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Article ; Online: A dynamical model of

Roman, Ahmed / Palanski, Konstantine / Nemenman, Ilya / Ryu, William S

Proceedings of the National Academy of Sciences of the United States of America

2023 Volume 120, Issue 13, Page(s) e2215191120

Abstract: Caenorhabditis ... ...

Abstract	Caenorhabditis elegans
MeSH term(s)	Animals ; Caenorhabditis elegans/metabolism ; Behavior, Animal/physiology ; Learning ; Temperature ; Caenorhabditis elegans Proteins/genetics ; Caenorhabditis elegans Proteins/metabolism
Chemical Substances	Caenorhabditis elegans Proteins
Language	English
Publishing date	2023-03-20
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	209104-5
ISSN	1091-6490 ; 0027-8424
ISSN (online)	1091-6490
ISSN	0027-8424
DOI	10.1073/pnas.2215191120
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Article ; Online: Targeted thermal stimulation and high-content phenotyping reveal that the C. elegans escape response integrates current behavioral state and past experience.

Byrne Rodgers, Jarlath / Ryu, William S

PloS one

2020 Volume 15, Issue 3, Page(s) e0229399

Abstract: The ability to avoid harmful or potentially harmful stimuli can help an organism escape predators and injury, and certain avoidance mechanisms are conserved across the animal kingdom. However, how the need to avoid an imminent threat is balanced with ... ...

Abstract	The ability to avoid harmful or potentially harmful stimuli can help an organism escape predators and injury, and certain avoidance mechanisms are conserved across the animal kingdom. However, how the need to avoid an imminent threat is balanced with current behavior and modified by past experience is not well understood. In this work we focused on rapidly increasing temperature, a signal that triggers an escape response in a variety of animals, including the nematode Caenorhabditis elegans. We have developed a noxious thermal response assay using an infrared laser that can be automatically controlled and targeted in order to investigate how C. elegans responds to noxious heat over long timescales and to repeated stimuli in various behavioral and sensory contexts. High-content phenotyping of behavior in individual animals revealed that the C. elegans escape response is multidimensional, with some features that extend for several minutes, and can be modulated by (i) stimulus amplitude; (ii) other sensory inputs, such as food context; (iii) long and short-term thermal experience; and (iv) the animal's current behavioral state.
MeSH term(s)	Animals ; Avoidance Learning/physiology ; Behavior, Animal/physiology ; Caenorhabditis elegans/physiology ; Escape Reaction/physiology ; Hot Temperature ; Phenotype ; Sensory Receptor Cells/cytology ; Sensory Receptor Cells/metabolism ; Thermosensing/physiology
Language	English
Publishing date	2020-03-27
Publishing country	United States
Document type	Journal Article
ZDB-ID	2267670-3
ISSN	1932-6203 ; 1932-6203
ISSN (online)	1932-6203
ISSN	1932-6203
DOI	10.1371/journal.pone.0229399
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Book ; Online: Multi-dimensional structure of C. elegans thermal learning

Roman, Ahmed / Palanski, Konstantine / Nemenman, Ilya / Ryu, William S

2022

Abstract: Quantitative models of associative learning that explain the behavior of real animals with high precision have turned out very difficult to construct. We do this in the context of the dynamics of the thermal preference of C. elegans. For this, we ... ...

Abstract	Quantitative models of associative learning that explain the behavior of real animals with high precision have turned out very difficult to construct. We do this in the context of the dynamics of the thermal preference of C. elegans. For this, we quantify C. elegans thermotaxis in response to various conditioning parameters, genetic perturbations, and operant behavior using a fast, high-throughput microfluidic droplet assay. We then model this data comprehensively, within a new, biologically interpretable, multi-modal framework. We discover that the dynamics of thermal preference are described by two independent contributions and require a model with at least four dynamical variables. One pathway positively associates the experienced temperature independently of food and the other negatively associates to the temperature when food is absent.
Keywords	Physics - Biological Physics ; Quantitative Biology - Neurons and Cognition
Publishing date	2022-06-01
Publishing country	us
Document type	Book ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: Automated, predictive, and interpretable inference of

Daniels, Bryan C / Ryu, William S / Nemenman, Ilya

Proceedings of the National Academy of Sciences of the United States of America

2019 Volume 116, Issue 15, Page(s) 7226–7231

Abstract: ... The ... ...

