Language：English   Publishing type：Research paper (scientific journal)  

Animals navigate toward favorable locations using various environmental cues. However, the mechanism of how the goal information is encoded and decoded to generate migration toward the appropriate direction has not been clarified. Here, we describe the mechanism of migration towards a learned concentration of NaCl in Caenorhabditis elegans. In the salt-sensing neuron ASER, the difference between the experienced and currently perceived NaCl concentration is encoded as phosphorylation at Ser65 of UNC-64/Syntaxin 1 A through the protein kinase C(PKC-1) signaling pathway. The phosphorylation affects basal glutamate transmission from ASER, inducing the reversal of the postsynaptic response of reorientation-initiating neurons (i.e., from inhibitory to excitatory), guiding the animals toward the experienced concentration. This process, the decoding of the context, is achieved through the differential sensitivity of postsynaptic excitatory and inhibitory receptors. Our results reveal the mechanism of migration based on the synaptic plasticity that conceptually differs from the classical ones.

DOI： 10.1038/s41467-022-30279-7

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Authorship：Lead author,　Corresponding author   Language：English   Publishing type：Research paper (scientific journal)  

To reveal the neural mechanisms that control animal behavior, it is necessary to link the neural responses to behavioral changes and interpret them. We have developed a protocol to simultaneously record the behavior and neural activity of freely moving C. elegans by combining a microfluidic device and a tracking stage. Here we detail the protocol for the experiment, with an example of behavioral and neural responses of nematodes to salt concentration changes. For complete details on the use and execution of this protocol, please refer to Sato et al. (2021).

DOI： 10.1016/j.xpro.2021.101011

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Authorship：Lead author   Language：English   Publishing type：Research paper (scientific journal)  

Orientation and navigation behaviors of animals are modulated by past experiences. However, little is known about the mechanisms by which sensory inputs are translated into multi-directional orientation behaviors in an experience-dependent manner. Here, we report a neural mechanism for bidirectional salt-concentration chemotaxis of Caenorhabditis elegans. The salt-sensing neuron ASE right (ASER) is always activated by a decrease of salt concentration, while the directionality of reorientation behaviors is inverted depending on previous salt experiences. AIB, the interneuron postsynaptic to ASER, and neurons farther downstream of AIB show experience-dependent bidirectional responses, which are correlated with reorientation behaviors. These bidirectional behavioral and neural responses are mediated by glutamate released from ASER. Glutamate acts through the excitatory glutamate receptor GLR-1 and inhibitory glutamate receptor AVR-14, both acting in AIB. These findings suggest that experience-dependent reorientation behaviors are generated by altering the magnitude of excitatory and inhibitory postsynaptic signals from a sensory neuron to interneurons.

DOI： 10.1016/j.celrep.2021.109177

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Language：English   Publishing type：Research paper (scientific journal)  

The ability of animals to process dynamic sensory information facilitates foraging in an ever-changing environment. However, molecular and neural mechanisms underlying such ability remain elusive. The ClC anion channels/transporters play a pivotal role in cellular ion homeostasis across all phyla. Here, we find a ClC chloride channel is involved in salt concentration chemotaxis of Caenorhabditis elegans. Genetic screening identified two altered-function mutations of clh-1 that disrupt experience-dependent salt chemotaxis. Using genetically encoded fluorescent sensors, we demonstrate that CLH-1 contributes to regulation of intracellular anion and calcium dynamics of salt-sensing neuron, ASER. The mutant CLH-1 reduced responsiveness of ASER to salt stimuli in terms of both temporal resolution and intensity, which disrupted navigation strategies for approaching preferred salt concentrations. Furthermore, other ClC genes appeared to act redundantly in salt chemotaxis. These findings provide insights into the regulatory mechanism of neuronal responsivity by ClCs that contribute to modulation of navigation behavior.

DOI： 10.7554/eLife.55701

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Language：English   Publishing type：Research paper (scientific journal)  

BACKGROUND: Annotation of cell identity is an essential process in neuroscience that allows comparison of cells, including that of neural activities across different animals. In Caenorhabditis elegans, although unique identities have been assigned to all neurons, the number of annotatable neurons in an intact animal has been limited due to the lack of quantitative information on the location and identity of neurons. RESULTS: Here, we present a dataset that facilitates the annotation of neuronal identities, and demonstrate its application in a comprehensive analysis of whole-brain imaging. We systematically identified neurons in the head region of 311 adult worms using 35 cell-specific promoters and created a dataset of the expression patterns and the positions of the neurons. We found large positional variations that illustrated the difficulty of the annotation task. We investigated multiple combinations of cell-specific promoters driving distinct fluorescence and generated optimal strains for the annotation of most head neurons in an animal. We also developed an automatic annotation method with human interaction functionality that facilitates annotations needed for whole-brain imaging. CONCLUSION: Our neuron ID dataset and optimal fluorescent strains enable the annotation of most neurons in the head region of adult C. elegans, both in full-automated fashion and a semi-automated version that includes human interaction functionalities. Our method can potentially be applied to model species used in research other than C. elegans, where the number of available cell-type-specific promoters and their variety will be an important consideration.

