Biology subjects

Dondorp, D.

Publications and source records attributed to Dondorp, D..

7 recordsLinked to original sources

bioRxiv2023

Polymodal sensory perception of mechanical and chemical cues drives robust settlement and metamorphosis of a marine pre-vertebrate zooplanktonic larva.

The Earths oceans brim with an incredible diversity of microscopic planktonic animals, many of which correspond to the transient larval stage in the life cycles of benthic marine organisms. The mechanisms by which marine larvae use their nervous system to sense and process diverse environmental cues (physical and chemical) in the water column and the benthos to settle and metamorphose is a major problem across the fields of neuroscience, development, evolution and ecology, yet they remain largely unclear. Here, we employ Ca2+ imaging and behavioral assays using the larval form of the protochordate Ciona intestinalis to characterise the mechanical and chemical stimuli these larvae respond to during settlement and metamorphosis. We also identify the polymodal sensory cells that detect these stimuli. Whole brain Ca2+ imaging further revealed that the presentation or removal of ethological chemosensory stimuli engages the activities of different neuronal sub-populations resulting in brain state changes, which may underlie behavioral action selections and metamorphosis. Finally, chemogenetic interrogation coupled to behavioral analysis reveals that peptidergic sensory neurons including polymodal cells capable of chemotactile perception and chemosensory/neurosecretory cells of proto-placodal ectoderm origin play a pivotal role in regulating stimulus induced settlement and metamorphosis. This work suggests that marine zooplanktonic larvae utilise their streamlined nervous systems to perform multimodal integration of ethologically physical and chemical cues to explore the oceanic water column and benthos.

neuroscience↗

bioRxiv2023

Anoctamin 10/TMEM16K mediates convergent extension and tubulogenesis during notochord formation in the early chordate Ciona intestinalis.

During embryonic development, cells are organized into complex tissues and organs. A highly conserved organ shape across metazoans is the epithelial tube. Tube morphogenesis is a complex multistep process where the molecular mechanisms underlying the diversity of cell behaviors such as convergent extension, cell elongation, and lumen formation are still intensely studied. Here, using genome editing and quantitative imaging in the early chordate Ciona intestinalis we show that Ano10/Tmem16k, a member of the evolutionarily ancient family of transmembrane proteins called Anoctamin/TMEM16 is required for convergent extension, lumen expansion and connection during notochord morphogenesis. In addition, we find that loss of Cii.Ano10/Tmem16k hampers cell behavior and cytoskeletal organization during tubulogenesis. In vivo Ca2+ imaging revealed that genetic ablation of Cii.Ano10/Tmem16k hinders the ability of notochord cells to regulate bioelectrical signaling. Finally, we use electrophysiological recordings and a scramblase assay in tissue culture to demonstrate that Cii.Ano10/Tmem16k likely acts as an ion channel but not as a phospholipid scramblase. More generally, this work provides insights into the pre-vertebrate functions of Anoctamins and raises the possibility that Anoctamin/Tmem16 family members have an evolutionarily conserved role in tube morphogenesis.

developmental biology↗

bioRxiv2021

Comprehensive analysis of behavioral dynamics in the protochordate Ciona intestinalis

Vertebrate nervous systems can generate a remarkable diversity of behaviors. However, our understanding of how behaviors may have evolved in the chordate lineage is limited by the lack of neuroethological studies leveraging our closest invertebrate relatives. Here we combine high-throughput video acquisition with pharmacological perturbations of bioamine signaling to systematically reveal the global structure of the motor behavioral repertoire in the Ciona intestinalis larvae. Most of Cionas postural variance can be captured by six basic shapes, which we term "Eigencionas". Motif analysis of postural time series further demonstrated that bioamines influence numerous stereotyped behavioral maneuvers including "startle-like" and "beat-and-glide". Employing computational modeling of swimming dynamics and spatio-temporal embedding of postural features revealed that subtle behavioural differences are generated at the levels of motor modules and the transitions between, both modulated by bioamines. Finally, we show that flexible motor module usage gives rise to diverse behaviors in response to different light stimuli.

animal behavior and cognition↗

bioRxiv2021

The unique neuronal structure and neuropeptide repertoire in the ctenophore Mnemiopsis leidyi shed light on the evolution of animal nervous systems

The ctenophore nerve net represents one of the earliest evolved nervous system of animals. Due to the uncertainties of their phylogenetic placement of ctenophores and the absence of several key bilaterian neuronal genes, it has been hypothesized that their neurons have evolved independently. Whether this is indeed the case remains unclear, and thus the evolutionary history of neurons is still contentious. Here, we have characterized the neuropeptide repertoire of the ctenophore Mnemiopsis leidyi. Using the machine learning NeuroPID tool1 129 new putative neuropeptide precursors were predicted. Sixteen of them are detected in the subepithelial nerve net (SNN), aboral organ (AO) and epithelial sensory cells (ESC) of early cydippid-stage M. leidyi by in situ hybridization (ISH) and immunohistochemistry (IHC). Four of these neuropeptides increase the animals swimming velocity in a behavioral essay. The new neuropeptides were used as markers to identify neuronal cell types in single cell transcriptomic data2. To unravel the neuronal architecture, we 3D reconstructed the SNN underlying the comb plates using serial block-face scanning electron microscopy (SBF-SEM). For the first time, we confirm a more than 100 years old hypothesis about anastomoses between neurites of the same cell in ctenophores and reveal that they occur through a continuous membrane. Our findings reveal the unique neuronal structure and neuropeptide repertoire of ctenophores and are important for reconstructing the evolutionary origin of animal neurons and nervous systems.

evolutionary biology↗

bioRxiv2020

Mapping calcium dynamics in a developing tubular structure.

