11/13/14 1:33 PMA Face to Remember | The Scientist Magazine®

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A Face to RememberOnce dominated by correlational studies, face-perception research is moving into the realm ofexperimentation—and gaining tremendous insight.

By Kerry Grens | November 1, 2014

on Blackwell reclined in a hospital bed at Stanford University, bandages from his recent brainsurgery wrapped snugly around his head. Doctors had just removed a piece of his cranium,

implanted electrodes on the surface of his brain, and closed him back up. He waited for a seizure.

Blackwell, 49, had his first seizure when he was 11 and had experienced similar incidents periodicallythereafter. But after he turned 40, the seizures became more frequent. He wanted to feel secure whencaring for his two young children instead of worrying that he might have a seizure while bringing them tothe park. So in 2012 he gave doctors the OK to implant the electrodes, which were designed to pinpointthe epicenter of his seizures as they came and help determine whether he’d be good candidate forsurgery to remove the culprit tissue.

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Once such electrodes are in place, the wait for a seizure can take days, so to pass the time Blackwellparticipated in some cognitive and perceptual tests. On occasion, researchers visited him and presentedhim with tasks to perform on a computer, such as clicking a button when a particular object appeared ona screen. After days with no sign of a seizure, Josef Parvizi, Blackwell’s neurologist, asked for permissionto stimulate the electrodes on Blackwell’s brain as part of an experiment. Blackwell agreed.

Parvizi instructed Blackwell to look at objects in the room: a Mylar balloon, a TV screen. The doctorclicked a button, but nothing happened. “Then he said, ‘Look at my face,’ and he hit the button, and itwas the most bizarre thing,” Blackwell recalls. In that brief moment when Parvizi zapped the electrodes,Blackwell saw the doctor’s face “metamorphose.”

“His face just sagged. His eyes drooped; his nose drooped and just shifted. It was very cartoonish,” hesays. The face looked somewhat familiar, but it was no longer Parvizi’s—until the doctor stoppedstimulating the electrodes on Blackwell’s brain. As soon as the stimulus was over, the familiar face of theneurologist returned.

Wanting to learn more, Parvizi asked Blackwell some questions: Could he still tell that Parvizi was amale? “Oh, yeah,” Blackwell replied. “How did you know?” asked Parvizi. “Because you’re still wearing asuit and tie. Only your face changed. Everything else was the same.” And with that, Blackwell gave toscience the best experimental evidence yet that humans have what researchers call a face-selective

area, or “face patch” for short—a region of the brain specialized for the perception of faces.1

Previous human studies had relied on imaging techniques to link face perception to face patches byassociation; none of them showed that disrupting the face patch could alter face perception. But morerecent research provides evidence that face patches, generally recognized as three chunks of thetemporal lobe, are critical to the everyday observation of faces. Blackwell is now just one of about adozen patients in whom Parvizi and Stanford colleague Kalanit Grill-Spector have demonstrated theelectrical disruption of face perception.

“It’s just so striking how specific the perceptual distortion is to the face,” says Grill-Spector. “This is whyit’s a very important discovery, because it shows the specificity of the cortical region to processingfaces.”

Neuroscientists are now capitalizing on this specificity to unpack the fundamental computationalprocesses that go into identifying a face, a feat most of us perform without thought or effort. The facepatches—and even individual neurons in them—appear to do different jobs, such as analyzing thefeatures of the face, responding to how the head is tilted, and, ultimately, determining someone’sidentity.

“We meet thousands of individuals . . . and we can differentiate them, we can recognize them in differentconditions: when there are shadows on them, when the face is turned at different angles, if they get ahaircut,” says Marlene Behrmann, a cognitive neuroscientist at Carnegie Mellon University. “It’s anincredibly robust human ability.”

Natural experiments

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It appears that theprosopagnosics’ facepatches operate well enoughto determine that a face is aface, but the poorconnection to the extendedregions prevents them fromestablishing that person’s

The neural stimulation Parvizi gave to Blackwellcaused momentary prosopagnosia?,? or faceblindness—an inability to discern the identity of aperson by his face. There are those who have hadprosopagnosia all their lives. Author andneurologist Oliver Sacks famously documented hisown condition in his writings. In a 2010 NewYorker article, Sacks wrote that he often cannotrecognize people he knows well; he has evenbumped into his own reflection, thinking it was

another bearded man walking toward him.2

Given face perception’s importance and ubiquity insocial interactions, prosopagnosia is a stressfuldeficiency to live with. “I avoid conferences,parties, and large gatherings as much as I can,knowing that they will lead to anxiety andembarrassing situations, since I not only fail torecognize people that I know well but tend also togreet strangers as old friends,” Sacks wrote. “I ammuch better at recognizing my neighbors’ dogs(they have characteristic shapes and colors) thanmy neighbors themselves.”