DOI： 10.1186/s12915-020-0745-2

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Publisher：Cold Spring Harbor Laboratory  

<title>Abstract</title>Annotation of cell identity is an essential process in neuroscience that allows for comparing neural activities across different animals. In <italic>C. elegans</italic>, although unique identities have been assigned to all neurons, the number of annotatable neurons in an intact animal is limited in practice and comprehensive methods for cell annotation are required. Here we propose an efficient annotation method that can be integrated with the whole-brain imaging technique. We systematically identified neurons in the head region of 311 adult worms using 35 cell-specific promoters and created a dataset of the expression patterns and the positions of the neurons. The large positional variations illustrated the difficulty of the annotation task. We investigated multiple combinations of cell-specific promoters to tackle this problem. We also developed an automatic annotation method with human interaction functionality that facilitates annotation for whole-brain imaging.

DOI： 10.1101/698241

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Language：Japanese   Publisher：The Physical Society of Japan  

DOI： 10.11316/jpsgaiyo.73.2.0_2315

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Language：Japanese   Publisher：The Physical Society of Japan  

DOI： 10.11316/jpsgaiyo.73.1.0_2853

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Language：English   Publishing type：Research paper (scientific journal)  

Animals show various behaviors in response to environmental chemicals. These behaviors are often plastic depending on previous experiences. Caenorhabditis elegans, which has highly developed chemosensory system with a limited number of sensory neurons, is an ideal model for analyzing the role of each neuron in innate and learned behaviors. Here, we report a new type of memory-dependent behavioral plasticity in Na+ chemotaxis generated by the left member of bilateral gustatory neuron pair ASE (ASEL neuron). When worms were cultivated in the presence of Na+, they showed positive chemotaxis toward Na+, but when cultivated under Na+-free conditions, they showed no preference regarding Na+ concentration. Both channelrhodopsin-2 (ChR2) activation with blue light and up-steps of Na+ concentration activated ASEL only after cultivation with Na+, as judged by increase in intracellular Ca2+ Under cultivation conditions with Na+, photoactivation of ASEL caused activation of its downstream interneurons AIY and AIA, which stimulate forward locomotion, and inhibition of its downstream interneuron AIB, which inhibits the turning/reversal behavior, and overall drove worms toward higher Na+ concentrations. We also found that the Gq signaling pathway and the neurotransmitter glutamate are both involved in the behavioral response generated by ASEL.SIGNIFICANCE STATEMENT Animals have acquired various types of behavioral plasticity during their long evolutionary history. Caenorhabditis elegans prefers odors associated with food, but plastically changes its behavioral response according to previous experience. Here, we report a new type of behavioral response generated by a single gustatory sensory neuron, the ASE-left (ASEL) neuron. ASEL did not respond to photostimulation or upsteps of Na+ concentration when worms were cultivated in Na+-free conditions; however, when worms were cultivated with Na+, ASEL responded and inhibited AIB to avoid turning and stimulated AIY and AIA to promote forward locomotion, which collectively drove worms toward higher Na+ concentrations. Glutamate and the Gq signaling pathway are essential for driving worms toward higher Na+ concentrations.

DOI： 10.1523/JNEUROSCI.1774-16.2017

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Language：English   Publishing type：Research paper (scientific journal)  

The nematode Caenorhabditis elegans changes its chemotaxis to NaCl depending on previous experience. At the behavioral level, this chemotactic plasticity is generated by reversing the elementary behaviors for chemotaxis, klinotaxis, and klinokinesis. Here, we report that bidirectional klinotaxis is achieved by the proper use of at least two different neural subcircuits. We simulated an NaCl concentration change by activating an NaCl-sensitive chemosensory neuron in phase with head swing and successfully induced klinotaxis-like curving. The curving direction reversed depending on preconditioning, which was consistent with klinotaxis plasticity under a real concentration gradient. Cell-specific ablation and activation of downstream interneurons revealed that ASER-evoked curving toward lower concentration was mediated by AIY interneurons, whereas curving to the opposite direction was not. These results suggest that the experience-dependent bidirectionality of klinotaxis is generated by a switch between different neural subcircuits downstream of the chemosensory neuron.

DOI： 10.1523/JNEUROSCI.1757-14.2014

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Authorship：Lead author   Language：English   Publishing type：Research paper (scientific journal)  

It is poorly understood how sensory systems memorize the intensity of sensory stimulus, compare it with a newly sensed stimulus, and regulate the orientation behaviour based on the memory. Here we report that Caenorhabditis elegans memorizes the environmental salt concentration during cultivation and exhibits a strong behavioural preference for this concentration. The right-sided amphid gustatory neuron known as ASER, senses decreases in salt concentration, and this information is transmitted to the postsynaptic AIB interneurons only in the salt concentration range lower than the cultivation concentration. In this range, animals migrate towards higher concentration by promoting turning behaviour upon decreases in salt concentration. These observations provide a mechanism for adjusting the orientation behaviour based on the memory of sensory stimulus using a simple neural circuit.

DOI： 10.1038/ncomms3210

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Language：Japanese   Presentation type：Symposium, workshop panel (nominated)  

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