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  • The Royal Society  (12)
  • Levin, Michael  (12)
  • 1
    Online Resource
    Online Resource
    Top-down models in biology: explanation and control of complex living systems above the molecular level
    The Royal Society ; 2016
    In:  Journal of The Royal Society Interface Vol. 13, No. 124 ( 2016-11), p. 20160555-
    Details
    In: Journal of The Royal Society Interface, The Royal Society, Vol. 13, No. 124 ( 2016-11), p. 20160555-
    Abstract: It is widely assumed in developmental biology and bioengineering that optimal understanding and control of complex living systems follows from models of molecular events. The success of reductionism has overshadowed attempts at top-down models and control policies in biological systems. However, other fields, including physics, engineering and neuroscience, have successfully used the explanations and models at higher levels of organization, including least-action principles in physics and control-theoretic models in computational neuroscience. Exploiting the dynamic regulation of pattern formation in embryogenesis and regeneration requires new approaches to understand how cells cooperate towards large-scale anatomical goal states. Here, we argue that top-down models of pattern homeostasis serve as proof of principle for extending the current paradigm beyond emergence and molecule-level rules. We define top-down control in a biological context, discuss the examples of how cognitive neuroscience and physics exploit these strategies, and illustrate areas in which they may offer significant advantages as complements to the mainstream paradigm. By targeting system controls at multiple levels of organization and demystifying goal-directed (cybernetic) processes, top-down strategies represent a roadmap for using the deep insights of other fields for transformative advances in regenerative medicine and systems bioengineering.
    Type of Medium: Online Resource
    ISSN: 1742-5689 , 1742-5662
    URL: Article
    DOI: 10.1098/rsif.2016.0555
    Language: English
    Publisher: The Royal Society
    Publication Date: 2016
    detail.hit.zdb_id: 2156283-0
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  • 2
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    Knowing one's place: a free-energy approach to pattern regulation
    The Royal Society ; 2015
    In:  Journal of The Royal Society Interface Vol. 12, No. 105 ( 2015-04), p. 20141383-
    Details
    In: Journal of The Royal Society Interface, The Royal Society, Vol. 12, No. 105 ( 2015-04), p. 20141383-
    Abstract: Understanding how organisms establish their form during embryogenesis and regeneration represents a major knowledge gap in biological pattern formation. It has been recently suggested that morphogenesis could be understood in terms of cellular information processing and the ability of cell groups to model shape. Here, we offer a proof of principle that self-assembly is an emergent property of cells that share a common (genetic and epigenetic) model of organismal form. This behaviour is formulated in terms of variational free-energy minimization—of the sort that has been used to explain action and perception in neuroscience. In brief, casting the minimization of thermodynamic free energy in terms of variational free energy allows one to interpret (the dynamics of) a system as inferring the causes of its inputs—and acting to resolve uncertainty about those causes. This novel perspective on the coordination of migration and differentiation of cells suggests an interpretation of genetic codes as parametrizing a generative model—predicting the signals sensed by cells in the target morphology—and epigenetic processes as the subsequent inversion of that model. This theoretical formulation may complement bottom-up strategies—that currently focus on molecular pathways—with (constructivist) top-down approaches that have proved themselves in neuroscience and cybernetics.
    Type of Medium: Online Resource
    ISSN: 1742-5689 , 1742-5662
    URL: Article
    DOI: 10.1098/rsif.2014.1383
    Language: English
    Publisher: The Royal Society
    Publication Date: 2015
    detail.hit.zdb_id: 2156283-0
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  • 3
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    From cytoskeletal dynamics to organ asymmetry: a nonlinear, regulative pathway underlies left–right patterning
    The Royal Society ; 2016
    In:  Philosophical Transactions of the Royal Society B: Biological Sciences Vol. 371, No. 1710 ( 2016-12-19), p. 20150409-
    Details
    In: Philosophical Transactions of the Royal Society B: Biological Sciences, The Royal Society, Vol. 371, No. 1710 ( 2016-12-19), p. 20150409-
    Abstract: Consistent left–right (LR) asymmetry is a fundamental aspect of the bodyplan across phyla, and errors of laterality form an important class of human birth defects. Its molecular underpinning was first discovered as a sequential pathway of left- and right-sided gene expression that controlled positioning of the heart and visceral organs. Recent data have revised this picture in two important ways. First, the physical origin of chirality has been identified; cytoskeletal dynamics underlie the asymmetry of single-cell behaviour and patterning of the LR axis. Second, the pathway is not linear: early disruptions that alter the normal sidedness of upstream asymmetric genes do not necessarily induce defects in the laterality of the downstream genes or in organ situs . Thus, the LR pathway is a unique example of two fascinating aspects of biology: the interplay of physics and genetics in establishing large-scale anatomy, and regulative (shape-homeostatic) pathways that correct molecular and anatomical errors over time. Here, we review aspects of asymmetry from its intracellular, cytoplasmic origins to the recently uncovered ability of the LR control circuitry to achieve correct gene expression and morphology despite reversals of key ‘determinant’ genes. We provide novel functional data, in Xenopus laevis , on conserved elements of the cytoskeleton that drive asymmetry, and comparatively analyse it together with previously published results in the field. Our new observations and meta-analysis demonstrate that despite aberrant expression of upstream regulatory genes, embryos can progressively normalize transcriptional cascades and anatomical outcomes. LR patterning can thus serve as a paradigm of how subcellular physics and gene expression cooperate to achieve developmental robustness of a body axis. This article is part of the themed issue ‘Provocative questions in left–right asymmetry’.
