Single-Cell Memory Regulates a Neural Circuit for Sensory Behavior

• Published in: Cell reports (Cambridge) Vol. 14; no. 1; pp. 11 - 21
• Main Authors: Kobayashi, Kyogo, Nakano, Shunji, Amano, Mutsuki, Tsuboi, Daisuke, Nishioka, Tomoki, Ikeda, Shingo, Yokoyama, Genta, Kaibuchi, Kozo, Mori, Ikue
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 05.01.2016; Elsevier
• Subjects: Animals; Caenorhabditis elegans - genetics; Caenorhabditis elegans - metabolism; Caenorhabditis elegans Proteins - metabolism; Calcium-Calmodulin-Dependent Protein Kinase Type 1 - metabolism; Calcium-Calmodulin-Dependent Protein Kinase Type 4 - metabolism; Memory - physiology; Nerve Net - physiology; Neuronal Plasticity - physiology; raf Kinases - metabolism; Signal Transduction - physiology
• ISSN: 2211-1247; 2639-1856; 2211-1247
• DOI: 10.1016/j.celrep.2015.11.064

Unveiling the molecular and cellular mechanisms underlying memory has been a challenge for the past few decades. Although synaptic plasticity is proven to be essential for memory formation, the significance of “single-cell memory” still remains elusive. Here, we exploited a primary culture system for the analysis of C. elegans neurons and show that a single thermosensory neuron has an ability to form, retain, and reset a temperature memory. Genetic and proteomic analyses found that the expression of the single-cell memory exhibits inter-individual variability, which is controlled by the evolutionarily conserved CaMKI/IV and Raf pathway. The variable responses of a sensory neuron influenced the neural activity of downstream interneurons, suggesting that modulation of the sensory neurons ultimately determines the behavioral output in C. elegans. Our results provide proof of single-cell memory and suggest that the individual differences in neural responses at the single-cell level can confer individuality. [Display omitted] •A single thermosensory neuron is capable of memorizing a temperature•This single-cell memory shows variability between individuals•The CaMKI/IV and Raf pathway modulates variability in single-cell memory•The variability of the single-cell memory underlies premotor neuron activity Kobayashi et al. show that a single sensory neuron can memorize information without any neural connections and suggest that single-cell memory can underlie differences between individual responses.