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Random chance in early brain development sets adult fruit flies’ personalities

Brain wiring asymmetry established as animals grow influences their innate behavior, a new study finds

March 24, 2020

undefinedA new study led by Allen Distinguished Investigator Bassem Hassan, Ph.D., found a set of fruit fly neurons that influence the animals' personalities.

Imagine yourself on a round platform surrounded on all sides by an impassable moat and, on the other side of that water, high white walls. An uncomfortably bright light shines directly on you. You feel exposed.

It sounds weird, but this scenario is about free choice. In the stark white walls, there are two black areas. Could they be hiding spots, a refuge from the blinding white light? You start to walk toward one, and realize the water blocks your way. You turn and head toward the other one.

How long would you spend pacing between these two unreachable goals before you gave up in desperation? Would you march straight toward the black stripe, or would you spend more time exploring your surroundings?

If you were a fruit fly — the creature this bizarre contraption was designed for — the answer to these questions would be: It depends on your brain wiring, according to a new study published in the journal Science earlier this month. The strange set-up is a very specialized behavioral experiment known as Buridan’s paradigm, named after the 14th century French philosopher Jean Buridan.

The new study found that asymmetry in how neurons connect from one side of the fly brain to the other, established early in development and based solely on random chance, irreversibly establishes adult flies’ behavior in this David Lynch-ian experiment. 

A fruit fly personality test

undefinedThis image, taken from a movie by Hassan and his laboratory team, shows the paths walked by a fruit fly in an unusual experimental setup known as Buridan's paradigm. Reprinted with permission from GA Linneweber et al., Science 367:6482 (2020).

Of course, we can’t know the emotional motivation of a fruit fly, said Bassem Hassan, Ph.D., a researcher at the Institut du Cerveau – Paris Brain Institute in Paris and lead author of the newly published study. To say they feel desperation is probably a stretch.

“If I or anybody could read the mind of a fly, that would be great,” said Hassan, who is also an Allen Distinguished Investigator. “We know that high-contrast objects are attractive. And we know that the fly is in the middle of this brightly lit arena with two identical objects on either end, this bizarre symmetrical world. Its behavior could be trying to get out of the light into the dark to hide, or it could be the desire to explore these landmarks, or some combination.”

What Hassan and his colleagues do know, after running Buridan’s paradigm on many, many different fruit flies, is that each individual insect tends to do the same thing each time it’s placed in the tiny arena. One fly will make a beeline from one black stripe to the other, while its more freewheeling neighbor will meander all over the white platform.

And it’s not too much of a stretch to call these behaviors personality traits, if you will, Hassan said. Generally, a straight-line walker always walks a straight line, and a meanderer always wanders, no matter how many times they repeat the experiment.

Brain imbalance

undefinedDorsal cluster neurons and their connections light up under the fluorescent microscope in this movie by Hassan's laboratory team. Reprinted with permission from GA Linneweber et al., Science 367:6482 (2020).

Hassan and his team, with support directed by The Paul G. Allen Frontiers Group, a division of the Allen Institute, identified the root cause of those two types of fruit fly personalities: asymmetry in brain wiring in the insects’ visual system, specifically in a group of neurons known as the dorsal cluster neurons. These neurons sit in two bundles on either side of the fly’s head, with crisscrossing connections between the two clumps. It turns out those connections aren’t even though — some flies have more wires going from right to left, some have more going from left to right.

The scientists found that flies with the largest imbalance in this wiring walked the straightest lines, and those with more balanced wiring were the meanderers. If they silenced the activity of these particular neurons, the correlation between behavior and asymmetry was lost. That correlation was so strong that the researchers could predict a fly’s brain wiring diagram just by observing the way it walked the platform.

The research team also noticed that these personality traits weren’t inherited in any kind of pattern. Two meandering parents could produce a bee-liner, and two straight-line walkers could have a litter of wanderers.

Dorsal cluster neurons and their wiring are established early in fruit fly development. And the asymmetry between them is random — random chance isn’t unusual in biology, but we don’t have many known instances of biological happenstance influencing a fixed personality trait, Hassan said.

“No two flies have exactly the same brain. Does this explain why individuals — flies, like humans, like any other animal — behave very differently from one another?” Hassan asked. “In this case, we found that the answer to that was yes.” 

Nature, nurture or other? 

It’s not clear whether anything similar is happening in our own brains — nobody’s yet studied whether human brain asymmetry correlates with innate personality traits. But some studies have found that physical features in our brains, the patterns of folds in the outer shell of the brain, correlate with learning. Like the flies’ wiring, these physical features are established early in development, before we’re born.

The Paris research team didn’t stumble across these particular neurons by chance. They’d been studying these brain cells and how they develop for many years, including discovering that their asymmetry is established randomly. That was key to figuring out the link between this developmental event and the adults insects’ behavior, Hassan said.

“If you read the genome of any given individual, you wouldn’t be able to predict its behavior,” he said. “It’s not only in the genome, and it’s not only in the experience, it’s also in this step in between — namely brain development — that you need to study independently.”


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