To investigate the roots of such face blindness, Behrmann is studying the brains of prosopagnosiapatients. In one study, she asked such patients to view faces while they sat in a functional magneticresonance imaging (fMRI) scanner. Like people without the perceptual deficiency, the patients showednormal activity in what Behrmann refers to as the “core” patches involved in face perception: thefusiform face area (FFA), the occipital face area (OFA), and the superior temporal sulcus (STS). “Wewere perplexed,” says Behrmann. “We knew [the patients’ brains] were impaired, but we couldn’t findwhere.”

So Behrmann’s team, using an MRI approach called diffusion tensor imaging, embarked on a high-resolution sleuthing trip through the hills and valleys of the brain’s morphology to find the differences.The researchers found a reduction in two white-matter tracts—the myelin-wrapped axons connectingneurons of different brain regions—between these core face patches in the back of the brain and

“extended” face-processing areas toward the front of the brain.3 (See illustration below.) The frayedcabling “suggests it’s a failure to propagate signals from the core to the extended regions,” saysBehrmann. (For more information on the technique of diffusion tension imaging, see “White’s theMatter,” The Scientist, November 2014.)

“Intriguingly, the magnitude of the compromise[in white matter] was correlated with themagnitude of the prosopagnosia,” saysBehrmann. “It was a key piece of the puzzle.”

More recently, the group has found, through fMRIcomparisons between people with and withoutprosopagnosia, that activity in the extendedregions contacted by these white matter tracts is

indeed reduced during face perception.4 Itappears that the prosopagnosics’ face patchesoperate well enough to know that a face is a face,but the poor connection to the extended regionsprevents them from determining that person’sidentity.

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identity.

PATCHWORK: In the 1990s, researchers published dataidentifying a face “patch,” dubbed the fusiform facearea (FFA), which lit up more in response to faces thanto other objects.1 Soon, other researchers identifiedtwo additional face patches, the occipital face area(OFA) and the superior temporal sulcus (STS).Together, the FFA, OFA, and STS comprise what somecall the core regions of face perception.See full infographic: JPG | PDF© CATHERINE DELPHIA

Also using fMRI, Ida Gobbini and James Haxby ofDartmouth College have shown that the extendedregions are much more active when viewing

familiar faces than unfamiliar ones.5 “Myinterpretation is, when you see someone familiar, you retrieve the ‘person knowledge’ of that person,”says Gobbini. By recruiting extended brain regions such as the precuneus or amygdala, people may beable to pull together the memories and emotions that go along with seeing someone’s face.

“Something [cognitive neuroscience] is working really hard on is trying to understand the relativecontribution of these different areas,” Behrmann says.

Manipulating humans

In September, Stanford’s Parvizi and Grill-Spectorpublished data from electrode-stimulationexperiments on 10 participants, all of them withmedical situations like Blackwell’s who werehoping to find a surgical solution to their maladiesand willing to lend their brains for study. Half thepatients had electrodes implanted on the fusiformgyrus in their right cerebral hemispheres; theother half, on the same area on the left side oftheir brains. Although both areas were activeduring face perception, only when Parvizi “tickled”the right hemisphere face patch with electricalstimulation did the patients report seeing an

altered face.6 Intriguingly, some patients also sawfaces that weren’t really there. One reported: “Theblack spot on the top of the TV shows some kindof face expression. It looked like a human face,then disappeared.” Another patient had anexperience similar to Blackwell’s, in which thedoctor’s face morphed: “It was almost like youwere a cat.”

The results support the idea that face perceptionis lateralized, which scientists had suspected sincethe first documented cases of prosopagnosia inpatients with damage to the right-hemispherefusiform gyrus. “Only the right side is importantfor changing conscious perception of faces,” saysParvizi. “We think the left side might be importantfor retrieving names or anything language-related,but it’s probably not doing the same thing as theright hemisphere.”

Parvizi says additional studies of this sort could help to determine how the patches are connected andwhat jobs they perform, as well as the precise brain regions where the visual decoding involved in faceperception takes place. Intracranial recordings could also help resolve questions about the specificity ofthe face patches and the role of neighboring cells. Of course, patients who require brain electrodeimplantation and are willing to participate in such neuroscience studies are few and far between, makingit difficult to amass data. To achieve bigger sample sizes, Brad Duchaine of Dartmouth College and DavidPitcher of the National Institute of Mental Health have used transcranial magnetic stimulation (TMS) tononinvasively excite brain regions of healthy volunteers. (See “Brain Massage,” The Scientist, November2014.) A magnetic coil delivers short bursts of electrical stimulation, which interrupts normal brainactivity for about 20 minutes. By placing the coil close to a face patch, “we can temporarily make youbad at face perception,” says Pitcher.

