Angular velocity integration in a fly heading circuit

Abstract

Many animals maintain an internal representation of their heading as they move through their surroundings. Such a compass representation was recently discovered in a neural population in the Drosophila melanogaster central complex, a brain region implicated in spatial navigation. Here, we use two-photon calcium imaging and electrophysiology in head-fixed walking flies to identify a different neural population that conjunctively encodes heading and angular velocity, and is excited selectively by turns in either the clockwise or counterclockwise direction. We show how these mirror-symmetric turn responses combine with the neurons’ connectivity to the compass neurons to create an elegant mechanism for updating the fly’s heading representation when the animal turns in darkness. This mechanism, which employs recurrent loops with an angular shift, bears a resemblance to those proposed in theoretical models for rodent head direction cells. Our results provide a striking example of structure matching function for a broadly relevant computation.DOI: http://dx.doi.org/10.7554/eLife.23496.001

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.…”

“…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.…”

“…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). 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.…”

Choosing the right bar: a complex problem

“…Specifically, some neurons of the ellipsoid body represent heading direction in flies 8,9 . This representation is similar to that of head-direction cells in rodents 10 or bats 11 .…”