eukaroytic development is the generative spatial emergence and self-organization of cell populations. As cells divide and differentiate, they and their descendants form a spatiotemporally explicit and increasingly compartmentalized complex system. Yet despite this compartmentalization, there is selective functional overlap between these structural components. While contemporary tools such as lineage trees and molecular signaling networks provide a window into this complexity, they do not characterize embryogenesis as a global process. Using a four-dimensional spatial representation, major features of the developmental process are revealed. To establish the role of developmental mechanisms that turn a spherical embryo into a highly asymmetrical adult phenotype, we can map the outcomes of the cell division process to a complex network model. This type of representational model provides information about the top-down mechanisms relevant to the differentiation process. In a complementary manner, looking for phenomena such as superdiffusive positioning and sublineage-based anatomical clustering incorporates dynamic information to our parallel view of embryogenesis. Characterizing the spatial organization and geometry of embryos in this way allows for novel indicators of developmental patterns both within and between organisms.

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Origins of the Embryo: Self-organization through cybernetic regulation

Cited by 10 publications

References 90 publications

Raising the Connectome: The Emergence of Neuronal Activity and Behavior in Caenorhabditis elegans

Raising the Connectome: The Emergence of Neuronal Activity and Behavior in Caenorhabditis elegans

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