Assembly of a functional neuronal circuit in embryos of an ancestral metazoan is influenced by environmental signals including the microbiome DOI
Christopher Noack, Sebastian Jenderny, Christoph Giez

et al.

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2024, Volume and Issue: unknown

Published: Dec. 15, 2024

Abstract Understanding how neural populations evolve to give rise behavior is a major goal in neuroscience. However, the complexity of nervous system most invertebrates and vertebrates complicates deciphering underlying fundamental processes. Here, we explore self-assembly circuits Hydra , an organism with simple but no centralized information processing, improve understanding evolution. The N4 neuronal circuit embryos develops through activity-driven self-assembly, where neurons distinct regions increase connectivity synchronization. Gap junctions vesicle-mediated communication between non-neuronal cells drive rapid assembly, embryo’s prospective oral region exhibiting highest density. An artificial electrical circuit-based model demonstrates dynamic increases synchronization over time, along predictions for selective adaptions connections. Environmental factors, like temperature absent microbiome, modify architecture, suggesting existence certain plasticity development. We propose that these features originated last common bilaterian ancestor, supporting hypothesis basic architecture universal.

Language: Английский

New Perspectives on Semiconducting Conjugated Oligomers for Neuromodulation in Hydra vulgaris DOI Creative Commons
Giuseppina Tommasini, Mariarosaria De Simone, Martina Blasio

et al.

Advanced Materials Interfaces, Journal Year: 2025, Volume and Issue: unknown

Published: March 22, 2025

Abstract A general overview is provided on the neuromodulatory function of thiophene‐based semiconductors discovered and characterized in invertebrate model organism, cnidarian Hydra vulgaris . The small freshwater polyp an attractive animal for neuromodulation due to its simple body anatomy a nervous system with hundreds thousands neurons organized distinct circuits, each controlling limited set behaviors. With aim characterizing polymerization trimers soft tissues this model, unexpected behavior observed addition polymerization, involved possible underlying mechanisms are identified. To date, action these compounds other vivo models has not been observed. Here, recent data double showed by summarized, from into conductive structures driven endogenous enzymatic activities specific neuronal circuits. open intriguing research possibilities offered organism field organic bioelectronics both situ production conducting interfaces influence biological processes functions.

Language: Английский

Citations

0

Phototaxis is a satiety-dependent behavioral sequence in Hydra vulgaris DOI Creative Commons
Soonyoung Kim, Krishna N. Badhiwala, Guillaume Duret

et al.

Journal of Experimental Biology, Journal Year: 2024, Volume and Issue: 227(18)

Published: Aug. 19, 2024

Understanding how internal states such as satiety are connected to animal behavior is a fundamental question in neuroscience. Hydra vulgaris, freshwater cnidarian with only 12 neuronal cell types, serves tractable model system for studying state-dependent behaviors. We found that starved hydras consistently move towards light, while fed do not. By modeling this set of three sequences head orientation, jump distance and rate, we demonstrate the state affects rate jumping new position, orientation unaffected. These findings yield insights into simple organism, Hydra, affect specific elements behavior, offer general principles relationship between behaviors their underlying molecular mechanisms.

Language: Английский

Citations

2

A new look at the architecture and dynamics of the Hydra nerve net DOI Creative Commons
Athina Keramidioti,

Sandra Schneid,

Christina Busse

et al.

eLife, Journal Year: 2023, Volume and Issue: 12

Published: June 20, 2023

The Hydra nervous system is the paradigm of a 'simple nerve net'. Nerve cells in Hydra, as many cnidarian polyps, are organized net extending throughout body column. This required for control spontaneous behavior: elimination leads to polyps that do not move and incapable capturing ingesting prey (Campbell, 1976). We have re-examined structure by immunostaining fixed with novel antibody stains all Hydra. Confocal imaging shows there two distinct nets, one ectoderm endoderm, unexpected absence endoderm tentacles. nets contact each other. High-resolution TEM (transmission electron microscopy) serial block face SEM (scanning show consist bundles parallel overlapping neurites. Results from transgenic lines neurite include different neural circuits hence neurites require circuit-specific recognition. cell-specific innexins indicate gap junctions can provide this specificity. occurrence supports model continuous growth differentiation lateral addition new existing net. was confirmed tracking newly differentiated cells.