    Type of Medium: Online Resource
    ISSN: 0962-8436 , 1471-2970
    URL: Article
    DOI: 10.1098/rstb.2015.0409
    RVK:
    WA 15000
    Language: English
    Publisher: The Royal Society
    Publication Date: 2016
    detail.hit.zdb_id: 1462620-2
    SSG: 12
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  • 4
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    Introduction to provocative questions in left–right asymmetry
    The Royal Society ; 2016
    In:  Philosophical Transactions of the Royal Society B: Biological Sciences Vol. 371, No. 1710 ( 2016-12-19), p. 20150399-
    Details
    In: Philosophical Transactions of the Royal Society B: Biological Sciences, The Royal Society, Vol. 371, No. 1710 ( 2016-12-19), p. 20150399-
    Abstract: Left–right asymmetry is a phenomenon that has a broad appeal—to anatomists, developmental biologists and evolutionary biologists—because it is a morphological feature of organisms that spans scales of size and levels of organization, from unicellular protists, to vertebrate organs, to social behaviour. Here, we highlight a number of important aspects of asymmetry that encompass several areas of biology—cell-level, physiological, genetic, anatomical and evolutionary components—and that are based on research conducted in diverse model systems, ranging from single cells to invertebrates to human developmental disorders. Together, the contributions in this issue reveal a heretofore-unsuspected variety in asymmetry mechanisms, including ancient chirality elements that could underlie a much more universal basis to asymmetry development, and provide much fodder for thought with far reaching implications in biomedical, developmental, evolutionary and synthetic biology. The new emerging theme of binary cell-fate choice, promoted by asymmetric cell division of a deterministic cell, has focused on investigating asymmetry mechanisms functioning at the single cell level. These include cytoskeleton and DNA chain asymmetry—mechanisms that are amplified and coordinated with those employed for the determination of the anterior–posterior and dorsal–ventral axes of the embryo. This article is part of the themed issue ‘Provocative questions in left–right asymmetry’.
    Type of Medium: Online Resource
    ISSN: 0962-8436 , 1471-2970
    URL: Article
    DOI: 10.1098/rstb.2015.0399
    RVK:
    WA 15000
    Language: English
    Publisher: The Royal Society
    Publication Date: 2016
    detail.hit.zdb_id: 1462620-2
    SSG: 12
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  • 5
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    Uncovering cognitive similarities and differences, conservation and innovation
    The Royal Society ; 2021
    In:  Philosophical Transactions of the Royal Society B: Biological Sciences Vol. 376, No. 1821 ( 2021-03-29), p. 20200458-
    Details
    In: Philosophical Transactions of the Royal Society B: Biological Sciences, The Royal Society, Vol. 376, No. 1821 ( 2021-03-29), p. 20200458-
    Abstract: This article is part of the theme issue ‘Basal cognition: multicellularity, neurons and the cognitive lens'.
