Presynaptic MAST kinase controls opposing postsynaptic responses to convey stimulus valence in
            <i>Caenorhabditis elegans</i>

Nakano, Shunji; Ikeda, Motoko; Tsukada, Yuki; Fei, Xianfeng; Suzuki, Takamasa; Niino, Yusuke; Ahluwalia, Rhea; Sano, Ayana; Kondo, Rumi; Ihara, Kenji; Miyawaki, Atsushi; Hashimoto, Koichi; Higashiyama, Tetsuya; Mori, Ikue

doi:10.1073/pnas.1909240117

Cited by 26 publications

(63 citation statements)

References 74 publications

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“…4G (a)). This interpretation is in agreement with the previous studies on the relationship between AFD-AIY communication and thermotaxis (Hawk et al, 2018;Luo et al, 2014;Nakano et al, 2020). On the other hand, for starved animals, AIY responses are delayed to AFD responses or are synchronized in anti-phase with the AFD responses ( Fig.…”

Section: Discussionsupporting

confidence: 93%

“…The Multi-Worm Tracker (MWT) detects animals and measure the positions of their centroids and 11 segments along their bodies (Swierczek et al, 2011). Based on these data, the quantitative analysis was performed by MATLAB (MathWorks) scripts (Ikeda et al, 2018;Nakano et al, 2020;Yamaguchi et al, 2018). Several 9 behavioral components were categorized and their frequencies were calculated by the script as follows.…”

Section: Behavioral Analysismentioning

confidence: 99%

“…C. elegans is known to build their behavioral strategies by combining several behavioral components (Croll, 1975;Iino and Yoshida, 2009;Kim et al, 2011;Pierce-Shimomura et al, 1999;Salvador et al, 2014;Schild and Glauser, 2013). By using Multi-Worm Tracking system (Ikeda et al, 2018;Nakano et al, 2020;Swierczek et al, 2011), we analyzed frequencies of the behavioral components in thermotaxis (Fig. 4A).…”

Section: Starvation Altered Curving Behavior On a Linear Thermal Gradmentioning

confidence: 99%

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Neural Coding of Thermal Preferences in the NematodeCaenorhabditis elegans

Matsuyama

Mori

2020

eNeuro

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Animals are capable to modify sensory preferences according to past experiences. Surrounded by ever-changing environments, they continue assigning a hedonic value to a sensory stimulus. It remains to be elucidated however how such alteration of sensory preference is encoded in the nervous system. Here we show that past experiences alter temporal interaction between the calcium responses of sensory neurons and their postsynaptic interneurons in the nematode Caenorhabditis elegans. C. elegans exhibits thermotaxis, in which its temperature preference is modified by the past feeding experience: well-fed animals are attracted toward their past cultivation temperature on a thermal gradient, whereas starved animals lose that attraction. By monitoring calcium responses simultaneously from both AFD thermosensory neurons and their postsynaptic AIY interneurons in well-fed and starved animals under time-varying thermal stimuli, we found that past feeding experiences alter phase shift between AFD and AIY calcium responses. Furthermore, the difference in neuronal activities between well-fed and starved animals observed here are able to explain the difference in the behavioral output on a thermal gradient between well-fed and starved animals. Although previous studies have shown that C. elegans executes thermotaxis by regulating amplitude or frequency of the AIY response, our results proposed a new mechanism by which thermal preference is encoded by phase shift between AFD and AIY activities. Given these observations, thermal preference is likely to be computed on synapses between AFD and AIY neurons. Such a neural strategy may enable animals to enrich information processing within defined connectivity via dynamic alterations of synaptic communication. 4 Significance Statement C. elegans can assign a hedonic value to a temperature depending on past feeding experiences. They prefer the temperature associated with food intake, whereas lose the preference to one associated with starvation. This paradigm provides a model to elucidate how the sensory preference is encoded by the nervous system. We show here that thermal preference is encoded by temporal interaction, especially phase shift, between the responses of sensory neurons and their postsynaptic interneurons. Furthermore, the neuronal activity patterns we observed here were well correlated with behavioral outputs. Although previous studies have revealed that amplitude or frequency of interneuron responses encodes temperature information, we added a new mechanism by which phase shift between sensory neurons and interneurons encode thermal preference.

