ARE WHA C DO WE HEADED D - Nicolelis Lab

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W H AT W E CA N D OW H E R E W E’ R E H E A D E DBLIME Y OITS N DWHO WE AREneuroengineeringMind inMotionThe idea that paralyzed peoplemight one day control their limbsjust by thinking is no longera Hollywood-style fantasyBy Miguel A. L. Nicolelisin 2014 billions of viewers worldwide mayremember the opening game of theWorld Cup in Brazil for more than justthe goals scored by the Brazilian nationalteam and the red cards given to its adversary. On that day my laboratory at DukeUniversity, which specializes in developing technologies that allow electrical signals from the brain to control roboticlimbs, plans to mark a milestone in overcoming paralysis.If we succeed in meeting still formidable challenges, the first ceremonialkick of the World Cup game may be madeby a paralyzed teenager, who, flanked bythe two contending soccer teams, willsaunter onto the pitch clad in a roboticbody suit. This suit—or exoskeleton, aswe call it—will envelop the teenager’slegs. His or her first steps onto the fieldwill be controlled by motor signals originating in the kicker’s brain and transmitted wirelessly to a computer unit the sizeof a laptop in a backpack carried by ourpatient. This computer will be responsi-58 Scientific American, September 2012ble for translating electrical brain signalsinto digital motor commands so that theexoskeleton can first stabilize the kicker’s body weight and then induce the robotic legs to begin the back-and-forth coordinated movements of a walk over themanicured grass. Then, on approachingthe ball, the kicker will visualize placinga foot in contact with it. Three hundredmilliseconds later brain signals will instruct the exoskeleton’s robotic foot tohook under the leather sphere, Brazilianstyle, and boot it aloft.This scientific demonstration of a radically new technology, undertaken withcollaborators in Europe and Brazil, willconvey to a global audience of billions thatbrain control of machines has moved fromlab demos and futuristic speculation to anew era in which tools capable of bringingmobility to patients incapacitated by injury or disease may become a reality. We areon our way, perhaps by the next decade, totechnology that links the brain with mechanical, electronic or virtual machines.This development will restore mobility,not only to accident and war victims butalso to patients with ALS (also known asLou Gehrig’s disease), Parkinson’s and other disorders that disrupt motor behaviorsthat impede arm reaching, hand grasping,locomotion and speech production. Neuroprosthetic devices—or brain-machineinterfaces—will also allow scientists to domuch more than help the disabled. Theywill make it possible to explore the worldin revolutionary ways by providinghealthy human beings with the ability toaugment their sensory and motor skills.In this futuristic scenario, voluntaryelectrical brain waves, the biological alphabet that underlies human thinking,will maneuver large and small robots remotely, control airships from afar, andperhaps even allow the sharing ofthoughts and sensations of one individu-

Illustration by Kemp RemillardSeptember 2012, ScientificAmerican.com 59

BLIME Y OITS N DWHO WE AREW H AT W E CA N D OW H E R E W E’ R E H E A D E Dal with another over what will become acollective brain-based network.Thought MachinesMiguel A. L. Nicolelis has pioneeredthe field of neuroprosthetics. Heis Duke School of Medicine Professorof Neurosciences and co-directorof the Duke University Center forNeuroengineering.In BriefBrain waves can now control thefunctioning of computer cursors,robotic arms and, soon, an entire suit:an exoskeleton that will allowa paraplegic to walk and maybeeven move gracefully.Sending signals from the brain’souter rindlike cortex to initiatemovement in the exoskeletonrepresents the state of the artfor a number of bioelectricaltechnologies perfectedin recent years.The 2014 World Cup in Brazil willserve as a proving ground for abrain-controlled exoskeleton if, asexpected, a handicapped teenagerdelivers the ceremonial opening kick.60 Scientific American, September 2012the lightweight body suit intended forthe kicker, who has not yet been selected,is still under development. A prototype,though, is now under construction at thelab of my great friend and collaboratorGordon Cheng of the Technical University of Munich—one of the founding members of the Walk Again Project, a nonprofit, international collaboration among theDuke University Center