    Type of Medium: Online Resource
    ISSN: 0962-8436 , 1471-2970
    URL: Article
    DOI: 10.1098/rstb.2020.0458
    RVK:
    WA 15000
    Language: English
    Publisher: The Royal Society
    Publication Date: 2021
    detail.hit.zdb_id: 1462620-2
    SSG: 12
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  • 6
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    Bistability of somatic pattern memories: stochastic outcomes in bioelectric circuits underlying regeneration
    The Royal Society ; 2021
    In:  Philosophical Transactions of the Royal Society B: Biological Sciences Vol. 376, No. 1821 ( 2021-03-29), p. 20190765-
    Details
    In: Philosophical Transactions of the Royal Society B: Biological Sciences, The Royal Society, Vol. 376, No. 1821 ( 2021-03-29), p. 20190765-
    Abstract: Nervous systems’ computational abilities are an evolutionary innovation, specializing and speed-optimizing ancient biophysical dynamics. Bioelectric signalling originated in cells' communication with the outside world and with each other, enabling cooperation towards adaptive construction and repair of multicellular bodies. Here, we review the emerging field of developmental bioelectricity, which links the field of basal cognition to state-of-the-art questions in regenerative medicine, synthetic bioengineering and even artificial intelligence. One of the predictions of this view is that regeneration and regulative development can restore correct large-scale anatomies from diverse starting states because, like the brain, they exploit bioelectric encoding of distributed goal states—in this case, pattern memories. We propose a new interpretation of recent stochastic regenerative phenotypes in planaria, by appealing to computational models of memory representation and processing in the brain. Moreover, we discuss novel findings showing that bioelectric changes induced in planaria can be stored in tissue for over a week, thus revealing that somatic bioelectric circuits in vivo can implement a long-term, re-writable memory medium. A consideration of the mechanisms, evolution and functionality of basal cognition makes novel predictions and provides an integrative perspective on the evolution, physiology and biomedicine of information processing in vivo . This article is part of the theme issue ‘Basal cognition: multicellularity, neurons and the cognitive lens’.
    Type of Medium: Online Resource
    ISSN: 0962-8436 , 1471-2970
    URL: Article
    DOI: 10.1098/rstb.2019.0765
    RVK:
    WA 15000
    Language: English
    Publisher: The Royal Society
    Publication Date: 2021
    detail.hit.zdb_id: 1462620-2
    SSG: 12
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  • 7
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    Making and breaking symmetries in mind and life
    The Royal Society ; 2023
    In:  Interface Focus Vol. 13, No. 3 ( 2023-06-06)
    Details
    In: Interface Focus, The Royal Society, Vol. 13, No. 3 ( 2023-06-06)
    Abstract: Symmetry is a motif featuring in almost all areas of science. Symmetries appear throughout the natural world, making them particularly important in our quest to understand the structure of the world around us. Symmetries and invariances are often first principles pointing to some lawful description of an observation, with explanations being understood as both ‘satisfying’ and potentially useful in their regularity. The sense of aesthetic beauty accompanying such explanations is reminiscent of our understanding of intelligence in terms of the ability to efficiently predict (or compress) data; indeed, identifying and building on symmetry can offer a particularly elegant description of a physical situation. The study of symmetries is so fundamental to mathematics and physics that one might ask where else it proves useful. This theme issue poses the question: what does the study of symmetry, and symmetry breaking, have to offer for the study of life and the mind?
    Type of Medium: Online Resource
    ISSN: 2042-8901
    URL: Article
    DOI: 10.1098/rsfs.2023.0015
    Language: English
    Publisher: The Royal Society
    Publication Date: 2023
    detail.hit.zdb_id: 2585655-8
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  • 8
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    Bioelectric gene and reaction networks: computational modelling of genetic, biochemical and bioelectrical dynamics in pattern regulation
    The Royal Society ; 2017
    In:  Journal of The Royal Society Interface Vol. 14, No. 134 ( 2017-09), p. 20170425-
    Details
    In: Journal of The Royal Society Interface, The Royal Society, Vol. 14, No. 134 ( 2017-09), p. 20170425-
    Abstract: Gene regulatory networks (GRNs) describe interactions between gene products and transcription factors that control gene expression. In combination with reaction–diffusion models, GRNs have enhanced comprehension of biological pattern formation. However, although it is well known that biological systems exploit an interplay of genetic and physical mechanisms, instructive factors such as transmembrane potential ( V mem ) have not been integrated into full GRN models. Here we extend regulatory networks to include bioelectric signalling, developing a novel synthesis: the bioelectricity-integrated gene and reaction (BIGR) network. Using in silico simulations, we highlight the capacity for V mem to alter steady-state concentrations of key signalling molecules inside and out of cells. We characterize fundamental feedbacks where V mem both controls, and is in turn regulated by, biochemical signals and thereby demonstrate V mem homeostatic control, V mem memory and V mem controlled state switching. BIGR networks demonstrating hysteresis are identified as a mechanisms through which more complex patterns of stable V mem spots and stripes, along with correlated concentration patterns, can spontaneously emerge. As further proof of principle, we present and analyse a BIGR network model that mechanistically explains key aspects of the remarkable regenerative powers of creatures such as planarian flatworms. The functional properties of BIGR networks generate the first testable, quantitative hypotheses for biophysical mechanisms underlying the stability and adaptive regulation of anatomical bioelectric pattern.
