scholarly journals Whole-organism behavioral profiling reveals a role for dopamine in state-dependent motor program coupling in C. elegans

2020 ◽  
Author(s):  
Nathan Cermak ◽  
Stephanie K. Yu ◽  
Rebekah Clark ◽  
Yung-Chi Huang ◽  
Steven W. Flavell
Keyword(s):  
Motor Program ◽  
Egg Laying ◽  
Neural Mechanisms ◽  
Dependent Manner ◽  
Motor Programs ◽  
C Elegans ◽  
Motor Circuits ◽  
State Dependent ◽  
Behavioral States ◽  
Behavioral Profiling

AbstractAnimal behaviors are commonly organized into long-lasting states that coordinately impact the generation of diverse motor outputs such as feeding, locomotion, and grooming. However, the neural mechanisms that coordinate these diverse motor programs remain poorly understood. Here, we examine how the distinct motor programs of the nematode C. elegans are coupled together across behavioral states. We describe a new imaging platform that permits automated, simultaneous quantification of each of the main C. elegans motor programs over hours or days. Analysis of these whole-organism behavioral profiles shows that the motor programs coordinately change as animals switch behavioral states. Utilizing genetics, optogenetics, and calcium imaging, we identify a new role for dopamine in coupling locomotion and egg-laying together across states. These results provide new insights into how the diverse motor programs throughout an organism are coordinated and suggest that neuromodulators like dopamine can couple motor circuits together in a state-dependent manner.

scholarly journals Whole-organism behavioral profiling reveals a role for dopamine in state-dependent motor program coupling in C. elegans

eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Nathan Cermak ◽  
Stephanie K Yu ◽  
Rebekah Clark ◽  
Yung-Chi Huang ◽  
Saba N Baskoylu ◽  
...  
Keyword(s):  
Motor Program ◽  
Egg Laying ◽  
Neural Mechanisms ◽  
Dependent Manner ◽  
Motor Programs ◽  
C Elegans ◽  
Motor Circuits ◽  
State Dependent ◽  
Behavioral States ◽  
Behavioral Profiling

Animal behaviors are commonly organized into long-lasting states that coordinately impact the generation of diverse motor outputs such as feeding, locomotion, and grooming. However, the neural mechanisms that coordinate these distinct motor programs remain poorly understood. Here, we examine how the distinct motor programs of the nematode C. elegans are coupled together across behavioral states. We describe a new imaging platform that permits automated, simultaneous quantification of each of the main C. elegans motor programs over hours or days. Analysis of these whole-organism behavioral profiles shows that the motor programs coordinately change as animals switch behavioral states. Utilizing genetics, optogenetics, and calcium imaging, we identify a new role for dopamine in coupling locomotion and egg-laying together across states. These results provide new insights into how the diverse motor programs throughout an organism are coordinated and suggest that neuromodulators like dopamine can couple motor circuits together in a state-dependent manner.

scholarly journals Author response: Whole-organism behavioral profiling reveals a role for dopamine in state-dependent motor program coupling in C. elegans

2020 ◽  
Author(s):  
Nathan Cermak ◽  
Stephanie K Yu ◽  
Rebekah Clark ◽  
Yung-Chi Huang ◽  
Saba N Baskoylu ◽  
...  
Keyword(s):  
Motor Program ◽  
Author Response ◽  
C Elegans ◽  
State Dependent ◽  
Behavioral Profiling

scholarly journals Modeling of a negative feedback mechanism explains age-dependent genetic architecture in reproduction in domesticated C. elegans strains

2017 ◽  
Author(s):  
Edward E. Large ◽  
Raghavendra Padmanabhan ◽  
Kathie L. Watkins ◽  
Richard F. Campbell ◽  
Wen Xu ◽  
...  
Keyword(s):  
Negative Feedback ◽  
Effect Size ◽  
Genetic Variants ◽  
Communication Systems ◽  
Genetic Architecture ◽  
Egg Laying ◽  
Biological Traits ◽  
Dependent Manner ◽  
C Elegans ◽  
Age Dependent

ABSTRACTMost biological traits and common diseases have a strong but complex genetic basis, controlled by large numbers of genetic variants with small contributions to a trait or disease risk. The effect-size of most genetic variants is not absolute, but can depend on a number of factors including the age and genetic background of an organism. In order to understand the mechanisms that cause these changes, we are studying heritable trait differences between two domesticated strains of C. elegans. We previously identified a major effect locus, caused by a mutation in a component of the NURF chromatin remodeling complex, that regulated reproductive output in an age-dependent manner. The effect-size of this locus changes from positive to negative over the course of an animal’s reproductive lifespan. Using a previously published macroscale model of egg-laying rate in C. elegans, we show how time-dependent effect-size can be explained by an unequal use of sperm combined with negative feedback between sperm and ovulation rate. We validate a number of key predictions of this model using controlled mating experiments and quantification of oogenesis and sperm use. By incorporating this model into QTL mapping, we identify and partition new QTLs into specific aspects of the egg-laying process. Finally, we show how epistasis between two genetic variants is predicted by this modeling as a consequence of unequal use of sperm. This work demonstrates how modeling of multicellular communication systems can improve our ability to predict and understand the role of genetic variation on a complex phenotype. Negative autoregulatory feedback loops, common in transcriptional regulation, could play an important role in modifying genetic architecture in other traits.AUTHOR SUMMARYComplex traits are influenced not only by the individual effects of genetic variants, but also how these variants interact with the environment, age, and each other. While complex genetic architectures seem to be ubiquitous in natural traits, little is known about the mechanisms that cause them. Here we identify an example of age-dependent genetic architecture controlling the rate and timing of reproduction in the hermaphroditic nematode C. elegans. Using computational modeling, we demonstrate how this age-dependent genetic architecture can arise as a consequence of two factors: hormonal feedback on oocytes mediated by major sperm protein (MSP) released by sperm stored in the spermatheca and life history differences in sperm use caused by genetic variants. Our work also suggests how age-dependent epistasis can emerge from multicellular feedback systems.