for Neuroengineering, the Technical University of Munich, the Swiss Federal Institute of Technology in Lausanne, and the Edmondand Lily Safra International Institute ofNeuroscience of Natal in Brazil. A fewnew members, including major researchinstitutes and universities all over theworld, will join this international team inthe next few months.The project builds on nearly two decades of pioneering work on brain-machine interfaces at Duke—research thatitself grew out of studies dating back tothe 1960s, when scientists first attemptedto tap into animal brains to see if a neuralsignal could be fed into a computer andthereby prompt a command to initiatemotion in a mechanical device. Back in1990 and throughout the first decade ofthis century, my Duke colleagues and I pioneered a method through which thebrains of both rats and monkeys could beimplanted with hundreds of hair-thinand flexible sensors, known as micro wires. Over the past two decades we haveshown that, once implanted, the flexibleelectrical prongs can detect minute electrical signals, or action potentials, generated by hundreds of individual neuronsdistributed throughout the animals’ frontal and parietal cortices—the regions thatdefine a vast brain circuit responsible forthe generation of voluntary movements.This interface has for a full decadeused brain-derived signals to generatemovements of robotic arms, hands andlegs in animal experiments. A criticalbreakthrough occurred last year when twomonkeys in our lab learned to exert neuralcontrol over the movements of a computer-generated avatar arm that touched objects in a virtual world but also providedan “artificial tactile” feedback signal directly to each monkey’s brain. The software allowed us to train the animals tofeel what it was like to touch an objectwith virtual fingers controlled directly bytheir brain.The Walk Again consortium—assistedby its international team of neuroscientists, roboticists, computer scientists,neurosurgeons and rehabilitation professionals—has begun to take advantage ofthese animal research findings to create acompletely new way to train and rehabilitate severely paralyzed patients in how touse brain-machine interface technologiesto regain full-body mobility. Indeed, thefirst baby steps for our future ceremonialkicker will happen inside an advancedvirtual-reality chamber known as a CaveAutomatic Virtual Environment, a roomwith screens projected on every wall, including the floor and ceiling. After donning 3-D goggles and a headpiece thatwill noninvasively detect brain waves(through techniques known as electroencephalography—EEG—and magnetoencephalography), our candidate kicker—by necessity a lightweight teenager forthis first iteration of the technology—willbecome immersed in a virtual environment that stretches out in all directions.There the youngster will learn to controlthe movements of a software body avatarthrough thought alone. Little by little, themotions induced in the avatar will increase in complexity and will ultimatelyend with fine-motor movements such aswalking on a changing terrain or unscrewing a virtual jelly jar top.Plugging into Neuronsthe mechanical movements of an exoskeleton cannot be manipulated as readily as those of a software avatar, so thetechnology and the training will be morecomplicated. It will be necessary to implant electrodes directly in the brain tomanipulate the robotic limbs. We willneed not only to place the electrodes under the skull in the brain but also to increase the number of neurons to be“read” simultaneously throughout thecortex. Many of the sensors will be implanted in the motor cortex, the region ofthe frontal lobe more readily associatedwith the generation of the motor program that is normally downloaded to thespinal cord, from which neurons directlycontrol and coordinate the work of ourmuscles. (Some neuroscientists believethat this interaction between mind andmuscle may be achieved through a nonin-