    Type of Medium: Online Resource
    ISSN: 1742-5689 , 1742-5662
    URL: Article
    DOI: 10.1098/rsif.2017.0425
    Language: English
    Publisher: The Royal Society
    Publication Date: 2017
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  • 9
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    A linear-encoding model explains the variability of the target morphology in regeneration
    The Royal Society ; 2014
    In:  Journal of The Royal Society Interface Vol. 11, No. 92 ( 2014-03-06), p. 20130918-
    Details
    In: Journal of The Royal Society Interface, The Royal Society, Vol. 11, No. 92 ( 2014-03-06), p. 20130918-
    Abstract: A fundamental assumption of today's molecular genetics paradigm is that complex morphology emerges from the combined activity of low-level processes involving proteins and nucleic acids. An inherent characteristic of such nonlinear encodings is the difficulty of creating the genetic and epigenetic information that will produce a given self-assembling complex morphology. This ‘inverse problem’ is vital not only for understanding the evolution, development and regeneration of bodyplans, but also for synthetic biology efforts that seek to engineer biological shapes. Importantly, the regenerative mechanisms in deer antlers, planarian worms and fiddler crabs can solve an inverse problem: their target morphology can be altered specifically and stably by injuries in particular locations. Here, we discuss the class of models that use pre-specified morphological goal states and propose the existence of a linear encoding of the target morphology, making the inverse problem easy for these organisms to solve. Indeed, many model organisms such as Drosophila , hydra and Xenopus also develop according to nonlinear encodings producing linear encodings of their final morphologies. We propose the development of testable models of regeneration regulation that combine emergence with a top-down specification of shape by linear encodings of target morphology, driving transformative applications in biomedicine and synthetic bioengineering.
    Type of Medium: Online Resource
    ISSN: 1742-5689 , 1742-5662
    URL: Article
    DOI: 10.1098/rsif.2013.0918
    Language: English
    Publisher: The Royal Society
    Publication Date: 2014
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  • 10
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    The scaling of goals from cellular to anatomical homeostasis: an evolutionary simulation, experiment and analysis
    The Royal Society ; 2023
    In:  Interface Focus Vol. 13, No. 3 ( 2023-06-06)
    Details
    In: Interface Focus, The Royal Society, Vol. 13, No. 3 ( 2023-06-06)
    Abstract: Complex living agents consist of cells, which are themselves competent sub-agents navigating physiological and metabolic spaces. Behaviour science, evolutionary developmental biology and the field of machine intelligence all seek to understand the scaling of biological cognition: what enables individual cells to integrate their activities to result in the emergence of a novel, higher-level intelligence with large-scale goals and competencies that belong to it and not to its parts? Here, we report the results of simulations based on the TAME framework, which proposes that evolution pivoted the collective intelligence of cells during morphogenesis of the body into traditional behavioural intelligence by scaling up homeostatic competencies of cells in metabolic space. In this article, we created a minimal in silico system (two-dimensional neural cellular automata) and tested the hypothesis that evolutionary dynamics are sufficient for low-level setpoints of metabolic homeostasis in individual cells to scale up to tissue-level emergent behaviour. Our system showed the evolution of the much more complex setpoints of cell collectives (tissues) that solve a problem in morphospace: the organization of a body-wide positional information axis (the classic French flag problem in developmental biology). We found that these emergent morphogenetic agents exhibit a number of predicted features, including the use of stress propagation dynamics to achieve the target morphology as well as the ability to recover from perturbation (robustness) and long-term stability (even though neither of these was directly selected for). Moreover, we observed an unexpected behaviour of sudden remodelling long after the system stabilizes. We tested this prediction in a biological system—regenerating planaria—and observed a very similar phenomenon. We propose that this system is a first step towards a quantitative understanding of how evolution scales minimal goal-directed behaviour (homeostatic loops) into higher-level problem-solving agents in morphogenetic and other spaces.
    Type of Medium: Online Resource
    ISSN: 2042-8901
    URL: Article
    DOI: 10.1098/rsfs.2022.0072
    Language: English
    Publisher: The Royal Society
    Publication Date: 2023
    detail.hit.zdb_id: 2585655-8
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