scholarly journals Circuit Degeneracy Facilitates Robustness and Flexibility of Navigation Behavior in C.elegans

2018 ◽  
Author(s):  
Muneki Ikeda ◽  
Shunji Nakano ◽  
Andrew C. Giles ◽  
Wagner Steuer Costa ◽  
Alexander Gottschalk ◽  
...  

AbstractAnimal behaviors are robust and flexible. To elucidate how these two conflicting features of behavior are encoded in the nervous system, we analyzed the neural circuits generating a C. elegans thermotaxis behavior, in which animals migrate toward the past cultivation temperature (Tc). We identified multiple circuits that are highly overlapping but individually regulate distinct behavioral components to achieve thermotaxis. When the regulation of a behavioral component is disrupted following single cell ablations, the other components compensate the deficit, enabling the animals to robustly migrate toward the Tc. Depending on whether the environmental temperature surrounding the animals is above or below the Tc, different circuits regulate the same behavioral components, mediating the flexible switch between migration up or down toward the Tc. These context-dependencies within the overlapping sub-circuits reveal the implementation of degeneracy in the nervous system, providing a circuit-level basis for the robustness and flexibility of behavior.

eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Lori Glenwinkel ◽  
Seth R Taylor ◽  
Kasper Langebeck-Jensen ◽  
Laura Pereira ◽  
Molly B Reilly ◽  
...  

The generation of the enormous diversity of neuronal cell types in a differentiating nervous system entails the activation of neuron type-specific gene batteries. To examine the regulatory logic that controls the expression of neuron type-specific gene batteries, we interrogate single cell expression profiles of all 118 neuron classes of the Caenorhabditis elegans nervous system for the presence of DNA binding motifs of 136 neuronally expressed C. elegans transcription factors. Using a phylogenetic footprinting pipeline, we identify cis-regulatory motif enrichments among neuron class-specific gene batteries and we identify cognate transcription factors for 117 of the 118 neuron classes. In addition to predicting novel regulators of neuronal identities, our nervous system-wide analysis at single cell resolution supports the hypothesis that many transcription factors directly co-regulate the cohort of effector genes that define a neuron type, thereby corroborating the concept of so-called terminal selectors of neuronal identity. Our analysis provides a blueprint for how individual components of an entire nervous system are genetically specified.


Science ◽  
2019 ◽  
Vol 365 (6459) ◽  
pp. eaax1971 ◽  
Author(s):  
Jonathan S. Packer ◽  
Qin Zhu ◽  
Chau Huynh ◽  
Priya Sivaramakrishnan ◽  
Elicia Preston ◽  
...  

Caenorhabditis elegans is an animal with few cells but a wide diversity of cell types. In this study, we characterize the molecular basis for their specification by profiling the transcriptomes of 86,024 single embryonic cells. We identify 502 terminal and preterminal cell types, mapping most single-cell transcriptomes to their exact position in C. elegans’ invariant lineage. Using these annotations, we find that (i) the correlation between a cell’s lineage and its transcriptome increases from middle to late gastrulation, then falls substantially as cells in the nervous system and pharynx adopt their terminal fates; (ii) multilineage priming contributes to the differentiation of sister cells at dozens of lineage branches; and (iii) most distinct lineages that produce the same anatomical cell type converge to a homogenous transcriptomic state.


1959 ◽  
Vol 105 (440) ◽  
pp. 852-862 ◽  
Author(s):  
J. P. Baker

Over the past few years, there has been an increasing interest in drugs having a tranquillizing or ataractic effect on the central nervous system. Pharmaceutical houses, both here and on the other side of the Atlantic, have vied with one another to be the first to introduce the perfect tranquillizer, providing relief from tension and anxiety with no unpleasant or dangerous side-effects or tendency to addiction, and at the same time if possible to effect an improvement in the management of, if not the cure of, the psychoses.