Abstract	The roundworm
MeSH term(s)	Animals ; Caenorhabditis elegans/physiology ; Escape Reaction/physiology ; Hot Temperature ; Models, Biological
Language	English
Publishing date	2019-03-22
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	209104-5
ISSN	1091-6490 ; 0027-8424
ISSN (online)	1091-6490
ISSN	0027-8424
DOI	10.1073/pnas.1816531116
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Article ; Online: Genetically Distinct Behavioral Modules Underlie Natural Variation in Thermal Performance Curves.

Stegeman, Gregory W / Baird, Scott E / Ryu, William S / Cutter, Asher D

G3 (Bethesda, Md.)

2019 Volume 9, Issue 7, Page(s) 2135–2151

Abstract: Thermal reaction norms pervade organismal traits as stereotyped responses to temperature, a fundamental environmental input into sensory and physiological systems. Locomotory behavior represents an especially plastic read-out of animal response, with its ...

Abstract	Thermal reaction norms pervade organismal traits as stereotyped responses to temperature, a fundamental environmental input into sensory and physiological systems. Locomotory behavior represents an especially plastic read-out of animal response, with its dynamic dependence on environmental stimuli presenting a challenge for analysis and for understanding the genomic architecture of heritable variation. Here we characterize behavioral reaction norms as thermal performance curves for the nematode
MeSH term(s)	Animals ; Behavior, Animal ; Caenorhabditis ; Chromosome Mapping ; Gene-Environment Interaction ; Genetic Association Studies ; Genetic Variation ; Genotype ; Locomotion ; Models, Biological ; Phenotype ; Quantitative Trait Loci ; Quantitative Trait, Heritable ; Temperature
Language	English
Publishing date	2019-07-09
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2629978-1
ISSN	2160-1836 ; 2160-1836
ISSN (online)	2160-1836
ISSN	2160-1836
DOI	10.1534/g3.119.400043
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Article ; Online: Neuro-genetic plasticity of Caenorhabditis elegans behavioral thermal tolerance.

Stegeman, Gregory W / Medina, Denise / Cutter, Asher D / Ryu, William S

BMC neuroscience

2019 Volume 20, Issue 1, Page(s) 26

Abstract: Background: Animal responses to thermal stimuli involve intricate contributions of genetics, neurobiology and physiology, with temperature variation providing a pervasive environmental factor for natural selection. Thermal behavior thus exemplifies a ... ...

Abstract	Background: Animal responses to thermal stimuli involve intricate contributions of genetics, neurobiology and physiology, with temperature variation providing a pervasive environmental factor for natural selection. Thermal behavior thus exemplifies a dynamic trait that requires non-trivial phenotypic summaries to appropriately capture the trait in response to a changing environment. To characterize the deterministic and plastic components of thermal responses, we developed a novel micro-droplet assay of nematode behavior that permits information-dense summaries of dynamic behavioral phenotypes as reaction norms in response to increasing temperature (thermal tolerance curves, TTC). Results: We found that C. elegans TTCs shift predictably with rearing conditions and developmental stage, with significant differences between distinct wildtype genetic backgrounds. Moreover, after screening TTCs for 58 C. elegans genetic mutant strains, we determined that genes affecting thermosensation, including cmk-1 and tax-4, potentially play important roles in the behavioral control of locomotion at high temperature, implicating neural decision-making in TTC shape rather than just generalized physiological limits. However, expression of the transient receptor potential ion channel TRPA-1 in the nervous system is not sufficient to rescue rearing-dependent plasticity in TTCs conferred by normal expression of this gene, indicating instead a role for intestinal signaling involving TRPA-1 in the adaptive plasticity of thermal performance. Conclusions: These results implicate nervous system and non-nervous system contributions to behavior, in addition to basic cellular physiology, as key mediators of evolutionary responses to selection from temperature variation in nature.
MeSH term(s)	Adaptation, Physiological/genetics ; Adaptation, Physiological/physiology ; Animals ; Caenorhabditis elegans ; Caenorhabditis elegans Proteins/biosynthesis ; Caenorhabditis elegans Proteins/genetics ; Caenorhabditis elegans Proteins/physiology ; Calcium-Calmodulin-Dependent Protein Kinase Type 2/genetics ; Calcium-Calmodulin-Dependent Protein Kinase Type 2/physiology ; Hot Temperature ; Ion Channels/genetics ; Ion Channels/physiology ; Life Cycle Stages/physiology ; Locomotion/physiology ; Mutation ; Nervous System/metabolism ; TRPA1 Cation Channel/biosynthesis ; TRPA1 Cation Channel/physiology ; Thermosensing/physiology
Chemical Substances	Caenorhabditis elegans Proteins ; Ion Channels ; TRPA1 Cation Channel ; tax-4 protein, C elegans ; trpa-1 protein, C elegans ; Calcium-Calmodulin-Dependent Protein Kinase Type 2 (EC 2.7.11.17) ; cmk-1 protein, C elegans (EC 2.7.11.17)
Language	English
Publishing date	2019-06-10
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ISSN	1471-2202
ISSN (online)	1471-2202
DOI	10.1186/s12868-019-0510-z
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: The nematode C. elegans as a complex viscoelastic fluid.

