Abstract

The brain adaptively integrates present sensory input, past experience, and options for future action. The insect mushroom body exemplifies how a central brain structure brings about such integration. Here we use a combination of systematic single-cell labeling, connectomics, transgenic silencing, and activation experiments to study the mushroom body at single-cell resolution, focusing on the behavioral architecture of its input and output neurons (MBINs and MBONs), and of the mushroom body intrinsic APL neuron. Our results reveal the identity and morphology of almost all of these 44 neurons in stage 3 Drosophila larvae. Upon an initial screen, functional analyses focusing on the mushroom body medial lobe uncover sparse and specific functions of its dopaminergic MBINs, its MBONs, and of the GABAergic APL neuron across three behavioral tasks, namely odor preference, taste preference, and associative learning between odor and taste. Our results thus provide a cellular-resolution study case of how brains organize behavior.

Highlights

  • The brain adaptively integrates present sensory input, past experience, and options for future action

  • A notable exception to stereotypy is that the olfactory projection neurons connect in a predominantly random fashion to ~800 mushroom body intrinsic Kenyon cells (KCs)[7, 20, 21]

  • The mushroom bodies are an example of a central brain structure integrating present sensory input and past experience associated with such input to provide instruction for future behavior

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Summary

Introduction

The brain adaptively integrates present sensory input, past experience, and options for future action. From the subesophageal zone taste information is passed on for steering innate gustatory behavior (throughout this study, “innate” is used in the sense of “experimentally naïve”), and toward the brain These brain projections connect, via an unknown number of synaptic steps, to MBINs. There follows a simplified account of how associative learning comes about at the interface of MBINs, KCs, and the MBONs (Fig. 1b). The mushroom bodies are an example of a central brain structure integrating present sensory input (projection neurons, MBINs) and past experience associated with such input (the modified KC-toMBON presynaptic terminals) to provide instruction for future behavior (via the MBONs)

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