Abstract
The central complex is a highly conserved insect brain region composed of morphologically stereotyped neurons that arborize in distinctively shaped substructures. The region has been implicated in a wide range of behaviors, including navigation, motor control and sleep, and has been the subject of several modeling studies exploring its circuit computations. Most studies so far have relied on assumptions about connectivity between neurons in the region based on their overlap in light-level microscopic images. Here, we present an extensive functional connectome of Drosophila melanogaster's central complex at cell-type resolution. Using simultaneous optogenetic stimulation, GCaMP recordings and pharmacology, we tested the connectivity between over 70 presynaptic-to-postsynaptic cell-type pairs. The results reveal a range of inputs to the central complex, some of which have not been previously described, and suggest that the central complex has a limited number of output channels. Additionally, despite the high degree of recurrence in the circuit, network connectivity appears to be sparser than anticipated from light-level images. Finally, the connectivity matrix we obtained highlights the potentially critical role of a class of bottleneck interneurons of the protocerebral bridge known as the Δ7 neurons. All data is provided for interactive exploration in a website with the capacity to accommodate additional connectivity information as it becomes available. Raw data and code are made available as an OpenScienceFramework project.
Highlights
Positioned in the middle of the insect brain, the central complex provides a unique opportunity to obtain mechanistic insights into the way brains build and use abstract representations (Turner-Evans and Jayaraman, 2016)
Detailed light level anatomy (Hanesch et al, 1989; Wolff et al, 2015; Lin et al, 2013) of a significant fraction of the cell types, along with the availability of tools to genetically target these neurons by type (Wolff et al, 2015), have given rise to the first mechanistic investigations of how the circuit constructs a stable heading representation (Kim et al, 2017), and how this representation updates as the animal turns in darkness (Turner-Evans et al, 2017; Green et al, 2017)
Such results and related findings from other insects have inspired a number of modeling studies aimed at predicting or reproducing physiologically and behaviorally relevant response patterns (Kakaria et al, 2017b; Givon et al, 2017; Chang et al, 2017; Cope et al, 2017; Su et al, 2017; Fiore et al, 2017; Kim et al, 2017; Stone et al, 2017; Turner-Evans et al, 2017). Many of these models make assumptions about connectivity within the central complex based on the degree of overlap at the light microscopy level between processes that look bouton-like and those that seem spiny, which are suggestive of pre- and post-synaptic specializations respectively
Summary
Positioned in the middle of the insect brain, the central complex provides a unique opportunity to obtain mechanistic insights into the way brains build and use abstract representations (Turner-Evans and Jayaraman, 2016). Detailed light level anatomy (Hanesch et al, 1989; Wolff et al, 2015; Lin et al, 2013) of a significant fraction of the cell types, along with the availability of tools to genetically target these neurons by type (Wolff et al, 2015), have given rise to the first mechanistic investigations of how the circuit constructs a stable heading representation (Kim et al, 2017), and how this representation updates as the animal turns in darkness (Turner-Evans et al, 2017; Green et al, 2017) Such results and related findings from other insects have inspired a number of modeling studies aimed at predicting or reproducing physiologically and behaviorally relevant response patterns (Kakaria et al, 2017b; Givon et al, 2017; Chang et al, 2017; Cope et al, 2017; Su et al, 2017; Fiore et al, 2017; Kim et al, 2017; Stone et al, 2017; Turner-Evans et al, 2017). Given the likely number of existing and undiscovered cell types in the central complex, the diversity of neurotransmitters and receptors they express, the mixture of pre- and post-synaptic specializations in their arbors, and the dense recurrence of the network, we see this map as an initial scaffold, which will allow new information to be incorporated as it becomes available
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