Smells shape our moods, behaviour and decisions, so why do they barely register in our conscious lives?
I TRY to forget about potential onlookers as I crawl around a central London park, blindfolded and on all fours. With a bit of luck, the casual passer-by might not notice the blindfold and think I'm just looking for a contact lens.
In fact, I'm putting my sense of smell to the test, and attempting to emulate the sensory skills of a sniffer dog. Just as a beagle can swiftly hunt down a pheasant using only its nasal organ, I am using mine to follow a 10-metre trail of cinnamon oil.
Such a challenge might sound doomed to failure. After all, dog noses are renowned for their sensitivity to smells, while human noses are poor by comparison. Yet that might be a misconception. According to a spate of recent studies, our noses are in fact exquisitely sensitive instruments that guide our everyday life to a surprising extent. Subtle smells can change your mood, behaviour and the choices you make, often without you even realising it. Our own scents, meanwhile, flag up emotional states such as fear or sadness to those around us. The big mystery is why we aren't aware of our nasal activity for more of the time.
Noses have certainly never been at the forefront of sensory research, and were pushed aside until recently in favour of the seemingly more vital senses of vision and hearing. "There has been a lot of prejudice that people are not that influenced by olfactory stimuli, especially compared to other mammals," says Lilianne Mujica-Parodi, who studies the neurobiology of human stress at Stony Brook University in New York.
One of the first people to assert the relative unimportance of human smelling was Pierre Paul Broca, an influential 19th-century anatomist. After comparing the proportion of the brain devoted to smell in different animals, he suggested that mammals can be classed into two broad groups: macrosmatic mammals, such as dogs, have a finely tuned sense of smell which they rely on to perceive the world, while we, along with other primates and the marine mammals, are microsmatic - we have a small and functionally redundant olfactory apparatus.
That idea seemed to fit with more recent studies in genetics, which found that the majority of mammals have genes coding for about 1000 different types of smell receptor. Most of these genes aren't expressed in humans, giving our noses just 400 different types of receptor (see chart).
Yet these findings may have been misleading. Brain scans now show that more of the brain is devoted to smell processing than Broca's anatomical studies would have suggested. And although we may have fewer types of receptor than other mammals, Charles Greer at Yale University has shown that the human nose and brain are unusually well connected, with each group of receptors linking to many more neural regions than is the case in other animals. That should give us a good ability to process incoming scents.
Once researchers began looking, they found the nose to be far more sensitive than its reputation suggested. One study, for example, found that we can detect certain chemicals diluted in water to less than one part per billion. That means that a person can detect just a few drops of a strong odorant like ethyl mercaptan in an Olympic-sized pool.
We are also exceptionally gifted at telling smells apart, even distinguishing between two molecules whose only difference is that their structures are mirror images of one another (Chemical Senses, vol 24, p 161). "That is fantastic sensitivity," says George Dodd, a perfumer and researcher at the olfaction group of the University of Warwick, UK.
What's more, it is becoming clear that the brain's olfactory centres are intimately linked to its limbic system, which is involved in emotion, fear and memory. That suggests a link between smell and the way we think.
The power of smell will be no news to estate agents, who often advocate the smell of baking bread or brewing coffee to promote the sale of a house. But there are more subtle and surprising effects too. For instance, when Hendrick Schifferstein from Delft University of Technology and colleagues pumped the smell of orange, seawater or peppermint into a nightclub, the revellers partied harder - they danced more, rated their night as more enjoyable, and even thought the music was better - than when there was no added scent (Chemosensory Perception, vol 4, p 55). Rob Holland and colleagues at the University of Utrecht in the Netherlands, meanwhile, have found that the hint of aroma wafting out of a hidden bucket of citrus-scented cleaner was enough to persuade students to clean up after themselves - even though the vast majority of them hadn't actually registered the smell (Psychological Science, vol 16, p 689).
Other work has found that scent can influence our cognitive skills. A study this year by William Overman and colleagues at the University of North Carolina Wilmington found that when men were subjected to a novel smell - either good or bad - during a gambling task used to test decision-making skills, they performed significantly worse than normal. The researchers conclude the scent stimulated brain areas connected with emotion, making their decisions emotional rather than rational (Behavioral Brain Research, vol 218, p 64). Smells also seem to direct our visual attention, and they may play a key role in consolidating memories too(see "Blast from the past").
Our sense of smell may even help us to pick up on the emotional state of those around us. This idea has been highly controversial, but work by Mujica-Parodi suggests we can sense another's fear from their sweat. At the time, she was working on a way to assess a person's vulnerability to stress, and needed a reliable way to scare her subjects, without socially loaded words or pictures that might mean different things to different people. That's hard to do, says Mujica-Parodi: "You can't mug somebody in a scanner."
The answer came from nature. Rats are known to be able to smell each other's fear, leading them to "freak out" if placed in an empty cage in which another rat has just seen a predator. Mujica-Parodi figured humans might do the same thing. To test the idea, her team took sweat samples from people doing a skydive for the first time. When they presented the samples to unrelated subjects in an fMRI scanner, they saw activation of the amygdala - the brain area that normally lights up in studies of emotion. This did not happen when sweat samples came from the same skydivers pounding a treadmill.
Mujica-Parodi's team next tested whether the smell of fear sweat affected people's responses to various facial expressions - angry, ambiguous or neutral. Normally, we would pay more attention to angry faces, because they pose a threat, but after smelling the fear sweat, the participants gave all three types the same attention (Social Cognitive and Affective Neuroscience, in press, DOI: 10.1093/scan/nsq097). "It forced the brain to pay attention to things that otherwise it wouldn't consider worth its time," Mujica-Parodi says.
