Modeling spontaneous activity across an excitable epithelium: Support for a coordination scenario of early neural evolution

Internal coordination models hold that early nervous systems evolved in the first place to coordinate internal activity at a multicellular level, most notably the use of multicellular contractility as an effector for motility. A recent example of such a model, the skin brain thesis, suggests that excitable epithelia using chemical signaling are a potential candidate as a nervous system precursor. We developed a computational model and a measure for whole body coordination to investigate the coordinative properties of such excitable epithelia. Using this measure we show that excitable epithelia can spontaneously exhibit body-scale patterns of activation. Relevant factors determining the extent of patterning are the noise level for exocytosis, relative body dimensions, and body size. In smaller bodies whole-body coordination emerges from cellular excitability and bidirectional excitatory transmission alone. Our results show that basic internal coordination as proposed by the skin brain thesis could have arisen in this potential nervous system precursor, supporting that this configuration may have played a role as a proto-neural system and requires further investigation.

[1]  J. Albert,et al.  Computational modeling of an early evolutionary stage of the nervous system. , 1999, Bio Systems.

[2]  S. Grant,et al.  The origin and evolution of synapses , 2009, Nature Reviews Neuroscience.

[3]  J. Cotton,et al.  The Ediacaran emergence of bilaterians: congruence between the genetic and the geological fossil records , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[4]  Frederick Sachs,et al.  Stretch-activated ion channels: what are they? , 2010, Physiology.

[5]  G. Augustine How does calcium trigger neurotransmitter release? , 2001, Current Opinion in Neurobiology.

[6]  L. Moroz On the Independent Origins of Complex Brains and Neurons , 2009, Brain, Behavior and Evolution.

[7]  G. Miller Origins. On the origin of the nervous system. , 2009, Science.

[8]  T. Fujisawa,et al.  Cnidarians and the evolutionary origin of the nervous system , 2009, Development, growth & differentiation.

[9]  P. Brink,et al.  Gap junctions in excitable cells , 1996, Journal of bioenergetics and biomembranes.

[10]  P. Hunter,et al.  Computational Mechanics of the Heart , 2000 .

[11]  Richard D Emes,et al.  Evolution of synapse complexity and diversity. , 2012, Annual review of neuroscience.

[12]  B. Walz,et al.  Serotonin‐induced intercellular calcium waves in salivary glands of the blowfly Calliphora erythrocephala. , 1997, The Journal of physiology.

[13]  E. Kandel,et al.  Essentials of Neural Science and Behavior , 1996 .

[14]  A. Karschin,et al.  Evolutionary link between prokaryotic and eukaryotic K+ channels. , 1998, The Journal of experimental biology.

[15]  M. Nash,et al.  Electromechanical model of excitable tissue to study reentrant cardiac arrhythmias. , 2004, Progress in biophysics and molecular biology.

[16]  A. van Ooyen,et al.  Impact of Dendritic Size and Dendritic Topology on Burst Firing in Pyramidal Cells , 2010, PLoS computational biology.

[17]  M. Brasier Darwin's Lost World: The Hidden History of Animal Life , 2010 .

[18]  T. Sejnowski,et al.  Model of traveling waves in a coral nerve network , 2008, Journal of Comparative Physiology A.

[19]  A. Patapoutian,et al.  The role of Drosophila Piezo in mechanical nociception , 2011, Nature.

[20]  G. E. Smith The Elementary Nervous System , 1919, Nature.

[21]  P. Bressloff Waves in Neural Media , 2014 .

[22]  R. Greenberg,et al.  Phylogeny of ion channels: clues to structure and function. , 2001, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[23]  Michele Giugliano,et al.  Accurate and Fast Simulation of Channel Noise in Conductance-Based Model Neurons by Diffusion Approximation , 2011, PLoS Comput. Biol..

[24]  Dirk Fasshauer,et al.  SNAREing the basis of multicellularity: consequences of protein family expansion during evolution. , 2008, Molecular biology and evolution.

[25]  V. Shestopalov,et al.  Pannexins and gap junction protein diversity , 2008, Cellular and Molecular Life Sciences.

[26]  S. Munro,et al.  An elaborate classification of SNARE proteins sheds light on the conservation of the eukaryotic endomembrane system. , 2007, Molecular biology of the cell.

[27]  F. Strumwasser,et al.  Comparative neurobiology : modes of communication in the nervous system , 1985 .

[28]  G. Jékely Origin and early evolution of neural circuits for the control of ciliary locomotion , 2011, Proceedings of the Royal Society B: Biological Sciences.

[29]  D. Arendt,et al.  The evolution of nervous system centralization , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[30]  I. Farkas,et al.  Social behaviour: Mexican waves in an excitable medium , 2002, Nature.

[31]  A. Ghysen,et al.  The origin and evolution of the nervous system. , 2003, The International journal of developmental biology.

[32]  O. Hamill,et al.  Molecular basis of mechanotransduction in living cells. , 2001, Physiological reviews.

