Abstract
The ability to learn new skills and to store them as memory entities is one of the most impressive features of higher evolved organisms. However, not all memories are created equal; some are short-lived forms, and some are longer lasting. Formation of the latter is energetically costly and by the reason of restricted availability of food or fluctuations in energy expanses, efficient metabolic homeostasis modulating different needs like survival, growth, reproduction, or investment in longer lasting memories is crucial. Whilst equipped with cellular and molecular pre-requisites for formation of a protein synthesis dependent long-term memory (LTM), its existence in the larval stage of Drosophila remains elusive. Considering it from the viewpoint that larval brain structures are completely rebuilt during metamorphosis, and that this process depends completely on accumulated energy stores formed during the larval stage, investing in LTM represents an unnecessary expenditure. However, as an alternative, Drosophila larvae are equipped with the capacity to form a protein synthesis independent so-called larval anaesthesia resistant memory (lARM), which is consolidated in terms of being insensitive to cold-shock treatments. Motivated by the fact that LTM formation causes an increase in energy uptake in Drosophila adults, we tested the idea of whether an energy surplus can induce the formation of LTM in the larval stage. Suprisingly, increasing the metabolic state by feeding Drosophila larvae the disaccharide sucrose directly before aversive olfactory conditioning led to the formation of a protein synthesis dependent longer lasting memory. Moreover, formation of this memory component is accompanied by the suppression of lARM. We ascertained that insulin receptors (InRs) expressed in the mushroom body Kenyon cells suppresses the formation of lARM and induces the formation of a protein synthesis dependent longer lasting memory in Drosophila larvae. Given the numerical simplicity of the larval nervous system this work offers a unique prospect to study the impact of insulin signaling on the formation of protein synthesis dependent memories on a molecular level.
Highlights
Harboring the ability to deal with novelties and unpredictable complexities provides the key to successfully adapt to unforeseen events in an ever-changing environment
The protein synthesis dependent formation of long-term memory (LTM) is accompanied by a drastic increase in energy uptake and is disabled after reduced food availability
We tested whether an energy surplus can induce the formation of a protein synthesis dependent longer lasting memory in Drosophila larvae, and correlate this with molecular events in identifiable neurons
Summary
Harboring the ability to deal with novelties and unpredictable complexities provides the key to successfully adapt to unforeseen events in an ever-changing environment. Establishing a memory is a highly complex and dynamic process. Apart from the involvement of multilayered neuronal circuitries and cellular machineries [1], the capacity to form memories comes with energetic costs since activation and maintenance of synaptic connections involved in integrating, storing and retrieving information are energy demanding [2,3]. These circumstances can either lead to trade-offs with other phenotypic traits or to learning and memory impairments, when available energy resources are restricted [4,5]. Formation of LTM led to reduced resistance to food and water stress in Drosophila [14] and during food deprivation the formation of energetically costly LTM is disabled [15]
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