A major goal in neuroscience is to elucidate the principles by which memories are stored in a neural network. Here, we have systematically studied how four types of associative memories (short-and long-term memories, each as positive and negative associations) are encoded within the compact neural network of Caenorhabditis elegans worms. Interestingly, sensory neurons were primarily involved in coding short-term, but not long-term, memories, and individual sensory neurons could be assigned to coding either the conditioned stimulus or the experience valence (or both). Moreover, when considering the collective activity of the sensory neurons, the specific training experiences could be decoded. Interneurons integrated the modulated sensory inputs and a simple linear combination model identified the experience-specific modulated communication routes. The widely distributed memory suggests that integrated network plasticity, rather than changes to individual neurons, underlies the fine behavioral plasticity. This comprehensive study reveals basic memory-coding principles and highlights the central roles of sensory neurons in memory formation.
Bibliographical noteFunding Information:
We thank the reviewers and the editors for the very helpful suggestions which eventually greatly improved the final version of this manuscript. We also thank Paul Sternberg in which lab we generated several of the strains used herein, and Cori Bargmann and Einav Gross for sharing strains. Some strains were provided by the CGC, which is funded by the NIH Office of Research Infrastructure Programs (P40 OD010440). Research in the AZ lab was supported by ERC (336803), ICORE (1902/12), and ISF (1300/17). COP postdoctoral fellowship was also supported by the David-Herzog-Funds at Styrian Universities. EB, RR, and EI were supported by the Jerusalem Brain Center. AZ is the Greenfield chair in Neurobiology.
© Pritz et al.