EVER had a feeling come over you that you just can’t explain? Like suddenly getting all warm and fuzzy when you meet someone for the first time, while somebody else who looks just as good leaves you cold? Or experiencing a sudden pang of fear on a plane even though you’re totally at ease with flying?
These seemingly unrelated and illogical human reactions may have a reasonable explanation after all, although one that not everyone will be happy to hear. They may be reactions to other people’s pheromones.
Pheromones are something of a sensitive subject in human biology. Though they are found across the animal world from insects to mammals, research into human pheromones has been dogged by flaky experimental designs and dubious commercial endorsements, with the result that the entire field has a whiff of the disreputable about it. “It’s not so much that the jury is out, but that the jury has been dismissed before the trial has begun,” says Mike Meredith, a neuroscientist at Florida State University in Tallahassee, who studies animal pheromones.
In recent years, though, this has begun to change. Evidence that animal pheromones don’t always work in they way we thought, backed up by a growing number of brain-imaging studies in humans, is convincing some researchers that we really do make and respond to pheromones. As a result some think it’s time to stop asking if human pheromones exist and start investigating exactly how they affect our behaviour.
The term pheromone was coined in 1959 to describe chemicals released by insects to trigger hard-wired behaviours in other members of the same species. The classic example is female moths releasing sex pheromones to attract a mate. When pheromones were discovered in mammals, their more complex behaviour meant this definition no longer fitted the bill. Researchers have been debating the meaning of the word ever since (see “What are pheromones?”) (http://www.newscientist.com/article/mg20026851.800-the-secret-sex-signals-in-human-sweat.html?full=true#bx268518B1). One useful working definition is that pheromones are chemicals which send a message that, in evolutionary terms, benefits both sender and receiver.
Whatever definition you go for, pheromones are a big part of the animal world. Animals use pheromones to transmit useful information about themselves, such as gender or sexual receptiveness; to change others’ physiology, for example by stimulating ovulation; and to directly affect others’ behaviour. Examples of these behaviour-changing or “releaser” pheromones include sexual attractants and the alarm pheromones many mammals - among them rats and deer - use to put others on alert without giving away their location with an alarm call.
For many years, it was assumed that humans did not produce or respond to any of these types of pheromones. In part that was down to a reluctance to admit that humans might respond in such an “animal” way. There is also no clear mechanism for how they might act on the human brain. In animals, pheromones are usually detected by the vomeronasal organ (VNO), a pair of mini-nostrils inside the nose which detect airborne pheromones and relay messages directly to the brain. Although humans have something resembling a VNO, there are no neurons linking it to the brain. And while we have the genes required for a working VNO, they no longer code for functional pheromone receptor proteins (New Scientist, 17 May, p 42) (http://www.newscientist.com/article/mg19826562.100-vestigial-organs-remnants-of-evolution.html). The obvious conclusion was that we had lost this method of communication at some point in our evolution.
That hasn’t stopped researchers from making claims about human pheromones. In 1971 Martha McClintock, a social psychologist at Harvard University, famously reported that women who live together gradually synchronise their menstrual cycles. McClintock, now at the University of Chicago, suggested that this might be mediated by pheromones (Nature, vol 229, p 244 (Menstrual Synchrony and Suppression | Nature)). In 1998, along with her Chicago colleague Kathleen Stern, McClintock found evidence to support this idea, showing that sweat from women in different stages of their menstrual cycle either extended or shortened the cycles of other women (Nature, vol 392, p 177 (Regulation of ovulation by human pheromones | Nature)). Despite this evidence, McClintock’s conclusions remain contentious because nobody has yet isolated the actual chemicals that cause the effect.
Sexy scents
More controversial still are claims that pheromones are involved in human sexual attraction. This is partly due to some high-profile yet scientifically questionable research done by David Berliner and Luis Monti-Bloch of the University of Utah in the mid-1990s. They claimed that when they exposed people to reproductive hormones from the opposite sex, they could see an electrical response from the part of the nose where the vomeronasal organ would be.
