How a fly's brain calculates its position in space



Fly brains can perform math to calculate direction of travel. Credit: Meishel Desouto.

A lesson that flies learn the hard way is when a strong wind pushes them backward in defiance of their wings. The brain calculates an animal's direction of travel when the head is pointing one way and the body is moving in another.
A new study shows that the fly brain has a set of neurons that signal the direction in which the body is traveling, regardless of the direction in which the head is pointing. The fly's brain calculates this signal from more basic sensory inputs according to the findings published in Nature.
Rockefeller neuroscientist Gaby Maimon says that the fly's direction of travel is communicated by these neurons in a world-centered reference frame. Cheng Lyu, a graduate student in the Maimon lab, says that these insects are transforming body-referenced sensory inputs into a world-referenced signal, allowing the fly to know that it is traveling.
Finding a place.
We retain a good idea of where we are in a room when we close our eyes. Our brains are able to understand where we are in space even in darkness. Scientists discovered in the 1980s that a group of cells called head direction cells play a key role in letting us know our orientation and later found flies have cells with similar function. The activity of the cells indicates the angle in which the head is pointing.
All is well if we're walking in the same direction that the head is facing. The internal sense of where one is going can be updated by the head-direction cells. The head direction cells point in the wrong direction if we walk north while facing east or if a fly tries to buzz forward while the wind pushes it back. The system still works. Humans don't get lost when they go to take in the scenery, and flies are unperturbed by wind currents. Lyu and Maimon wondered how flies know where they're going, even when their head direction cells are not telling the whole story.
To answer this question, Lyu put fruit flies in miniature harnesses that held their heads in place, so that he could record brain activity while leaving the flies free to flap their wings and steer their bodies through a virtual environment. A bright light representing the sun and a field of dimmer dots that could be adjusted made the fly feel like it was being blown backwards or sideways.
The head direction cells consistently indicated the fly's orientation to the sun, regardless of the dimmer dots' motion. The researchers found a new set of cells that indicated which way the flies were traveling. If the flies were oriented toward the sun in the east while being blown backward, these cells indicated that the flies were traveling west. Maimon says that this is the first set of cells known to indicate which way an animal is moving.
Mental math.
The team wondered how fly brains compute the animal's travel direction at the cellular level. Lyu and Maimon were able to demonstrate that the fly brain engages in a sort of mathematics exercise.
A physics student will plot the trajectory of an object along the x- and y- axis. The fly brain has four classes of neurons that are sensitive to visual motion and indicate the fly's traveling direction as components along four axes. Each class can be thought of as a mathematical representation. The angle of the vector's axis is related to it. The fly's length indicates how fast it is moving. The fly brain has a neural circuit that rotates the four vectors so that they are aligned to the angle of the sun. The result is an output that points to the direction the fly is traveling.
It is more than just an analogy for computation. The fly brain appears to be performing operations. In this circuit, populations of neurons represent waves of activity, with the position of the wave and the height of the wave representing the angle and length of the wave. The idea was tested by manipulating the length of the four input and four output files and showing that the output file changes just as it would if flies were adding up the files.
"We make a strong argument that what's happening here is an explicit implementation of math in the brain." Maimon says something. The study is unique because it shows how the circuits implement mathematical operations.
Understanding spatial thinking.
The research shows how flies figure out which way to go. Future studies will look at how these insects keep track of their travel direction over time to know where they end up. The brain integrates signals related to the animal's travel-direction and speed over time to form memories. Researchers can use our findings to study what working memory looks like in the brain.
The findings might have implications for human disease. Because spatial confusion is 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 have explicit knowledge of their traveling direction should compel researchers to look for similar signals and operations in mammals.
It is possible that a discovery will inform aspects of the underlying Alzheimer's disease and other neurological disorders that afflict spatial cognitive impairment.
Gaby Maimon is building an allocentric traveling-direction signal via vector computation. www.nature.com/articles/s41586-021-04067-0

Nature journal information.

A fly's brain calculates its position in space in December of 2021.

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