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Beyond Boundaries
The New Neuroscience of Connecting Brains with Machines-and How It Will Change Our Lives
By Miguel Nicolelis Henry Holt and Company
Copyright © 2011 Miguel Nicolelis
All rights reserved.
ISBN: 978-1-4299-5079-4
CHAPTER 1
WHAT IS THINKING?
By the time the rainy days of the tropical autumn of 1984 arrived, most Brazilians had had enough. For twenty years, their beloved country had been ruled by a vicious dictatorship, brought to power by a military coup d'état that triumphed, emblematically, on April Fools' Day 1964. For the next two decades the military regime built an infamous legacy, marked primarily by its rampant incompetence, widespread corruption, and shameful political violence against its own people.
By 1979, thanks to the growing popular opposition to the regime, the latest four-star general installed in the presidential palace had no alternative but to grant amnesty to the political leaders, scientists, and intellectuals who had fled into exile abroad. A gradual, controlled return to civilian rule had been mapped out by the generals, beginning with popular elections for state governorships in the fall of 1982.
That November, the opposition parties won by a landslide. By the next year, however, that small token of democracy had been all but forgotten. Brazilians realized they had the right and, more importantly, the power to demand more than a dictator's political bread crumbs. They wanted to oust the military government, but not through another coup d'état. Instead, they wanted to vote it into retirement through a direct election for president. That is how, seemingly out of nowhere, a nationwide movement demanding immediate direct elections for president (diretas já in Portuguese) broke loose. The first rally took place in the tiny northeastern city of Abreu e Lima on March 31, 1983. By November, a somewhat shy crowd of ten thousand people had gathered to protest in Brazil's most populous and wealthy city, Sào Paulo. From that point, the movement grew exponentially. Two months later, on January 25, 1984, the day Sào Paulo celebrated its 430th anniversary, more than two hundred thousand people were chanting their collective demand for immediate presidential elections. In a matter of days, gigantic crowds started to converge on the main squares of Rio de Janeiro, Brasilia, and other major cities.
On the evening of April 16, 1984, more than one million people congregated in the heart of downtown Sào Paulo to participate in the largest political rally ever staged in the country's history. In a matter of hours, a river of people, most dressed in the Brazilian national colors, green and yellow, inundated the valley where the city was originally founded. Every new group of people that arrived immediately joined into an already familiar, two-word rhythmic chant that erupted briskly somewhere in the crowd, every minute or so, and spread like thunder through space: "Diretas já, diretas já" (Elections now, elections now). If you have never taken part in a chorale formed by one million people, I recommend the experience. Nothing can prepare you for its penetrating sound, and nothing this side of the Milky Way will allow you to forget it. It is the sort of sound that carves memories for a lifetime.
Pressed by the ever-increasing flow of people, I climbed to the roof of a newsstand and, for the first time that night, gained a panoramic view of the entire citizenry that was conquering Sào Paulo's Anhangabaú Valley with its two-word song. For the long-vanished Tupi-Guarani, the native Indian tribe that inhabited that land before the Portuguese arrived in the sixteenth century, the stream that had run through the valley was known as the "river of the bad spirits." Not anymore. That night, the only river visible was a mighty Amazon of people. No bad spirit would have dared to exert itself in such a purposeful human ocean.
"What do we want?" part of the crowd spontaneously asked.
"Diretas" (elections), the rest of us answered.
"Quando" (when)? another group provoked.
"Já, já, já!" (now, now, now!) the whole crowd screamed back.
When that million-people choir began to sing the Brazilian anthem, not even the sky could hold its tears anymore. As the traditional Sào Paulo drizzle descended, I absorbed this resounding demonstration of what a population of individuals can do when they collaborate in harmony to achieve a common goal. Even though the message transmitted by the crowd (Diretas já!) was always the same, at any moment in time, a different combination of many voices was recruited to produce the crowd's roar. People weren't necessarily able to scream every time. Some were talking to their neighbors; others became temporarily hoarse, or were distracted while waving their flags; others simply dropped out of the chorale due to sheer emotion. Moreover, even as handfuls of people began to leave the rally later on, the crowd continued to thunder. For any observer, the loss of those few protesters did not make any difference at all — the overall potential population was so huge that the loss of a few people did not meaningfully alter the result.
