scholarly journals Multiple neuronal networks coordinate Hydra mechanosensory behavior

eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Krishna N Badhiwala ◽  
Abby S Primack ◽  
Celina Juliano ◽  
Jacob T Robinson

Hydra vulgaris is an emerging model organism for neuroscience due to its small size, transparency, genetic tractability, and regenerative nervous system; however, fundamental properties of its sensorimotor behaviors remain unknown. Here, we use microfluidic devices combined with fluorescent calcium imaging and surgical resectioning to study how the diffuse nervous system coordinates Hydra's mechanosensory response. Mechanical stimuli cause animals to contract, and we find this response relies on at least two distinct networks of neurons in the oral and aboral regions of the animal. Different activity patterns arise in these networks depending on whether the animal is contracting spontaneously or contracting in response to mechanical stimulation. Together, these findings improve our understanding of how Hydra’s diffuse nervous system coordinates sensorimotor behaviors. These insights help reveal how sensory information is processed in an animal with a diffuse, radially symmetric neural architecture unlike the dense, bilaterally symmetric nervous systems found in most model organisms.

2020 ◽  
Author(s):  
Krishna N. Badhiwala ◽  
Abby S. Primack ◽  
Celina E. Juliano ◽  
Jacob T. Robinson

AbstractHydra vulgaris is an emerging model organism for neuroscience due to its small size, transparency, genetic tractability, and regenerative nervous system; however, fundamental properties of its sensorimotor behaviors remain unknown. Here, we use microfluidic devices combined with fluorescent calcium imaging and surgical resectioning to study how the nervous system coordinates Hydra’s mechanosensory response. We find that mechanical stimuli cause animals to contract, and this response relies on both the oral and aboral nerve rings. We also find that these nerve rings work together to coordinate spontaneous contractions suggesting that spontaneous behavior and sensorimotor responses converge on to a common neural circuit. These findings improve our understanding of how Hydra’s diffuse nervous system supports sensorimotor behaviors, which is needed to increase the utility of Hydra as a model organism for neuroscience.


2019 ◽  
Author(s):  
Constantine N. Tzouanas ◽  
Soonyoung Kim ◽  
Krishna N. Badhiwala ◽  
Benjamin W. Avants ◽  
Jacob T. Robinson

AbstractMany 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 StatementThe 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.


2019 ◽  
Vol 7 (2) ◽  
pp. 8 ◽  
Author(s):  
DiLoreto ◽  
Chute ◽  
Bryce ◽  
Srinivasan

The complete structure and connectivity of the Caenorhabditis elegans nervous system (“mind of a worm”) was first published in 1986, representing a critical milestone in the field of connectomics. The reconstruction of the nervous system (connectome) at the level of synapses provided a unique perspective of understanding how behavior can be coded within the nervous system. The following decades have seen the development of technologies that help understand how neural activity patterns are connected to behavior and modulated by sensory input. Investigations on the developmental origins of the connectome highlight the importance of role of neuronal cell lineages in the final connectivity matrix of the nervous system. Computational modeling of neuronal dynamics not only helps reconstruct the biophysical properties of individual neurons but also allows for subsequent reconstruction of whole-organism neuronal network models. Hence, combining experimental datasets with theoretical modeling of neurons generates a better understanding of organismal behavior. This review discusses some recent technological advances used to analyze and perturb whole-organism neuronal function along with developments in computational modeling, which allows for interrogation of both local and global neural circuits, leading to different behaviors. Combining these approaches will shed light into how neural networks process sensory information to generate the appropriate behavioral output, providing a complete understanding of the worm nervous system.


FACETS ◽  
2018 ◽  
Vol 3 (1) ◽  
pp. 358-374 ◽  
Author(s):  
Maddie J. Venables ◽  
Lei Xing ◽  
Connor C. Edington ◽  
Vance L. Trudeau

