Targeted thermal stimulation and high-content phenotyping reveal that the C. elegans escape response integrates current behavioral state and past experience

Rodgers, Jarlath Byrne; Ryu, William S.

doi:10.1371/journal.pone.0229399

Cited by 10 publications

(12 citation statements)

References 69 publications

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“…elegans (Ardiel et al, 2017;Byrne Rodgers and Ryu, 2020;Chew et al, 2018). Therefore, we delivered a sudden, noxious heat stimulus to animals part way through our recordings (Figure 6A,E).…”

Section: An Atlas Of How the Defined Neuron Types In The C Elegans Co...mentioning

confidence: 99%

Brain-wide representations of behavior spanning multiple timescales and states inC. elegans

Atanas

Kim

Wang

et al. 2022

Preprint

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Changes in an animal's behavior and internal state are accompanied by widespread changes in activity across its brain. However, how neurons across the brain encode behavior and how this is impacted by state is poorly understood. We recorded brain-wide activity and the diverse motor programs of freely-moving C. elegans and built probabilistic models that explain how each neuron encodes quantitative features of the animal's behavior. By determining the identities of the recorded neurons, we created, for the first time, an atlas of how the defined neuron classes in the C. elegans connectome encode behavior. Many neuron classes have conjunctive representations of multiple behaviors. Moreover, while many neurons encode current motor actions, others encode recent actions. Changes in behavioral state are accompanied by widespread changes in how neurons encode behavior, and we identify these flexible nodes in the connectome. Our results provide a global map of how the cell types across an animal's brain encode its behavior.

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Section: An Atlas Of How the Defined Neuron Types In The C Elegans Co...mentioning

confidence: 99%

Brain-wide representations of behavior spanning multiple timescales and states inC. elegans

Atanas

Kim

Wang

et al. 2022

Preprint

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“…In a thermal barrier assay, heat avoidance relies on the NPR-1/FLP-21 receptor in the interneuron RMG [ 38 ]. The noxious heat escape response of C. elegans proved to exhibit high plasticity, modulated by the thermal context as well as the past thermal experience, food and behavioral state of the animals [ 40 , 46 ]. Furthermore, the avoidance response seems to integrate information from several, parallel neural circuits, with partial functional redundancy, in order to allow a robust behavior strategy under dynamic environmental conditions [ 23 ].…”

Section: The Thermosensory Circuitmentioning

confidence: 99%

The Thermal Stress Coping Network of the Nematode Caenorhabditis elegans

Kyriakou

Taouktsi

Syntichaki

2022

IJMS

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Response to hyperthermia, highly conserved from bacteria to humans, involves transcriptional upregulation of genes involved in battling the cytotoxicity caused by misfolded and denatured proteins, with the aim of proteostasis restoration. C. elegans senses and responds to changes in growth temperature or noxious thermal stress by well-defined signaling pathways. Under adverse conditions, regulation of the heat shock response (HSR) in C. elegans is controlled by a single transcription factor, heat-shock factor 1 (HSF-1). HSR and HSF-1 in particular are proven to be central to survival under proteotoxic stress, with additional roles in normal physiological processes. For years, it was a common belief that upregulation of heat shock proteins (HSPs) by HSF-1 was the main and most important step toward thermotolerance. However, an ever-growing number of studies have shown that targets of HSF-1 involved in cytoskeletal and exoskeletal integrity preservation as well as other HSF-1 dependent and independent pathways are equally important. In this review, we follow the thermal stimulus from reception by the nematode nerve endings till the activation of cellular response programs. We analyze the different HSF-1 functions in HSR as well as all the recently discovered mechanisms that add to the knowledge of the heat stress coping network of C. elegans.

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“…A constitutive input from AVA may reflect a tonic activation of its synaptic activity. We examined this possibility through dosage-dependent chemogenetic hyperpolarization by a histamine-gated chloride channel (HisCl) 31 .…”

Section: Titrated Chemogenetic Hyperpolarization Isolates Ava's Poten...mentioning

confidence: 99%

“…Previous measurements of C. elegans locomotion have revealed additional features not captured by this model. Examples include the continuous decay of forward speed prior to the transition into backward movement 6, 18, 22, 30 , the period of post-stimulus arousal, during which animals exhibit a higher than pre-stimulus velocity after they exit escape responses 31 , and the observation that reducing the activity of premotor interneurons of the backward module decreases not only the backward but also forward speed 32 .…”

Section: Introductionmentioning

confidence: 99%

A tonically active master neuron modulates mutually exclusive motor states at two timescales

Meng

Ahamed

et al. 2022

Preprint

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Mutually exclusive behaviors in animals are often driven by independent motor subcircuits that directly or indirectly inhibit each other. For example, in the nematode C. elegans, motor circuits for forward and backward locomotion are gated by premotor interneurons AVB and AVA respectively, which are thought to be connected via reciprocal inhibition. In this study, we dissect the interactions between forward and motor subcircuits in C. elegans by genetic manipulation of AVA's activity via cell-specific characterization of a two-pore potassium channel (TWK-40). AVA has an unusually depolarized resting membrane potential (RMP). Perturbations to its RMP through AVA-specific TWK-40 loss-of-function and AVA-specific TWK-40 gain-of-function, led to dramatic changes in both forward and backward motor activity. AVA, thus regulated both backward and forward locomotion in C. elegans, functioning as a master neuron for overall locomotion. These effects required chemical transmission from AVA and were dependent on AVB neurons. We were able to reconcile results of genetic perturbation with optogenetic manipulation by carefully designed stimulation protocols. Finding that phasic optogenetic activation of AVA leads to backward locomotion, while tonic optogenetic activation potentiates forward locomotion. These results propose that a single neuron can regulate the activity of motor circuits generating two mutually exclusive behaviors.

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Targeted thermal stimulation and high-content phenotyping reveal that the C. elegans escape response integrates current behavioral state and past experience

Cited by 10 publications

References 69 publications

Brain-wide representations of behavior spanning multiple timescales and states inC. elegans

Brain-wide representations of behavior spanning multiple timescales and states inC. elegans

The Thermal Stress Coping Network of the Nematode Caenorhabditis elegans

A tonically active master neuron modulates mutually exclusive motor states at two timescales

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