Dimensionality and Dynamics in the Behavior of C. elegans

Stephens, Greg J.; Johnson-Kerner, Bethany L.; Bialek, William; Ryu, William S.

doi:10.1371/journal.pcbi.1000028

Cited by 452 publications

(691 citation statements)

References 35 publications

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“…To demonstrate this more quantitatively, simulations were also performed using a network producing two simultaneous outputs which were used to control the motion of a two-mode (eigenworm) swimmer as studied in Refs. [11,44]. As would be expected, the motion of the two-mode crawling behavior is negatively impacted by introducing FAS into the simulated network.…”

Section: Proxy For Behavioral Deficitssupporting

confidence: 60%

“…Importantly, the FORCE model suggests an underlying biological mechanism by which collections of neurons can organize their behavior into target functions in order to enact sophisticated control protocols associated with behavior and/or functional activity. In living organisms, these target functions encode important biological functions such as motor actions [11] or sensory information [12,13]. In fact, simpler organisms like the nematode exhibit complex motor behaviors by combining a small number of body-shape modes [11], thus suggesting how target functions can be used for simple tasks like locomotion.…”

Section: Introductionmentioning

confidence: 99%

“…In living organisms, these target functions encode important biological functions such as motor actions [11] or sensory information [12,13]. In fact, simpler organisms like the nematode exhibit complex motor behaviors by combining a small number of body-shape modes [11], thus suggesting how target functions can be used for simple tasks like locomotion. In this study, we simulate networks with these key properties but in the presence of injurious effects arising from FAS that are believed to occur in many neural pathologies and TBI.…”

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Cognitive and behavioral deficits arising from neurodegeneration and traumatic brain injury: a model for the underlying role of focal axonal swellings in neuronal networks with plasticity

Rudy¹,

Maia²,

Kutz³

2016

J Integr Syst Neurosci

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Neurodegenerative diseases and traumatic brain injury, whose hallmark features are the presence of focal axonal swellings (FAS), are leading causes of cognitive dysfunction. By leveraging biophysical observations of FAS statistics, we develop a theoretical model of functional neural network activity driven by adaptive changes from plasticity. Based upon the FORCE model of Sussillo and Abbott [1], our innovations highlight the role of plasticity in overcoming injuries and degeneration of neurons in a network architecture. We provide a quantitative measure, on a network level, of cognitive deficits arising from injury. We demonstrate that plasticity is capable of overcoming mild injuries while failing to compensate for more severe injuries. Such injuries are characterized by their underlying effect on spike trains propagating through the neurons in a network architecture. Specifically, spike trains can be filtered in firing rate, or blocked under more severe FAS. The level of injury dictates the FORCE model's ability to produce a desired output functionality (and associated behavior) and allows for quantitative metrics for accessing cognitive and behavioral deficits. Thus a direct link between FAS in neural networks and compromised functional response can be established. The theoretical framework developed is a promising computational framework for providing a deeper understanding of the cognitive deficits arising in, for instance, Alzheimer's, Parkinson's, Multiple-Sclerosis, and TBI.

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Section: Proxy For Behavioral Deficitssupporting

confidence: 60%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Cognitive and behavioral deficits arising from neurodegeneration and traumatic brain injury: a model for the underlying role of focal axonal swellings in neuronal networks with plasticity

Rudy¹,

Maia²,

Kutz³

2016

J Integr Syst Neurosci

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“…One such intermediate system is the multicellular round worm Caenorhabditis elegans, a widely studied model organism. The importance of C. elegans mechanics is highlighted by previous studies suggesting that the worm's locomotory patterns and foraging behaviors are strongly dependent on mechanical and osmotic stresses (13)(14)(15). Indeed, external mechanical forces lead to the activation of known mechanosensory signal transduction pathways (16,17).…”

Section: Introductionmentioning

confidence: 99%

Worms under Pressure: Bulk Mechanical Properties of C. elegans Are Independent of the Cuticle

Gilpin

Uppaluri

Brangwynne

2015

Biophysical Journal

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The mechanical properties of cells and tissues play a well-known role in physiology and disease. The model organism Caenorhabditis elegans exhibits mechanical properties that are still poorly understood, but are thought to be dominated by its collagen-rich outer cuticle. To our knowledge, we use a novel microfluidic technique to reveal that the worm responds linearly to low applied hydrostatic stress, exhibiting a volumetric compression with a bulk modulus, k ¼ 140 5 20 kPa; applying negative pressures leads to volumetric expansion of the worm, with a similar bulk modulus. Surprisingly, however, we find that a variety of collagen mutants and pharmacological perturbations targeting the cuticle do not impact the bulk modulus. Moreover, the worm exhibits dramatic stiffening at higher stresses-behavior that is also independent of the cuticle. The stress-strain curves for all conditions can be scaled onto a master equation, suggesting that C. elegans exhibits a universal elastic response dominated by the mechanics of pressurized internal organs.

