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Beyond the Neuron Doctrine New Experiments Sliced the Heart in Two with a Big Kitchen Knife

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Beyond the Neuron Doctrine New Experiments Sliced the Heart in Two with a Big Kitchen Knife 20 SCIENTIFIC AMERICAN MIND June/July 2006 ESSAY Beyond the Neuron Doctrine New experiments sliced the heart in two with a big kitchen knife. All was revealed—the four chambers separated by moist, are settling gristly valves that suck blood into auricles and a century-long squeeze it out ventricles. Eleven years old and fasci- debate between nated, I asked my mother if, next time, she could Ibring me a brain. When she returned from the butcher shop two camps over with a calf brain, I beamed and cleaved the melon in two. how neurons But inside I saw nothing notable. Just a hollow cavity at the core of a fl eshy mush. communicate. AS How did it work? Books offered names for its bumps and The surprise: M both sides folds but failed to provide a detailed explanation for how this supreme organ functioned. My parents, teachers—no are right one seemed to have the answer. Today we know the brain’s power comes from compo- nents so miniaturized they are invisible. But even though technology now allows us to see individual neurons, our VOL. 310; NOVEMBER 4, 2005, © AA , models of how they function en masse are still inadequate. REPRINTED PERMISSION WITH FRO We like to think of each cell as a microprocessor linked to SCIENCE billions of others. But how sure can we be that this analogy is accurate? Are we held captive by our analogies just as NIH Medical Arts, Medical NIH tightly as the scientists who preceded us were bound by their own now obsolete ideas? DON BLISS T. H. BULLOCK ET AL. IN By R. Douglas Fields www.sciammind.com SCIENTIFIC AMERICAN MIND 21 Camillo Golgi Santiago Ramón y Cajal The answer is yes. The discoveries are con- One man looking at this world saw some- vincing neuroscientists that our fundamental thing different, however. The great Spanish anat- concept of how the brain works is naive. Yet iron- omist Santiago Ramón y Cajal was at heart an ically, the two prevailing models, which have artist. As a boy, he sketched cadavers dissected been at odds since their founders were jointly by his physician father before he, too, became a awarded the Nobel Prize 100 years ago, are both doctor. With an artist’s ability to see motion in relevant. Indeed, by joining the models and add- the curve of a line, Ramón y Cajal began to see a ing a third, yet unanswered piece to the puzzle logic in the tangle of cells and pipes. His vision, raised by recent research—how brain cells give hotly contested for the next 50 years, became rise to brain waves—we can fi nally explain not known as the neuron doctrine. only how the human brain works but also what Ramón y Cajal observed that a single, long ) makes it unique in the animal world. axon running from one neuron tended to end in right a fi eld of dendrites—other, short tubes attached Networked or Isolated to another neuron. He maintained, however, that Analogies are helpful because they make com- the tubes were not interconnected everywhere. In plicated situations more accessible. But such sim- a brilliant deduction, Ramón y Cajal concluded plifi cation also encourages rigid thinking. As the that each neuron was an island unto itself, not a 20th century approached, anatomists probed the node in a network. Moreover, he surmised that brain with the most powerful instrument avail- information fl owed in one direction: into den- able: the newly perfected microscope. They drites, then through a neuron cell body, and out ); THE NOBEL FOUNDATION ( left peered into an invisible world of baffl ing com- its axon. plexity, a densely tangled mass of microscopic, Furthermore, the axon did not connect with interconnected fi bers. Anatomists naturally pre- the dendrites. It remained separated by a minus- sumed that these tiny tubes, called axons, were cule gap, or synapse. This gap functioned as a like pipes, plumbed into a Byzantine network that switch that allowed information to pass to the allowed sensations and commands to fl ow freely next neuron—or not. The space of separation to wherever they were required. The neuron was was so small it was beyond the resolution of the simply a node in the interconnected network. best microscopes. Scientists would not get their RESEARCHERS,PHOTO ( INC. 22 SCIENTIFIC AMERICAN MIND June/July 2006 fi rst fuzzy glimpse of the synapse until the 1950s, connection appeared to be direct and electrical. when focused electron beams replaced light When the electron microscope finally re- beams in microscopes. vealed the synapse in 1955, scientists again were In 1906 the Nobel Prize in Physiology or faced with evidence for both sides. There was no Medicine was awarded jointly to Ramón y Cajal longer any doubt that neurons were stand-alone and his rival, Italian physician Camillo Golgi. entities or that they communicated across