WHEN four male experimental subjects were found peeking at explicit images of naked female bottoms on laboratory computer screens, you might have expected disciplinary action, a review of internet security, or at the very least a new batch of subjects. Not in this case. Instead, Michael Platt and his colleagues at Duke University, North Carolina, actually encouraged the voyeurs to keep looking. They set up a pay-per-view system and even tried bribing them to look at less desirable images, all the while monitoring their sleazy viewing habits in the name of science.
It won’t help to know that those bared rumps belonged to female macaque monkeys. Don’t jump to hasty conclusions, though, because the male subjects mesmerised by these images were macaques too. What’s more, the payments and bribes associated with these slide shows of simian smut were not financial, but rewards or forfeiture of fruit juices depending on what they chose to view.
You’ll also be relieved to hear that there is a serious point to the project. Primate soft porn may just help solve one of the central questions about how our brains work – how, faced with all the choices we have to make every second of every day, we weigh up the options and convert disparate information about them into a common neurobiological currency. The research could even unravel some of the mysteries of autism. Honest!
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It began in the mid-1990s, when Platt and his colleague Paul Glimcher, then both at New York University, decided to study how we make decisions. “Neurobiologists were just starting to scratch the surface of trying to understand decision-making,” says Platt. They knew a lot about how we collect relevant information with our senses, and how we direct our actions, but almost nothing about how we link the two processes in the brain; how we evaluate the options we see and make informed choices about how to act.
Platt and Glimcher reasoned that an efficient brain ought to weigh up all possible choices as if they were part of a mathematical or economic equation, and that two key pieces of information would be vital: an estimate of the reward at stake and the probability of achieving it – or not – by acting a certain way. In theory, by combining the two, and doing the same for all the alternatives, the brain could compare them and then select the best-value option on offer. Is this what actually happens, though?
“We need to weigh up the reward at stake and the probability of achieving it by acting a certain way”
In an attempt to find out, the researchers began an experiment that involved rewarding monkeys with squirts of juice for moving their eyes towards one spot or another. They could vary the size of the reward associated with each position, and the probability that the monkey would receive it. Sure enough, both factors affected where the monkeys preferred to look, and their brains told a similar story. Recordings from electrodes revealed that the activity of neurons in the brain area controlling and planning eye movements – in the “motor” regions of the parietal cortex to the side of the brain – was in proportion to how much juice was on offer and how likely they were to receive it. This suggests that the neurons are involved in weighing up the expected pay-off or value of each alternative. The decision seems to be made on the basis of which bunch of location-tuned cells “wins” by reaching a certain threshold of activity (Nature, and ). Here was evidence of some sort of neurobiological abacus in action, which could help us judge, for example, when a big but rare pay-off is more advantageous than a smaller, more certain one.
Platt was not satisfied, however. He felt the experiments were too far removed from real-world situations. He had spent months watching various species of wild monkey in Mexico and South America to get a better idea of what sorts of choices they routinely have to make, and knew that most decisions are social in nature – who to ally with, who to watch, who to mate with, who to consider a threat and so on. He decided that a good way to study decision-making in social primates, including humans, would be to find out how the brain deals with these dilemmas. To do that, he would have to venture into the nascent field of social neuroscience, a discipline that has been described as the next big thing by the founder of cognitive neuroscience, Mike Gazzaniga at the University of California, Santa Barbara.
How could Platt get an insight into these everyday decisions? Now running his own lab at Duke University, he decided to build on his previous study, but this time using pictures of what monkeys naturally like to look at – other monkeys. Platt and his colleagues, Robert Deaner and Amit Khera, initiated the pay-per-view system, and began to test how male macaques reacted to images of faces and bottoms – two things the researchers were convinced would capture their attention.
Four macaques learned to look at a screen with two targets. Looking at one earned them some juice, the other earned them less juice but also a glimpse of an image of a bottom or a face. Platt reasoned that if the monkeys valued the images, then they might give up juice or “pay” to look. What’s more, he should be able to judge the value an individual monkey gave an image by measuring how much juice had to be in the reward before the monkey would ignore the image and go for the juice instead.
“If the monkeys valued images of bottoms, then they might give up juice, or ‘pay’ to look”
“Male macaques consistently gave up some juice when they were presented with images of the perineum of females,” Platt says. To them, this is valuable information. “Males use the coloration and turgidity as a cue for receptivity and ovulation,” he explains. Moreover, the amount of juice any individual monkey gave up for a particular type of image – its value, in other words – was highly consistent in different trials and experiments.
Face value
The monkeys also deemed faces worth paying to see, but only those of dominant males. “This might seem a bit surprising but it makes some sense as well,” says Platt. “These are the guys who are pumped up with testosterone, and are the biggest threat. They can drive you away from food, or females.” When it came to faces of subordinate males or females, however, the researchers had to actually pay their viewer extra juice to convince them to take a look (Current Biology, ).
At the University of Oxford, Matthew Rushworth and Peter Rudebeck have conducted a similar experiment to see how the brain compares and prioritises social information. They measured how long macaques could be distracted from claiming a food reward by the sight of other macaques on video. “They are quick to pick up food unless the other animals are of a higher social status,” says Rushworth. “And most monkeys agree on what social stimuli are interesting.” The high-status males come out on top, then female rumps. Lower-status monkeys are far less interesting, even if they have food, the researchers found. Only moving snakes distracted them more than dominant males (Science, ).
