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Developmental biology - Brain

To Flee or Not to Flee: How the Brain Decides

Scientists identify variables leading the brain to engage defense strategies - uncovering a pair of neurons crucial to the process...


Though it has been many millennia since humans were regularly threatened by predatory wild animals, the brain circuits that ensure our survival are still very much alive. "Just like any other animal in nature, our reaction to a threat is invariably one of the following three: escape, fight, or freeze in place with the hope of remaining unnoticed," says Marta Moita, who with Maria Luisa Vasconcelos led the study conducted at the Champalimaud Centre for the Unknown in Lisbon, Portugal.

According to Ricardo Zacarias, the first author of the study: "These behaviors are fundamental, but we still don't know what the rules of the game are: in each situation, how does the brain decide which of the three strategies to implement and how does it ensure that the body carries it through?" The work published today (September 12th) in the scientific journal Nature Communications.

Remarkably, unprecedented insight into these questions came from the common fruit fly. Marta Moita: "When we started working on these issues most people believed that flies only escape, but we wondered if that was really true. Even though it's an insect, the fruit fly is an incredibly powerful model organism that has helped shed light on many difficult problems in biology. So when we decided to delve into the neural basis of defensive behavior, we asked, what will happen if we expose flies to a threat in a situation where they couldn't just fly away?"

The results were immediately clear she explains: "When we placed the flies in a covered dish and exposed them to an expanding dark circle (which is how a threat looks like to a fly), we saw something completely new: they froze. In fact, just like mammals, they would remain perfectly motionless for minutes on end, sometimes in very awkward positions, such as half crouching, or with a leg or two suspended in the air."

But the story didn't end there. Many of the flies froze, but some didn't - some ran away from the threat. Vasconcelos: "This was very exciting because it meant that similar to humans, flies were choosing between alternative strategies."
Using imaging software to take a closer look at what triggers different responses in fly behavior, they discovered the unexpected — a fly's response hinged on its walking speed at the moment a threat appeared. If a fly was moving slowly, it would freeze — but if it was walking quickly, it would run from the threat.

"This result is very important. It is the first showing how the behavioral state of an animal can influence its choice of defensive strategy," Vasconcelos points out. These observations opened the door to identifying the actual neurons that determined whether the fly would flee or freeze. Using state-of-the-art genetic tools, the team found a single pair of neurons important for the flies' defensive behaviors.

Vasconcelos: "It was quite incredible. There are hundreds of thousands of neurons in the brain of the fly, and among all of those, we found that freezing was controlled by two identical neurons, one on each side of the brain."
When the team turned the neurons off, flies didn't freeze anymore, they escaped from the threat. But, when they turned the neurons on without the presence of a threat — flies would freeze in a manner dependent on their walking speed.

Zacarias: "If we turned the neurons on when the fly was walking slowly, it would freeze. But, not if it was walking quickly. This result places these neurons directly at the gateway of the circuit of choice!"

Moita: "This is exactly what we were looking for: how the brain decides between competing strategies. And moreover, these neurons are of the type that sends motor commands from the brain to the 'spinal cord' of the fly. This means that they may be involved not only in the choice, but also in the execution."
"We can now study directly how the brain makes choices between very different defensive behaviors. And because defensive behaviors are common to all animals, our discoveries provide a good starting point towards identifying the 'rules of the game' that define how all animals choose to defend themselves."

Marta A. Moita PhD, Champalimaud Research, Champalimaud Centre for the Unknown, 1400-038, Lisbon, Portugal.

Abstract
The most fundamental choice an animal has to make when it detects a threat is whether to freeze, reducing its chances of being noticed, or to flee to safety. Here we show that Drosophila melanogaster exposed to looming stimuli in a confined arena either freeze or flee. The probability of freezing versus fleeing is modulated by the fly’s walking speed at the time of threat, demonstrating that freeze/flee decisions depend on behavioral state. We describe a pair of descending neurons crucially implicated in freezing. Genetic silencing of DNp09 descending neurons disrupts freezing yet does not prevent fleeing. Optogenetic activation of both DNp09 neurons induces running and freezing in a state-dependent manner. Our findings establish walking speed as a key factor in defensive response choices and reveal a pair of descending neurons as a critical component in the circuitry mediating selection and execution of freezing or fleeing behaviors.

Authors
Ricardo Zacarias, Shigehiro Namiki, Gwyneth M. Card, Maria Luisa Vasconcelos and Marta A. Moita.
The authors declare no competing interests.


Funding
Champalimaud Research, Champalimaud Centre for the Unknown, 1400-038, Lisbon, Portugal
Ricardo Zacarias, Maria Luisa Vasconcelos and Marta A. Moita.

Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, VA 20147, USA
Shigehiro Namiki and Gwyneth M. Card.


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Sep 12, 2018   Fetal Timeline   Maternal Timeline   News   News Archive




How the brain decides what to do in the face of danger? Image credit: Gil Costa.


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