The constitutive regenerative ability of the goldfish central nervous system makes them an excellent model organism to study neurogenesis. Intraperitoneal injection of neurotoxin 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) was used to deplete tyrosine hydroxylase-positive neurons in the adult goldfish telencephalon. We report novel information on the ability of the goldfish to regenerate (∼3–4 d post-MPTP insult) damaged neurons in telencephalic tissue by observing the rapid incorporation of bromodeoxyuridine into newly generated cells, which precedes the recovery of motor function in MPTP-treated animals. Specifically, the telencephalon area telencephali pars dorsalis in female goldfish, which is associated with fish motor activity, regenerates following MPTP toxicity. The remarkable ability of goldfish to rapidly regenerate damaged neurons provides insight into their use as model organisms to study neuroregenerative abilities within a few days following injury. We provide evidence that goldfish are able to regenerate neurons in ∼3–4 d to both replenish and recover baseline catecholaminergic levels, thus enabling the fish to reestablish basic activities such as swimming. The study of neuron regeneration in the damaged goldfish brain will increase our understanding of vertebrate neurogenesis and regeneration processes following central nervous system injury.


1989 ◽  
Vol 146 (1) ◽  
pp. 165-176
Author(s):  
J. H. Kaas

Much of the forebrain of many extant species of mammals appears to be sensory-perceptual in nature. Thus, much of the forebrain, especially the dorsal thalamus and neocortex, consists of nuclei and areas that are parts of complex systems that analyze sensory information and allow behavior to be guided by accurate inferences about the external world. Since mammals vary tremendously in brain size, they vary in the amount of tissue devoted to sensory processing. In addition, mammals vary in the sizes and numbers of processing nuclei and areas, and in how neurons and neuron groups (modules) are differentiated within such structures. Sensory-perceptual systems with more, larger and more differentiated parts may allow more stimulus parameters to be considered, experience to play a greater role, and speed calculations through increased parallel processing. The evolution of species differences in brain size, the sizes of individual parts, and internal structure of these parts are potentially understandable within a theoretical framework of gradual modifications of developmental processes. In addition to changes in the generation and specialization of neurons, alterations in the developmental timing that modify internal and external influences on neuron activity patterns seem to have a major role in the construction and maintenance of organization in the nervous system. Because similar selection pressures may arise over and over again and the mechanisms for producing changes may be few, similar changes in the nervous system are likely to occur in independent lines of evolution. It is uncertain how new cortical areas and nuclei evolve. Comparative studies suggest that: (1) all mammals have a few basic sensory areas and nuclei in common, (2) the number of areas and nuclei has increased independently in several lines of mammalian evolution, and (3) new areas have been added to the middle levels of cortical processing sequences. New areas and nuclei may have evolved as a result of sudden duplications and/or by the process of single areas or nuclei gradually differentiating into two or more areas or nuclei. The process of gradual differentiation may have involved the initial step of differentiating functionally distinct classes of cells that are mixed in a representation, followed by the local groupings of such cells into functionally distinct sets, and finally the fusion of cell groups of the same types to form separate representations.


2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Yukihiko Noro ◽  
Hiroshi Shimizu ◽  
Katsuhiko Mineta ◽  
Takashi Gojobori

AbstractThe last common ancestor of Bilateria and Cnidaria is believed to be one of the first animals to develop a nervous system over 500 million years ago. Many of the genes involved in the neural function of the advanced nervous system in Bilateria are well conserved in Cnidaria. Thus, the cnidarian Hydra vulgaris is a good model organism for the study of the putative primitive nervous system in its last common ancestor. The diffuse nervous system of Hydra consists of several peptidergic neuron subsets. However, the specific functions of these subsets remain unclear. Using calcium imaging, here we show that the neuron subsets that express neuropeptide, Hym-176, function as motor circuits to evoke longitudinal contraction. We found that all neurons in a subset defined by the Hym-176 gene (Hym-176A) or its paralogs (Hym-176B) expression are excited simultaneously, followed by longitudinal contraction. This indicates not only that these neuron subsets have a motor function but also that a single molecularly defined neuron subset forms a single coactive circuit. This is in contrast with the bilaterian nervous system, where a single molecularly defined neuron subset harbors multiple coactive circuits, showing a mixture of neurons firing with different timings. Furthermore, we found that the two motor circuits, one expressing Hym-176B in the body column and the other expressing Hym-176A in the foot, are coordinately regulated to exert region-specific contraction. Our results demonstrate that one neuron subset is likely to form a monofunctional circuit as a minimum functional unit to build a more complex behavior in Hydra. This simple feature (one subset, one circuit, one function) found in Hydra may represent the simple ancestral condition of neural evolution.