Recently, Platt, Ben Hayden and colleagues have tried their pay-per-view experiments with humans. They used images from a database of men and women’s faces (no rear ends this time) downloaded from and rated for attractiveness by an independent panel. Of course, humans have more complex ideas of attractiveness than monkeys, but it is likely that social status influences things here too. Factors such as symmetry may reflect good genes or good immune function and are often judged attractive. The researchers found that people preferred to look at images of attractive faces of the opposite sex and would give up money to do so (see “Celebrity worship”). To view unattractive faces, they needed the incentive of extra payments. A more complex study showed that people would also trade between shorter but immediate peeks at attractive faces and longer but delayed viewings. They were also willing to perform tasks requiring effort, such as making a particular sequence of key presses, to view attractive faces.
These findings all go to show that these people used trade-offs and economic principles when deciding which faces to look at, suggesting there is a “value” implicit in gaining the social information they contain (Proceedings of the Royal Society B, ). It also suggests that whatever brain circuits motivate our choices, they are converting all possible options and pay-offs into some form that can be compared. To get an idea where and how this “common currency” works in the brain, Platt and Rushworth studied the activity of neurons in the reward circuits of both monkeys and people, as well as activity in the frontal emotional regions. Platt says there seems to be some relationship between “value” and activity in parts of the reward system, with positive values correlating with activity in a reward area called the striatum and negative values in the nearby insula.
Previous studies suggest that a frontal lobe region called the anterior cingulate sulcus deals with reward-guided decisions, including tasks and situations that are quite straightforward, such as seeking food. Meanwhile other areas in the frontal lobes seem to add emotional qualities, such as deciding whether something is nice or nasty. But more recent work by Rushworth and Rudebeck suggests it is the neighbouring anterior cingulate gyrus that busies itself with social information. They found that monkeys with damage to this region no longer showed any interest in looking at video clips of high-ranking individuals. Different types of information are processed by separate brain systems in the anterior cingulate cortex, Rushworth says. “A common currency may be a consequence of an interaction between these areas,” he says. Preliminary results from Rushworth’s latest research with Tim Behrens, using fMRI to look at human brains, suggests that there may be a confluence of all this information near a region of the frontal lobe called the ventromedial prefrontal cortex. “This may be where the common currency is,” says Rushworth.
This work is not just shedding light on the anatomy of decision-making, however. One intriguing possibility is that it could reveal something about the origins of autism. While autism is a spectrum of disorders, at one end lie some serious social difficulties, including failing to respond to faces and interpret their expressions. Platt suggests there could be a domino effect starting with problems very early in life. Recent studies tracking the gaze of people with autism indicate they do not look at the same features of a face that people commonly focus on, particularly the eyes and mouth. “If a child doesn’t look at the parent’s face, they can’t follow their gaze to the object they’re talking about, so the child has impairments in learning to share attention and in learning what other people are talking about,” he says.
Rushworth also sees an autism connection. “It is worth noting that one of the areas altered in autistic people is in the anterior cingulate gyrus,” he says. Tasks that many autistic people find difficult trigger strong activity in this region in people without the condition. “I do feel that there could be a link.”
When it comes to targets for therapy, Platt has a few ideas. “What we’re really interested in right now is whether we can manipulate how monkeys orient to social stimuli by manipulating their internal chemical milieu,” he says. His team believes that they may be able to turn up the system that attributes importance to social stimuli, making monkeys see them as highly interesting, by administering oxytocin – a hormone important for bonding. The team has also had some early success in causing deficits in social orienting by depleting levels of the neurotransmitter serotonin. They have also found that dominant males with high levels of circulating testosterone are much less bothered about scrutinising other individuals than low-ranking, low-testosterone individuals. Platt now plans to quantify the effects of these chemicals.
Platt is acutely aware of how sensitive this whole area is. “Anything we say about autism is going to be incredibly controversial.” Nevertheless, he notes that some researchers have argued that the autistic brain is hyper-masculine, while others have discovered a possible link to certain variants of serotonin genes. He also thinks the potential of this work could extend beyond autism to conditions such as social anxiety disorders. “It’s all pretty crude at the moment,” he admits, “but the start of a very interesting line of enquiry.” Still, that’s not bad for a project that began with monkeys watching blue movies. •
The Human Brain – With one hundred billion nerve cells, the complexity is mind-boggling. Learn more in our cutting edge special report.
Celebrity worship
Why do many of us pay good money to bury our noses in Hello! magazine or scan the photos from the latest red carpet event, becoming almost obsessed by the lives of people we may never even meet? One possibility is that it taps into a primitive system by which we find paying attention to attractive and socially dominant individuals intrinsically valuable and rewarding. This idea has been around since the 1960s, when anthropologists Clifford Jolly and Michael Chance first suggested that for social primates the desire to look at high-ranking individuals might act like a kind of social glue, keeping a group together. In that sense it does sound rather like the way we treat celebrities and our more exuberant leaders.
Michael Platt at Duke University, North Carolina, favours a more down-to-earth view, however. He believes that the value of looking at dominant individuals is that it allows subordinates to assess threats and risk. Still, he admits that images of attractive people could co-opt the brain’s system for attending to high-status group members in much the same way as an addictive drug can co-opt the brain’s appetite systems. This idea may even be provable, if scans were to reveal hyperactivity in the brains of celebrity worshippers on a par with that found in drug addicts. “Looking at celebrities should activate reward systems in a really deranged way,” Platt says.
