Humans have a stereo sense of smell that subconsciously guides navigation

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“If in doubt, always follow your nose,” said Gandalf in “The Lord of the Rings.” Despite Gandalf’s advice, humans tend to regard themselves as “microsmatic” – having a poor sense of smell.

Human navigation is thought to rely primarily on vision and audition.

Specifically, subtle differences between the inputs to the paired eyes and ears are exploited by the brain to construct three-dimensional experiences that guide navigation.

Although humans also have two separate nasal passages that simultaneously sample from nonoverlapping regions in space, it is widely held that inter-nostril differences in odor concentration do not provide directional information in humans unless that odor also stimulates the trigeminal nerve (i.e., elicits hot, cold, spicy, tingling, or electric feelings), in which case it is really the trigeminal system that generates a directional cue.

However, a new study conducted by graduate student Wu Yuli and his colleagues at the Institute of Psychology of the Chinese Academy of Sciences argues otherwise.

Wu and his colleagues introduced various levels of binaral concentration disparity to a heading judgment paradigm based on optic flow – a unique type of visual stimulus that captures the pattern of apparent motion of surface elements in a visual scene and induces the illusory feeling of self-movement in stationary observers.

The odorants they used were phenylethyl alcohol and vanillin, which smell like rose and vanilla, respectively, and are known to activate only the olfactory nerve.

Results from stringent psychophysical testing in four experiments involving a total of 180 participants consistently showed that a moderate binaral disparity biases recipients’ perceived direction of self-motion toward the higher-concentration side in manners reminiscent of stereo vision (i.e., binocular stereopsis), despite not being able to verbalize which nostril smells a stronger odor.

In addition, the effect depends on the inter-nostril ratio of odor concentrations as opposed to the numeric difference in concentration between the two nostrils.

“Our work presents clear behavioral evidence that humans have a stereo sense of smell that subconsciously guides navigation,” said Dr. Zhou Wen, senior author of the study.

“The findings underscore the multisensory nature of heading perception and could provide guidance for the design and development of olfactory virtual-reality systems for humans.”

The study, titled “Humans navigate with stereo olfaction,” was published online on PNAS on June 22.


There are two very different ways to use odors to orient in space. The first is odor tracking, where an animal tracks an odor to its source. This behavior has been demonstrated in walking, flying and swimming invertebrate species [1–3] as well as walking, flying and swimming vertebrates [4–6].

Even blindfolded humans can crawl and track an odor across grass, and their accuracy in tracking decreases if they are deprived of bilateral nostril input [7]. Orienting more accurately with stereo-olfaction is evidence that an animal is using odors to compute the direction to the source [8–10]. Blindfolded humans can also localize an odor’s source by sampling from a central, sitting location [11].

The second way to use odors is to detect the statistical regularities of airborne odors distributed above a landscape and to use this information to define a terrestrial location. This behavior is much less well understood in humans or any other species, although there are many anecdotes of such mapping from sailors, hunters, and early aviators [12].

The idea of atmospheric odors providing stable spatial landmarks was first proposed for the homing pigeon by Floriano Papi in the 1970’s, conceptualized as a mosaic of odor patches [13].

Later, Wallraff proposed that pigeons could also orient to odor gradients organized in a coordinate system. He has since shown, using data from the sampling of atmospheric odors and computational models, that such stable odor gradients could exist and provide sufficient information to explain the navigational accuracy seen in pigeons [14–17].

Strong evidence for olfactory navigation in homing pigeons continues to accumulate, and has accelerated with the invention of global positioning systems [18]. The neural basis for olfactory navigation in pigeons has also been identified; the olfactory bulb and hippocampus are key brain substrates for navigation, both in pigeons and mammals [19,20].

Despite the obvious structural and functional connections between the hippocampus and the olfactory system in mammals [21], studies of hippocampal function, even in rodents, use odors only as identifiers of objects, i.e., as an associative cue [22].

What is rarely manipulated is the use of an extended gradient of odors as an orientation cue, though there are exceptions [23–25]. Odors in rodent studies are thus mostly used in two ways: as a unique feature of a location or object and as a rodent’s orientation to naturally deposited odors—either volitional scent marks or passive odor trails created by the animal’s feet on the apparatus surface.

It is unclear whether any study of rodents has required them to navigate to a diffuse odor landscape. However, recently Zhang and Manahan-Vaughn have shown that hippocampal place cells in the rat can be controlled by the position of odors emanating from the four corners of a rectangular space.

These hippocampal place fields then rotated when the odors were rotated, and remapped when the odor array was jumbled [26]. This suggests that the rats may have been orienting to a grid formed from the experimental odors.

Because the bird and the mammalian hippocampus are homologous and because both mediate spatial navigation [19], it seems likely that the hippocampus in both groups could be encoding odors as a multi-coordinate bearing map, as originally proposed in the parallel map theory of hippocampal function.

In this hypothesis, the cognitive map is unpacked into two maps, one ancestral to all vertebrates (the bearing map) and one map more recently evolved (the sketch map), and which is found only in mammals and birds.

The bearing map is proposed as a low resolution grid map, built from extended stimuli such as gradients; the sketch maps are high resolution topological maps that represent arrays of local landmarks.