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'Pretty much everybody youspeak to has the totalintuition that face recognitionis seamless, rapid, effortless.

Two patches—the OFA and the posterior STS (pSTS)—lie at the surface of the brain. With fMRI, theresearchers can determine the precise location of the patches in an individual, then use TMS at aparticularly high frequency (called theta burst TMS, or TBS) to scramble the neurons’ normal function.Volunteers then reenter the brain scanner to look at various images as the researchers observe theactivity in the patches.

A prevailing model has held that visual information about faces first comes into the OFA from the earlyvisual cortex, then branches out to the other face patches. According to this view, the OFA acts “kind oflike a gatekeeper,” says Pitcher. But his latest work shows that, although disrupting the OFA reducesbrain activity in the pSTS when the participants view photographs of faces, pSTS activity remains normal

when they view videos.7 These results suggest that facial information reaches more than just the OFAinitially and does not travel linearly through the patches. “What people have been arguing more andmore so, and my paper is one of the first to show it experimentally, is that all the patches are connectedto each other,” says Pitcher. The face patches “all get information round about the same time and sharethat information.” (See illustration above.)

For all that’s been gleaned from the human experiments, there is still much left to be discovered. Pitcherpoints out that the neuronal connections between patches are still largely unmapped in humans, forinstance. Additionally, “we don’t have a good feel for how the division of labor is being set up” among thevarious face patches, says Duchaine. Such work would require invasiveness so far impossible in humans,he notes, but research on face perception in other animals is beginning to yield clues.

Monkey business

Much of what scientists can only dream of doing in human brains, Doris Tsao and Winrich Freiwald haveaccomplished in macaques. As a graduate student in Margaret Livingstone’s lab at Harvard, Tsao readabout the discovery of the FFA, finding it “astonishing” that there would be a region specialized for faceswhen there are so many other objects humans have to identify. But the fMRI data that revealed theexistence of the FFA couldn’t explain what the cells themselves were doing. To get at function on thecellular level, Tsao says, “it seemed easy to test in a monkey.”

So, in the early 2000s, she teamed up with Freiwald, then a postdoc in Nancy Kanwisher’s lab at MIT.The duo would insert electrodes into the brain region that responded to faces as the monkeys viewed aslide show of a variety of objects and human faces. Freiwald, now at Rockefeller University, vividlyrecalls those initial trials as the researchers guided electrodes slowly through the brain toward what theycall the “middle face patch” while pictures flashed before the monkey. A crackling sound heard overspeakers connected to the electrophysiology rig would alert the researchers to a neuron firing. Onoccasion, a little rumbling would sound and then fade away. Then, just as a face popped up on thescreen, they heard a loud “kkkrrrr,” and made a note of it as a cell that “likes faces.”

Then they got another. “Kkkrrr.” And another. “And then we realized, ‘Wow, every time we stuck our

electrode into that patch we got face cell after face cell after face cell,’?” says Tsao.8 “It wastremendously exciting. It meant we could now have hope to understand the brain’s vocabulary for howthe brain codes objects.”

The study also provided strong support for the specificity of face patches. The response to the otherobjects the macaques viewed was much smaller, sometimes silence altogether, compared to the neuralactivity triggered by faces. (See “Just for Faces?” at bottom.)

Freiwald and Tsao spent hours Photoshoppingfaces for new experiments. To see whetherindividual neurons respond to particular featuresin the face, they created a simple cartoon inwhich the parts could change independently ofone another—the eyebrows could be removed,the eyes spaced far apart, and so on. They foundthat within the same face patch, individual

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—Marlene Behrmann,Carnegie Mellon University

And yet it’s probably themost difficult problem thevisual system has to solve.

neurons were tuned to respond more readily toparticular features, such as the eyes or hair, andthat many of the cells were especially keen onfacial geometry, such as the roundness of theface, the size of the irises, or the space between

the eyes.9 “Here you can have neighboring cells,cells separated by microns, doing totally separatethings,” says Tsao, who pursued this work as apostdoc with Livingstone and, later, Roger Tootellat Massachusetts General Hospital.

