Fruit flies manage chaotic scent navigation using a sophisticated memory system rather than simple reflexes, a discovery that challenges long-held biological models. Researchers at Rockefeller University led by Vanessa Ruta demonstrated that when hunting for a mate or rotting food, the insects track the edge of a turbulent odor plume by holding a “mental map” of the target’s location.
Testing the insect brain
For a long time, biologists stood by the “surge and cast” model, which posited that insects solved this with hardwired reflexes. The idea was that, when a fly registers the plume with olfactory neurons in its antennae, it simply flies upwind until it’s gone and then flies side to side attempting to catch it again. The trouble with the traditional model is that it struggles to explain how an insect tracks a meandering plume across long distances.
To test this, the team designed a virtual reality system for tethered flies. They placed the insects on a ball floating on air in the dark, allowing the researchers to control the wind and odor plumes precisely. In a straight corridor of vinegar about 50 millimeters wide, the flies did not do the obvious thing and march up the middle. Instead, they hugged one edge, riding it through a repeating two-step process.
The moment a fly crossed into the odor, it would whip around and move back out, loop through the clean air outside, then make a beeline back to the boundary. The team called this behavior edge tracking. The flies also spent far more time loitering outside the plume than inside it, even though nearly all their forward progress toward the source happened during those brief dips into the scent.
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It’s a little fly-sized treadmill, Ruta explains. As the fly walked on the surface of the ball, its turns steered a nozzle that blew a steady stream of air at its antennae, so the insect always felt wind coming from a fixed direction, as if it were walking across an open field.
When the team reversed the gradient, so the vinegar grew fainter as the fly advanced, the flies tracked the edge just as well. This suggests the insects aren’t climbing a rising gradient of odor toward the source.
Memory and a compass
The team also worked with flies genetically engineered so light could switch their olfactory neurons on directly, in both antennae at once. When scientists swapped real odor for a beam of 660-nanometer red light, the insects tracked the edge of this light plume flawlessly.
The real surprise, though, came when the team took a close look at what the flies were doing when there was no smell at all to guide them. When the researchers made a plume vanish while a fly was outside it, the insect kept heading back to where the edge should have been. Rather than searching at random, they were heading to where they knew the odorant should be. It looked as if they had a stored memory that was still steering them in that direction.
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The neuronal compass, though, was just one piece of the puzzle. To find the smell that got lost in the wind, the fly must have a goal—a memory of what to search for. The team located olfactory memories in another group of neurons found in something called the fan-shaped body, already known to encode where a fly wants to go. Out in the clean air, this pointer swung away from the compass to aim at the plume’s edge, several seconds before the fly physically turned to head back.
Like in a compass, the activity of these neurons acts like a pointer, but in this case, the one that marks the fly’s intended destination. When they get out, they have no immediate sensory information to guide them back to the plume. That’s when the memory becomes important, Ruta says.
To confirm whether the flies memorize where the plume’s edge is, the team tested whether the insects could update these memories. They had flies track a plume tilted 45 degrees, then abruptly flipped it to the opposite 45-degree angle. At first the insects were lost, searching in the old direction. But a single training session—a puff of vinegar delivered whenever a fly happened to walk the correct new angle—was enough to fix the issue. The flies instantly rewrote their internal goal and began tracking the new segment.
“We could write in new entry angles,” Ruta says. To her that was some of the strongest evidence that a memory, not a reflex, was responsible for fruit flies’ olfactory navigation.
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When the team ran the flies through a simulated natural plume in their computer model, the entry-angle memory worked best near the source, where the plume held together as a coherent ribbon. Farther downwind, where it shattered into chaotic filaments arriving from every direction, the memory quickly grew unreliable and got overridden. The team speculates that’s likely where the flies fall back on simpler reflexes. Animals are adapting their strategy, Ruta says.
She suggests they probably lean on memory when the world is predictable and abandon it when it isn’t. One of the first things the team wants to examine now is whether the memories are relevant for tracking very turbulent plumes in living flies or are in fact replaced by other mechanisms when things calm down, as their model suggested.
There’s an increasing appreciation of Drosophila and the power of this fly to provide insights into core computations translating fleeting sensory signals into stored spatial goals, Ruta argues. Because the fruit fly has one of the simplest and most extensively studied brains, such insights, she thinks, should be relevant for how this process works in the rest of the animal kingdom. It’s a fundamental feature that all animals are able to carry out, including ones with more sophisticated, complex brains like our own, she adds.