the gap The unusual pairing sparked a standoff in mod- using chemical messengers. But some images eling how the brain works that is only being set- showed individual neurons to be connected to tled today, on the award’s centennial. Like many one another, as though spot-welded. Researchers others, Golgi assailed the validity of the neuron soon determined that protein channels, called doctrine and vigorously defended the free-fl ow- gap junctions, formed these welds—like a short ing network view of the brain. The great irony coupling that joins two hoses. Ions and organic was that Ramón y Cajal used an ingenious lab molecules passed freely, allowing impulses to technique Golgi had invented to provide evidence speed directly from one neuron to the next. Neurons can release neurotransmitters far away from ()synapses, an overlooked form of communication. for his neuron doctrine. Golgi had devised a way Transmission of signals across “chemical” to stain nerve cells with silver nitrate, making synapses—the basis for learning and memory— their features visible against background tissue. could be regulated by the release or uptake of For reasons that are still not understood, the Gol- neurotransmitters, so they drew most of the at- gi method stains only a fraction of neurons in a tention from neuroscientists. In contrast, “elec- sample, but the neurons that absorb the stain are trical” synapses appeared static, and their role in revealed in exquisite detail. Ramón y Cajal’s pen- brain function was much less interesting. Electri- and-ink drawings of Golgi-stained neurons were cal synapses seemed peculiar, relevant only when the basis of his theory. Golgi was backed into the very rapid communication was necessary or uncomfortable predicament of arguing that his when a bunch of neurons needed to be tethered marvelous Nobel Prize–winning procedure was to a group. merely producing an artifact when it showed Yet recent work by neuroscientist Michael neurons as individual cells. V. L. Bennett of Albert Einstein College of Med- icine and others shows that simple view to be Welded Together wrong: conduction through gap junctions can be The debate between doctrinaires who support- regulated by changes in the voltage of cell mem- ed Ramón y Cajal’s neuron doctrine and reticular- branes and by biochemical reactions that control ists (from the Latin for “network”) who supported the size of the channel through the junction. Golgi’s scheme raged for decades because every There are even cases where chemical and electri- new tool turned up evidence fueling both argu- cal synapses form together at the same junction. ments. For example, electrophysiologists, using One thing is certain: Golgi was right. Neurons electrodes and electronic amplifi ers to study the can be networked together. transmission of electrical signals from axon to dendrite, proved in fi ne detail that when an im- A Changing Tide pulse reached the end of an axon, the axon re- Whether signals travel one way down a chain leased chemical substances called neurotransmit- of neurons or back and forth across a network, ters. This event was followed by a delay of about using chemical or electrical messengers, even 1/1,000 of a second, as the substances diffused more fundamental questions remain: What do across the tiny synapse and stimulated an electri- the signals mean? How do traveling impulses cal response in the neighboring dendrite. Yet in translate into a visual image, a feeling, a thought? some cases, the recordings showed that an electri- What’s the code? Neither model has provided an- cal signal swept from axon to dendrite with no swers, yet proponents have generated surprising delay at all, as if the two nerve cells were fused. insights that undermine the exclusivity of each No neurotransmitters were involved, and the theory. www.sciammind.com SCIENTIFIC AMERICAN MIND 23 One of the great discoveries made in examin- firmed that many such neurons did not emit ing the neuron doctrine is that neural impulses sharp, spiked impulses at all. (called action potentials) carry information in These small, tightly packed “interneurons” one direction, from the cell body to the axon tip. process information within internal circuits of Every morsel we taste, every idea we have, is de- the brain, rather than communicating directly scribed by a pattern of impulses fi ring through with the body or environment as motor and sen- axons. Neuroscientists were eager to decipher sory neurons do. Interneurons are concerned this code, and they did. They found that the with the fundamental, internal workings of the codebook changes constantly depending on the brain rather than with transmitting commands Glia broadcast signals across hardwired neurons, ()coupling them together into functional groups. prior history of stimulation. The same frequency or sensations, and the neuron doctrine did not fi t of impulses might signify very bright light when well for many of these internal processors.
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