neuroscience Uncanny sight in the Blind Some people who are blind because of brain damage have “blindsight”: an extraordinary ability to react to emotions on faces and even navigate around obstacles without knowing they can see anything By Beatrice de Gelder

he video my colleagues and I shot is incoming signals he became completely blind. amazing. A blind man is making his way This study of TN navigating along the hall- Key Concepts down a long corridor strewn with boxes, way is probably the most dramatic demonstra- T ■ ■ Some people who are chairs and other office paraphernalia. The man, tion of blindsight ever reported. Other patients blind because of brain known to the medical world as TN, has no idea who have lost vision because of damage to the damage exhibit “blind­ the obstacles are there. And yet he avoids them primary visual cortex have exhibited less spec- sight”—responses to all, here sidling carefully between a wastepaper tacular but equally mysterious cases of the phe- objects and images they basket and the wall, there going around a cam- nomenon—responding to things they cannot cannot consciously see. era tripod, all without knowing he has made consciously see, ranging from simple geometric any special maneuvers. TN may be blind, but he shapes to the complex image of a person’s face ■ ■ Blindsight can detect many visual features, has “blindsight”—the remarkable ability to re- expressing an emotion. Scientists have also in- including colors, motion, spond to what his eyes can detect without know- duced a similar effect in healthy people, by tem- simple shapes, and the ing he can see anything at all. [To see the film of porarily “switching off” their visual cortex or emotion expressed by a the experiment, go to www.ScientificAmerican. by outfoxing it in other ways. person’s face or posture. com/may2010/blindsight.] Today research into blindsight seeks to un- ■ ■ Researchers are mapping TN’s blindness is of an extremely rare type, derstand the range of perceptual abilities that the ancient brain areas caused by two strokes he suffered in 2003. The may be retained by the cortically blind and to responsible for blindsight strokes injured an area at the back of his brain determine which brain regions and neuronal and exploring the limits of called the primary visual cortex, first on his pathways are responsible. The knowledge being this remarkable ability. left hemisphere and five weeks later on the right. gained says something about us all, because His eyes remained perfectly healthy, but even if we never suffer a catastrophic injury re- —The Editors

darren braun darren with his visual cortex no longer receiving the sembling TN’s, the same unconscious brain

www.ScientificAmerican.com SCIENTIFIC AMERICAN 61 [BASICS] What Is Blindsight? Conscious vision in humans depends on a region of the brain called the primary visual cortex (below). Damage there causes blindness in corresponding areas of the visual field. “Blindsight” occurs when patients respond in some way to an item displayed in their blind area, where they cannot consciously see it. In a dramatic demonstration of the phenomenon, a patient called “TN” navigated an obstacle course despite his total blindness (right). Visual Pathways Signals from the retina go to the primary visual cortex via the lateral geniculate nucleus in the midbrain and ultimately to higher areas for conscious processing. Right Nerves also send visual information to areas such as visual the pulvinar nucleus and superior colliculus in the field midbrain. Those areas do not seem to produce any conscious vision, but some must underlie blindsight.

Blind area Nerves Light Damage Left Navigating Blind visual Suspecting patient TN might exhibit blindsight, researchers, field Retina Primary visual including Lawrence Weiskrantz (shown with TN above), asked him to walk down a cluttered hallway, telling him it was empty. Pulvinar nucleus cortex TN avoided all the obstacles, even though he remained unaware Lateral geniculate nucleus of them and of his meandering path. Video of the experiment is Superior colliculus online at www.ScientificAmerican.com/may2010/blindsight.

functions manifest in him as the astonishing gery to remove a tumor. The wider research com- ability to see without knowing are surely a con- munity, however, initially greeted reports of hu- stant, invisible part of our own daily existence. man blindsight with great skepticism. Disbelief about blindsight is not surprising, A Controversial History because the phenomenon seems counterintui- As long ago as 1917, doctors reported cases like tive, if not outright contradictory. After all, how blindsight—then called residual vision—in sol- could people see without knowing that they see? diers injured in World War I. Half a century Just as it does not make sense to say that I do not would pass, however, before more organized know if I am in pain, it also does not make and objective research into the capacity began. sense, on the face of it, to suggest that somebody First, Lawrence Weiskrantz and his student can see something when he insists he is blind. Nicholas K. Humphrey, both then at the Univer- Yet we do not always know that we can see. sity of Cambridge, studied surgically altered Nor do we always know that we cannot. The re- monkeys in 1967. Then, in 1973, Ernst Pöppel, lation between seeing and knowing is more Richard Held and Douglas Frost of the Massa- complicated than we commonly assume. For in- chusetts Institute of Technology measured the stance, people with normal sight have a blind It is now clear eye movements of a patient and found he had a spot, although we are not usually aware of this that many slight tendency to look toward stimuli that he hole in our sight or handicapped by it. could not see consciously. Another reason for disbelief was the paucity ) more patients These discoveries spurred further systematic of human evidence: subjects with cortical blind- with damage investigations of animals lacking the primary vi- ness who can be studied are rare. The primary photograph sual cortex (also called V1), most of them con- visual cortex is only a few centimeters across in to the visual ducted by Weiskrantz and his collaborators. A adults, and brain damage is seldom restricted to cortex have number of studies established that animals re- just that area, knocking out the patient’s vision tain significant visual abilities after removal of yet leaving other faculties intact enough for ); beatrice de gelder ( blindsight than their visual cortex (for example, detecting move- meaningful research on what the brain contin-