Science & Society Picture Library (artificial leg and Paré); Corbis (Civil War officer)vasive method of recording brain activity,like EEG, but that goal has yet to be practically achieved.)Gary Lehew in my group at Duke hasdevised a new type of sensor: a recordingcube that, when implanted, can pick upsignals throughout a three-dimensionalvolume of cortex. Unlike earlier brain sensors, which consist of flat arrays of microelectrodes whose tips record neuronalelectrical signals, Lehew’s cube extendssensing microwires up, down and sidewaysthrough out the length of a central shaft.The current version of our recordingcubes contains up to 1,000 active recording microwires. Because at least four tosix single neurons can be recorded fromeach microwire, every cube can potentially capture the electrical activity of between 4,000 to 6,000 neurons. Assumingthat we could implant several of thosecubes in the frontal and parietal cortices—areas responsible for high-level control of movement and decision making—we could obtain a simultaneous sampleof tens of thousands of neurons. According to our theoretical software modeling,this design would suffice for controllingthe flexibility of movement required tooperate an exoskeleton with two legs andto restore autonomous locomotion in ourpatients.To handle the avalanche of data fromthese sensors, we are also moving aheadon making a new generation of customdesigned neurochips. Implanted in a patient’s skull along with the microelectrodes, they will extract the raw motorcommands needed to manipulate a wholebody exoskeleton.Of course, the signals detected fromthe brain will then need to be broadcast tothe prosthetic limbs. Recently Tim Hanson, a newly graduated Ph.D. student atDuke, built a 128-channel wireless recording system equipped with sensors andchips that can be encased in the craniumand that is capable of broadcasting recorded brain waves to a remote receiver. Thefirst version of these neurochips is currently being tested successfully in monkeys. Indeed, we have recently witnessedthe first monkey to operate a brain-machine interface around the clock usingwireless transmission of brain signals. Wefiled in July with the Brazilian government for permission to use this technology in humans. For our future soccer ball kicker, thechronologyThe Long Road toBrain-Controlled ProstheticsReplacement limbs have existed for millennia—a rational response to the needto address war wounds or other types of trauma and birth defects. Today thetechnology is so sophisticated that an artificial limb can be controlled by electricalsignals channeled directly from the brain.1500–1000 B.C.FIRST HISTORICAL REFERENCEA Hindu holy book written during this periodmentioned Vishpala, who had a leg amputation aftera wound sustained during battle. She had the limbreplaced with an iron version that let her walk andreturn to her troops.Fourth Century B.C.Ancient artifactOne of the oldest artificial limbs discovered—a copyof which is shown here—was dug up in southern Italyin 1858. Fabricated in about 300 B.C., it was made ofcopper and wood and designed, it appears, for a belowknee amputee.14th CenturyGUNS AND AMPUTATIONSThe arrival of gunpowder at the European battlefrontgreatly amplified the number of injuries sustained bysoldiers. In response, in the 16th century AmbroiseParé, the royal surgeon for several French kings,developed techniques to attach both upper and lowerlimbs to patients and reintroduced the use of ligaturesto tie off blood vessels.1861–1865Civil WarThe War between the States resulted in many amputations.One person affected was Brigadier GeneralStephen Joseph McGroarty, who lostan arm. An influx of government funding and the avail ability of anesthetics that allowed for longer operationsimproved prosthetic technology during this era.1963 PRIMITIVE BRAIN INTERFACEJosé Manuel Rodriguez Delgado implanted a radiocontrolled electrode in the caudate nucleus deepin a bull’s brain and stopped the animal dead in itstracks by pressing a button on a remote transmitter;his device was a predecessor to contemporary brainmachine interfaces.1969 PIONEERING EXPERIMENTSEberhard Fetz of the University of Washingtonperformed a study in which monkeys were trainedto activate electrical signals in their brain to controlthe firing of a single neuron, duly recorded bya metal microelectrode.September 2012, ScientificAmerican.com 61

chronology1980sLISTENING TO BRAIN WAVESApostolos Georgopoulos of Johns Hopkins Universitydiscovered an electrical firing pattern in the motorneurons of rhesus macaques that occurred when theyrotated their arm in a particular direction.Early 1990s PLUGGING INJohn Chapin, now at S.U.N.Y. Downstate University,and Miguel A. L. Nicolelis introduced a techniquethat allowed for simultaneous recording of dozensof widely dispersed neurons using permanentlyimplanted electrodes, thus paving the way forresearch on brain-machine interfaces.1997 BETTER MOVESThe microprocessor-controlled C-Leg kneeprosthesis, which in its current version allowsthe wearer to turn on customized settings that can beused for activities such as