2018 ◽  
Author(s):  
Fernando Calahorro ◽  
Francesca Keefe ◽  
James Dillon ◽  
Lindy Holden-Dye ◽  
Vincent O’Connor

ABSTRACTThe integration of distinct sensory modalities is essential for behavioural decision making. In C. elegans this process is coordinated by neural circuits that integrate sensory cues from the environment to generate an appropriate behaviour at the appropriate output muscles. Food is a multimodal cue that impacts on the microcircuits to modulating feeding and foraging drivers at the level of the pharyngeal and body wall muscle respectively. When food triggers an upregulation in pharyngeal pumping it allows the effective ingestion of food. Here we show that a C. elegans mutant in the single orthologous gene of human neuroligins, nlg-1 are defective in food induced pumping. This is not explained by an inability to sense food, as nlg-1 mutants are not defective in chemotaxis towards bacteria. In addition, we show that neuroligin is widely expressed in the nervous system including AIY, ADE, ALA, URX and HSN neurones. Interestingly, despite the deficit in pharyngeal pumping neuroligin is not expressed within the pharyngeal neuromuscular network, which suggests an extrapharyngeal regulation of this circuit. We resolve electrophysiologically the neuroligin contribution to the pharyngeal circuit by mimicking a food-dependent pumping, and show that the nlg-1 phenotype is similar to mutants impaired in GABAergic and/or glutamatergic signalling. We suggest that neuroligin organizes extrapharyngeal circuits that regulate the pharynx. These observations based on the molecular and cellular determinants of feeding are consistent with the emerging role of neuroligin in discretely impacting functional circuits underpinning complex behaviours.


2019 ◽  
Author(s):  
Seth R Taylor ◽  
Gabriel Santpere ◽  
Molly Reilly ◽  
Lori Glenwinkel ◽  
Abigail Poff ◽  
...  

AbstractA single neuron and its synapses define the fundamental structural motif of the brain but the underlying gene expression programs that specify individual neuron types are poorly understood. To address this question in a model organism, we have produced a gene expression profile of >90% of the individual neuron classes in the C. elegans nervous system, an ensemble of neurons for which both the anatomy and connectivity are uniquely defined at single cell resolution. We generated single cell transcriptomes for 52,412 neurons that resolve as clusters corresponding to 109 of the canonical 118 neuron classes in the mature hermaphrodite nervous system. Detailed analysis revealed molecular signatures that further subdivide identified classes into specific neuronal subtypes. Notably, neuropeptide-related genes are often differentially expressed between subtypes of the given neuron class which points to distinct functional characteristics. All of these data are publicly available at our website (http://www.cengen.org) and can be interrogated at the web application SCeNGEA (https://cengen.shinyapps.io/SCeNGEA). We expect that this gene expression catalog will spur the goal of delineating the underlying mechanisms that define the developmental lineage, detailed anatomy, synaptic connectivity and function of each type of C. elegans neuron.


Author(s):  
Elizabeth M. DiLoreto ◽  
Christopher D. Chute ◽  
Samantha Bryce ◽  
Jagan Srinivasan

The complete structure and connectivity of the Caenorhabditis elegans nervous system was first published in 1986. The ‘mind of a worm’ was the first organism to have its nervous system to be reconstructed at the level of synapses, and represented a critical milestone considering today it remains the only organism to be mapped to that level of connection. Recently, the extrasynaptic connectome of neuropeptides and monoamines has been described. This review discusses recent technological advances used to perturb whole-organism neuronal function, such as: whole brain imaging, optogenetics, sonogenetics and mutant analysis, which have allowed for interrogations of both local and global neural circuits, leading to different behaviors. A better understanding of a whole organism requires combining experimental datasets with biophysical neuronal modelling, and behavioral quantification. Combining these approaches will provide a complete understanding of the worm nervous system and shed light into how networks function and interact with the synaptic network to modulate information processing and behavioral output.


