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

Animals Caenorhabditis elegans Cellular Senescence Neurons / cytology Taxis Response Temperature
Caenorhabditis elegans actin aging behavior calcium cilia neural plasticity sensory neuron

Journal

Aging cell
ISSN: 1474-9726
Titre abrégé: Aging Cell
Pays: England
ID NLM: 101130839

Informations de publication

Date de publication:
05 2020
Historique:
received: 07 07 2019
revised: 09 02 2020
accepted: 06 03 2020
pubmed: 21 4 2020
medline: 2 7 2021
entrez: 21 4 2020
Statut: ppublish

Résumé

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.

Identifiants

DOI: 10.1111/acel.13146 PMID: 32307902 PMC: PMC7253067
pubmed: 32307902
doi: 10.1111/acel.13146
pmc: PMC7253067
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e13146

Subventions

Organisme : NIH HHS
ID : P40 OD010440
Pays : United States
Organisme : NINDS NIH HHS
ID : R35 NS105094
Pays : United States
Organisme : NIH HHS
ID : R35NS105094
Pays : United States
Organisme : NIH Office of Research Infrastructure Program
ID : P40OD010440
Pays : International

Commentaires et corrections

Type : ErratumIn

Informations de copyright

© 2020 The Authors. Aging Cell published by the Anatomical Society and John Wiley & Sons Ltd.

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Auteurs

Tzu-Ting Huang (TT)

Neuroscience Institute, Graduate School of Science, Nagoya University, Nagoya, Japan.
Group of Molecular Neurobiology, Graduate School of Science, Nagoya University, Nagoya, Japan.
Institute of Molecular Medicine, College of Medicine, National Taiwan University, Taipei, Taiwan.

Hironori J Matsuyama (HJ)

Neuroscience Institute, Graduate School of Science, Nagoya University, Nagoya, Japan.
Group of Molecular Neurobiology, Graduate School of Science, Nagoya University, Nagoya, Japan.

Yuki Tsukada (Y)

Neuroscience Institute, Graduate School of Science, Nagoya University, Nagoya, Japan.
Group of Molecular Neurobiology, Graduate School of Science, Nagoya University, Nagoya, Japan.

Aakanksha Singhvi (A)

Laboratory of Developmental Genetics, The Rockefeller University, New York, NY, USA.

Ru-Ting Syu (RT)

Institute of Molecular Medicine, College of Medicine, National Taiwan University, Taipei, Taiwan.
Center of Precision Medicine, College of Medicine, National Taiwan University, Taipei, Taiwan.

Yun Lu (Y)

Laboratory of Developmental Genetics, The Rockefeller University, New York, NY, USA.

Shai Shaham (S)

Laboratory of Developmental Genetics, The Rockefeller University, New York, NY, USA.

Ikue Mori (I)

Neuroscience Institute, Graduate School of Science, Nagoya University, Nagoya, Japan.
Group of Molecular Neurobiology, Graduate School of Science, Nagoya University, Nagoya, Japan.

Chun-Liang Pan (CL)

Institute of Molecular Medicine, College of Medicine, National Taiwan University, Taipei, Taiwan.
Center of Precision Medicine, College of Medicine, National Taiwan University, Taipei, Taiwan.
ORCID: 0000-0003-0108-3138

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Classifications MeSH

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