Jim DiCarlo and his colleagues at MIT have used optogenetics to actually turn off some of those neuronsand see what happens. In a recent study demonstrating the technique, they asked what would happen ifthey silenced the neurons in and around a particular face patch in macaques that had been trained todiscriminate the gender of human faces. “The field’s hypothesis would be that silencing the face patchshould produce deficits [in discrimination], and silencing other tissue should affect [perception ofnonface] objects,” says DiCarlo. Sure enough, with suppressed face-patch activity, the monkeys wereless able to distinguish men from women. Inhibition of neighboring regions, on the other hand, had no

such effect.10

DiCarlo says this study, presented by lead author Arash Afraz at the Vision Sciences Society meetingearlier this year, is just the beginning of what optogenetics can bring to the study of object and faceperception. DiCarlo’s group is now conducting extensive face and object discrimination tests, with plansto silence bits of neural tissue in one or more brain regions.

Tsao and Freiwald’s studies have also supported the idea that faces are processed across a network ofpatches. After working with the middle face patch in macaques, the researchers identified a number ofother regions active during face perception. They found that these regions are tightly coupledanatomically; one patch communicates with multiple other patches, each of which appears to perform adistinct task. In one region, for instance, the cells responded only to faces in particular orientations—say,profile or straight-on. A different patch might respond to just one individual face, but will do soregardless of the face’s orientation.

Many consider Tsao and Freiwald’s work the best evidence to date that face perception operates like anorchestra, with units cooperating, communicating, and building upon one another to provide aharmonious picture of facial identity. “I’ve learned more from one of their papers than from 10 to 20human papers because you can get in there and record from single neurons,” says Duchaine. “They getso much interesting evidence out of their recordings, it blows me away.”

Points of view

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—Winrich Freiwald,Rockefeller University

Faces are such potent stimulito get us into the emotionaland social brain in ways thatescape cognitive control inthe first pass.

Comprehending how the brain computes faces hasobvious implications for understandingprosopagnosia. Working with Behrmann, AdrianNestor of the University of Toronto Scarboroughaims to build a face from the fMRI data of aviewer. The researchers have built an algorithmthat attempts to link the objective pictorialqualities of a face with the corresponding neuralcode. Then, starting with the neural code, thesoftware can work backward to construct the face.By analyzing the neural codes of healthyparticipants, researchers could uncover newinsights into the computation of face perception,and the scans of prosopagnosia patients mayprove even more interesting.

“If we can approximate the face [seen by]prosopagnosics, we can finally not only theorizeand hypothesize as to why they cannot recognizefaces at the individual level, we can see what theysee,” says Nestor. “That’s a very powerfuldemonstration of what’s wrong—what’s notfunctioning at the neural level.”

The early results show that the reconstructedfaces formed by the data from congenital prosopagnosics are remarkably alike. “The neural patterns areso similar,” Nestor says. “We’re still trying to figure out why.” In a person without face blindness, on theother hand, the neural responses to viewing two different faces would be measurably different.

For Freiwald and many others, face perceptionalso offers a window into the mechanismunderlying our nature as social beings. “Over thelast [few] years, I realized that faces are suchpotent stimuli to get us into the emotional andsocial brain in ways that escape cognitive controlin the first pass,” he says. Take, for instance, theway humans “ooh” and “aah” and feel warmth forthe face of a baby animal. “We’re just showingpixels of colors,” says Freiwald, “but by the waythey’re arranged we’re getting into the emotionalbrain.”

Could this social nature be at the heart of how we so easily identify faces—three-dimensional objects thatfollow the same basic pattern, yet carry so much significance individually? “The face is what one goes by,generally,” Alice tells Humpty Dumpty in Lewis Carroll’s Through the Looking Glass. Yet, as HumptyDumpty rightly responds, “Your face is the same as everybody has—the two eyes, so . . . nose in themiddle, mouth under.”

“That’s exactly why this is such an interesting domain to be in,” says Behrmann. “Pretty much everybodyyou speak to has the total intuition that face recognition is seamless, rapid, effortless. And yet . . . it’sprobably the most difficult problem the visual system has to solve. There’s a real disconnect between ourintrospection and the nature of the computation.”

JUST FOR FACES?

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While plenty of imaging data support theinvolvement of several brain regions inperceiving faces, there remains considerabledebate about each area’s precise function,especially regarding whether the neurons areexclusively devoted to facial recognition. IsabelGauthier of Vanderbilt University makes theargument that the patches may not be face-specific at all, but might simply reflect ourexpertise in facial recognition.

She and her colleagues have asked experts inrecognizing particular objects, say, carenthusiasts or bird watchers, to view faces,cars, birds, and other items while in an fMRIscanner. “And over and over again, we find thesame relationship: the response to nonfaceobjects in the fusiform face area [FFA] predictsyour performance in recognizing objects,” she says. In other words, experts use the FFA todiscriminate the objects of their expertise, just as they do when perceiving faces.1 “It’s not surprisingfaces would activate this region, because we’re experts at [recognizing faces],” Gauthier says.

