A neural circuit architecture for angular integration in Drosophila

Abstract

Many animals keep track of their angular heading over time while navigating through their environment. However, a neural-circuit architecture for computing heading has not been experimentally defined in any species. Here we describe a set of clockwise- and anticlockwise-shifting neurons in the Drosophila central complex whose wiring and physiology provide a means to rotate an angular heading estimate based on the fly's angular velocity. We show that each class of shifting neurons exists in two subtypes, with spatiotemporal activity profiles that suggest different roles for each subtype at the start and end of tethered-walking turns. Shifting neurons are required for the heading system to properly track the fly's heading in the dark, and stimulation of these neurons induces predictable shifts in the heading signal. The central features of this biological circuit are analogous to those of computational models proposed for head-direction cells in rodents and may shed light on how neural systems, in general, perform integration.

Building a functional connectome of the Drosophila central complex

“…Second, a class of LAL-NO interneurons (the GL-N1 neuron) provides another source of inhibitory input into the EB columnar system by targeting the P-EN neurons ( Figure S5Aii and S3Aii). This connection is particularly interesting in the light of the finding that the P-EN neurons drive the rotation of the bump of activity in the heading representation system (Green et al, 2017;Turner-Evans et al, 2017). Since the left/right noduli segregation corresponds to individual cells coding turns in opposite direction (Turner-Evans et al, 2017), the GL-N1 neurons are likely involved in strengthening or refining those turn related signals.…”

“…Connectivity in the EB columnar system, the ring attractor network Figure S5Dii shows the subpart of the network that has been proposed to sustain the ring attractor representation of heading (Green et al, 2017;Turner-Evans et al, 2017). One hypothesized feature of such a circuit is a large degree of recurrence between the different EB columnar types.…”

“…"Wolff Type Name" refers to the type names as described in (Wolff et al, 2015), "New Type Name" to the nomenclature for short names adopted in this paper (following Kakaria et al 2017a; Turner-Evans et al 2017; Green et al 2017). Type description is the long name, following the guidelines of (Wolff et al, 2015).…”

“…The list of drivers used and the corresponding cell types are given in Table 1. Throughout this paper we follow the naming convention set out in Wolff et al 2015 for full names, and abbreviated following the scheme described in Kakaria et al 2017a and used in Green et al 2017 andTurner-Evans et al 2017. For each cell type, we labeled every region innervated as pre-or post-synaptic (or both): this was done at the resolution of the glomerulus for the PB, the layer for the FB and the individual nodulus.…”

“…Moreover, the scale of the network -a few thousands of neurons in the fly central complex-and the ease of genetic access to individual cell types in Drosophila melanogaster, make this circuit tractable with existing theoretical and experimental methods. 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 , 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 also 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;Fiore et al, 2017;Stone et al, 2017;Turner-Evans et al, 2017).…”