How a fly’s brain calculates its position in space
Sailing doesn’t always go as planned – a lesson flies learn the hard way, when a strong headwind pushes them astern in defiance of their forward flapping wings. Fish swimming upstream, crabs rushing sideways, and even humans hanging left while looking right face similar challenges. How the brain calculates the direction an animal is moving when the head is pointing one way and the body is moving another is a mystery in neuroscience.
A new study makes significant progress in solving this mystery by reporting that the fly’s brain has a set of neurons that signal the direction the body is moving, regardless of which direction the head is pointing. The findings, published in Nature, also describe in detail how the fly brain calculates this signal from more basic sensory inputs.
“Not only do these neurons signal the direction of travel of the fly, but they also do so in a world-centered frame of reference,” says Gaby Maimon, a neuroscientist at Rockefeller. What’s remarkable, adds first author Cheng Lyu, a graduate student in the Maimon lab, is that these insects transform body-referenced sensory inputs into a world-referenced signal, letting the fly know it’s traveling. , for example, at 90 degrees. to the right of the sun or to the north.
Find his place
Even when we close our eyes, we generally retain a good sense of where we are in a room and the direction we are facing. That’s because, even in the dark, our brain builds an internal understanding of where we are in space. In the 1980s scientists discovered that a group of cells called head steering cells played a key role in letting us know our angular orientation and it was later discovered that flies had cells with a function similar. Cell activity indicates the angle at which the head is pointing, similar to how a compass needle indicates its orientation in an environment.
All is well as long as we walk – or the flies fly – in the same direction as the head is turned. Head direction cells can be used to update the internal sense of where one is going. But if we walk north while facing east, or if a fly tries to buzz forward as the wind pushes it back, the head direction cells point the wrong direction. . Yet the system still works. Flies are relatively undisturbed by the indignities of wind currents, and humans don’t get lost as they pivot to admire the scenery. Lyu and Maimon wondered how flies know where they are going, even when their head direction cells were apparently transmitting inaccurate information.
To answer this question, Lyu glued fruit flies to miniature harnesses that only hold the insects’ heads in place, allowing him to record brain activity while leaving the flies free to flap their wings and steer. their bodies in a virtual environment. The setup contained several visual cues, including a bright light representing the sun and a field of dimming dots that could be adjusted to make the fly appear to be blown backwards or sideways.
As expected, the head direction cells consistently indicated the orientation of the fly relative to the sun, simulated by the bright light, independent of the movement of the dimming points. Additionally, the researchers identified a new set of cells that indicated which direction the flies were moving, not just which direction their heads were pointing. For example, if the flies were pointing directly at the sun in the east while being blown backwards, these cells indicated that the flies were moving (virtually) west. “This is the first set of cells known to indicate which direction an animal is moving in a world-centered frame of reference,” Maimon explains.
But the team also wondered how the flies’ brains calculated the animal’s direction of movement at the cellular level. In collaboration with Larry Abbott, a theorist of Colombia Universityfrom the Zuckerman Institute, Lyu and Maimon were able to demonstrate that the fly’s brain engages in a kind of mathematical exercise.
A student of physics tracing the trajectory of an object will break down the trajectory into components of motion, plotted along the x and y axes. Similarly, in the fly brain, four classes of visual motion-sensitive neurons indicate the direction of fly movement as components along four axes. Each neuronal class can be considered as representing a mathematical vector. The angle of the vector points in the direction of its associated axis. The length of the vector indicates how fast the fly is moving in that direction. “Amazingly, a neural circuit in the fly’s brain spins these four vectors so they’re correctly aligned with the angle of the sun, and then adds them together,” Maimon explains. “The result is an output vector that points in the direction the fly is moving, referenced to the sun.”
Vector math is more than just an analogy for running calculus. On the contrary, the fly’s brain seems to literally perform vector operations. In this circuit, the populations of neurons explicitly represent the vectors as waves of activity, with the position of the wave representing the angle of the vector and the height of the wave representing its length. The researchers even tested this idea by precisely manipulating the length of the four input vectors and showing that the output vector changes as it would if the flies literally added vectors together.
“We argue that what’s happening here is an explicit implementation of vector math in a brain.” said Maimon. “What makes this study unique is that we show, with ample evidence, how neural circuits implement relatively sophisticated mathematical operations.”
Understanding Spatial Cognition
This research clarifies how flies determine which direction they are going, at the time. Future studies will examine how these insects keep track of their direction of travel over time to find out where they ultimately ended up. “A central question is how the brain integrates signals related to the direction and speed of the animal’s movement over time to form memories,” says Lyu. “Researchers can use our findings as a platform to study what working memory looks like in the brain.”
The findings could also have implications for human disease. Because spatial confusion is often an early sign of Alzheimer’s disease, many neuroscientists are interested in understanding how brains construct an internal sense of space. “The fact that insects, with their small brains, have explicit knowledge of their direction of travel should compel researchers to look for similar signals and analogous quantitative operations in mammalian brains,” Maimon says.
“Such a finding could shed light on some aspects of the dysfunction underlying Alzheimer’s disease, as well as other neurological disorders that affect spatial cognition.”
Reference: “Building an allocentric displacement direction signal via vector calculus” by Cheng Lyu, LF Abbott and Gaby Maimon, December 15, 2021, Nature.