Donut-shaped 'compass' glimpsed inside fly brain

By Jonathan Webb
Science reporter, BBC News

Media caption,
A concentrated patch of activity shifted around the ring as the fly turned (Footage: Johannes Seelig / Nature)

A cluster of cells in the brain of a fly can track the animal's orientation like a compass, a study has revealed.

Fixed in place on top of a spherical treadmill, a fruit fly walked on the spot while neuroscientists peered into its brain using a microscope.

Watching the neurons fire inside a donut-shaped brain region, they saw activity sweep around the ring to match the direction the animal was headed.

Mammals have similar "head direction cells" but this is a first for flies.

The findings are reported in the journal Nature.

Crucially, the compass-like activity took place not only when the animal was negotiating a virtual-reality environment, in which screens gave the illusion of movement, but also when it was left in the dark.

"The fly is using a sense of its own motion to pick up which direction it's pointed," said senior author Dr Vivek Jayaraman, from the Howard Hughes Medical Institute's Janelia Research Campus.

In some other insects, such as monarch butterflies and locusts, brain cells have been observed firing in a way that reflects the animal's orientation to the pattern of polarised light in the sky - a "sun compass".

But the newly discovered compass in the fly brain works more like the "head directions cells" seen in mammals, which rapidly set up a directional system for the animal based on landmarks in the surrounding scene.

'Fly whisperer'

"A key thing was incorporating the fly's own movement," Dr Jayaraman told the BBC.

"To see that its own motion was relevant to the functioning of this compass - that was something we could only see if we did it in a behaving animal."

Hence, Dr Jayaraman and his colleague Johannes Seelig built an intricate set-up where the fly, already manipulated so that its brain cells would glow when they fired, walked on top of a freely rotating ball. They glued the fly to a metal rod, to hold it stationary, and focussed a powerful laser microscope on its brain.

For the virtual reality experiments, they surrounded the fly with screens displaying simple patterns of lines, whose movement was controlled by that of the ball.

Image source, Igor Siwanowicz

It was time-consuming and fiddly work, for which Jayaraman praised the dexterity of his postdoctoral researcher Dr Seelig.

"We call him 'the fly whisperer' in the lab. He has a magic set of hands that allow him to do the most remarkably fine dissections, while leaving the fly comfortable enough to actually behave in its environment."

Unlike the situation in mammals, where this type of direction-sensitive cell seems to be quite scattered within the brain, the fly compass appears to be packed into a particular area called the "ellipsoid body" - which also happens to be circular.

This meant that the researchers could zoom in on this region and watch the compass in action.

"It's very seldom that you have a compass in the brain that really looks like a compass," Dr Jayaraman said.

He added that it was Dr Seelig who first saw the sweeping pattern of activity unfolding as the "needle" of the compass swung around to match the fly's own turning.

"He's an understated, Swiss guy. He came into my office and plonked this video down and he said, I think maybe there's something here.

"I looked at it and I wanted to jump up and hug him."

Abstract information

The researchers argue that the compass is surprisingly complex, considering the size of the brain making the calculations. As such, Dr Jayaraman said, "the fly may have a lot to tell us" about how bigger brains, including ours, accomplish similar tasks.

Image source, Tanya Wolff/Nirmala Iyer/Gerry Rubin
Image caption,
The "ellipsoid body" is tucked deep in the middle of the fly brain

Prof Kate Jeffery studies head direction cells in mammals, in her own lab at University College London. She told BBC News this was a striking set of results.

"The novelty is that they're seeing a signal that isn't a simple transformation of what the sensory receptors see," Prof Jeffery said.

"These neurons are not purely visual. They're integrating information and they're abstracting something at a higher level."

To build up its representation of direction, she explained, this system must distil information from across different senses.

"It's a bit more like cognition - in a fly - which is kind of cool."

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