Distributed Representation of Limb Motor Programs in Arrays of Adjustable Pattern Generators

1993 ◽  
Vol 5 (1) ◽  
pp. 56-78 ◽  
Author(s):  
N. E. Berthier ◽  
S. P. Singh ◽  
A. G. Barto ◽  
J. C. Houk
Keyword(s):  
Red Nucleus ◽  
Motor Program ◽  
Neural Mechanisms ◽  
Computational Framework ◽  
Motor Programs ◽  
Reaching Task ◽  
Anatomy And Physiology ◽  
Current State ◽  
Simplifying Assumptions ◽  
Pattern Generators

This paper describes the current state of our exploration of how motor program concepts may be related to neural mechanisms. We have proposed a model of sensorimotor networks with architectures inspired by the anatomy and physiology of the cerebellum and its interconnections with the red nucleus and the motor cortex. We proposed the concept of rubrocerebellar and corticocerebellar information processing modules that function as adjustable pattern generators (APGs) capable of the storage, recall, and execution of motor programs. The APG array model described in this paper extends the single APG model of Houk et al. (1990) to an array of APGs whose collective activity controls movement of a simple two degree-of-freedom simulated limb. Our objective was to examine the APG array theory in a simple computational framework with a plausible relationship to anatomy and physiology. Results of simulation experiments show that the APG array model is capable of learning how to control movement of the simulated limb by adjusting distributed motor programs. Although the model is based on many simplifying assumptions, and the simulated motor control task is much simpler than an actual reaching task, these results suggest that the APG array model may provide a useful step toward a more comprehensive understanding of how neural mechanisms may generate motor programs.

A Cuticle Collagen Encoded by the lon-3 Gene May Be a Target of TGF-β Signaling in Determining Caenorhabditis elegans Body Shape

Genetics ◽  
2002 ◽  
Vol 162 (4) ◽  
pp. 1631-1639
Author(s):  
Yo Suzuki ◽  
Gail A Morris ◽  
Min Han ◽  
William B Wood
Keyword(s):  
Caenorhabditis Elegans ◽  
Body Shape ◽  
Small Body ◽  
Dependent Manner ◽  
Loss Of Function ◽  
Cellular Mechanisms ◽  
C Elegans ◽  
Gene Expression Analyses ◽  
Dose Dependent

Abstract The signaling pathway initiated by the TGF-β family member DBL-1 in Caenorhabditis elegans controls body shape in a dose-dependent manner. Loss-of-function (lf) mutations in the dbl-1 gene cause a short, small body (Sma phenotype), whereas overexpression of dbl-1 causes a long body (Lon phenotype). To understand the cellular mechanisms underlying these phenotypes, we have isolated suppressors of the Sma phenotype resulting from a dbl-1(lf) mutation. Two of these suppressors are mutations in the lon-3 gene, of which four additional alleles are known. We show that lon-3 encodes a collagen that is a component of the C. elegans cuticle. Genetic and reporter-gene expression analyses suggest that lon-3 is involved in determination of body shape and is post-transcriptionally regulated by the dbl-1 pathway. These results support the possibility that TGF-β signaling controls C. elegans body shape by regulating cuticle composition.

scholarly journals Effect of a Neuropeptide Gene on Behavioral States in Caenorhabditis elegans Egg-Laying

Genetics ◽  
2000 ◽  
Vol 154 (3) ◽  
pp. 1181-1192 ◽  
Author(s):  
Laura E Waggoner ◽  
Laura Anne Hardaker ◽  
Steven Golik ◽  
William R Schafer
Keyword(s):  
Caenorhabditis Elegans ◽  
Active Phase ◽  
Egg Laying ◽  
Sensory Cues ◽  
Nematode Caenorhabditis Elegans ◽  
Inactive State ◽  
Recessive Mutations ◽  
Inactive Phase ◽  
Behavioral States ◽  
Stimulation Of

Abstract Egg-laying behavior in the nematode Caenorhabditis elegans involves fluctuation between alternative behavioral states: an inactive state, during which eggs are retained in the uterus, and an active state, during which eggs are laid in bursts. We have found that the flp-1 gene, which encodes a group of structurally related neuropeptides, functions specifically to promote the switch from the inactive to the active egg-laying state. Recessive mutations in flp-1 caused a significant increase in the duration of the inactive phase, yet egg-laying within the active phase was normal. This pattern resembled that previously observed in mutants defective in the biosynthesis of serotonin, a neuromodulator implicated in induction of the active phase. Although flp-1 mutants were sensitive to stimulation of egg-laying by serotonin, the magnitude of their serotonin response was abnormally low. Thus, the flp-1-encoded peptides and serotonin function most likely function in concert to facilitate the onset of the active egg-laying phase. Interestingly, we observed that flp-1 is necessary for animals to down-regulate their rate of egg-laying in the absence of food. Because flp-1 is known to be expressed in interneurons that are postsynaptic to a variety of chemosensory cells, the FLP-1 peptides may function to regulate the activity of the egg-laying circuitry in response to sensory cues.

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