Thermal stimulation temperature is encoded as a firing rate in a Hydra nerve ring

Many animals that lose neural tissue due to injury or disease have the ability to maintain their behavioral abilities by regenerating new neurons or reorganizing existing neural circuits. However, most small model organisms used for neuroscience like nematodes and flies lack this high degree of neural plasticity. These animals often show significant behavioral deficits if they lose even a single neuron. Here we show that the small freshwater cnidarian Hydra vulgaris can maintain stable sensory motor behaviors even after losing half of the neurons in its body. Specifically, we find that both the behavioral and neural response to a rapid change in temperature is maintained if we make their nervous system roughly 50% smaller by caloric restriction or surgery. These observations suggest that Hydra provides a rich model for studying how animals maintain stable sensory-motor responses within dynamic neural circuit architectures, and may lead to general principles for neural circuit plasticity and stability. Significance Statement The ability of the nervous system to restore its function following injury is key to survival for many animals. Understanding this neural plasticity in animals across the phylogenetic tree would help reveal fundamental principles of this important ability. To our knowledge, the discovery of a set of neurons in the jellyfish polyp Hydra vulgaris that stably support a response to thermal stimulation is the first demonstration of large-scale neural plasticity in a genetically tractable invertebrate model organism. The small size and transparency of Hydra suggests that it will be possible to study large-scale neural circuit plasticity in an animal where one can simultaneously image the activity of every neuron.

[1]  R. Yuste,et al.  Non-overlapping Neural Networks in Hydra vulgaris , 2017, Current Biology.

[2]  P. Reddien,et al.  Orthogonal muscle fibers have different instructive roles in planarian regeneration , 2017, Nature.

[3]  R. Yuste,et al.  Comprehensive machine learning analysis of Hydra behavior reveals a stable basal behavioral repertoire , 2018, eLife.

[4]  R. D. Campbell Taxonomy of the European Hydra (Cnidaria: Hydrozoa): a re-examination of its history with emphasis on the species H. vulgaris Pallas, H. attenuata Pallas and H. circumcincta Schulze , 1989 .

[5]  W. A. Kepner,et al.  Reactions of Hydra to chloretone , 1924 .

[6]  L. Passano,et al.  Pacemaker Hierarchies Controlling the Behaviour of Hydras , 1963, Nature.

[7]  P. Reddien The Cellular and Molecular Basis for Planarian Regeneration , 2018, Cell.

[8]  J. Lohmann,et al.  Transgenic Hydra allow in vivo tracking of individual stem cells during morphogenesis. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[9]  Vasu Sheeba,et al.  Axonal Injury and Regeneration in the Adult Brain of Drosophila , 2008, The Journal of Neuroscience.

[10]  F. Noel,et al.  Recovery of tail-elicited siphon-withdrawal reflex following unilateral axonal injury is associated with ipsi- and contralateral changes in gene expression in Aplysia californica , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  J. A. Farrell,et al.  Stem cell differentiation trajectories in Hydra resolved at single-cell resolution , 2018 .

[12]  R. D. Campbell,et al.  Tissue economics of hydra: regulation of cell cycle, animal size and development by controlled feeding rates. , 1977, Journal of cell science.

[13]  L. Passano,et al.  Co-Ordinating Systems and Behaviour In Hydra : I. Pacemaker System of the Periodic Contractions , 1964 .

[14]  E. Walters,et al.  Recovery of function, peripheral sensitization and sensory neurone activation by novel pathways following axonal injury in Aplysia californica. , 1995, The Journal of experimental biology.

[15]  J. A. Farrell,et al.  Stem cell differentiation trajectories in Hydra resolved at single-cell resolution , 2018, Science.

[16]  N. Rushforth BEHAVIORAL AND ELECTROPHYSIOLOGICAL STUDIES OF HYDRA. I. ANALYSIS OF CONTRACTION PULSE PATTERNS , 1971 .