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“…Behavior can often be accurately quantified by tracking and video microscopy [15,16,18] and by using respective analysis software [53]. Sophisticated analysis algorithms permit behavior analysis in simple as well as complex parameters [42,43,44], or by principal components analysis (PCA; [14,36]). For certain mutations, or when individual neurons are silenced optogenetically or laser ablated, one can often observe measurable characteristic changes in behavioral parameters.…”

Section: Simple Nervous System Complex Behaviormentioning

confidence: 99%

Optogenetic analyses of neuronal network function and synaptic transmission in Caenorhabditis elegans

Gottschalk

2014

E-Neuroforum

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Caenorhabditis elegans is a popular model organism in the neurosciences [4]. This animal stands out in particular due to a (seemingly) simple nervous system consisting of only 302 neurons. Based on the fundamental research by John White and colleagues from the 1970s and 1980s, these neurons are precisely mapped in the entirety of their synaptic connections (chemical and electrical synapses; [51]): by means of serial electron microscopy, the entire nervous system, synapse by synapse and including all anatomical connections, has been unraveled. Since eutely (having a fixed number of somatic cells) occurs in every single individual of C. elegans and since it can be expected that the synapses are genetically determined and not destined by plasticity or learning, one can expect consistency of synapses between individuals. However, evidence for this still needs to be provided by serial electron microscopy and connectomics being conducted on several individuals; even with modern block-face imaging and semi-automatic segmentation, this requires huge effort. White et al. [51] have been able to map about 7000 synapses in between the 302 neurons and muscle cells. In this neuronal network, elementary circuits can be found which, in an analogous, logical way of operation, can also be found in the nervous system of higher animals, with the difference that they exist in myriads of copies and work in parallel in order to comply with more complex tasks. The majority of synaptic key factors is highly conserved between humans and nematodes and, in most cases, these have been identified in C. elegans for the first time [6,29]. Thus, the nervous system of C. elegans is not only a valid model for higher nervous systems on the protein level, but also on the level of basic circuits or logical circuitry modules. Simple nervous system, complex behaviorAs simple as C. elegans seems to be as an animal, the more versatile upon closer analysis are the behavioral patterns this animal is able to generate [39]. C. elegans carries out several types of locomotion, navigation in two and three dimensions, as well as complex mating behaviors [5]. The nematode has sensors for numerous modalities, e.g., temperature, chemicals, tastants, oxygen and CO 2 , perception of light and magnetic fields, as well as various types of mechano-and nociception. Most of these sensory modalities lead to responses in the form of taxis, escape behavior, or altered navigation. However, long-term changes in behavior can also occur, as well as switching between different behavioral states (mainly regulated by neuromodulators). The animal exhibits several types of quiescence behaviors, which feature characteristics of sleep [31]. Furthermore, the nervous system features habituation as well as simple forms of (associative) learning [2,34]. Single modes of behavior are often controlled by a few neurons that form simple circuits. This means that the control of behavior is determined by the physiological characteristics and synaptic connections of the 302 neurons.Cultivation of...

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Dimensionality and Dynamics in the Behavior of C. elegans

Cited by 452 publications

References 35 publications

Cognitive and behavioral deficits arising from neurodegeneration and traumatic brain injury: a model for the underlying role of focal axonal swellings in neuronal networks with plasticity

Cognitive and behavioral deficits arising from neurodegeneration and traumatic brain injury: a model for the underlying role of focal axonal swellings in neuronal networks with plasticity

Worms under Pressure: Bulk Mechanical Properties of C. elegans Are Independent of the Cuticle

Optogenetic analyses of neuronal network function and synaptic transmission in Caenorhabditis elegans

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