Language: Английский

Citations

3

Hunger and satiety: Neuronal dynamics in Hydra behavior DOI Creative Commons
Thomas W. Holstein

Cell Reports, Journal Year: 2024, Volume and Issue: 43(6), P. 114264 - 114264

Published: May 23, 2024

Hormonal and neuronal inputs to the brain control how much animals eat. The origins of this behavior were unclear, but in issue Cell Reports, Giez et al.1Giez C. Noack Sakib E. Hofacker L.-M. Repnik U. Bramkamp M. Bosch T.C.G. Satiety controls Hydra through an interplay pre-enteric central nervous system-like neuron populations.Cell Rep. 2024; https://doi.org/10.1016/j.celrep.2024.114210Abstract Full Text PDF Google Scholar describe specific neurons inhibiting feeding evolutionary ancient without brain. Human animal centers around essential need for food. This leads appetite hunger, internal states ensuring energy replenishment until sufficient levels are reached that induce satiety. Concurrently, regulating food intake, terms quantity timing, is vital prevent adverse effects. Various mechanisms have evolved appetite, feeding. In vertebrates, hormones such as ghrelin leptin mediate satiety while hypothalamus hippocampus maintain homeostatic between two states.2Wee R.W.S. Mishchanchuk K. AlSubaie R. Church T.W. Gold M.G. MacAskill A.F. Internal-state-dependent via hippocampal signaling.Neuron. 112: 288-305.e7https://doi.org/10.1016/j.neuron.2023.10.016Abstract PubMed Scopus (3) regulation also manifests insects,3Odell S.R. Clark D. Zito N. Jain Gong H. Warnock Carrion-Lopez Maixner Prieto-Godino L. Mathew Internal state affects local function early sensory processing center shape olfactory Drosophila larvae.Sci. 2022; 1215767https://doi.org/10.1038/s41598-022-20147-1Crossref (2) yet these pivotal neural circuits remain largely elusive. Recent publications shown Cnidaria (the sister group Bilateria) already display a spectrum behaviors,4Yuste Breaking code cnidarian: Learning principles neuroscience from "vulgar" Hydra.Curr. Opin. Neurobiol. 86102869https://doi.org/10.1016/j.conb.2024.102869Crossref (0) encompassing larval predation responses satiety.5Maegele I. Rupp S. Özbek Guse A. Hambleton E.A. Holstein A predatory gastrula symbiosis-independent settlement Aiptasia.Proc. Natl. Acad. Sci. USA. 2023; 120e2311872120https://doi.org/10.1073/pnas.2311872120Crossref (4) their article Reports,1Giez colleagues now made substantial progress our understanding hunger-satiety homeostasis one simplest systems known. They hunger freshwater polyp (Cnidaria). system comprises 200–2000 bi- multipolar young mature polyps organized simple network with higher density at oral aboral ends, or any other ganglia-like centralization4Yuste Scholar,6Holstein stem cell - Revisited.Cells Dev. 174203846https://doi.org/10.1016/j.cdev.2023.203846Crossref Scholar,7Keramidioti Schneid Busse Cramer von Laue Bertulat B. Salvenmoser W. Hess Alexandrova O. Glauber K.M. Steele R.E. al.A new look architecture dynamics nerve net.Elife. 12https://doi.org/10.7554/eLife.87330Crossref (see Figure 1). Neurons form both chemical electrical synapses release transmitters neuropeptides.4Yuste Despite organization, exhibit range behavioral patterns, including Hunting mediated by cnidocytes, highly specialized neurosecretory cells used prey capture defense.8Bosch Klimovich Domazet-Lošo T. Gründer Jékely G. Miller D.J. Murillo-Rincon A.P. Rentzsch F. Richards G.S. al.Back Basics: Cnidarians Start Fire.Trends Neurosci. 2017; 40: 92-105https://doi.org/10.1016/j.tins.2016.11.005Abstract (78) Both cnidocytes derived interstitial cells; they constantly forming reorganizing due continuous growth tissue flow during asexual reproduction (budding), which requires high degree plasticity.6Holstein Scholar,8Bosch ability image activity epitheliomuscular using Ca2+ imaging has revealed Hydra's subdivided into distinct networks,4Yuste Scholar,9Giez Pinkle Giencke Y. Wittlieb J. Herbst Spratte Lachnit Selhuber-Unkel Multiple populations eating responsive microbial signals.Curr. Biol. 33: 5288-5303.e6https://doi.org/10.1016/j.cub.2023.10.038Abstract opening up possibility investigating basis different states. basic readout study animals' hunting behavior, consists successive phases capture, tentacle movements, mouth opening. Prey initiated when comes contact ciliary chemo-mechano-sensor embedded tentacles8Bosch discharge hungry animals, injuring prey, releases reduced glutathione (GSH), among substances. previous laboratory, primarily focused on head region Hydra, showed opening, can be triggered exposing GSH, N6 cells, followed ganglion endodermal N4 become activated.9Giez complex mirrors live stimuli failed well-fed lacking do not respond GSH.9Giez While fact response strongly inhibited fed long-known phenomenon, was understood so far. To activation upon satiation, transgenic lines calcium reporters (GCaMP6s) established under promoters originally identified single-cell sequencing ectoderm (N6, N3, N1) endoderm (N4).1Giez analysis combined ablation experiments nitro-reductase (NTR)-metronidazole approach, allowed functional dissection circuits. These subpopulation (N4) governs feeding-related ectodermal subpopulations (N1, N6) involved physiology motor activity.1Giez population, enriched neurons, had its highest regulated dynamics.1Giez N3 population significant change compared lower frequency starved polyps, i.e., spiking pattern more regular after Analysis circuit hierarchy demonstrated behaviors attributed (such somersault, foot detachment, stretching glutathione-induced response) influenced satiety, observed experiments. suggests dominant role network, reminiscent enteric Bilateria, encodes overall metabolic state, indicating regulatory satiety.1Giez striking difference Bilateria appears interaction neurons.1Giez No physical interactions7Keramidioti direct interdependencies germ layers been reported Cnidaria. indicates if connections exist, must extremely rare. authors speculate presence neurites extending mesoglea volume transmission communication pathway layers, there no physiological evidence this. However, connect each epithelial muscle themselves. projections gap junctions enable exchange small molecules signals. Because junctions7Keramidioti conduct signals, connection would interesting coupling investigate further.1Giez classical neurotransmitters GABA/dopamine, genes key enzymes GABA/dopamine synthesis expressed only support scenario.1Giez possible involvement opens scenario type evolution according could still possess some functions Cnidaria, purely Bilateria. future, it will important analyze distributed anthozoans, basal clade whose larvae earliest developmental stage on.5Maegele competing interests declare. populationsGiez al.Cell ReportsMay 23, 2024In BriefGiez al. demonstrate ancestral metazoan controlled patterns. show either pre-enteric- functions. contributes system. Full-Text Open Access

