The head direction (HD) system is classically modeled as a ring attractor network which ensures a stable representation of the animal’s head direction. This unidimensional description popularized the view of the HD system as the brain’s internal compass. However, unlike a globally consistent magnetic compass, the orientation of the HD system is dynamic, depends on local cues and exhibits remapping across familiar environments5. Such a system requires mechanisms to remember and align to familiar landmarks, which may not be well described within the classic 1-dimensional framework. To search for these mechanisms, we performed large population recordings of mouse thalamic HD cells using calcium imaging, during controlled manipulations of a visual landmark in a familiar environment. First, we find that realignment of the system was associated with a continuous rotation of the HD network representation. The speed and angular distance of this rotation was predicted by a 2nd dimension to the ring attractor which we refer to as network gain, i.e. the instantaneous population firing rate. Moreover, the 360-degree azimuthal profile of network gain, during darkness, maintained a ‘memory trace’ of a previously displayed visual landmark. In a 2nd experiment, brief presentations of a rotated landmark revealed an attraction of the network back to its initial orientation, suggesting a time-dependent mechanism underlying the formation of these network gain memory traces. Finally, in a 3rd experiment, continuous rotation of a visual landmark induced a similar rotation of the HD representation which persisted following removal of the landmark, demonstrating that HD network orientation is subject to experience-dependent recalibration. Together, these results provide new mechanistic insights into how the neural compass flexibly adapts to environmental cues to maintain a reliable representation of the head direction.

The ability to keep track of one’s location in space is a critical behavior for animals navigating to and from a salient location, and its computational basis is now beginning to be unraveled. Here, we tracked flies in a ring-shaped channel as they executed bouts of search triggered by optogenetic activation of sugar receptors. Unlike experiments in open field arenas, which produce highly tortuous search trajectories, our geometrically constrained paradigm enabled us to monitor flies’ decisions to move toward or away from the fictive food. Our results suggest that flies use path integration to remember the location of a food site even after it has disappeared, and flies can remember the location of a former food site even after walking around the arena one or more times. To determine the behavioral algorithms underlying Drosophila search, we developed multiple state transition models and found that flies likely accomplish path integration by combining odometry and compass navigation to keep track of their position relative to the fictive food. Our results indicate that whereas flies re-zero their path integrator at food when only one feeding site is present, they adjust their path integrator to a central location between sites when experiencing food at two or more locations. Together, this work provides a simple experimental paradigm and theoretical framework to advance investigations of the neural basis of path integration.

Every autumn, monarch butterflies migrate from North America to their overwintering sites in Central Mexico. To maintain their southward direction, these butterflies rely on celestial cues as orientation references. The position of the sun combined with additional skylight cues are integrated in the central complex, a region in the butterfly’s brain that acts as an internal compass. However, the central complex does not solely guide the butterflies on their migration but also helps monarchs in their non-migratory form manoeuvre on foraging trips through their habitat. By comparing the activity of input neurons of the central complex between migratory and non-migratory butterflies, we investigated how a different lifestyle affects the coding of orientation information in the brain.

I am working on the vertebrate retina, with a main focus on the mouse and bird retina. Currently my work is focused on three major topics: Functional and molecular analysis of electrical synapses in the retina Circuitry and functional role of retinal interneurons: horizontal cells Circuitry for light-dependent magnetoreception in the bird retina Electrical synapses Electrical synapses (gap junctions) permit fast transmission of electrical signals and passage of metabolites by means of channels, which directly connect the cytoplasm of adjoining cells. A functional gap junction channel consists of two hemichannels (one provided by each of the cells), each comprised of a set of six protein subunits, termed connexins. These building blocks exist in a variety of different subtypes, and the connexin composition determines permeability and gating properties of a gap junction channel, thereby enabling electrical synapses to meet a diversity of physiological requirements. In the retina, various connexins are expressed in different cell types. We study the cellular distribution of different connexins as well as the modulation induced by transmitter action or change of ambient light levels, which leads to altered electrical coupling properties. We are also interested in exploiting them as therapeutic avenue for retinal degeneration diseases. Horizontal cells Horizontal cells receive excitatory input from photoreceptors and provide feedback inhibition to photoreceptors and feedforward inhibition to bipolar cells. Because of strong electrical coupling horizontal cells integrate the photoreceptor input over a wide area and are thought to contribute to the antagonistic organization of bipolar cell and ganglion cell receptive fields and to tune the photoreceptor–bipolar cell synapse with respect to the ambient light conditions. However, the extent to which this influence shapes retinal output is unclear, and we aim to elucidate the functional importance of horizontal cells for retinal signal processing by studying various transgenic mouse models. Retinal circuitry for light-dependent magnetoreception in the bird We are studying which neuronal cell types and pathways in the bird retina are involved in the processing of magnetic signals. Likely, magnetic information is detected in cryptochrome-expressing photoreceptors and leaves the retina through ganglion cell axons that project via the thalamofugal pathway to Cluster N, a part of the visual wulst essential for the avian magnetic compass. Thus, we aim to elucidate the synaptic connections and retinal signaling pathways from putatively magnetosensitive photoreceptors to thalamus-projecting ganglion cells in migratory birds using neuroanatomical and electrophysiological techniques.

