Visualization of a Distributed Synaptic Memory Code in the Drosophila Brain

Abstract

During associative conditioning animals learn which sensory cues are predictive for positive or negative conditions. Because neurons that encode sensory cues are sparsely distributed across neuronal assemblies, it is difficult to comprehensively monitor the synaptic plasticity that underlies learning and memory formation. One can either observe individual synapses, or large numbers of neurons without synaptic resolution. To combine both aspects we focused on synaptic boutons of Kenyon cells of the Drosophila mushroom body γ-lobe, a brain structure that mediates olfactory learning. A fluorescent Ca²⁺ sensor was stochastically expressed in single Kenyon cells so that axonal boutons could be assigned to distinct cells, and Ca²⁺ could be measured across many animals. We show that odor-evoked Ca²⁺ dynamics across boutons decorrelate as a result of associative learning. These data reveal a synaptic rather than cellular distribution of a memory code and coherence of distributed synaptic activity as a memory-encoding parameter.

Keywords: Drosophila melanogaster, learning and memor, insect brain, Kenyon cell, mushroom body, odor representation, olfactory coding, optical calcium imaging, synaptic plasticity, Neuronal assemblies