Apr. 10, 2001 With only 32 of its 302 nerves dedicated to detecting the odors that drift through its world, the lowly roundworm seems hard pressed to smell food, let alone discriminate friend from foe. But researchers have discovered a unique system of overlapping sensors that enables the creature to tell smells apart.
The system seems well designed for the nerve-challenged worm. In mice and humans, each of millions of odor sensing nerves has only one type of odor detecting receptor, allowing the brain to distinguish between odors by tracking which nerve did the sensing. But in a compromise between the need to detect many odors and the scarcity of available nerves, the roundworm's odor sensing neurons are studded with receptors for different odors. It has been a biological puzzle how a nerve that senses many odors can distinguish between them.
Scientists at the University of California, San Francisco uncovered a clever combination strategy in the worm's odor sensing nerves. Paired nerves, they found, have receptors tuned to some of the same odors, yet each member of the pair also supports receptors tuned to unique odors not detected by the partner.
With this partially overlapping detection system, the nerve pairs can sense more odors than would be possible if they had identical receptors or even if each were tuned to completely different smells, the scientists found. More importantly, the combinatorial approach allows the nerve pairs to discriminate between different odors, a lifesaving trait if the worm has to find one source of food in a bewildering array of aromas.
"The worm can solve amazingly complex sensory problems with few olfactory nerves," said senior investigator of the study, Cornelia I. Bargmann, PhD, an investigator in the Howard Hughes Medical Institute and professor and vice chair of anatomy at UCSF.
"Each nerve cell has a private window into the world of smells and a shared window with its partner. Any one nerve cell can get confused, but by comparing the private and shared information, the animal sorts out and distinguishes all possible combinations of odors."
The combinatorial approach may be unique to this simple creature, Bargmann suggests, or it may be a clue to how higher organisms including humans solve the same problem: how a sensory system or another part of the brain can process a nearly limitless number of environmental cues with a finite number of nerves.
"We want to understand the relationship between genes, cells and behavior in the brain," she said, "but our own brains are complex beyond belief. In this fairly simple animal, we can decode the 'thinking strategy' used by every cell in the brain."
The research is published in the April 5 issue of Nature. Lead author is Paul D. Wes, PhD, a post-doctoral scientist in Bargmann's laboratory. (In a parallel paper in the same issue, a research group in Oregon found similar results in the worm's taste center, a system that is organized much like the taste system in humans.)
The worm in question is C. elegans, or more elegantly, Caenorhabditis elegans, a millimeter-long soil dweller widely studied by geneticists and developmental biologists because it displays many developmental processes and instinctive behaviors common to higher organisms. The worm is tiny and transparent, with a very small brain that can be studied in detail.
The key odors of interest in the UCSF study were benzaldehyde, which gives off a scent somewhat like almond, and butanone which has an oily smell. Both are thought to be produced by bacteria, the worm's food, but both can also be pervasive smells without useful information. Under those circumstances a sensible worm ought to ignore them, Bargmann said.
The scientists assayed a worm's ability to distinguish between the two odors by exposing it to a high concentration of butanone and then testing its ability to be attracted to benzaldehyde in this odor environment.
They examined the odor sensing abilities of a pair of olfactory neurons, known as AWC, which has been the focus of the Bargmann lab for ten years. Her research group has determined that this nerve pair not only senses at least five attractive odors, but can also distinguish between the odors.
The lab recently discovered that the two neurons, which had been thought to be identical left-right members of a pair, actually differ in one subtle, but critical respect. During the development of the nerves, an odor receptor known as STR-2 becomes active on one of the nerves but not on the other. Whether the receptor is expressed on the left or the right nerve is apparently random, they found.
Bargmann and Wes used standard techniques to search among mutant worms for those that were unable to detect the difference between benzaldehyde and butanone and then showed that these genetic mutants, known as ky542, possess an active STR-2 receptor on both members of the AWC neuron pair, unlike normal worms.
They further showed that they could induce this odor discrimination deficit in normal worms by killing one of the paired AWC cells with a laser beam. Either the mutant worms or the operated worms could sense both odors perfectly well, but with a change in one of the AWC neurons, discrimination was lost. The difference between detection and discrimination is the first step in higher processing in the senses, Bargmann said, and the experiment showed where that step occurs.
Only one of the paired AWC nerves, the one that expresses STR-2, responds to butanone, the scientists found, while both this neuron and its STR-2-silent partner can detect benzaldehyde. The nerve with the silenced STR-2 is required for discrimination between butanone and benzaldehyde, because it can smell benzaldehyde without sensing the confusing butanone odor. In turn, that silenced nerve senses a third odor, a buttery smell, that its partner can't detect. So, each nerve cell can recognize smells that are either buttery or oily but not both, and they both recognize almond-like smells. By comparing the private and shared information, the animal can detect more odors than if each of the paired nerves sensed entirely different smells.
The research is funded by the Howard Hughes Medical Institute and the National Institutes of Health.
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