Backholm, Matilda / Ryu, William S / Dalnoki-Veress, Kari

The European physical journal. E, Soft matter

2015 Volume 38, Issue 5, Page(s) 118

Abstract: The viscoelastic material properties of the model organism C. elegans were probed with a micropipette deflection technique and modelled with the standard linear solid model. Dynamic relaxation measurements were performed on the millimetric nematode to ... ...

Abstract	The viscoelastic material properties of the model organism C. elegans were probed with a micropipette deflection technique and modelled with the standard linear solid model. Dynamic relaxation measurements were performed on the millimetric nematode to investigate its viscous characteristics in detail. We show that the internal properties of C. elegans can not be fully described by a simple Newtonian fluid. Instead, a power-law fluid model was implemented and shown to be in excellent agreement with experimental results. The nematode exhibits shear thinning properties and its complex fluid characteristics were quantified. The bending-rate dependence of the internal damping coefficient of C. elegans could affect its gait modulation in different external environments.
MeSH term(s)	Animals ; Caenorhabditis elegans/physiology ; Elasticity ; Hydrodynamics ; Models, Biological ; Viscosity
Language	English
Publishing date	2015-05
Publishing country	France
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2004003-9
ISSN	1292-895X ; 1292-8941
ISSN (online)	1292-895X
ISSN	1292-8941
DOI	10.1140/epje/i2015-15036-1
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Article ; Online: (with research data) Resolving coiled shapes reveals new reorientation behaviors in C. elegans.

Broekmans, Onno D / Rodgers, Jarlath B / Ryu, William S / Stephens, Greg J

eLife

2016 Volume 5

Abstract: We exploit the reduced space of C. elegans postures to develop a novel tracking algorithm which captures both simple shapes and also self-occluding coils, an important, yet unexplored, component of 2D worm behavior. We apply our algorithm to show that ... ...

Abstract	We exploit the reduced space of C. elegans postures to develop a novel tracking algorithm which captures both simple shapes and also self-occluding coils, an important, yet unexplored, component of 2D worm behavior. We apply our algorithm to show that visually complex, coiled sequences are a superposition of two simpler patterns: the body wave dynamics and a head-curvature pulse. We demonstrate the precise Ω-turn dynamics of an escape response and uncover a surprising new dichotomy in spontaneous, large-amplitude coils; deep reorientations occur not only through classical Ω-shaped postures but also through larger postural excitations which we label here as δ-turns. We find that omega and delta turns occur independently, suggesting a distinct triggering mechanism, and are the serpentine analog of a random left-right step. Finally, we show that omega and delta turns occur with approximately equal rates and adapt to food-free conditions on a similar timescale, a simple strategy to avoid navigational bias.
MeSH term(s)	Algorithms ; Animals ; Behavior, Animal ; Caenorhabditis elegans/physiology ; Computer Simulation ; Locomotion ; Models, Biological
Language	English
Publishing date	2016-09-20
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2687154-3
ISSN	2050-084X ; 2050-084X
ISSN (online)	2050-084X
ISSN	2050-084X
DOI	10.7554/eLife.17227
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Article ; Online: Stereotypical Escape Behavior in Caenorhabditis elegans Allows Quantification of Effective Heat Stimulus Level.

