title: Reconstruction of Spatial Thermal Gradient Encoded in Thermosensory Neuron AFD in Caenorhabditis elegans.
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.
  
  
  CONCLUSIONS
  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.
authors.affiliation: Group of Molecular Neurobiology, Division of Biological Science, Graduate School of Science, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8602, Japan.
authors.forename: Yuki
authors.initials: Y
authors.lastname: Tsukada
authors.affiliation: Department of Systems Science, Graduate School of Informatics, Kyoto University, Yoshida-honmachi, Sakyo-ku, Kyoto 606-8501, Japan.
authors.forename: Masataka
authors.initials: M
authors.lastname: Yamao
authors.affiliation: Department of Systems Science, Graduate School of Informatics, Kyoto University, Yoshida-honmachi, Sakyo-ku, Kyoto 606-8501, Japan.
authors.forename: Honda
authors.initials: H
authors.lastname: Naoki
authors.affiliation: Group of Molecular Neurobiology, Division of Biological Science, Graduate School of Science, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8602, Japan.
authors.forename: Tomoyasu
authors.initials: T
authors.lastname: Shimowada
authors.affiliation: Group of Molecular Neurobiology, Division of Biological Science, Graduate School of Science, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8602, Japan.
authors.forename: Noriyuki
authors.initials: N
authors.lastname: Ohnishi
authors.affiliation: Laboratory of Molecular and Cellular Regulation, Faculty of Science and Engineering, Institute for Integrative Neurobiology, Konan University, Higashinada-ku, Kobe 658-8501, Japan.
authors.forename: Atsushi
authors.identifier: http://orcid.org/0000-0003-2994-8658
authors.initials: A
authors.lastname: Kuhara
authors.affiliation: Department of Systems Science, Graduate School of Informatics, Kyoto University, Yoshida-honmachi, Sakyo-ku, Kyoto 606-8501, Japan.
authors.forename: Shin
authors.initials: S
authors.lastname: Ishii
authors.affiliation: Group of Molecular Neurobiology, Division of Biological Science, Graduate School of Science, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8602, Japan, m46920a@nucc.cc.nagoya-u.ac.jp.
authors.forename: Ikue
authors.initials: I
authors.lastname: Mori
mesh_terms: D000818:Animals; D030801:Animals, Genetically Modified; D017173:Caenorhabditis elegans; D029742:Caenorhabditis elegans Proteins / Q000235:genetics / Q000378:metabolism; D002118:Calcium / Q000378:metabolism; D008124:Locomotion / Q000502:physiology; D008164:Luminescent Proteins / Q000235:genetics / Q000378:metabolism; D009474:Neurons / Q000502:physiology*; D009475:Neurons, Afferent / Q000502:physiology; D013696:Temperature; D013697:Thermosensing / Q000502:physiology*
chemical_list: D029742:Caenorhabditis elegans Proteins; D008164:Luminescent Proteins; D002118:Calcium
keywords: C. elegans; imaging; reconstruction; response function; thermosensory neuron; tracking