Abstract
Animal navigation is accomplished by a combination of landmark-following and dead reckoning based on estimates of self motion. Both of these approaches require the encoding of heading information, which can be represented as an allocentric or egocentric azimuthal angle. Recently, Ca2+ correlates of landmark position and heading direction, in egocentric coordinates, were observed in the ellipsoid body (EB), a ring-shaped processing unit in the fly central complex (CX; Seelig and Jayaraman, 2015). These correlates displayed key dynamics of so-called ring attractors, namely: (1) responsiveness to the position of external stimuli; (2) persistence in the absence of external stimuli; (3) locking onto a single external stimulus when presented with two competitors; (4) stochastically switching between competitors with low probability; and (5) sliding or jumping between positions when an external stimulus moves. We hypothesized that ring attractor-like activity in the EB arises from reciprocal neuronal connections to a related structure, the protocerebral bridge (PB). Using recent light-microscopy resolution catalogs of neuronal cell types in the PB (Lin et al., 2013; Wolff et al., 2015), we determined a connectivity matrix for the PB-EB circuit. When activity in this network was simulated using a leaky-integrate-and-fire model, we observed patterns of activity that closely resemble the reported Ca2+ phenomena. All qualitative ring attractor behaviors were recapitulated in our model, allowing us to predict failure modes of the putative PB-EB ring attractor and the circuit dynamics phenotypes of thermogenetic or optogenetic manipulations. Ring attractor dynamics emerged under a wide variety of parameter configurations, even including non-spiking leaky-integrator implementations. This suggests that the ring-attractor computation is a robust output of this circuit, apparently arising from its high-level network properties (topological configuration, local excitation and long-range inhibition) rather than fine-scale biological detail.
Highlights
An animal navigating in its environment relies on landmarks to estimate its orientation and position (Collett and Graham, 2004)
With a leaky integrate-and-fire model and simple connectivity rules, derived from light-microscopy resolution neuronal morphologies, we have found that a simple model recapitulates the bump of Ca2+ activity and essentially all of the in vivo dynamics previously observed (Seelig and Jayaraman, 2015)
With a small amount of manual parameter searching, we found that if the inhibitory synapses between the Pintrs and the P-ENs and those between the Pintrs and P-EGs had strengths of 15, circuit activity recapitulated several key phenomena that have been observed in Ca2+ recordings of the E-PGs (Figures 2B,C; Movie 1): (1) a stable ‘‘bump’’ of activity appeared at one position in the glomerular axis of the protocerebral bridge (PB) and the corresponding ellipsoid body (EB) position, as observed by Seelig and Jayaraman (2015)
Summary
An animal navigating in its environment relies on landmarks to estimate its orientation and position (Collett and Graham, 2004). In the absence of visual cues, many animals maintain a representation of their heading and position without landmarks by continuously tracking their own motion to calculate navigation vectors to return to a specific location, a process called. Numerous studies have identified patterns of neural activity that could represent heading, one of the elements needed for path integration. These studies have further shown that heading representations are tuned by visual information but can be updated in the dark, without any visual feedback (Taube, 2007; Seelig and Jayaraman, 2015; Varga and Ritzmann, 2016), presumably by exploiting self-generated motion cues like efference copy (Kim et al, 2015). Heading estimation requires the tracking of variables in angular coordinates, a computation that can be accomplished by ‘‘ring attractor networks’’ (Skaggs et al, 1995; Zhang, 1996; Solovyeva et al, 2016)
Sign-in/Register to view highlights & summary Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a callDisclaimer: All third-party content on this website/platform is and will remain the property of their respective owners and is provided on "as is" basis without any warranties, express or implied. Use of third-party content does not indicate any affiliation, sponsorship with or endorsement by them. Any references to third-party content is to identify the corresponding services and shall be considered fair use under The CopyrightLaw.