Ultimately, the voices of those millions of Brazilians were heard. A few days later, I met with my mentor, Dr. César Timo-Iaria, to discuss a paper by David Hubel and Torsten Wiesel, who had shared the Nobel Prize in Physiology or Medicine in 1981 for their groundbreaking research on the visual cortex. Hubel and Wiesel had recorded the electrical activity of single neurons in the visual cortex, using the classical reductionist approach that was the norm in labs around the world at the time. I innocently asked Timo-Iaria why we did not do the same. His reply was as forceful as the roar that I had experienced as a member of the crowd in Sào Paulo: "We do not record from a single neuron, my son, for the same reason that the rally you attended a few days ago would be a disaster if, instead of one million people, only one person had showed up to protest," he said. "Do you think that anyone would pay attention to the plea of a single person screaming at a political rally? The same is true for the brain: it does not pay attention to the electrical screaming of a single noisy neuron. It needs many more of its cells singing together to decide what to do next."
* * *
Had I been more observant on that historic night in 1984, I may have understood that the dynamic social behavior of that thundering crowd had set before me most of the neurophysiological principles that I would obsessively investigate over the next quarter of a century. But instead of listening to a chorus of political protesters, I would be listening for the virtually unheard electrical symphonies created by large populations of neurons.
These neural ensembles would eventually provide the means for liberating a primate brain from its biological body. But in the mid-1980s, very few neuroscientists saw any reason to relinquish the reductionist experimental paradigm and its focus on single neurons. Perhaps this was because other scientific fields, including particle physics and molecular biology, had experienced extraordinary success with reductionism; in particle physics, for instance, the theory and ultimate discovery of smaller and smaller particles, such as quarks, proved to be a linchpin in the definition of the so-called standard model, which continues to be the basis of our understanding of the physical universe.
Roughly speaking, in mainstream twentieth-century neuroscience, the reductionist approach meant breaking the brain into individual regions that contained a high density of neurons, known as brain areas or nuclei, and then studying the individual neurons and their connections within and between each of these structures, one at a time and in great detail. It was hoped that once a large enough number of these neurons and their connections had been analyzed exhaustively, the accumulated information would explain how the central nervous system works as a whole. Allegiance to reductionism led most neuroscientists to dedicate their entire careers to describing the anatomical, physiological, biochemical, pharmacological, and molecular organization of individual neurons and their structural components. This painstaking and wonderful collective effort generated a tremendous wealth of data from which many outstanding discoveries and breakthroughs resulted. With the unfair benefit of hindsight, today one could argue that neuroscientists were trying to decipher the workings of the brain in the same way as an ecologist would attempt to study the physiology of a single tree at a time in order to understand the rain forest ecosystem, or an economist would monitor a single stock to predict the stock market, or a military dictator would try to arrest a single protester at a time to reduce the effectiveness of a million-strong Brazilian chorus chanting diretas já in 1984.
For an observer who benefits today from the century-old work of the true giants of brain research, it seems that what much of neuroscience still lacks is an experimental paradigm for dealing with the complexity of brain circuits. Today, systems formed by large numbers of interacting elements — things like a political movement, the global financial market, the Internet, the immune system, the planet's climate, and an ant colony — are known as complex systems whose most fundamental properties tend to emerge through the collective interactions of many elements. Typically, such complex systems do not reveal their intimate collective secrets when approached by the reductionist method. With its billions of interconnected neurons, whose interactions change from millisecond to millisecond, the human brain is an archetypal complex system.
Part of the neglect toward exploring the complexity of the brain could be justified by the tremendous experimental challenges involved in "listening" simultaneously to the electrical signals produced by large numbers of individual single neurons, distributed across multiple brain areas, in a behaving animal. For example, at the time Brazilian crowds were fighting for presidential elections, no one in the neuroscience community was sure what type of sensor could be implanted in the brains of animals so that many of these minute neuronal electrical signals could be sampled simultaneously for many days or weeks, while subjects performed a variety of behavioral tasks. Moreover, there was no electronic hardware or sufficiently powerful computer available that neurophysiologists could readily utilize to filter, amplify, display, and store the electrical activity generated by tens of individual neurons simultaneously. Neurophysiologists wondered, almost in despair, how they might choose which neurons to record from in each brain structure. Worst of all, nobody had any idea how to analyze the huge mountain of neurophysiological data that would be generated in case these technical bottlenecks could somehow be solved.
