Theme 1: Neural Mechanisms for Navigation
This theme is investigating neural mechanisms for navigation in insects via electrophysiology and behavioural observation. This research is helping design computationally efficient and reliable algorithms for autonomous navigation.
Project Members
Theme Leader
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Mandyam
Srinivasan
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Insect Navigation
Tien Luu
Summary
Honeybees are excellent foragers, able to find food sources at sites up to 10km away from their hive. Their ability to find these sites and subsequently communicate the location of the food source to other worker bees upon their return clearly demonstrates their exceptional navigational abilities. Thus the honeybee provides an ideal experimental model to better understand the neural substrates of insect navigation.
Honeybee and Virtual Reality
A large body of published experimental data exists on freely flying honeybees in tunnel and maze experiments, much of which were conducted by theme leader M. Srinivasan and colleagues. Under Professor Srinivasan’s leadership, we have recently developed an experimental paradigm to investigate visually guided insect flight and navigation using tethered honeybees in a virtual reality arena. The virtual arena was constructed with the help of my Thinking System colleagues, Allen Cheung and David Ball. With their help, geometrically accurate 3D arenas could be rendered in real time on up to 4 monitors simultaneously, creating a panoramic visual environment which simulates motion. This 3D environment has been successful in initiating and maintaining flight behaviour in tethered honeybees.
The successful use of virtual reality in studying insect navigation has also paved the way for Gavin Taylor, a PhD student, who has adapted the current experimental paradigm to include force sensor measurements. It is envisaged that these measurements may be used to control movement within the virtual world, thus allowing the tethered honeybee to perform virtual free flights. This experimental setup allows for precise control of the visual environment, tracking of flight trajectories and being tethered, it will be possible to carry out electrical recordings from neurons in the honeybee brain during navigation and other tasks.
Honeybee flight: A novel ‘streamlining’ response (manuscript under revision)
The simulation of moving scenes shown across two standard LCD computer monitors, constituting less than half the visual panorama, has been shown to be sufficient to induce flight-like behaviour in tethered honeybees. The initiation and maintenance of flight-like behaviour purely by image motion (optic flow) has not been shown in insects. Using this virtual reality experimental setup an interesting, novel behavioural response was observed. The abdomen showed a ‘streamlining’ response when the bee was exposed to image motion that simulated forward flight (Fig. 1). Interestingly, this response is visually driven, and not due to aerodynamic drag, since there is no change in air resistance whilst tethered. We also observed this ‘streamlining’ response in 7 day old bees, which are known to be too young to have flight experience let alone performed outdoor foraging. This suggests the ‘streamlining’ behaviour may be an innate response of the honeybee and possibly of insects.
Figure 1. Changes in the abdominal position of the honeybee were observed when it was exposed to simulated forward image motion. The video footage of the flight behaviour were analysed using Matlab. The positional changes of the abdomen were tracked by measuring the long axis of the abdomen relative to the horizontal axis through the head and thorax
Panoramic motion vision in honeybees
In further experiments, we have implemented a panoramic virtual arena consisting of four LCD monitors. The ‘streamlining’ flight response was observed in both the 2- and 4-monitor setups. However, bees were observed to maintain the ‘streamlining’ posture for much longer periods when tested in the four monitor setup. Strikingly, this streamlining response remained the same irrespective of whether the virtual world was displayed with the two front, two rear or two diagonal monitors only. When two active monitors were presented to the bee, as the speed of image motion was progressively increased, the abdomen was raised progressively higher, up to a certain speed, beyond which the abdomen dropped with further increase of image speed. In contrast, using the same image speed protocol in the 4-monitor setup, the abdomen was raised progressively higher and would then remain elevated for the entire image speed stimulus (Fig. 2). Other flight properties have also been investigated using this 4-monitor setup. Some of the properties that we have examined include the honeybee’s abdominal flight response to contrast and to spatial frequency.
In addition, we have also completed studies examining the changes in wingbeat amplitude during the honeybee’s streamlining response. Combining these data with flight thrust measurements, a second manuscript is in preparation tentatively titled “Relationship between flight thrust, wingbeat amplitude and streamlining response in tethered, flying honeybees.”
Figure 2. The abdominal positions of tethered bee flights were tracked during testing in the various 2 and 4 monitor configurations. All flights were presented with the ascending image motion speed protocol. Note that the abdominal positional changes were similar regardless of the different 2 monitor configurations, but were in stark contrast to those flights tested in the 4 monitor set up, in which the abdomen remained in an elevated position for most the image speed protocol.
Honeybee electrophysiology
Colleagues from the Drosophila lab (B. van Swinderen, A. Paulk) at QBI routinely obtain multi-unit recordings from the honeybee and Drosophila brain. With their help a rig for honeybee electrophysiology has been set up and preliminary extracellular spike recordings from the honeybee brain have been successfully obtained. By performing extracellular recordings in live honeybees in the virtual reality arena, a number of interesting projects are being pursued. One of the projects is to identify the candidate cellular substrates of navigation, for example, the honeybee odometer. Another ongoing project is to examine the responses of motion sensitive neurons to the alarm pheromone. In the wild, when freely flying honeybees catch a whiff of the alarm pheromone, their flight behaviour changes dramatically, from normal meandering flying to increased speed and straight flight attack trajectory to the nearest perceived predator/intruder.