Author(s):  
Bob Goldstein

Experimentally tractable organisms like C. elegans, Drosophila, zebrafish, and mouse are popular models for addressing diverse questions in biology. In 1997, two of the most valuable invertebrate model organisms to date – C. elegans and Drosophila – were found to be much more closely related to each other than expected. C. elegans and Drosophila belong to the nematodes and arthropods respectively, and these two phyla and six other phyla make up a clade of molting animals referred to as the Ecdysozoa. The other ecdysozoan phyla could be valuable models for comparative biology, taking advantage of the rich and continual sources of research findings as well as tools from both C. elegans and Drosophila. But when the Ecdysozoa was first recognized, few tools were available for laboratory studies in any of these six other ecdysozoan phyla. In 1999 I began an effort to develop tools for studying one such phylum, the tardigrades. Here, I describe how the tardigrade species Hypsibius exemplaris and tardigrades more generally have emerged over the past two decades as valuable new models for answering diverse questions. To date, these questions have included how animal body plans evolve and how biological materials can survive some remarkably extreme conditions.


2018 ◽  
Vol 41 (1) ◽  
pp. 349-369 ◽  
Author(s):  
Scott W. Emmons

The recently determined connectome of the Caenorhabditis elegans adult male, together with the known connectome of the hermaphrodite, opens up the possibility for a comprehensive description of sexual dimorphism in this species and the identification and study of the neural circuits underlying sexual behaviors. The C. elegans nervous system consists of 294 neurons shared by both sexes plus neurons unique to each sex, 8 in the hermaphrodite and 91 in the male. The sex-specific neurons are well integrated within the remainder of the nervous system; in the male, 16% of the input to the shared component comes from male-specific neurons. Although sex-specific neurons are involved primarily, but not exclusively, in controlling sex-unique behavior—egg-laying in the hermaphrodite and copulation in the male—these neurons act together with shared neurons to make navigational choices that optimize reproductive success. Sex differences in general behaviors are underlain by considerable dimorphism within the shared component of the nervous system itself, including dimorphism in synaptic connectivity.


1994 ◽  
Vol 21 (1) ◽  
pp. 9-31 ◽  
Author(s):  
Martin D. S. Braine

ABSTRACTThe past and present state of the empiricism–nativism issue is analysed. Empiricist philosophical doctrine (‘no innate ideas’) distinguished idea from structure or mechanism. However, Chomsky's conception of innate linguistic universals erased this distinction. The elimination left would-be empiricists without a coherent and defensible position. I argue that the issue remains alive primarily because of tension between two scientific tasks that face students of development. One is to discover what is cognitively and linguistically primitive, a task that encourages nativism. However, nativism is ultimately unsatisfactory because it systematically neglects the other task, which is to account for development, including the emergence of postulated innate primitives. To account for such primitives, it is necessary to relate them to particular central nervous System structures in such a way as to explain how the structure has the particular cognitive effects that define the primitive. That is likely to be difficult, and I show how the study of learning – much neglected in recent years – can help by reducing the number and type of innate primitives whose origin must be explained in that way.


1960 ◽  
Vol 106 (442) ◽  
pp. 76-92 ◽  
Author(s):  
Edward Marley

Nearly one hundred years ago, Anstie (1864) wrote: “Among the too frequent instances which are to be found in medical nomenclature, of confusion and uncertainty in the application of descriptive terms, there is none, perhaps, more striking than is occupied by the words Narcotic and Stimulant.” Both classes of substance embrace drugs of antiquity. Thus of the depressants, alcohol dates from the time of the Thracian god, Dionysus, while the earliest use of stimulants such as caffeine and xanthine is lost in the obscurity of the past (Goodman and Gilman, 1955a). Even today, there exists no systematized codification of response to the two classes of drug, although it is implicitly assumed that stimulants and depressants are invariably and mutually antagonistic in their effect on the central nervous system. Advantage was therefore taken of phenomena arising during drug intoxications to categorize abnormal features in the central nervous system common to each of the two classes of intoxicant and to essay a comparison, the one with the other.


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