TY - JOUR
T1 - Single-Cell Memory Regulates a Neural Circuit for Sensory Behavior
AU - Kobayashi, Kyogo
AU - Nakano, Shunji
AU - Amano, Mutsuki
AU - Tsuboi, Daisuke
AU - Nishioka, Tomoki
AU - Ikeda, Shingo
AU - Yokoyama, Genta
AU - Kaibuchi, Kozo
AU - Mori, Ikue
N1 - Funding Information:
We thank C. Bargmann for the GCaMP3 construct and the str-1 promoter; Y. Iino for the gcy-5 promoter; P. Sengupta for the cmk-1 cDNA; A. Fire for pPD plasmids; J. McGhee for the ges-1 promoter; T. Ishihara for the H13 (nhr-38) promoter; K. Suzuki for sharing unpublished strains; and T. Jiang for sharing unpublished results; Some strains were provided by the Caenorhabditis Genetic Center (CGC), which is funded by the NIH Office of Research Infrastructure Programs ( P40 OD010440 ). We thank C. Yokoyama for critical advice; A. Giles and P. Jurado for helpful comments; and members of the I.M. laboratory for helpful discussion. K. Kobayashi was a Research Fellow of the Japan Society for the Promotion of Science (JSPS) . I.M. is a Scholar of the Institute for Advanced Research in Nagoya University. This work was supported by a Grant-in-Aid for JSPS Fellows ; a Grant-in-Aid for Scientific Research on Innovative Areas “Neural Diversity and Neocortical Organization” (grant number 22123010 ); the Strategic Research Program for Brain Sciences “Bioinformatics for Brain Sciences” from the Ministry of Education, Culture, Sports, Science and Technology (MEXT) ; the Brain/MIND project from the Japan Agency for Medical Research and Development (AMED) ; and CREST, JST .
Publisher Copyright:
© 2016 The Authors.
PY - 2016/1/5
Y1 - 2016/1/5
N2 - 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. 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.
AB - 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. 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.
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U2 - 10.1016/j.celrep.2015.11.064
DO - 10.1016/j.celrep.2015.11.064
M3 - Article
C2 - 26725111
AN - SCOPUS:84952979600
VL - 14
SP - 11
EP - 21
JO - Cell Reports
JF - Cell Reports
SN - 2211-1247
IS - 1
ER -