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Uncovering The Mysteries Of Smell
November 8, 2018

“A rose by any other name would smell as sweet,” says Juliet in William Shakesphere’s romantic play, Romeo and Juliet. But what is a smell actually? How does a sensory input becomes an experience? For example, how do molecules released by a blooming flower become the internal experience of smelling a rose?

Barani Raman. Credit: Washington University.

One approach to better understand the process is to understand the physical brain processes behind sensory experiences. Scientists have proposed different ways to describe what is happening by suggesting that a certain set of neurons must fire; a certain sequence of firing that must occur; or a combination of the two.

But according to information provided by the School of Engineering & Applied Science at Washington University in St. Louis, a research team has advanced the idea that these descriptions do not account for the variability of the real world. Because smells do not occur in a vacuum, the researchers wanted to find out what happens when sensory input was presented in sequences, more akin to what happens in the real world.

In a paper published in the journal Nature Communications, the researchers discovered that in locusts, only a subset of neurons associated with a particular scent would fire when that scent was presented in a dynamic environment that included other scents. Although there was not a one-to-one relationship between a pattern of neurons activated and a specific smell, the researchers were able to determine how the locusts could still recognize a scent; it comes down to the locust being flexible in its interpretation.

“There is variability because of stimulus history,” explained Barani Raman, associate professor of biomedical engineering, “so flexibility is necessary to compensate.”

With funding for their research provided by the Office of Naval Research and the National Science Foundation, the team of Washington University engineers first had to train the locusts in the much same way as Pavlov trained dogs. A machine administered a puff of the target scent, hexanol, to hungry locusts, then rewarded the locusts with a treat: grass. After enough rounds (usually six), the locusts would open up palps — small organs outside of their mouths that function in a similar way to lips or tongues in humans — after they smelled hexanol, in anticipation of the grass.

Once the locusts were trained, the testing began. The locusts were exposed to the “target” odor, hexanol either on its own, or after the introduction of a different scent, called a “distractor.”

Each time the target odor was introduced on its own, a locust’s neural activity was the same. But when the locusts were exposed to a distractor smell first, different combinations of neurons fired when the locusts were subsequently exposed to the target.

This is the variability based on context. What has been previously smelled (and even unrelated brain states, such as hunger) can affect how a brain reacts to the same input. If that were the end of it, though, smells would rarely, if ever, be recognizable.

However, the locusts recognized the target — even though their neurons were firing in a variety of different ways — as evidenced by their palps, which opened as per their conditioning.

So there had to be more to the story than variability when it came to recognizing smells. The team wanted to know if there was a pattern, or a way to discern, via brain activity, how the locusts were smelling the target odorant despite the variability in brain activity.

“The rules are very simple,” Prof. Raman said. “An ‘or-of-ands’ logical operation was sufficient to compensate for variability and allow flexible decoding.”

According to the research results, the locusts show a fixed pattern of brain activity when smelling the target odorant alone, but only some flexible combination involving just some of those same neurons will fire when smelling the target after smelling a distractor, such as fruit.

What subset of neurons that fire depends, in large part, on what the distractor smell is; the neurons that are activated by the target alone will continue to fire, but those that are in common to both the distractor and the target will either not be activated or their activity will be reduced.

Going forward, the team plans to see if its results hold in another organism: the fruit fly. The researchers also will investigate how other sources of variability such as short-term memory might affect how smells are perceived.

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