scientists ment and discriminating shapes). ues to perceive. Even so, it is now clear that many illustration Weiskrantz and his co-workers also began more patients with damage to the visual cortex realized in studies in 1973 with a person known as DB who have blindsight than scientists realized in the

the past. had recently lost part of his visual cortex in sur- past, and skepticism has abated. keith kasnot (

62 Scientific American May 2010 Most of these patients still have some func- reminiscent of sleepwalking, another phenom- tioning in the primary visual cortex. Many have enon in which people exhibit a capacity to per- damage to only a small part of V1, leading to a form in some way without having any awareness small island of blindness in their visual field; of their actions. Indeed, when we questioned him others lose the entire left or right half of V1, leav- afterward, he insisted he had simply walked along ing them blind across the corresponding (oppo- the hallway: he was not only unaware of seeing site) half of their visual field. Blindsight in these What can anything but also oblivious to how he had ma- cases involves detecting objects or images pre- be detected? neuvered around the unseen objects. He was at sented in the blind area, where the patient can- a loss to explain or even to describe his actions. Blindsight is strongest when not see them consciously. visual details are about the size Traditional methods for studying vision in of a quarter viewed from five to Blindsight for Emotions humans have relied on the viewers’ verbal re- 15 feet away. It can detect an Moving around is one of the most fundamental ports of what they perceive. Tested in that way, assortment of basic visual proper- tasks an animal faces, so perhaps it should not ties, including: subjects will report not seeing anything in the be surprising that the brain has ways to support blind part of their visual field. More indirect ■ Simple shapes navigation even when the primary visual cortex methods, however, can reveal that these unseen ■ Arrays of lines and conscious vision are hobbled. As a social visual stimuli actually do influence how a pa- ■ Objects appearing or disappearing species, humans also depend for their survival tient responds. ■ Movement on successful communication with others. They In some experiments, patients show clear ■ Color must recognize other people, along with their physiological changes, such as constriction of ■ Orientation of lines gestures and signs of what they are thinking. the pupil, as signs of unconscious seeing. And With such thoughts in mind, my collaborators subjects can react differently to items shown in and I began to wonder in the late 1990s if people the intact visual field depending on what is pre- with cortical damage could detect visual dis- sented at the same time in the blind field. When plays such as the emotion on a face or the mean- asked to guess which of several alternative items ing of a body posture in the usually inaccessible are displayed in the blind field, a patient may an- parts of their visual field. swer correctly almost every time. In 1999 we started conducting tests using Another important experimental tool is neu- movies of faces. Vision researchers generally roimaging, which can provide direct evidence consider faces to be visually complex—far more about the brain regions involved in blindsight difficult to process than gratings and other ele- and the pathways that the visual information mentary shapes—but a face is a very natural travels. Brain imaging has been instrumental in form for the human brain to handle. Our pa- dispelling lingering suspicions that some spared tient, GY, had lost all of his primary visual cor- pieces of cortex might explain residual vision. tex on the left side in childhood, rendering him Collectively, these various kinds of experi- blind on the right side of his visual field. We ments have revealed that people can uncon- found he could reliably guess the expression ap- sciously detect a wide range of visual attributes, pearing on faces he did not consciously perceive, including color, simple shapes such as X and O, but he seemed truly blind to a variety of non- simple motion, and the orientation of lines or emotional facial attributes such as personal iden- gratings. Large shapes, as well as very fine detail, tity and gender. seem hard to detect. For instance, patients detect To study blindsight of emotions further, in features of a grating most effectively if its lines 2009 we exploited a phenomenon called emo-

) are comparable to venetian blinds viewed from tional contagion, a tendency to match one’s own sad about 1.5 to 4.5 meters (five to 15 feet). facial expressions to those of others that we see.

ages ( We were inspired to try the navigation exper- Researchers measure emotional contagion with m iment with TN by research Weiskrantz and Hum- a procedure called facial electromyography, by