[33]  P. A. Anderson,et al.  Epithelial conduction: Its properties and functions , 1980, Progress in Neurobiology.

[34]  H. Zhang,et al.  A modified FitzHugh-Nagumo model that allows control of action potential duration and refractory period , 2009, 2009 36th Annual Computers in Cardiology Conference (CinC).

[35]  G. Mackie Central Neural Circuitry in the Jellyfish Aglantha , 2004, Neurosignals.

[36]  Shilpa Chakravartula,et al.  Complex Networks: Structure and Dynamics , 2014 .

[37]  N. V. Davydov,et al.  Critical properties of autowaves propagating on deformed cylindrical surfaces , 2003 .

[38]  R. Yuste,et al.  High Speed Two-Photon Imaging of Calcium Dynamics in Dendritic Spines: Consequences for Spine Calcium Kinetics and Buffer Capacity , 2007, PLoS ONE.

[39]  F. Keijzer Moving and sensing without input and output: early nervous systems and the origins of the animal sensorimotor organization , 2015, Biology & Philosophy.

[40]  P. Godfrey‐Smith,et al.  An Option Space for Early Neural Evolution , 2015, bioRxiv.

[41]  Victor V. Solovyev,et al.  The Ctenophore Genome and the Evolutionary Origins of Neural Systems , 2014, Nature.

[42]  V. Schmid,et al.  Evolution of striated muscle: jellyfish and the origin of triploblasty. , 2005, Developmental biology.

[43]  G. Mackie CONDUCTION IN THE NERVE-FREE EPITHELIA OF SIPHONOPHORES. , 1965, American zoologist.

[44]  M. Paulin,et al.  Predation and the Origin of Neurones , 2014, Brain, Behavior and Evolution.

[45]  R. Meech,et al.  Impulse conduction in a sponge. , 1999, The Journal of experimental biology.

[46]  G. Horridge,et al.  Primitive Nervous Systems , 1968, Nature.

[47]  L. Moroz The genealogy of genealogy of neurons , 2014, Communicative & integrative biology.

[48]  Terrence J. Sejnowski,et al.  Synthesis of models for excitable membranes, synaptic transmission and neuromodulation using a common kinetic formalism , 1994, Journal of Computational Neuroscience.

[49]  B. Calcott Lineage Explanations: Explaining How Biological Mechanisms Change , 2009, The British Journal for the Philosophy of Science.

[50]  A. Hodgkin,et al.  A quantitative description of membrane current and its application to conduction and excitation in nerve , 1952, The Journal of physiology.

[51]  S. Ovsepian,et al.  Wiring prior to firing: the evolutionary rise of electrical and chemical modes of synaptic transmission , 2014, Reviews in the neurosciences.

[52]  P. Mackenzie,et al.  Vesicle number does not predict postsynaptic measures of miniature synaptic activity frequency in cultured cortical neurons , 2000, Neuroscience.

[53]  F. Arecchi,et al.  Spatiotemporal dynamics of the electrical network activity in the root apex , 2009, Proceedings of the National Academy of Sciences.

[54]  R. Satterlie Do jellyfish have central nervous systems? , 2011, Journal of Experimental Biology.

[55]  Todd H. Oakley,et al.  A Post-Synaptic Scaffold at the Origin of the Animal Kingdom , 2007, PloS one.

[56]  M. Dahlem,et al.  Nucleation of reaction-diffusion waves on curved surfaces , 2014, 1403.1716.

[57]  P. Hogeweg,et al.  Spiral breakup in a modified FitzHugh-Nagumo model , 1993 .

[58]  Ralph J. Greenspan An introduction to nervous systems , 2007 .

[59]  K. T. ten Tusscher,et al.  Alternans and spiral breakup in a human ventricular tissue model. , 2006, American journal of physiology. Heart and circulatory physiology.

[60]  Marc-Oliver Gewaltig,et al.  Towards Reproducible Descriptions of Neuronal Network Models , 2009, PLoS Comput. Biol..

[61]  G. Mackie The Elementary Nervous System Revisited , 1990 .

[62]  O. Kinouchi,et al.  Intensity coding in two-dimensional excitable neural networks , 2004, q-bio/0409032.

[63]  V. Braitenberg Vehicles, Experiments in Synthetic Psychology , 1984 .

[64]  Travis Monk,et al.  The Evolutionary Origin of Nervous Systems and Implications for Neural Computation , 2013 .

[65]  Fred Keijzer,et al.  What nervous systems do: early evolution, input–output, and the skin brain thesis , 2013, Adapt. Behav..

[66]  F. Sachs,et al.  Cell biology: The sensation of stretch , 2012, Nature.

[67]  Michael L. Hines,et al.  The NEURON Book , 2006 .

[68]  G. Mackie,et al.  Epithelial Conduction in Hydromedusae , 1968, The Journal of general physiology.

[69]  D. Arendt,et al.  Evolution: Ctenophore Genomes and the Origin of Neurons , 2014, Current Biology.