bicycling, was introduced.1999–2000 GOOD FEEDBACKThe Chapin and Nicolelis laboratories publishedthe first description of a brain-machine interfaceoperated by activity from rat brains, wherebythe animals sensed the movement through avisual feedback signal. The following year theNicolelis lab published the first study in which amonkey controlled the movements of a roboticarm using only brain activity.2008–2011 BLADE RUNNERAfter failing to qualify for the 2008 SummerOlympics Games, Oscar Pistoriusswept the 2008 Summer Paralympic Games andthen got to the 400-meter semifinals at the 2011International Association of Athletics FederationsWorld Championships in Daegu, South Korea.2011 MONKEY THINK, AVATAR DONicolelis’s team at the Duke University Centerfor Neuroengineering demonstrated that amonkey was able to use thoughts to manipulatethe movements of a software avatar.2012 FROM MY BRAINTO MY ROBOT ARMJohn Donoghue of Brown University and hiscolleagues showed with their BrainGateneural interface system thata subject with a brain implant could manipulatea robotic arm to pick up a drink.2014 CYBORG OPENING KICKThe Nicolelis lab intends to provide anexoskeleton for a handicapped teenagerto make the first kick of the opening eventof the World Cup in Brazil.62 Scientific American, September 2012W H E R E W E’ R E H E A D E Ddata from the recording systems will berelayed wirelessly to a small computerprocessing unit contained in a backpack.Multiple digital processors will run various software algorithms that translatemotor signals into digital commandsthat are able to control moving parts, oractuators, distributed across the joints ofthe robotic suit, hardware elements thatadjust the positioning of the exoskeleton’s artificial limbs.force of brainpowerthe commands will permit the exoskeleton wearer to take one step and then another, slow down or speed up, bend overor climb a set of stairs. Some low-level adjustments to the positioning of the prosthetic hardware will be handled directlyby the exoskeleton’s electromechanicalcircuits without any neural input. Thespace suit–like garment will remain flexible but still furnish structural support toits wearer, a surrogate for the human spinal cord. By taking full advantage of thisinterplay between brain-derived controlsignals and the electronic reflexes supplied by the actuators, we hope that ourbrain-machine interface will literally carry the World Cup kicker along by force ofwillpower.The kicker will not only move but alsofeel the ground underneath. The exoskeleton will replicate a sense of touch andbalance by incorporating microscopicsensors that both detect the amount offorce from a particular movement andconvey the information from the suitback to the brain. The kicker should beable to feel that a toe has come in contactwith the ball.Our decade-long experience with brainmachine interfaces suggests that as soonas the kicker starts interacting with thisexoskeleton, the brain will start incorporating this robotic body as a true extension of his or her own body image. Fromtraining, the accumulated experience obtained from this continuous feeling ofcontact with the ground and the positionof the robotic legs should enable movement with fluid steps over a soccer pitchor down any sidewalk. All phases of thisproject require continuous and rigoroustesting in animal experiments before webegin in humans. In addition, all procedures must pass muster with regulatoryagencies in Brazil, the U.S. and Europe toensure proper scientific and ethical re-courtesy of otto bock healthcare (artificial leg); andrew medichini AP Photo (Pistorius);courtesy of miguel a. l. nicolelis (monkey avatar); courtesy of braingate2.org (BrainGate)BLIME Y OITS N DW H AT W E CA N D OWHO WE ARE

view. Even with all the uncertainties involved and the short time required forthe completion of its first public demonstration, the simple idea of reaching forsuch a major milestone has galvanizedBrazilian society’s interest in science inways rarely seen before.Remote Controlthe opening kickoff of the World Cup—ora similar event, say, the 2016 Olympicand Paralympic Games in Rio de Janeiro,if we miss the first deadline for any reason—will be more than just a one-timestunt. A hint of what may be possiblewith this technology can be gleaned froma two-part experiment already completed with monkeys. As a prelude, back in2007, our research team at Duke trainedrhesus monkeys to walk upright on atreadmill as the electrical activity ofmore than 200 cortical neurons was recorded