Paradoxically, few neuroscientists ever doubted that the astonishing feats accomplished by the human mind — from the production of artificial tools to the generation of self-awareness and consciousness — arise from the brain's huge number of neurons combined with their intricate pattern of massive parallel connectivity. But for decades, any attempt to tackle the technical hurdles to listen to brain symphonies was dismissed as a chimera, a high-tech experimental utopia that might only be realized through an effort on the scale of the Manhattan Project.
Essentially, all expressions of human nature ever produced, from a caveman's paintings to Mozart's symphonies and Einstein's view of the universe, emerge from the same source: the relentless dynamic toil of large populations of interconnected neurons. Not one of the numerous complex behaviors that are vital for the survival and prosperity of our species — or, for that matter, of our close and distant cousins, primates and mammals — can be enacted by the action of a single neuron, no matter how special this individual cell may be. Thus, despite the great deal we have learned about how single neurons look and function, and despite innumerous scientific achievements of brain research for the past century, the straightforward application of reductionism to brain research has proven to be insufficient and improper as a strategy to deliver the field's most cherished promise, a comprehensive theory of thinking.
All this means that the traditional and well-disseminated view of the brain, the one espoused in artful prose and beautiful illustrations in most of the neuroscience textbooks, can no longer stand. In much the same way that Einstein's theory of relativity revolutionized the classic view of the universe, the traditional single neuron–based theory of brain function needs to be categorically replaced by what amounts to a relativistic view of the mind.
* * *
The first step in proposing any new scientific theory is to define a proper level of analysis for investigating phenomena and testing one's hypothesis about them. This allows for validating or falsifying the proposed theory — the essence of the scientific method. I contend that the most appropriate approach to understanding thinking is to investigate the physiological principles that underlie the dynamic interactions of large distributed populations of neurons that define a brain circuit (see Fig. 1.1). Neurons transmit information to one another through long, projecting structures — their axons — which make discrete, noncontinuous contact (the synapse) with nerve cell bodies and their protoplasmic, treelike structures, called dendrites. In my view, while the single neuron is the basic anatomical and information processing-signaling unit of the brain, it is not capable of generating behaviors and, ultimately, thinking. Instead, the true functional unit of the central nervous system is a population of neurons, or neural ensembles or cell assemblies. Such a functional arrangement, in which populations of neurons rather than single cells account for the information needed for the generation of behaviors, is also commonly referred to as distributed neuronal coding.
Thinking with populations of neurons! Even two of humanity's most intimate possessions — a sense of self and a body image — are fluid, highly modifiable creations of the brain's mischievous deployment of electricity and a handful of chemicals. They both can change or be changed on less than a second's notice. And, as we will see, they do.
During the first half of the twentieth century, so-called single-neuron neurophysiologists argued, with seemingly incontrovertible evidence, that after sensory information was sampled from the external world through specialized receptors — the skin, retina, inner ear, nose, and tongue — it ascended through specific sensory nerve pathways that terminated in specific cortical areas. These areas were identified as the primary sites for processing sensory information in the cortex, with the somatosensory (tactile), visual, and auditory areas gaining particular prominence. During the same period, however, an American psychologist, Karl Lashley, emerged as the poster boy for the opposition: the distributionist camp. Lashley's main obsession was to identify the location in which the brain stores a memory, which he called the engram. In his experiments, he would surgically remove cortical tissue from various areas of the brains of rats, monkeys, and apes, both before and after the animals had been taught to perform particular behaviors, which ranged from simple tasks (learning how to identify a particular object visually and then jump or reach for it) to complex problem solving (learning how to navigate an elaborate maze). After an animal was trained, he measured the impact of the cortical lesions he had created on the animal's capacity to acquire or retain the behavioral skill, or habit, it had learned. With this experimental process, he aimed to understand how associations were built between sensory information and motor behavior.
According to Lashley, after animals had been trained in a simple task, much of the remaining cortex could be removed without affecting significantly the animal's behavioral performance — provided that some volume of the primary sensory cortex involved in the task was left intact. In fact, if just one-sixtieth of the primary visual cortex remained, the animal would retain a visual-motor habit it had learned. Faced with simple tasks, the brain was amazingly resilient in handling sensory information. In his classic article, "In Search of the Engram," Lashley summarized his results as the "principle of equipotentiality," whereby memory traces were distributed throughout the sensory area, not in a specific neuron or small group of neurons.
(Continues...)
Excerpted from Beyond Boundaries by Miguel Nicolelis. Copyright © 2011 Miguel Nicolelis. Excerpted by permission of Henry Holt and Company.
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