Caenorhabditis elegans learning in a structured maze is a multisensory behavior

Eleni Gourgou; Kavya Adiga; Anne Goettemoeller; Chieh Chen; Ao-Lin Hsu

doi:10.1016/j.isci.2021.102284

Caenorhabditis elegans learning in a structured maze is a multisensory behavior

iScience. 2021 Mar 8;24(4):102284. doi: 10.1016/j.isci.2021.102284. eCollection 2021 Apr 23.

Authors

Eleni Gourgou^{1

2}, Kavya Adiga³, Anne Goettemoeller⁴, Chieh Chen⁵, Ao-Lin Hsu^{3

5

6}

Affiliations

¹ Department of Mechanical Engineering, University of Michigan, Ann Arbor, MI 48109, USA.
² Institute of Gerontology, University of Michigan Medical School, Ann Arbor, MI 41809, USA.
³ Department of Internal Medicine, Division of Geriatrics & Palliative Medicine, University of Michigan Medical School, Ann Arbor, MI 41809, USA.
⁴ Neuroscience Program, College of Literature, Science and the Arts, University of Michigan, Ann Arbor, MI 41809, USA.
⁵ Institute of Biochemistry and Molecular Biology, National Yang Ming University, Taipei, 112 Taiwan.
⁶ Research Center for Healthy Aging and Institute of New Drug Development, China Medical University, Taichung, 404, Taiwan.

Abstract

We show that C. elegans nematodes learn to associate food with a combination of proprioceptive cues and information on the structure of their surroundings (maze), perceived through mechanosensation. By using the custom-made Worm-Maze platform, we demonstrate that C. elegans young adults can locate food in T-shaped mazes and, following that experience, learn to reach a specific maze arm. C. elegans learning inside the maze is possible after a single training session, it resembles working memory, and it prevails over conflicting environmental cues. We provide evidence that the observed learning is a food-triggered multisensory behavior, which requires mechanosensory and proprioceptive input, and utilizes cues about the structural features of nematodes' environment and their body actions. The CREB-like transcription factor and dopamine signaling are also involved in maze performance. Lastly, we show that the observed aging-driven decline of C. elegans learning ability in the maze can be reversed by starvation.

Keywords: Behavioral Neuroscience; Biological Sciences; Neuroscience.

Grants and funding

K01 AG057833/AG/NIA NIH HHS/United States