In this larval fly nervous system, major structures are stained red and neurons expressing a specific neuropeptide are stained green. In the mammalian brain, many neuropeptides are produced in the hypothalamus to play a role in the control of emotional behaviors. Of the approximately 100,000 neurons in the fly's nervous system, only about 10 express this neuropeptide, suggesting that they have a very specific function.

Researchers can alter flies genetically, however, and use various imaging techniques and special microscopes to see which brain cells fluoresce or react in response to different stimuli or during various activities. Such processes, Anderson says, are not only informative but downright thrilling. “It's like flying over a city at night and watching the lights of the houses go on and off.”

But, he cautions, “Just because there is a correlation between neurons and an activity doesn't mean those neurons alone are responsible for the behavior. To test that hypothesis, you have to turn off the neurons, and see if the behavior goes away.” Using one such genetic technique, Anderson, with a team including Axel and Benzer, was able to engineer temperature-sensitive neurons that shut down at 90°F. In a series of experiments that pivoted around this temperature sensitivity, they discovered that “traumatized” fruit flies emit a stress odor containing carbon dioxide, repelling other flies, and that a single type of neuron in the nose of the fly is responsible for detecting the noxious gas.

Were the normal flies reacting to a “smell of fear”? Maybe, and maybe not, says Anderson. What he learned in additional experiments—that the target olfactory neuron is both activated by carbon dioxide and necessary for the response to carbon dioxide—still did not prove what actually triggered the avoidance behavior. So in a clever case of genetic manipulation, Anderson added a bit of algae DNA to the fruit fly's carbon-dioxide-sensitive neurons: specifically, an ion-channel gene that is activated by blue light.

The next step was to put these altered flies into an apparatus and give them a choice between flying into an empty tube or one illuminated with blue light. “We wanted to know if flies exposed to this light would think they smelled carbon dioxide and act to avoid it,” Anderson explains. Sure enough, when he flicked on the switch, the altered flies shunned the blue light, proving the primary link between neuronal activity and behavior.

In comparable research with mice, Anderson has also narrowed the search for genes that control whether a stressed mouse freezes or flees when hearing the mouse version of an alarm bell. But be they fruit flies or mice, is their behavior emotional behavior, and if so, so what?

Photo: Anne Hergarden and Timothy Tayler

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