Language: Английский

Citations

0

A functional network model for body column neural connectivity in Hydra DOI
Wilhelm Braun, Sebastian Jenderny, Christoph Giez

et al.

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2024, Volume and Issue: unknown

Published: June 27, 2024

Abstract Hydra is a non-senescent animal with relatively small number of cell types and overall low structural complexity, but surprisingly rich behavioral repertoire. The main drivers ’s behavior are neurons that arranged in two nerve nets comprising several distinct neuronal populations. Among these populations the ectodermal net N3 which located throughout animal. It has been shown necessary sufficient for complex somersaulting also involved feeding behavior. Despite being jack-of-all-trades, there insufficient knowledge on coupling structure N3, its connectome, role activity propagation function. We construct model connectome part body column. Using experimental data placement somata spatial dimensions column, we show generative network combining non-random preferred orientation primary neurites yields good agreement experimentally observed distributions connection distances, angles, per neuron. Having validated this fashion, place simple excitable dynamical each node column it generates directed, short-lived, fast propagating patterns activity. In addition, by slightly changing parameters model, same can generate persistent Finally, use neuromorphic circuit based Morris-Lecar to can, addition through-conductance biologically plausible time scales, host pattern related somersaulting. speculate such different regimes act as substrates functional roles allowing exhibit complexity nervous system does not possess modules or hubs.

Language: Английский

Citations

0

Assembly of a functional neuronal circuit in embryos of an ancestral metazoan is influenced by environmental signals including the microbiome DOI
Christopher Noack, Sebastian Jenderny, Christoph Giez

et al.

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2024, Volume and Issue: unknown

Published: Dec. 15, 2024

Abstract Understanding how neural populations evolve to give rise behavior is a major goal in neuroscience. However, the complexity of nervous system most invertebrates and vertebrates complicates deciphering underlying fundamental processes. Here, we explore self-assembly circuits Hydra , an organism with simple but no centralized information processing, improve understanding evolution. The N4 neuronal circuit embryos develops through activity-driven self-assembly, where neurons distinct regions increase connectivity synchronization. Gap junctions vesicle-mediated communication between non-neuronal cells drive rapid assembly, embryo’s prospective oral region exhibiting highest density. An artificial electrical circuit-based model demonstrates dynamic increases synchronization over time, along predictions for selective adaptions connections. Environmental factors, like temperature absent microbiome, modify architecture, suggesting existence certain plasticity development. We propose that these features originated last common bilaterian ancestor, supporting hypothesis basic architecture universal.

Language: Английский

Citations

0