simultaneously. Meanwhile Gordon Cheng, then at ATR Intelligent Robotics and Communication Laboratoriesin Kyoto, built an extremely fast Internetprotocol that allowed us to send thisstream of neuronal data directly to Kyoto, where it fed the electronic controllersof CB1, a humanoid robot. In the firsthalf of this across-the-globe experiment,Cheng and my group at Duke showedthat the same software algorithms developed previously for translating thoughtsinto control of robotic arms could alsoconvert patterns of neural activity involved in bipedal locomotion to maketwo mechanical legs walk.The second part of the experimentyielded a much bigger surprise. As one ofour monkeys, Idoya, walked on the treadmill in Durham, N.C., our brain-machineinterface broadcast a constant stream ofher brain’s electrical activity throughCheng’s Internet connection to Kyoto.There CB1 detected these motor commands and began to walk as well, almostimmediately. CB1 first needed some support at the waist, but in later experiments it began to move autonomously inresponse to the brain-derived commandsgenerated by the monkey on the otherside of the globe.What is more, even when the treadmill at Duke stopped and Idoya ceasedwalking, she could still control CB1’s legmovements in Kyoto by merely observing the robot’s legs moving on a live video feed and imagining each step CB1should take. Idoya continued to producethe brain patterns required to make CB1walk even though her own body was nolonger engaged in this motor task. Thistranscontinental brain-machine interface demonstration revealed that it ispossible for a human or a simian to readily transcend space, force and time byliberating brain-derived commands fromthe physical limits of the biological bodythat houses the brain and broadcastingthem to a man-made device located farfrom the original thought that generatedthe action.These experiments imply that brainmachine interfaces could make it possible to manipulate robots sent into environments that a human will never be ableto penetrate directly: our thoughts mightoperate a microsurgical tool inside thebody, say, or direct the activities of a humanoid worker trying to repair a leak at anuclear plant.The interface could also control toolsthat exert much stronger or lighter forcesthan our bodies can, thereby breaking freeof ordinary constraints on the amount offorce an individual can exert. Linking amonkey’s brain to a humanoid robot hasalready done away with constraints imposed by the clock: Idoya’s mental triparound the globe took 20 milliseconds—less time than was required to move herown limb.Along with inspiring visions of the farfuture, the work we have done with monkeys gives us confidence that our planmay be achievable. At the time of thiswriting, we are waiting to see whetherthe International Football Association(FIFA), which is in charge of organizingthe ceremony, will grant our proposal tohave a paraplegic young adult participatein the opening ceremony of the inauguralgame of the 2014 World Cup. The Brazilian government—which is still awaitingFIFA’s endorsement—has tentatively supported our application.Bureaucratic difficulties and scientificuncertainties abound before our visionis realized. Yet I cannot stop imaginingwhat it will be like during the brief buthistoric stroll onto a tropical green soccerpitch for three billion people to witness aparalyzed Brazilian youth stand up, walkagain by his or her own volition, and ultimately kick a ball to score an unforgettable goal for science, in the very land thatmastered the beautiful game.m o r e t o e x pl o r eControlling Robots with the Mind. Miguel A. L. Nicolelis and John K.Chapin in Scientific American, Vol. 287,No. 4, pages 46–53; October 2002.Cortical Control of a ProstheticArm for Self Feeding. Meel Vellisteet al. in Nature, Vol. 453, pages 1098–1101; June 19, 2008.Beyond Boundaries: The New Neuroscience of Connecting Brains withMachines—and How It Will ChangeOur Lives. Miguel Nicolelis. St. Martin’s Griffin, 2012.Scientific AmericanOnlineInspect an exoskeletonprototype at Scientific American.com/sep2012/exoskeletonSeptember 2012, ScientificAmerican.com 63

For our future soccer ball kicker, the chronology 1500–1000 B.C. FIRST HISTORICAL REFERENCE a Hindu holy book written during this period mentioned Vishpala, who had a leg amputation after a wound sustained during battle. She had the limb replaced with an iron version that let her walk and return to her troops. The Long Road to

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