In women, cells in this region responded most strongly to extracts containing androstadienone, a hormone related to testosterone found in male sweat. Men reacted similarly to estratetraenol, which is found in female urine. The same team also reported that releasing these compounds into the air subconsciously altered mood, having a calming effect on the opposite sex. The research was widely greeted with scepticism because of Berliner’s financial interest in a brand of perfume called Realm, which was laced with the supposed pheromones. The team’s insistence that the pheromones act through the VNO also raised eyebrows. With no convincing evidence for a functional human VNO, many people dismissed the research outright.
Despite this chequered past, there are still plenty of researchers who insist that human pheromones are alive and well. One is Johan Lundstrom, a neuropsychologist at the Monell Chemical Senses Center in Philadelphia. He has shown that women can consistently sniff out their sisters from friends and strangers even when they are not consciously aware of any difference in odour. A similar effect is our well-known ability to select mates based on genetic signatures evident in their body odour - a subconscious indicator of the compatibility of their immune system.
To Lundstrom, this is convincing evidence that human pheromones are real - it’s just that most researchers have a blind spot when it comes to using the P-word. “If you asked scientists whether one human can convey some sort of social message to another in their body odour, 99.9 per cent of them would say yes,” he says. “If you ask them if humans have pheromones they’ll say ‘that hasn’t been demonstrated’. It’s a semantic issue.”
That may all be about to change, thanks in part to the recent discovery that some animals detect pheromones using their normal olfactory system, not the VNO. “There are several well-established examples of pheromone communication in animals that don’t require the VNO,” says Meredith, who specialises in the animal VNO. For example, a recent study found that mice detect alarm pheromones via a bundle of nerve cells at the tip of their nose that is wired into the normal olfactory system (Science, vol 321, p 1092 (http://dx.doi.org/10.1126/science.1160770)).
Brain-imaging studies have also helped revive the idea that humans may respond to sex pheromones. In a series of recent experiments, neuroscientist Ivanka Savic of the Karolinska Institute in Stockholm, Sweden, exposed people to androstadienone and watched what happened in their anterior hypothalamus, a part of the brain thought to be involved in sexual behaviour.
In one study, published in 2005, Savic found that androstadienone activated that brain region in heterosexual women and homosexual men, but not in heterosexual men or homosexual women. She later found the opposite effect with estratetraenol.
Brain-imaging studies are also providing tantalising evidence that humans release and respond to alarm pheromones. These have been less well studied than those thought to be involved in attraction, but a handful of psychological studies have claimed to show that humans can detect the “scent of fear”. In 1999, Denise Chen, a psychologist now at Rice University in Houston, Texas, asked a group of volunteers to sniff sweat from people who had watched either funny or scary film clips. More than half of the volunteers successfully identified a sample of fearful sweat despite not being able to consciously smell any difference in the samples.
In a similar study in 2002, Kerstin Ackerl from the University of Vienna in Austria reported that women seemed to be able to detect the scent of fear. The 60 women rated sweat from women who had watched a scary movie as stronger, less pleasant and smelling more “like aggression” than sweat from women who had watched a neutral movie (Neuroendocrinology Letters, vol 23, p 79 (http://www.nel.edu/pdf_w/23_2/NEL230202R01_Grammer_rw.pdf)).
Yet these studies used relatively small sample sizes and failed to control for factors such as how strongly different people reacted to the scary movie. They also tended to use questionnaires that asked leading questions about whether the sweat smelled like someone who was happy, angry or scared.
Now, though, a study by Lilianne Mujica-Parodi at Stony Brook University in New York may have eliminated some of these problems by looking directly at what “fear” sweat does to the brain.
In the study, which is yet to be published, the team taped absorbent pads to the armpits of 40 volunteers who were about to do their first ever skydive, to collect their sweat as they hurtled towards the ground. Back in the lab, the team transferred the sweat - plus samples of normal, fear-free sweat - into nebulisers and asked a second group of volunteers to breathe samples while lying in an fMRI scanner, without telling them anything about the nature of the experiment. Sure enough, volunteers showed significantly more activity in the brain’s fear centres, the amygdala and hypothalamus, when breathing fear sweat.