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Section: Discussionsupporting

confidence: 93%

Section: Behavioral Analysismentioning

confidence: 99%

Section: Starvation Altered Curving Behavior On a Linear Thermal Gradmentioning

confidence: 99%

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Neural Coding of Thermal Preferences in the NematodeCaenorhabditis elegans

Matsuyama

Mori

2020

eNeuro

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“…Second, AFD calcium responses recorded from freely moving animals are sufficient to reconstruct the thermal environment and trajectories of an animal navigating on a temperature gradient (Tsukada et al, 2016). Third, recent work from one of our laboratories and others suggests that AFD generates distinct synaptic signals that are valued in the AIY interneuron to drive appropriate thermosensory behavior (Hawk et al, 2018; Kuhara et al, 2011; Nakano et al, 2020). While the calcium imaging results have hinted at the role of AFD in directing thermotaxis behaviors of young adult C. elegans , how aging affects AFD activities and influences thermotaxis behaviors is still unclear.…”

Section: Discussionmentioning

confidence: 99%

“…As GCY‐8 is localized to the microvilli (Nguyen et al, 2014), disorganized or shrunken microvilli associated with F‐actin loss may lead to redistribution of GCY‐8 and other molecules important for thermosensory transduction, such as the G protein‐coupled receptor SRTX‐1 and the CNG channel subunits TAX‐2 and TAX‐4 (Colosimo et al, 2004; Nguyen et al, 2014), which potentially change the spatiotemporal patterns of calcium dynamics. An intriguing hypothesis is that patterned AFD calcium dynamics evoked by thermal stimuli specify the valence and magnitude of synaptic signals to AIY that instruct thermotaxis behaviors (Kuhara et al, 2011; Hawk et al, 2018; Nakano et al, 2020). However, it should be noted that we did not find a correlation between deformed microvilli organization and prolonged calcium responses in AFDs of aged animals, although this conclusion should be cautioned and confirmed in future studies due to the small sample size of our experiments.…”

Section: Discussionmentioning

confidence: 99%

Age‐dependent changes in response property and morphology of a thermosensory neuron and thermotaxis behavior in Caenorhabditis elegans

et al. 2020

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Age‐dependent cognitive and behavioral deterioration may arise from defects in different components of the nervous system, including those of neurons, synapses, glial cells, or a combination of them. We find that AFD, the primary thermosensory neuron of Caenorhabditis elegans, in aged animals is characterized by loss of sensory ending integrity, including reduced actin‐based microvilli abundance and aggregation of thermosensory guanylyl cyclases. At the functional level, AFD neurons in aged animals are hypersensitive to high temperatures and show sustained sensory‐evoked calcium dynamics, resulting in a prolonged operating range. At the behavioral level, senescent animals display cryophilic behaviors that remain plastic to acute temperature changes. Excessive cyclase activity of the AFD‐specific guanylyl cyclase, GCY‐8, is associated with developmental defects in AFD sensory ending and cryophilic behavior. Surprisingly, loss of the GCY‐8 cyclase domain reduces these age‐dependent morphological and behavioral changes, while a prolonged AFD operating range still exists in gcy‐8 animals. The lack of apparent correlation between age‐dependent changes in the morphology or stimuli‐evoked response properties of primary sensory neurons and those in related behaviors highlights the importance of quantitative analyses of aging features when interpreting age‐related changes at structural and functional levels. Our work identifies aging hallmarks in AFD receptive ending, temperature‐evoked AFD responses, and experience‐based thermotaxis behavior, which serve as a foundation to further elucidate the neural basis of cognitive aging.

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Analyses of Neural Circuits Governing Behavioral Plasticity in the Nematode Caenorhabditis elegans

Huang,

Mori

2024

Methods in Molecular Biology

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Presynaptic MAST kinase controls opposing postsynaptic responses to convey stimulus valence in Caenorhabditis elegans

Cited by 26 publications

References 74 publications

Neural Coding of Thermal Preferences in the NematodeCaenorhabditis elegans

Neural Coding of Thermal Preferences in the NematodeCaenorhabditis elegans

Age‐dependent changes in response property and morphology of a thermosensory neuron and thermotaxis behavior in Caenorhabditis elegans

Analyses of Neural Circuits Governing Behavioral Plasticity in the Nematode Caenorhabditis elegans

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