Other researchers have countered Gauthier’s argument with their own data. Earlier this year, BradDuchaine of Dartmouth College and his colleagues showed that prosopagnosics can still becomeexperts in identifying particular objects when they’re trained to do so.2 “They were able to learn [thetask] even though they don’t have [a fully functioning] FFA,” says David Pitcher, a research fellow atthe National Institute of Mental Health who was a coauthor of the study. If the FFA is an expertisebrain region, the prosopagnosics should have failed to learn, just as they cannot be trained torecognize faces.

But others have also raised doubts about the idea that face patches are solely responsible forprocessing faces. It’s also possible that neurons neighboring the face patches contribute to detectingsomeone’s identity. To get to the bottom of face perception, Jim DiCarlo and Arash Afraz of MIT andother researchers are moving the field from one of observation and correlation to one ofexperimentation and causation. “If we can do causality studies, I think we will find [the so-called“face”] neurons are doing other things not face-related,” he says. So far though, their data seem tosupport the idea that face patches are specialized for recognizing faces, DiCarlo notes. “Thathypothesis is too simple, but we don’t have evidence to refute it. So it might be true.”

1. I. Gauthier et al., “Expertise for cars and birds recruits brain areas involved in facerecognition,” Nat Neurosci, 3:191-97, 2000.

2. C. Rezlescu et al., “Normal acquisition of expertise with greebles in two cases of acquiredprosopagnosia,” PNAS, 111:5123-28, 2014.

References

1. J. Parvizi et al., “Electrical stimulation of human fusiform face-selective regions distorts faceperception,” J Neurosci, 32:14915-20, 2012.

2. O. Sacks, “Face-blind,” The New Yorker, August 30, 2010.3. C. Thomas et al., “Reduced structural connectivity in ventral visual cortex in congenital

prosopagnosia,” Nat Neurosci, 12:29-31, 2008.4. G. Avidan et al., “Selective dissociation between core and extended regions of the face processing

network in congenital prosopagnosia,” Cereb Cortex, doi:10.1093/cercor/bht007, 2013.5. M.I. Gobbini, J.V. Haxby, “Neural systems for recognition of familiar faces,” Neuropsychologia,

45:32-41, 2007.6. V. Rangarajan et al., “Electrical stimulation of the left and right human fusiform gyrus causes

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You

Dr. SPosts: 1

different effects in conscious face perception,” J Neurosci, 34:12828-36, 2014.7. D. Pitcher et al., “Combined TMS and fMRI reveal dissociable cortical pathways for dynamic and

static face perception,” Curr Biol, 22:2066-70, 2014.8. D.Y. Tsao et al., “A cortical region consisting entirely of face-selective cells,” Science, 311:670-74,

2006.9. W.A. Freiwald et al., “A face feature space in the macaque temporal lobe,” Nature Neurosci,

12:1187-96, 2009.10. A. Afraz et al., “Optogenetic and pharmacological suppression of face-selective neurons reveal

their causal role in face discrimination behavior,” J Vision, 14:600, 2014.

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November 4, 2014

This is all very interesting--that there is a section of the brain specific forface recognition. But, although scientists have narrowed the search, theresults say nothing about how we learn to recognize faces. And, I doubtthat face recognition is so special. After all, we learn to recognize slightand subtle differences between an almost infinite number of other stimuli,not just faces. Faces get a lot of attention because of their social value,but I doubt that they are special otherwise.

Also, cognitive science offers no cogent theory of face perception. Andsaying that the brain perceives or organizes is misleading. To perceive isto behave and individual organisms, not brains, behave. The brain isprogrammed by a combination of genes and learning experiences, withthe latter surely more important, especially in humans. When we firstcome into the world there is little to no perception (i.e., reactingdifferentially to stimuli) of any kind; we have to learn it. And we do sothorugh operant conditioning from interactions with an ever increasingcomplex environment. In fact, no other theory besides an operant one canexplain why we cannot recognize someone when seeing them but can doso when we hear their voice, or see some other visual stimulus associatedwith that person. This is because we have been reinforced to call peopleby name in the presence of a variety of different stimuli associated withthem, faces being only one. I'm sure neuroscientists could look for theneurons that mediate voice recognition too. All of these efforts are a littlelike a more sophisticated phrenology. We may ultimately be able to pointto exact locations in the brain responsible for mediating thousands ofinteresting behaviors; but that will tell us nothing about the genesis orfunction of those behaviors.

Neurophysiology without an experimentally based theory of behavior--not

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