The two maps can be used independently for orientation but must be combined into a single map (the integrated map) for complex navigational problems [27].

We have recently proposed that certain characteristics of the vertebrate main olfactory system, such as the allometry of the olfactory bulb relative to brain size and the psychophysics of odor mixture perception, suggest that many vertebrates, not just birds, map locations in space using odor gradients [21].

If such navigation is a key function of olfaction, then the ability to encode an arbitrary location as a position on a bearing map constructed from odor gradients should therefore be widespread among vertebrates.

One reason that this hypothesis has not been tested, and no doubt an underlying reason for the continuing controversy on this subject [17,28], is the difficulty of measuring and manipulating the distribution of odors, particularly those in the atmosphere.

For this reason there is currently no direct evidence that a bird, or indeed any species, can map an arbitrary location in the atmosphere, using the coordinates defined by an olfactory bearing or grid map.

Because we predicted that this ability should be widespread in animals, we designed the current study to test this basic assumption of olfactory navigation not in a flying bird but in a terrestrial mammal. Employing a spatial match-to-sample design, we tested this prediction in humans.

Conclusion
The ability to navigate accurately is critical to survival for most species. Perhaps for this reason, it is a general property of navigation that locations are encoded redundantly, using multiple orientation mechanisms, often from multiple sensory systems [33,34].

Encoding the location with independent systems is also necessary to correct and calibrate the accuracy of any one system [35]. As a general principle, then, navigational accuracy and robustness should increase with the number of unique properties exhibited by redundant orientation systems.

Olfaction is perhaps the most universal of these redundant sensory systems, critical for navigation across animal species, even in birds [21]. The use of olfaction in navigation by humans, however, has not been studied in any detail, for at least two reasons.

First, it is generally assumed that humans—with so few functional olfactory receptor genes compared, for example, with the laboratory mouse or domestic dog—have a poor sense of smell. Yet olfaction plays a fundamental role in human cognition, where its importance for emotion, memory, and social cognition have been well studied [36,37].

And even though primates, such as humans or squirrel monkeys, have fewer olfactory receptor genes than rodents or dogs, their odor sensitivity can equal or surpass the performance seen in these other species [38].

In addition to sensitivity and despite their relative paucity of olfactory receptor genes, humans can discriminate over one trillion olfactory stimuli, significantly more than the number that can be discriminated by their visual or auditory systems [39].

As Gordon Shepherd suggests, primates, including humans, may accomplish sophisticated olfactory cognitive processing not at the periphery but in central processing, just as the complexity of human language is not limited by the auditory system but by higher order processes using auditory inputs [40].

Despite these advances in human olfactory cognition, it is still assumed that human olfaction functions primarily for discrimination of proximate stimuli, as a “near” sense, and plays little role in spatial orientation to distant stimuli, compared with vision and audition [41].

Yet olfaction offers unique properties for navigation, simultaneously encoding odor mixtures digitally, as unique “odor objects”, and as analog representations of odor gradients stretching across a landscape. These dual properties make olfaction an ideal sensory modality for navigation [21]. Perhaps for this reason, the use of chemical stimuli in spatial orientation is nearly universal among animals [42].

This last observation makes it even more surprising that so little is known about the mechanisms humans might use to orient to odors in space, despite anecdotal reports of sailors and early aviators navigating across land and seascapes using odor gradients [12,43].

Instead, there are only reports that humans can track odors [7] and that the visually impaired use odors to recognize locations [44]. Until now there has been no empirical evidence that humans can map an arbitrary location using only odors, an ability we have established in the present study.

This evidence, however, is not a demonstration of true navigation but rather a demonstration that humans can use this sensory modality to map and reorient to a learned location.

The recognition of such ability is the first step in the empirical study of human olfactory navigation, just as other orientation mechanisms, such as echolocation in microchiropteran bats or orientation to magnetic fields in sea turtles, were first demonstrated on a small scale under controlled conditions in the lab [45].

Once a novel orientation mechanism has been identified, it can then be studied under natural conditions where its employment may have a significant effect on survival. In the field, the utility of a sensory modality, and hence the weighting of the information derived from it, may be greater than in a laboratory setting [19].

Whether the role of olfaction in human navigation would be more important in a small interior space, as in the present study, or whether this advantage would be significantly magnified under more challenging conditions for orientation, such as in the field, awaits future research.

In conclusion, that humans can, with a single one-minute sampling, identify a location by its unique odor mixture and later return to that location with only the olfactory information to inform their subsequent orientation, is a surprising result.

It is surprising in part because we assume that humans have a poor sense of smell. It is also surprising because we assume that even if humans had a good sense of smell, they would not be using it for navigation but rather for the discrimination and identification of odors. Y

et because so many animals do use olfaction in navigation, perhaps it would be more surprising to find that humans do not. For whatever reason, it is clear that human olfactory navigation has been insufficiently studied.

If humans, a species specialized for long-distance walking [46], can employ olfaction in navigation, our results suggest that comparative studies of olfactory navigation across different kinds of vertebrates, whether flying or walking species, could have a rich future.

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Chinese Academy of Science

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