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Articles, Systems/Circuits

Reconstruction of Spatial Thermal Gradient Encoded in Thermosensory Neuron AFD in Caenorhabditis elegans

Yuki Tsukada, Masataka Yamao, Honda Naoki, Tomoyasu Shimowada, Noriyuki Ohnishi, Atsushi Kuhara, Shin Ishii and Ikue Mori
Journal of Neuroscience 2 March 2016, 36 (9) 2571-2581; DOI: https://doi.org/10.1523/JNEUROSCI.2837-15.2016
Yuki Tsukada
1Group of Molecular Neurobiology, Division of Biological Science, Graduate School of Science, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8602, Japan,
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Masataka Yamao
2Department of Systems Science, Graduate School of Informatics, Kyoto University, Yoshida-honmachi, Sakyo-ku, Kyoto 606-8501, Japan,
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Honda Naoki
2Department of Systems Science, Graduate School of Informatics, Kyoto University, Yoshida-honmachi, Sakyo-ku, Kyoto 606-8501, Japan,
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Tomoyasu Shimowada
1Group of Molecular Neurobiology, Division of Biological Science, Graduate School of Science, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8602, Japan,
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Noriyuki Ohnishi
1Group of Molecular Neurobiology, Division of Biological Science, Graduate School of Science, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8602, Japan,
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Atsushi Kuhara
3Laboratory of Molecular and Cellular Regulation, Faculty of Science and Engineering, Institute for Integrative Neurobiology, Konan University, Higashinada-ku, Kobe 658-8501, Japan
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Shin Ishii
2Department of Systems Science, Graduate School of Informatics, Kyoto University, Yoshida-honmachi, Sakyo-ku, Kyoto 606-8501, Japan,
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Ikue Mori
1Group of Molecular Neurobiology, Division of Biological Science, Graduate School of Science, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8602, Japan,
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Abstract

During navigation, animals process temporal sequences of sensory inputs to evaluate the surrounding environment. Thermotaxis of Caenorhabditis elegans is a favorable sensory behavior to elucidate how navigating animals process sensory signals from the environment. Sensation and storage of temperature information by a bilaterally symmetric pair of thermosensory neurons, AFD, is essential for the animals to migrate toward the memorized temperature on a thermal gradient. However, the encoding mechanisms of the spatial environment with the temporal AFD activity during navigation remain to be elucidated. Here, we show how the AFD neuron encodes sequences of sensory inputs to perceive spatial thermal environment. We used simultaneous calcium imaging and tracking system for a freely moving animal and characterized the response property of AFD to the thermal stimulus during thermotaxis. We show that AFD neurons respond to shallow temperature increases with intermittent calcium pulses and detect temperature differences with a critical time window of 20 s, which is similar to the timescale of behavioral elements of C. elegans, such as turning. Convolution of a thermal stimulus and the identified response property successfully reconstructs AFD activity. Conversely, deconvolution of the identified response kernel and AFD activity reconstructs the shallow thermal gradient with migration trajectory, indicating that AFD activity and the migration trajectory are sufficient as the encoded signals for thermal environment. Our study demonstrates bidirectional transformation between environmental thermal information and encoded neural activity.

SIGNIFICANCE STATEMENT Deciphering how information is encoded in the nervous system is an important challenge for understanding the principles of information processing in neural circuits. During navigation behavior, animals transform spatial information to temporal patterns of neural activity. To elucidate how a sensory system achieves this transformation, we focused on a thermosensory neuron in Caenorhabditis elegans called AFD, which plays a major role in a sensory behavior. Using tracking and calcium imaging system for freely moving animals, we identified the response property of the AFD. The identified response property enabled us to reconstruct both neural activity from a temperature stimulus and a spatial thermal environment from neural activity. These results shed light on how a sensory system encodes the environment.

  • C. elegans
  • imaging
  • reconstruction
  • response function
  • thermosensory neuron
  • tracking

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The Journal of Neuroscience: 36 (9)
Journal of Neuroscience
Vol. 36, Issue 9
2 Mar 2016
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Reconstruction of Spatial Thermal Gradient Encoded in Thermosensory Neuron AFD in Caenorhabditis elegans
Yuki Tsukada, Masataka Yamao, Honda Naoki, Tomoyasu Shimowada, Noriyuki Ohnishi, Atsushi Kuhara, Shin Ishii, Ikue Mori
Journal of Neuroscience 2 March 2016, 36 (9) 2571-2581; DOI: 10.1523/JNEUROSCI.2837-15.2016

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Reconstruction of Spatial Thermal Gradient Encoded in Thermosensory Neuron AFD in Caenorhabditis elegans
Yuki Tsukada, Masataka Yamao, Honda Naoki, Tomoyasu Shimowada, Noriyuki Ohnishi, Atsushi Kuhara, Shin Ishii, Ikue Mori
Journal of Neuroscience 2 March 2016, 36 (9) 2571-2581; DOI: 10.1523/JNEUROSCI.2837-15.2016
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Keywords

  • C. elegans
  • imaging
  • reconstruction
  • response function
  • thermosensory neuron
  • tracking

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