When a fruit fly selects a target, the insect locks it in its sight (fixates) and homes in. ‘But less was known about what happens when they actually reach those objects,’ explains Alice Robie from the California Institute of Technology. Explaining fixation, Robie's supervisor, Michael Dickinson, says, ‘It is often described as what happens when you hang a carrot in front of a donkey and it keeps following the carrot forever. We were curious about what happens when the “donkey” actually gets to the carrot. Andrew Straw in my lab has been working on developing software that allows us to track flies with high accuracy so we had the technology to allow us to see how the flies explore a simple but interesting landscape under conditions where we could know their position and velocity at all times’ (p. 2494).
But first Robie and Dickinson had to design their landscape. Filming the insects' movements from a single position, the duo settled on a landscape of cones arranged in an arena so that they could always see the fly's position and calculate the insect's vertical position as it scaled the heights. Robie built 4 cones ranging from 36 mm to 10 mm high each with the same surface area but with sides ranging from a steep 75 deg slope to a shallow 30 deg slope. Then she released individual flies, which were hungry and so highly motivated to explore their surroundings, into the arena and filmed them for 10 min in infra-red light. Robie was instantly struck that the flies explored all four cones equally, but once they'd found the highest cone they scaled it and spent more time there than on the shorter shallower cones. ‘We were surprised that they showed such a strong preference for the tallest, steepest object,’ says Dickinson.
Curious to know how the insects identified the tallest cone, Robie switched off the lights and filmed them with infra-red light to see how they coped in the dark. Without their sight, the flies could no longer fixate on the cones, so their paths became more wiggly as they explored the arena, but once they had stumbled upon the highest cone they reacted as if the lights were on, scaled it and stopped at the top. The insects were using some sense other than vision to identify the tallest cone.
Knowing that the insects sense gravity with sensors in their antennae (Johnston's organs) Robie wondered if the insects could use these gravity sensors to identify the steepest (and highest) cone. Putting a dab of glue on the joint between the second and third antennal segments to inactivate the Johnston's organs, Robie waited to see if the insect could identify the tallest cone by vision alone. Again the fly succeeded.
Finally, Robie decided to see whether a fly deprived of sight and its gravity sensors could identify the tallest cone, but this time it could not. ‘The movie was extraordinary,’ says Dickinson, ‘they would go up the cone over the top and down the other side. It was like they just didn't know they were on an object.’
Dickinson admits that he was surprised that the flies were unable to identify the tallest cone when deprived of both senses. He says, ‘The animal is covered with mechano receptors, especially on the legs, so we were almost certain that they could use information from their legs to tell them they are on a steep object.’ However, having convinced himself that fruit flies only require two senses to identify steep slopes, Dickinson is keen to find out more about the neural circuits that control how flies explore their environment.