); getty i phrey did in the 1970s: a monkey with no prima- which electrodes on a subject’s face record nerve ry visual cortex freely moved around a room signals going to muscles involved in smiling or happy ( cluttered with objects without bumping into any frowning. We used this technique on GY and of them. Nevertheless, we were amazed when T N DB while showing them still images of faces and

Getty Images made his way along the hallway with no collisions whole bodies expressing happiness or fear.

at all. Personalized psychophysical tests to assess  Blindsight can also recognize All the stimuli triggered emotional reactions his conscious vision had not found any visual emotions being expressed by a as measured by electromyography, irrespective functioning, including detection of big targets. person, but not who the person of whether the image was on the patient’s sight-

nthony Marsland Marsland A nthony TN’s ability to move down the corridor was is or the person’s gender. ed side or his blind side. In fact, surprisingly, the

www.ScientificAmerican.com SCIENTIFIC AMERICAN 63 [EXPERIMENTS] Investigating Blindsight Normal sight Small contraction Because total cortical blindness like patient TN’s is rare, studies of blindsight often use patients blind on one side of their visual field. The patient stares at a fixed point while imag­ es are presented on each side. The subject may be asked to “guess” what is on the blind side or to press a button on seeing items on the sighted side. Equipment may monitor brain activity and measure involuntary responses such as tiny facial movements and pupil dilation. Blind side Sighted side Blindsight Large contraction  does Blindsight See Emotions? Patients shown images on their blind side of people expressing emotions correctly guessed the emotion most of the time. Facial muscles used in smiling and frowning reacted in ways that matched the kind of emotion in the unseen image (below, exaggerated). Thus, the emotions were recognized without involv­ ing conscious sight. The effect worked with images of faceless bodies as well as faces, implying that patients were recognizing an emotion and not merely mimicking a facial expression unconsciously.

Patient with blindsight Normal sight Small contraction

No blindsight Small contraction

Sighted side Blind side ▲ What Brain Areas Does Blindsight Use? Electrodes measuring Researchers showed patients gray and purple squares, knowing the facial movements superior colliculus region in the midbrain receives no signals from the retina about purple objects. Gray squares but not purple ones triggered signs of blindsight such as greater pupil contractions. These results, along with neuroimaging of the patients in action, imply that the superior colliculus plays a critical role in blindsight.

unseen images produced a faster response than known as the use of subliminal images: a visual those seen consciously. We also monitored pu- stimulus flashes before the experimental subject pil dilations, a measure of physiological arous- very briefly, followed immediately by a pattern al. The unseen fearful images produced the in the same location. The pattern interferes with strongest effect—seemingly the more we are conscious processing of the fleeting subliminal consciously aware of an emotional signal, the image, leaving the subject with no conscious slower and weaker is our reaction. awareness of seeing it, but experiments can tease Mapping neural One school of thought holds that emotional out objective evidence that it was seen. Other pathways contagion arises because people unconsciously experiments temporarily disable the visual cor-

Researchers are using advanced mimic the expressions they see, without neces- tex by applying magnetic fields to the back of ) imaging techniques to attempt sarily recognizing the emotion itself. But be- the head, a technique called transcranial mag- to trace the neural pathways that squares visual information travels in the brain cause our patients reacted not only to faces but netic stimulation. to produce blindsight. also to bodies (which had blurred faces), we con- Numerous studies have shown that healthy One such method is a kind of cluded that they were perceiving and responding subjects can reliably “guess” the nature of a stim- magnetic resonance imaging called to the emotion. ulus even when it is presented too briefly for diffusion tensor imaging, which relies them to perceive it consciously or when transcra-

on water diffusing more rapidly along ); lucy reading-ikkanda ( Blindsight for All nial magnetic stimulation is disabling their visu-

neurons than across them. eyes

Diffusion tensor imaging has Because the number of suitable patients for al cortex. Much research has also investigated and mapped bundles of neurons that may blindsight studies is extremely small, inducing how normally sighted observers react to emo- be responsible for blindsight of

the phenomenon temporarily in people with tional stimuli they cannot see consciously. Even experiment emotions. The pathway connects the before such blindsight experiments got under pulvinar nucleus and superior collicu­ completely healthy brains is a valuable tool for lus to the amygdala, which plays conducting controlled experiments. One tech- way, studies in animals and humans suggested

a key role in processing emotions. nique uses visual “masking,” more popularly that structures in the subcortex (areas of the keith kasnot (