2018 ◽  
Author(s):  
John Szymanski ◽  
Rafael Yuste

SummaryAs a cnidarian, Hydra has an anatomically simple neuromuscular system likely similar to those of ancestral species, and its study could provide insights on the design logic and function of animal body plans throughout evolution. Here we have used calcium imaging to map the activity of the entire epitheliomuscular system of living Hydra in mounted preparations. We find seven basic spatiotemporal patterns of activation, with fast and slow kinetics of initiation and propagation. Contrary to previous assumptions, both endodermal and ectodermal epitheliomuscular tissues are systematically activated jointly during contractions, in spite of their muscle fibers being orthogonally arranged. We also find that individual cells surprisingly participate in multiple patterns, using different kinetics of activation. Our results reveal that Hydra’s epitheliomuscular tissue is a multifunctional system that can be flexibly reconfigured to generate different spatiotemporal activity patterns, enabling a structurally simple design to implement a varied behavior output.


The control of movement is essential for animals traversing complex environments and operating across a range of speeds and gaits. We consider how animals process sensory information and initiate motor responses, primarily focusing on simple motor responses that involve local reflex pathways of feedback and control, rather than the more complex, longer-term responses that require the broader integration of higher centers within the nervous system. We explore how local circuits facilitate decentralized coordination of locomotor rhythm and examine the fundamentals of sensory receptors located in the muscles, tendons, joints, and at the animal’s body surface. These sensors monitor the animal’s physical environment and the action of its muscles. The sensory information is then carried back to the animal’s nervous system by afferent neurons, providing feedback that is integrated at the level of the spinal cord of vertebrates and sensory-motor ganglia of invertebrates.


Animals ◽  
2021 ◽  
Vol 11 (8) ◽  
pp. 2226
Author(s):  
Sazia Kunvar ◽  
Sylwia Czarnomska ◽  
Cino Pertoldi ◽  
Małgorzata Tokarska

The European bison is a non-model organism; thus, most of its genetic and genomic analyses have been performed using cattle-specific resources, such as BovineSNP50 BeadChip or Illumina Bovine 800 K HD Bead Chip. The problem with non-specific tools is the potential loss of evolutionary diversified information (ascertainment bias) and species-specific markers. Here, we have used a genotyping-by-sequencing (GBS) approach for genotyping 256 samples from the European bison population in Bialowieza Forest (Poland) and performed an analysis using two integrated pipelines of the STACKS software: one is de novo (without reference genome) and the other is a reference pipeline (with reference genome). Moreover, we used a reference pipeline with two different genomes, i.e., Bos taurus and European bison. Genotyping by sequencing (GBS) is a useful tool for SNP genotyping in non-model organisms due to its cost effectiveness. Our results support GBS with a reference pipeline without PCR duplicates as a powerful approach for studying the population structure and genotyping data of non-model organisms. We found more polymorphic markers in the reference pipeline in comparison to the de novo pipeline. The decreased number of SNPs from the de novo pipeline could be due to the extremely low level of heterozygosity in European bison. It has been confirmed that all the de novo/Bos taurus and Bos taurus reference pipeline obtained SNPs were unique and not included in 800 K BovineHD BeadChip.


2019 ◽  
Vol 48 (D1) ◽  
pp. D650-D658 ◽  
Author(s):  
◽  
Julie Agapite ◽  
Laurent-Philippe Albou ◽  
Suzi Aleksander ◽  
Joanna Argasinska ◽  
...  

Abstract The Alliance of Genome Resources (Alliance) is a consortium of the major model organism databases and the Gene Ontology that is guided by the vision of facilitating exploration of related genes in human and well-studied model organisms by providing a highly integrated and comprehensive platform that enables researchers to leverage the extensive body of genetic and genomic studies in these organisms. Initiated in 2016, the Alliance is building a central portal (www.alliancegenome.org) for access to data for the primary model organisms along with gene ontology data and human data. All data types represented in the Alliance portal (e.g. genomic data and phenotype descriptions) have common data models and workflows for curation. All data are open and freely available via a variety of mechanisms. Long-term plans for the Alliance project include a focus on coverage of additional model organisms including those without dedicated curation communities, and the inclusion of new data types with a particular focus on providing data and tools for the non-model-organism researcher that support enhanced discovery about human health and disease. Here we review current progress and present immediate plans for this new bioinformatics resource.


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