A connectome of a learning and memory center in the adult Drosophila brain

TLDR

Memory formation, storage and retrieval depend on neuronal circuits, and in Drosophila the mushroom body is the key site of associative learning. The authors reconstructed all 983 neurons and their synaptic connections in the adult MB α lobe using 8 nm isotropic FIB‑SEM data. The connectome revealed that Kenyon cells form multiple en passant synapses onto MB output neurons, with some MBONs receiving input from all KCs while others sample specific modalities; only 6 % of KC→MBON synapses receive direct dopaminergic input, and two novel synapse classes—KC→DAN and DAN→MBON—were identified, the latter inducing slow depolarization of MBONs and potentially weakening memory recall.

Abstract

Understanding memory formation, storage and retrieval requires knowledge of the underlying neuronal circuits. In Drosophila, the mushroom body (MB) is the major site of associative learning. We reconstructed the morphologies and synaptic connections of all 983 neurons within the three functional units, or compartments, that compose the adult MB's α lobe, using a dataset of isotropic 8 nm voxels collected by focused ion-beam milling scanning electron microscopy. We found that Kenyon cells (KCs), whose sparse activity encodes sensory information, each make multiple en passant synapses to MB output neurons (MBONs) in each compartment. Some MBONs have inputs from all KCs, while others differentially sample sensory modalities. Only 6% of KC>MBON synapses receive a direct synapse from a dopaminergic neuron (DAN). We identified two unanticipated classes of synapses, KC>DAN and DAN>MBON. DAN activation produces a slow depolarization of the MBON in these DAN>MBON synapses and can weaken memory recall.