Multisensory learning recruits visual neurons into an olfactory memory engram

Abstract

Associating multiple sensory cues with a single experience or object is a fundamental process that improves object recognition and memory performance. However, neural mechanisms that bind sensory features during learning and augment memory expression are unknown. Here we demonstrate multisensory appetitive and aversive memory in Drosophila. Combining colours and odours improved memory performance, even when each sensory modality was tested alone. Temporal control of neuronal function revealed visually-selective mushroom body Kenyon Cells (KCs) to be required for enhancement of visual and olfactory memory recall after multisensory training. Synapse-level connectomics suggests that valence-relevant dopaminergic reinforcement could permit the KC-spanning serotonergic DPM neurons to bridge between previously modality-selective KC streams. Consistent with this model, DPM transmission is uniquely required during multisensory memory formation and for enhanced expression of olfactory memory afterwards. In addition, signalling via the DopR1 dopamine receptor is required in APL neurons, suggesting that reinforcing dopamine could locally release GABA-ergic inhibition to permit bridging microcircuits to function. Cross-modal binding thereby expands the KCs representing the olfactory memory engram into those representing the colour. We propose that broadening of the engram improves memory performance after multisensory learning and permits a single sensory feature to retrieve the memory of the multimodal experience.