The regions of the insect brain devoted to spatial navigation are beautifully orderly, with a remarkably precise pattern of synaptic connections. Thus, we can learn much about the neural mechanisms of spatial navigation by targeting identifiable neurons in these networks for in vivo patch clamp recording and calcium imaging. Our lab has recently discovered that the "compass system" in the Drosophila brain is anchored to not only visual landmarks, but also the prevailing wind direction. Moreover, we found that the compass system can re-learn the relationship between these external sensory cues and internal self-motion cues, via rapid associative synaptic plasticity. Postsynaptic to compass neurons, we found neurons that conjunctively encode heading direction and body-centric translational velocity. We then showed how this representation of travel velocity is transformed from body- to world-centric coordinates at the subsequent layer of the network, two synapses downstream from compass neurons. By integrating this world-centric vector-velocity representation over time, it should be possible for the brain to form a stored representation of the body's path through the environment.

Join the Department of Bioengineering on the 26th May at 9:00am for The 2021 Annual Bioengineering Lecture + Bioinspired Guidance, Navigation and Control Symposium. This year’s lecture speaker will be distinguished bioengineer and neuroscientist Professor Mandyam V. Srinivasan AM FRS, from the University of Queensland. Professor Srinivasan studies visual systems, particularly those of bees and birds. His research has revealed how flying insects negotiate narrow gaps, regulate the height and speed of flight, estimate distance flown, and orchestrate smooth landings. Apart from enhancing fundamental knowledge, these findings are leading to novel, biologically inspired approaches to the design of guidance systems for unmanned aerial vehicles with applications in the areas of surveillance, security and planetary exploration. Following Professor Srinivasan’s lecture will be the Bioinspired GNC Mini Symposium with guest speakers from Google Deepmind, Imperial College London, the University of Würzburg and the University of Konstanz giving talks on their research into autonomous robot navigation, neural mechanisms of compass orientation in insects and computational approaches to motor control.

Each spring, billions of Bogong moths escape hot conditions in different regions of southeast Australia by migrating over 1000 km to a limited number of cool caves in the Australian Alps, historically used for aestivating over the summer. At the beginning of autumn the same individuals make a return migration to their breeding grounds to reproduce and die. To steer migration Bogong moths sense the Earth’s magnetic field and correlate its directional information with visual cues. In this presentation, we will show that a critically important visual cue is the distribution of starlight within the austral night sky. By tethering spring and autumn migratory moths in a flight simulator, we found that under natural dorsally-projected night skies, and in a nulled magnetic field (disabling the magnetic sense), moths flew in their seasonally appropriate migratory directions, turning in the opposite direction when the night sky was rotated 180°. Visual interneurons in the moth’s optic lobe and central brain responded vigorously to identical sky rotations. Migrating Bogong moths thus use the starry night sky as a true compass to distinguish geographic cardinal directions, the first invertebrate known to do so. These stellar cues are likely reinforced by the Earth’s magnetic field to create a robust compass mechanism for long-distance nocturnal navigation.

For spatial orientation, heading information can be processed in two different frames of reference, a self-centered egocentric or a viewpoint allocentric frame of reference. Using the most efficient frame of reference is in particular important if an animal migrates over large distances, as it the case for the monarch butterfly (Danaus plexippus). These butterflies employ a sun compass to travel over more than 4,000 kilometers to their destination in central Mexico. We developed tetrode recordings from the heading-direction network of tethered flying monarch butterflies that were allowed to orient with respect to a sun stimulus. We show that the neurons switch their frame of reference depending on the animal’s locomotion state. In quiescence, the heading-direction cells encode a sun bearing in an egocentric reference frame, while during active flight, the heading-direction is encoded within an allocentric reference frame. By switching to an allocentric frame of reference during flight, monarch butterflies convert the sun to a global compass cue for long-distance navigation, an ideal strategy for maintaining a migratory heading.

In a cross wind, the direction a fly moves through the air may differ from its heading direction, the direction defined by its body axis. I will present a model based on experimental results that reveals how a heading direction “compass” signal is combined with optic flow to compute and represent the direction that a fly is traveling. This provides a general framework for understand how flies perform vector computations.