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Figure 3. Recordings from motion-sensitive neurons in live honeybees have recently been made. The figure below shows neuronal action potentials firing in response to a green horizontal bar that was moving upwards. There was no firing when the bar moved in the opposite direction, i.e. downwards. The bar was moving at a frequency of 1Hz.
Ongoing Collaborative Research
Properties of tethered honeybee flights in virtual reality – in collaboration with Thinking Systems colleagues, Allen Cheung and David Ball.
The effect of alarm pheromone on motion sensitive neuron in the honeybee - in collaboration with Dr Judith Reinhard.
Submissions
Luu, T., Cheung, A., Ball, D., Srinivasan, M. “Honeybee flight: A novel ‘streamlining’ response,” Journal of Experimental Biology (under revision).
Conference Abstracts or Poster
Luu, T., Cheung, A., Ball, D., Srinivasan, M.V. (2010) “Honeybee flight: A novel ‘streamlining’ response” Poster: 9th International Congress on Neuroethology. Salamanca, Spain.
Luu, T. (2009) Presented at the International Union for the Study of Social Insects conference (IUSSI), Brisbane, QLD.
Related Activities
Attended the Summer School of Animal Navigation held at the Australian National University, ACT, 2008.
Helped with the organization of the Summer School on Animal Navigation (UQ, 2009).
Demonstrator for the Bee Brain Challenge from 2008- 2010.
Media Coverage
Helped the SBS /BBC film crew (Stefan Moore, producer) shoot tethered honeybee flights. The movie clip was used in the “Honeybee Blues” documentary shown in Qantas iQ Inflight documentaries. Credited as “Bee wrangler”.
Supervision of student related to Thinking Systems
Supervising Gavin Taylor, a PhD student. Project title: Investigating visually guided flight behaviour of honeybees in a virtual-reality flight arena.
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Investigating Visually Guided Flight Behavior of Honeybees in Virtual-Reality Flight Arena
Gavin Taylor
Flying honeybees use visual information for tasks ranging from low-level speed control and obstacle avoidance to higher-level navigation tasks. Honeybee’s visual behavior can potentially be used to inspire novel visually guided robotic control systems. However, visually guided honeybee behavior has previously only been studied in free flight conditions. In laboratory studies, honeybees are typically placed in very restrained harnesses and have difficulty learning visual cues.
I have developed a novel assay where tethered honeybees fly in a virtual-reality flight arena. A panoramic visual stimulus is displayed to the tethered honeybee, and a force transducer measures the honeybees thrust. This feedback is used to close the loop between the bee’s decision and the movement speed of the visual panorama it experiences.
Figure 1: (a) Tethered honeybee, (b) View of tethered bee in virtual-reality arena.
Preliminary experiments show honeybees attempt to maintain a constant rate of optic flow in the arena, as expected from free flight studies. In the presence of a headwind, they raise their thrust output to restore the optic flow rate they experience. Honeybees are able to learn to use alternate motor outputs to control the speed of the visual panorama they see, showing low-level operant conditioning.
Figure 2: (a) Honeybees raise their thrust in the presence of headwind, which maintains a similar rate of optic flow as in the no wind condition (b).
When flying along a tunnel in free flight, honeybees fly centrally such that each eye experiences an equal rate of optic flow. When exposed to unbalanced optic flow cues in the arena, honeybees make ‘ruddering’ movement using their abdomens. This ruddering behavior may indicate the honeybees are trying to control their yaw when flying in the arena.
Figure 3: Honeybees display a ruddering behavior when shown unbalanced optic flow.
With the virtual-reality flight arena now nearly finished being developed, my future work will concentrate on behavioral studies using this assay:
• Analysis of the honeybees speed control system will be undertaken. This will look at the robustness, response to disturbances, and the effect of the scene’s visual properties.
• Operant conditioning of the honeybee to use alternate motor outputs to control its flight speed will be conducted. This efficacy will be compared to when it uses thrust.
• The correlation between the thrust produced by the honeybee and optical measurements of its wingbeat amplitude will be measured. I will evaluate the possibility of using optical measures of the wingbeat for closed loop control.
• Yaw control for the tethered bee using an optical measure of its ruddering will be implemented. This will allow investigation of the centring response and obstacle avoidance.
• Operant conditioning of the honeybee to visual cues that is similar to navigation in free flight will be developed. I will investigate how the honeybee uses landmarks and visual odometry to remember goals.
Ongoing Collaborative Research
This work is done in collaboration with my supervisors Tien Luu, David Ball and Mandyam Srinivasan. Tien Luu pioneered the method of open loop tethered flight in a virtual-reality arena that I have expanded on. David Ball wrote a program to display panoramic visual stimulus on four computer monitors that I have used.
Related Activities
I attended the 8th ACEVS-CVS Summer School on Animal Navigation.