Venkataraman, Gaurav Gokaran; (2020) Evidence for the transgenerational inheritance of memory in the planarian flatworm. Doctoral thesis (Ph.D), UCL (University College London).

Abstract

In the 1950s and 60s, it was reported that planarian flatworms could retain memories upon decapitation and regeneration of their heads, which include the most primitive known two-hemisphere brains. Because these worms reproduce by fissioning off their tails, this behavior can be considered a transgenerational memory. Mechanistic work in the 60s pointed towards RNA as the molecular substrate of this outside-ofthe-brain memory. This hypothesis is now discredited, and it is widely believed that memories are stored in the synaptic strengths and patterns between neurons. There have, however, been recent reasons to question the validity of the synaptic hypotheses. This thesis begins by considering recent challenges to the synaptic memory hypothesis in some detail. We conclude that these challenges, along with recent reports of RNA-mediated transgeneration inheritance, make the old RNA memory hypothesis worth revisiting. In particular, we arrive at the conclusion that the most desirable addition to the literature is a clear behavioral demonstration of nonsynaptic memory storage, relatively independent of any specific mechanism. Towards this end, we review the historical work done on planarian memory outside of the brain. We re-analyze a recent report of planarian memory outside of the brain, and conclude that a new planarian learning assay is needed. We therefore develop a new associative learning assay in the planarian flatworm; we provide evidence that this associative memory is retained upon decapitation and regeneration of the planarian brain. We determine that our developed learning assay is similar to flavor aversion learning, a type of associative learning which is known to induce associations particularly fast, and with exceptionally great strength. Contrary to reports in the 1960s, we find no evidence that RNA is the molecular substrate of planarian memory outside of the brain. We discuss potential reasons for this failure, and propose more targeted molecular experiments.

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