They put pads into skydivers’ armpits to collect sweat as they hurtled towards the ground
It’s not clear whether the volunteers actually felt scared after breathing it in - the researchers didn’t ask them in case this biased the results. But the team say the fact that their fear circuitry lit up in response to the putative pheromone “indicates that there may be a hidden biological component to human social dynamics, in which emotional stress is, quite literally, ‘contagious’”.
Taken together, Savic and Mujica-Parodi’s work adds considerable weight to the idea that humans produce and respond to pheromones. Yet many people feel it is too early to declare a truce in the pheromone war.
Lundstrom says there is still a missing piece of the puzzle. “To my mind, activation of brain is not enough,” he says. “I use brain imaging in my work but I like to see that there is a behavioural response - and to see it consistently. Not just once, but every time.”
To provide this evidence, any human pheromone will need to be identified, synthesised and - crucially - tested to see whether it triggers a reliable behavioural change. Only then will we be able to say definitively that human pheromones exist.
This is a tall order. As Lundstrom points out, human body odour contains more than 2000 different compounds. “Picking one is like putting a blindfold on someone, spinning them around and asking them to hit the centre of a dartboard,” he says.
If human pheromones are identified, however, a whole new debate would open up about how they could be used. Some uses raise more concerns than others. Spraying on some bottled sex appeal may be sneaky in the battlefield of modern dating, but the prospect of synthesising a substance that can induce fear in others is another matter entirely, not least because Mujica-Parodi’s research was funded by DARPA, the US military’s research arm. After seeing the team present their work at a recent conference, one blogger pondered whether the military was planning to use pheromones to send people “stampeding like spooked cattle”. DARPA, however, says it is not aware of any military plans for fear pheromones and has no plans to fund further research in this area.
According to Simon Wessely, a psychiatrist at the King’s Centre for Military Health Research at King’s College London and a health consultant to the British army, the idea is also scientifically implausible. He points to studies done by Stanley Schachter at the Massachusetts Institute of Technology in the 1960s, in which people were injected with adrenalin to create the physical symptoms of fear. These people only became fearful if the situation became threatening, suggesting that context is crucial. “You can generate the physical symptoms of fear but people don’t necessarily get scared,” says Wessely.
Similarly, Lundstrom has found that women only show a reliable response to androstadienone if there is a man in the room at the time of exposure. And since none of the subjects felt compelled to jump on the male in question, it seems fair to assume that in real life any pheromone-induced effects are likely to be small and influenced by other factors (Biological Psychology, vol 70, p 197 (Redirecting)).
As for whether it’s worth investing in pheromone-laced aftershave for that big night out, Lundstrom sounds a note of caution. “Most of these companies are selling andosterone - it’s a pig pheromone that 60 per cent of people can’t smell and the rest think smells like urine,” he says. On balance, it’s probably worth working on some witty conversation instead.
What are pheromones?
A major stumbling block in the debate over human pheromones is the exact meaning of the word. “Pheromone” was coined to refer to a chemical released by insects to trigger a stereotypical response that occurs every time, without fail. This definition is clearly too narrow for humans; even for insects it is proving inadequate, with many insect pheromones needing an additional environmental cue to have their full effect.Another question is whether pheromones operate strictly subconsciously, or whether detectable odours can be classed as pheromones. With tantalising evidence emerging that people respond behaviourally to each other’s body odours - plus research showing that some animals can sense pheromones through the normal olfactory system rather than a specialised organ - that’s an increasingly pressing issue.All this confusion is hampering serious attempts to find out how humans respond to airborne chemicals from each other, so perhaps we need a new term entirely. “Everyone agrees that there is a phenomenon that needs to be explained,” says Johan Lundstrom of the Monell Chemical Senses Center in Philadelphia. “Now we need to agree on what call it.”