The smell of fear may be just one of many olfactory signals emitted by the human body. Another study this year, by Yaara Yeshurun at the Weizmann Institute in Rehovot, Israel, and her team found that the imperceptible smell of women's tears decreases sexual arousal in men (Science, vol 331, p 226). "It's a way of giving power to females, to make men less attracted to them," she says. The role of scent, or pheromones, in sexual attraction remains controversial, however.
The surprising thing about these studies is that few of the subjects were aware of the smells that they were facing, yet their behaviour was altered nevertheless. The question, then, is why we pay so little conscious attention to our noses unless we get a whiff of something truly pungent?
Lee Sela and Noam Sobel, also at the Weizmann Institute, blame our obliviousness on two factors. Firstly, they point out that our noses just aren't equipped to locate the source of an odour. This makes the sense of smell fundamentally different to vision or hearing, which are built to pinpoint sights and sounds and turn them into a mental map. According to one leading theory of consciousness, we become aware of something when the brain's "attentional spotlight" focuses on a single location, after which it picks out the fine details, like a familiar face, from the scene. With such a poor map of smells, the spotlight can't shine on any particular part of the smellscape and make us aware of the details, say Sela and Sobel. It's for this reason that we can only ever pick out around four smells from a complex mixture, they say.
The other reason centres on a phenomenon called change blindness, which was first found to influence our vision. In 1999, Kevin O'Regan from the Laboratory for the Psychology of Perception in Paris, France, and colleagues found that people can miss even large changes to a visual scene when those changes are accompanied by an interruption, such as a camera cutting to a different viewpoint in a film (Nature, vol 398, p 34). They argued that the cut provides a fleeting distraction which means the change goes unnoticed. Since then, change blindness has been demonstrated in hearing and in touch.
Sela and Sobel think that smell could be next on the list. They point out that our sniffs are full of gaps as we breathe in and out, which could make it difficult for us to notice new odours wafting around - even if we do react to them subconsciously (Experimental Brain Research, vol 205, p 13).
It's an interesting idea, says O'Regan, but he's not yet convinced. In particular, he is critical of the suggestion that sniffing more quickly would dissipate the effect. "Even if you were going to sniff very quickly you would still have a break between each sniff." In visual change blindness, even the subtlest of cuts can mask large changes, he says.
There are other ways that we can improve our noses, though. "We all have the capacity to train our sense of smell," says Dodd, "but you have to work at it." Master perfumers, for instance, learn to recognise, name and imagine an extraordinary range of smells through years of training. This is accompanied by a significant reorganisation of the olfactory areas that helps them to process the scents more efficiently (Human Brain Mapping, in press, DOI: 10.1002/hbm.21207).
Jess Porter and colleagues at the University of California, Berkeley, have also been trying to train people's noses. They persuaded 32 students to wear blindfolds and ear defenders, and get down on all fours to see whether they could sniff out a trail of chocolate oil.Intrigued, I wanted to try it for myself, which is how I ended up on all fours in a London park.
My first attempt didn't go well - there seemed to be so many smells competing for my attention, including damp soil, grass and cigarette butts. But, like the majority of the participants in Porter's experiment, I did manage to follow the trail to the end on the subsequent attempts, even when it deviated off a straight path. For Porter's volunteers, repeated practice over three days brought greater accuracy and speed.
Of course you don't have to crawl on the grass to train your nose. Any attempt to consciously pay attention to what your nose is telling you should have some benefit. And even if you choose to ignore it entirely, there's no getting away from the fact that, behind the scenes, your nose is working overtime to make you who you are. That's one discovery that's not to be sniffed at.
Blast from the past
Smells are especially good memory evokers, but it's actually a myth that odours trigger more detailed memories than other stimuli. "The memory is not more accurate and you don't remember more details," says Yaara Yeshurun at the Weizmann Instititute of Science in Rehovot, Israel, "but it is unique in that it is more emotional." This isn't surprising when you consider that there are certain brain areas dedicated to both emotion and olfaction, such as the amygdala, and there is a strong link between emotion and memory.
That said, not all smell memories are created equal. In 2009, Yeshurun found that the link between a memory and a smell is stronger if the smell is an unpleasant rather than a pleasant one, which makes sense from an evolutionary perspective. She also discovered that the very first time we associate a smell with an object, it evokes a much greater response in our brains than for any subsequent encounter with the smell or object, laying down stronger foundations for the memory. That doesn't happen with any other sense. Since those first encounters with a smell would have happened at a young age, this might explain why smells often transport us back to our childhood.
Lost and found
Molly Birnbaum only realised the extent of her injuries from a car accident when she was at a family gathering a few weeks later. Her stepmother had baked an apple crumble. "It wasn't until she held it under my nose and I breathed in that I realised I could not smell a thing." Her doctors believe the impact she experienced must have disconnected the nerves between her nose and brain.
Without smell, Birnbaum knew her dreams of becoming a chef were over. What soon became clear, however, was that the loss also dulled her overall perception of the world. "It was as if the texture of my environment was wiped smooth," she says.
There was some hope for the future, however, since nerves can sometimes regenerate. To help them, she began by smelling spices from her cupboard for 10 minutes a day, before setting off on a more serious quest, picking up tips from some of the world's top perfumers and chefs. Slowly but surely, the nerves grew back and her sense of smell returned. In doing so, she experienced the strong link between smell and mood - during bouts of depression, she struggled to smell, but in happier times smells came back.
"Smell is one of the more important ways of understanding the world around us," she says. "It's just unfortunate that sometimes you have to lose something to understand how important it is."
Catherine de Lange is a freelance journalist based in London