[17]  Y. Jan,et al.  Regeneration of Drosophila sensory neuron axons and dendrites is regulated by the Akt pathway involving Pten and microRNA bantam. , 2012, Genes & development.

[18]  C. David,et al.  Regionalized nervous system in Hydra and the mechanism of its development. , 2019, Gene expression patterns : GEP.

[19]  Mehmet Fatih Yanik,et al.  Neurosurgery: Functional regeneration after laser axotomy , 2004, Nature.

[20]  S. O. Mast Reactions To Temperature Changes In Spirillum, Hydra, And Fresh-water Planarians , 2018 .

[21]  Y Sawada,et al.  Minimum tissue size required for hydra regeneration. , 1993, Developmental biology.

[22]  Jacob T. Robinson,et al.  Magnetic Entropy as a Proposed Gating Mechanism for Magnetogenetic Ion Channels. , 2019, Biophysical journal.

[23]  A. Gierer,et al.  Quantitative analysis of cell types during growth and morphogenesis in Hydra , 2004, Wilhelm Roux' Archiv für Entwicklungsmechanik der Organismen.

[24]  T. Murphy,et al.  Plasticity during stroke recovery: from synapse to behaviour , 2009, Nature Reviews Neuroscience.

[25]  Yishi Jin,et al.  Axon regeneration in C. elegans , 2014, Current Opinion in Neurobiology.

[26]  H. Bode,et al.  Thermotolerance and synthesis of heat shock proteins: these responses are present in Hydra attenuata but absent in Hydra oligactis. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[27]  Celina E. Juliano,et al.  Generation of transgenic Hydra by embryo microinjection. , 2014, Journal of visualized experiments : JoVE.

[28]  R. D. Campbell Tissue dynamics of steady state growth in Hydra littoralis. II. Patterns of tissue movement , 1967, Journal of morphology.

[29]  I Kupfermann,et al.  Dissociation of the appetitive and consummatory phases of feeding behavior in Aplysia: a lesion study. , 1974, Behavioral biology.

[30]  C. Govind,et al.  Morphological correlates of neural regeneration in the feeding system of Aplysia californica after central nervous system lesions , 1997, The Journal of comparative neurology.

[31]  Keith B. Hengen,et al.  Autism-Associated Shank3 Is Essential for Homeostatic Compensation in Rodent V1 , 2020, Neuron.

[32]  Matthias Bethge,et al.  Using DeepLabCut for 3D markerless pose estimation across species and behaviors , 2018, Nature Protocols.

[33]  G. Turrigiano The Self-Tuning Neuron: Synaptic Scaling of Excitatory Synapses , 2008, Cell.

[34]  W. Callaghan,et al.  Thermal tolerance and acclimation of two species of Hydra1 , 1981 .

[35]  Yishi Jin,et al.  Caenorhabditis elegans neuronal regeneration is influenced by life stage, ephrin signaling, and synaptic branching , 2007, Proceedings of the National Academy of Sciences.

[36]  Daniel L. Gonzales,et al.  Microfluidics for Electrophysiology, Imaging, and Behavioral Analysis of Hydra , 2018, bioRxiv.

[37]  Rafael Yuste,et al.  Mapping the Whole-Body Muscle Activity of Hydra vulgaris , 2019, Current Biology.

[38]  Gina G. Turrigiano,et al.  All for One But Not One for All: Excitatory Synaptic Scaling and Intrinsic Excitability Are Coregulated by CaMKIV, Whereas Inhibitory Synaptic Scaling Is Under Independent Control , 2017, The Journal of Neuroscience.

[39]  N. Rushforth,et al.  Behavior in Hydra: Contraction Responses of Hydra pirardi to Mechanical and Light Stimuli , 1963, Science.

[40]  C. N. David,et al.  Characterization of interstitial stem cells in hydra by cloning. , 1977, Developmental biology.

[41]  H. Bode,et al.  Parameters of self-organization in Hydra aggregates. , 2000, Proceedings of the National Academy of Sciences of the United States of America.