Leung, Kawai / Mohammadi, Aylia / Ryu, William S / Nemenman, Ilya

PLoS computational biology

2016 Volume 12, Issue 12, Page(s) e1005262

Abstract: A goal of many sensorimotor studies is to quantify the stimulus-behavioral response relation for specific organisms and specific sensory stimuli. This is especially important to do in the context of painful stimuli since most animals in these studies ... ...

Abstract	A goal of many sensorimotor studies is to quantify the stimulus-behavioral response relation for specific organisms and specific sensory stimuli. This is especially important to do in the context of painful stimuli since most animals in these studies cannot easily communicate to us their perceived levels of such noxious stimuli. Thus progress on studies of nociception and pain-like responses in animal models depends crucially on our ability to quantitatively and objectively infer the sensed levels of these stimuli from animal behaviors. Here we develop a quantitative model to infer the perceived level of heat stimulus from the stereotyped escape response of individual nematodes Caenorhabditis elegans stimulated by an IR laser. The model provides a method for quantification of analgesic-like effects of chemical stimuli or genetic mutations in C. elegans. We test ibuprofen-treated worms and a TRPV (transient receptor potential) mutant, and we show that the perception of heat stimuli for the ibuprofen treated worms is lower than the wild-type. At the same time, our model shows that the mutant changes the worm's behavior beyond affecting the thermal sensory system. Finally, we determine the stimulus level that best distinguishes the analgesic-like effects and the minimum number of worms that allow for a statistically significant identification of these effects.
MeSH term(s)	Animals ; Caenorhabditis elegans/physiology ; Computer Simulation ; Escape Reaction/physiology ; Heat-Shock Response/physiology ; Hot Temperature ; Models, Biological ; Pain Measurement/methods ; Pain Perception/physiology ; Physical Stimulation/methods ; Stereotyped Behavior/physiology
Language	English
Publishing date	2016-12
Publishing country	United States
Document type	Journal Article
ZDB-ID	2193340-6
ISSN	1553-7358 ; 1553-734X
ISSN (online)	1553-7358
ISSN	1553-734X
DOI	10.1371/journal.pcbi.1005262
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Article ; Online: Viscoelastic properties of the nematode Caenorhabditis elegans, a self-similar, shear-thinning worm.

Backholm, Matilda / Ryu, William S / Dalnoki-Veress, Kari

Proceedings of the National Academy of Sciences of the United States of America

2013 Volume 110, Issue 12, Page(s) 4528–4533

Abstract: Undulatory motion is common to many creatures across many scales, from sperm to snakes. These organisms must push off against their external environment, such as a viscous medium, grains of sand, or a high-friction surface; additionally they must work to ...

Abstract	Undulatory motion is common to many creatures across many scales, from sperm to snakes. These organisms must push off against their external environment, such as a viscous medium, grains of sand, or a high-friction surface; additionally they must work to bend their own body. A full understanding of undulatory motion, and locomotion in general, requires the characterization of the material properties of the animal itself. The material properties of the model organism Caenorhabditis elegans were studied with a micromechanical experiment used to carry out a three-point bending measurement of the worm. Worms at various developmental stages (including dauer) were measured and different positions along the worm were probed. From these experiments we calculated the viscoelastic properties of the worm, including the effective spring constant and damping coefficient of bending. C. elegans moves by propagating sinusoidal waves along its body. Whereas previous viscoelastic approaches to describe the undulatory motion have used a Kelvin-Voigt model, where the elastic and viscous components are connected in parallel, our measurements show that the Maxwell model, where the elastic and viscous components are in series, is more appropriate. The viscous component of the worm was shown to be consistent with a non-Newtonian, shear-thinning fluid. We find that as the worm matures it is well described as a self-similar elastic object with a shear-thinning damping term and a stiffness that becomes smaller as one approaches the tail.
MeSH term(s)	Animals ; Caenorhabditis elegans/physiology ; Elasticity ; Locomotion/physiology ; Models, Biological
Language	English
Publishing date	2013-03-04
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	209104-5
ISSN	1091-6490 ; 0027-8424
ISSN (online)	1091-6490
ISSN	0027-8424
DOI	10.1073/pnas.1219965110
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