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his level of insight had evaded olfaction researchers because odors travel through the air in chaotic, turbulent plumes. “You really don’t have the detailed, moment-to-moment information of what an animal is experiencing,” Ruta says.
So Ruta and her team created a virtual-reality setup that provided those details. In the paradigm, a tethered fruit fly walks on a foam ball about 6 millimeters across that functions as a tiny treadmill. As the fly turns itself in different directions, a tube delivering a stream of air rotates around it, simulating the wind. The researchers created odor plumes with customizable geometries and concentrations by adjusting the amount of apple cider vinegar vapor added to the air stream.
“Stimulus control with odors is a nightmare. I really hate it. But they cleverly designed their system to control the timing of odor concentration dynamics with high precision,” says Matt Smear, associate professor of neuroscience and psychology at the University of Oregon, who was not involved in the work.
Stimulus control with odors is a nightmare. I really hate it. But they cleverly designed their system to control the timing of odor concentration dynamics with high precision.
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Matt Smear
Almost immediately, the team noticed that the flies stuck to the edge of the plume, Ruta says. “It was a very striking behavior, and very robust.”
The flies tracked the plume’s edge irrespective of how the odor concentration changed as the fly kept walking. The behavior persisted when the plume’s trajectory tilted away from the wind direction or even ran perpendicular to it. “That was one of the wildest things for me,” Suver says. To pull this off, the flies must remember the angle to travel when returning to the plume, modeling experiments showed.
The memory is indeed directional and not positional: When tracking a jumping plume that shifts 20 millimeters away whenever the flies leave it, the flies walked past the plume’s old location and kept trekking in the direction that they expected would lead them to their goal. The researchers could even rewrite an entry-angle memory by delivering a whiff of vinegar when the flies spontaneously walked in the direction of the new plume.
A population of neurons in the central complex called FC2 signals the direction flies should walk just before they turn back toward the plume, imaging experiments showed. Silencing the FC2 neurons impaired the edge-tracking behavior.
“I’m convinced that they’re using a memory to go back to where they last encountered the odor,” Smear says.
Follow-up work should explore when edge tracking fails and which strategies take over, says Tobias Ackels, group leader at the University of Bonn, who was not involved in the study. “What happens when the signal gets noisy?” Other work could examine if flying, which adds a vertical component to plumes, requires a different tracking approach than walking, and if flies handle non-food-related and aversive odors in the same ways, Suver says.
It will also be interesting to see if these findings hold up in a freely moving fly, Louis says. The study is “a very solid basis on which to build.”