Calcium is a ubiquitous and versatile second messenger that plays a central role in the development and function of a wide range of cell types, tissues and organs. Despite significant recent progress in the understanding of calcium (Ca2+) signalling in organs such as the developing and adult brain, we have relatively little knowledge of the contribution of Ca2+ to the development of tubes, structures widely present in multicellular organisms. Here we image Ca2+ dynamics in the developing notochord of Ciona intestinalis. We show that notochord cells exhibit distinct Ca2+ dynamics during specific morphogenetic events such as cell intercalation, cell elongation and tubulogenesis. We used an optogenetically controlled Ca2+ actuator to show that sequestration of Ca2+ results in defective notochord cell intercalation, and pharmacological inhibition to reveal that stretch-activated ion channels (SACs), inositol triphosphate receptor (IP3R) signalling, Store Operated Calcium Entry (SOCE), Sarco/endoplasmic reticulum Ca2+-ATPase (SERCA) and gap junctions are required for regulating notochord Ca2+ activity during tubulogenesis. Cytoskeletal rearrangements drive the cell shape changes that accompany tubulogenesis. In line with this, we show that Ca2+ signalling modulates reorganization of the cytoskeletal network across the morphogenetic events leading up to and during tubulogenesis of the notochord. We additionally demonstrate that perturbation of the actin cytoskeleton drastically remodels Ca2+ dynamics, suggesting a feedback mechanism between actin dynamics and Ca2+ signalling during notochord development. This work provides a framework to quantitatively define how Ca2+ signalling regulates tubulogenesis using the notochord as model organ, a defining structure of all chordates.

developmental biology↗

bioRxiv2019

Mesmerize: A highly versatile platform for calcium imaging analysis and creation of self-contained FAIR datasets.

Calcium imaging is an increasingly valuable technique for understanding neural circuits, neuroethology, and cellular mechanisms. The analysis of calcium imaging data presents challenges in image processing, data organization, analysis, and accessibility. Tools have been created to address these problems independently, however a comprehensive user-friendly package does not exist. Here we present "Mesmerize", an efficient, expandable and user-friendly analysis platform, which uses a Findable, Accessible, Interoperable and Reproducible (FAIR) system to encapsulate the entire analysis process, from raw data to interactive visualizations for publication. Mesmerize provides a user-friendly graphical interface to state-of-the-art analysis methods for signal extraction & downstream analysis. We demonstrate the broad scientific scope of Mesmerizes applications by analyzing neuronal datasets from mouse and a volumetric zebrafish dataset. We also applied contemporary time-series analysis techniques to analyze a novel dataset comprising neuronal, epidermal, and migratory mesenchymal cells of the protochordate Ciona intestinalis.

neuroscience↗

bioRxiv2018

Quantitative analysis reveals the basic behavioural repertoire of the urochordate Ciona intestinalis.

Quantitative analysis of animal behaviour in model organisms is becoming an increasingly essential approach for tackling the great challenge of understanding how activity in the brain gives rise to behaviour. In addition, behavioural analysis can provide insight on the molecular basis of nervous system development and function as demonstrated by genetic screens focused on behavioural phenotyping in some genetically tractable model organisms. The progress in building low-cost automated tracking setups, together with advances in computer vision machine learning have expanded the repertoire of organisms which are amenable to quantitative behavioural analysis. Here we used automated image-based tracking to extract behavioural features from an organism of great importance in understanding the evolution of chordates, the free swimming larval form of the tunicate Ciona intestinalis which has a compact and fully mapped nervous system composed of only 231 neurons. We analysed hundreds of videos of larvae and we extracted basic geometric and physical descriptors of larval behaviour. Most importantly, we used machine learning methods to create an objective ontology of behaviours for C. intestinalis larvae. We identified eleven behavioural modes using agglomerative clustering. This approach enabled us to produce a quantitative description of the basic larval behavioural repertoire. Furthermore, we tested the robustness of this repertoire by comparing different rearing conditions and ages. Using our pipeline for quantitative behavioural analysis, we successfully reproduced the known photoresponsive behaviour and the first demonstration to our knowledge that C. intestinalis larvae exhibit sensory arousal and thigmotaxis, both of which can be modulated by the anxiotropic drug modafinil. Remarkably, by comparing the behaviour between animals assayed individually or in small groups, we found that crowd size influences larval behaviour. This study shows that C. intestinalis larval behaviour can be broken down to a set of stereotyped behaviours that are used to different extents in a context-dependent manner. Furthermore, it raises exciting possibilities such as mapping behaviour to specific neurons of this compact chordate nervous system and it paves the way for comparative quantitative behavioural studies as a means to reconstruct the evolution of behaviour, especially in the chordate lineage.

animal behavior and cognition↗