64 Scientific American May 2010 brain that are deeper and more evolutionarily [The Author] visual signal that cannot be consciously per- ancient than the cortex) can initiate appropriate ceived into an action. Specifically, we had a pa- responses before areas such as the visual cortex tient press a button whenever we showed him a have analyzed the stimulus in detail. This non- square on his sighted side. Sometimes we simul- conscious system seems to operate in parallel taneously presented a square on his blind side. with the normal, predominantly cortical, pro- Sometimes we used gray squares and sometimes cessing routes. These subcortical areas that are purple ones. We chose a purple hue that only one activated by subliminal emotional stimuli are the type of light-detecting cone cell in the retina de- leading suspects in processing emotions detected tects, knowing that the SC receives no inputs by blindsight in permanently blind patients. from that type; it is blind to this purple. Yet scientists continue to debate whether these Beatrice de Gelder is professor of A gray square on our patient’s blind side ac- temporary forms of blindness induced in normal- cognitive neuroscience and direc- celerated his response and made his pupils con- tor of the Cognitive and Affective ly sighted people are the true functional equiva- strict more—a sign of processing the stimulus— Neuroscience Laboratory at Tilburg lent of blindsight in patients with permanent cor- University in the Netherlands. She whereas a purple square had neither effect. In tical damage. In particular, visual-masking tech- is also on the faculty of the Athi- other words, he exhibited blindsight of gray niques, such as the use of subliminal images, noula A. Martinos Center for stimuli but not purple ones. Brain scans showed permit the visual cortex to process information Biomedical Imaging in Charles- that his SC was most strongly activated only by as usual but interfere with further conscious pro- town, Mass. De Gelder investigates the gray stimulus on his blind side. Some other the neuroscience behind process- cessing. Consequently, “blindsight” of sublimi- ing of faces and emotions and areas in the midbrain have been suspected of be- nal images could be a quite distinct phenomenon the ways cognition and emotion ing involved in blindsight instead of the SC, but from blindsight in patients, involving its own interact in both healthy and dam- in our experiment their activity seemed unrelat- characteristic assortment of brain regions. Trans­ aged brains. ed to the occurrence of blindsight. cranial magnetic stimulation presumably mimics These findings show that the SC acts in the cortical damage closely, but to know whether the human brain as an interface between sensory resulting blindsight actually involves the same processing (sight) and motor processing (leading neuronal pathways requires experiments that to the patient’s action), thereby contributing to combine the technique with neuroimaging. visually guided behavior in a way that is appar- Conversely, after an injury, a patient’s brain ently separate from the pathways involving the (even an adult’s) may start rewiring itself to com- cortex and entirely outside conscious visual ex- pensate for the loss. Such neural plasticity could perience. Blindsight of emotions displayed by well create pathways for blindsight that are not people also involves the SC as well as other areas present in the normally sighted people who are in the midbrain, such as the amygdala. studied using transcranial magnetic stimulation Blindsight has captured a lot of attention and visual masking. Until these issues are better ➥ More To from philosophers, who are intrigued by the par- understood, studies of patients with injuries will adoxical idea of seeing without knowing that remain crucial for fathoming how noncortical Explore one sees. The idea, of course, is only a paradox regions produce residual vision. Unseen Facial and Bodily Expres- if “seeing” is always taken to mean “consciously sions Trigger Fast Emotional Reac- tions. Marco Tamietto et al. in Pro- seeing.” That mind-set was a stumbling block to Neural Pathways ceedings of the National Academy of acceptance of blindsight by scientists, delaying Research has not yet fully determined the neural Sciences, Vol. 106, No. 42, pages progress in understanding the role of uncon- structures responsible for blindsight in the cor- 17661–17666; October 20, 2009. scious seeing in human cognition. tically blind, but the most likely candidate to It can also be a stumbling block for patients Collicular Vision Guides Noncon- play a central role is a brain region called the scious Behavior. Marco Tamietto suffering from cortex-based loss of vision, pre- superior colliculus (SC), which sits in a part of et al. in Journal of Cognitive Neurosci- venting them from unlocking the potential of the subcortex called the midbrain. In nonmam- ence, Vol. 22, No. 5, pages 888–902; their residual visual skills in their everyday lives. mals such as birds and fish, the SC is the main May 2010. For example, TN views himself as a blind per- structure receiving input from the eyes. In mam- son, and he will remain totally dependent on his Affective Blindsight. Beatrice de mals it is overshadowed by the visual cortex but Gelder and Marco Tamietto in white cane until he is convinced he can see with- remains involved in controlling eye movements, Scholarpedia, Vol. 2, No. 10, page out knowing it. Training may also help. After among other visual functions. Blindsight would 3555; 2007. Available at www. three months of daily stimulation, cortically exploit information that travels from the retina scholarpedia.org/article/ blind patients were better at detecting targets in Affective_blindsight

. kret to the SC without first going through the prima- their blind field. Whether training in realistic ry visual cortex. Helen, a Blind Monkey Who Sees conditions could lead to improved navigation Last year my colleagues and I showed that Everything. Video from 1971. Avail­ skills is, like so many other features of blind-

courtesy of m this midbrain area is essential for translating a able at bit.ly/blindsightmonkey sight, a question for future research. ■

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