Student volunteers presented with odors to one nostril or the other could reliably discern where the odor was coming from, and functional magnetic resonance images of their brains showed that the brain is set up to pay attention to the difference between what the left and right nostrils sense, much the way it can localize sounds by contrasting input from the ears.
"It has been very controversial whether humans can do egocentric localization, that is, keep their head motionless and say where the spatial source of an odor is," said study coauthor Noam Sobel, associate professor of psychology at UC Berkeley and a member of the campus's Helen Wills Neuroscience Institute. "It seems that we have this ability and that, with practice, you could become really good at it."
In future experiments, UC Berkeley biophysics graduate student Jess Porter and Sobel plan to train volunteers to track odors in the field and test the limits of odor localization in humans.
Porter, Sobel and their colleagues reported the results in the August 18 issue of the journal Neuron.
In a review appearing in the same issue of the journal, Jay A. Gottfried of the Department of Neurology at Northwestern University's Feinberg School of Medicine noted that the UC Berkeley findings open numerous avenues for further research. "Finally, what are the implications for the Provençal truffle hunt?" he wrote, only partly tongue-in-cheek. "In the traditional world of the truffle forests, the dog (or pig) is king. The evidence presented here suggests that humans are every bit as well equipped to carry out the search."
Forty years ago, Nobel Prize laureate Georg von Békésy claimed that humans had the ability to localize odors, based on experiments in 1964 with human subjects. He suggested this was done the same way we locate sounds: by contrasting either the intensity of the odor or the time of arrival.
Since then, however, scientists have had difficulty replicating his experiments, according to Sobel. One explanation for this failure was that von Békésy used chemicals that stimulate not only the olfactory nerve in the nose, but also a nasal sensory nerve, the trigeminal nerve. Most odors stimulate both, and some, like onions and ammonia, are stinging enough to bring tears to the eyes. Perhaps, some suggested, von Békésy's subjects were localizing odors based on trigeminal nerve stimulation, not olfactory nerve stimulation.
To eliminate this confusion, Porter and Sobel used two odors with minimal trigeminal stimulation - essence of rose (phenyl ethyl alcohol) and cloves (eugenol) - as well as two trigeminal odorants - propionic acid, which smells like vinegar, and amyl acetate, which smells like banana. They delivered the odors through a specially designed mask with an artificial septum that provided separate air flow to each nostril.
In addition, they conducted similar experiments on five volunteers who had no olfactory nerves and therefore couldn't smell at all, a condition known as anosmia.
Normal subjects, 16 in all, were able to tell which nostril was receiving a squirt of scent, but anosmic volunteers could only localize the trigeminal odorants, Sobel said. This shows that humans are able to localize odors through the olfactory nerves alone.
"One possible objection is that the experimental set-up, with a mask that provides separate air flow to each nostril, is artificial. How behaviorally relevant is that?" said Porter. Subsequent experiments not yet reported, however, provide additional support for their hypothesis that the ability to localize odors to one nostril or the other is realistic.
The experiments were conducted with the subjects' heads inside a functional MRI to allow the scientists to see which areas of the brain were most active during sniffing and attempts to identify and localize odors. They found that the left and right nostrils have separate areas of the primary olfactory cortex - the brain's smell center - devoted to them, indicating that the brain at least encodes information that could help it localize an odor. A successful detection of an odor is accompanied by more activity in the region of the olfactory cortex associated with the particular nostril.
"While a subject was doing this task, I could look at the brain and tell you how accurate he or she would be on every trial and on the task overall," Sobel said. "So the fact that we have this predictive value in the data really suggests that we have actually successfully captured the mechanism."
What's more, another area of the brain outside the olfactory cortex was very active during successful localization. This area, the superior temporal gyrus, is also involved in the localization of sounds and visual objects, Sobel said.
"It's actually a very nice and elegant convergence of this area, the superior temporal gyrus, that appears to transform non-spatial information into spatial information," he said. "Together, these results are the first description of the mammalian brain mechanisms for extracting spatial information from smell."
One key difference between their experiment and previous experiments to replicate the results of von Békésy is that Porter and Sobel asked their subjects to actively sniff, whereas many previous experiments prevented subjects from sniffing.
"We think that most people failed to replicate his results for that reason, that is, the extent to which they enabled natural behavior, specifically sniffing," Sobel said. "In some studies subjects asked to localize an odor wouldn't be allowed to sniff. That's almost like studying auditory localization but having your ears plugged. We actually enabled natural behavior, we enabled subjects to sniff, and we think that's a major difference."
In addition to Porter and Sobel, other authors of the Neuron paper were UC Berkeley senior scientist Rehan M. Khan of the Department of Psychology and graduate students Tarini Anand and Brad Johnson of the Department of Bioengineering. The work was supported by grants from the National Institutes of Health.