Descending neurons integrate learnt information from mushroom body with context to promote escape behaviour

Abstract

To behave adaptively in the environment and select appropriate responses to sensory stimuli, animals integrate learnt information about the valences of stimuli with contextual information. While significant progress has been made in understanding how animals learn which stimuli predict positive and negative outcomes, how the outputs of associative learning circuits flexibly promote different behaviours, depending on context, is not well understood. Addressing this question requires mapping the pathways from learning circuits to nerve cord command neurons that promote specific actions, and understanding where and how contextual information converges with these pathways to modulate their activity. These are daunting tasks in larger brains where synaptic-resolution connectivity maps are not available. We, therefore, addressed this question in the tractable Drosophila larva using a combination of connectomic analyses, imaging and manipulation of neural activity and behavioural analysis. We characterised, with synaptic-resolution, the pathways from the higher-order learning circuit (the mushroom body, MB) all the way to a specific cord command neuron (Goro) in the nerve cord that promotes the most vigorous escape response, rolling. Rolling is the fastest, but also the most energetically costly escape response and is activated by multisensory cues in the context of predator attack. We identify a pair of brain descending neurons, Ipsigoro, that integrate learnt information (via input from MBONs) and nociceptive context (via input from ascending neurons) to facilitate rolling via direct inputs to Goro. Our study reveals the circuit mechanism by which context and learnt information are integrated by brain descending neurons to activate specific nerve cord command neurons and promote specific actions.