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Authors: Luke Dittrich

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The functions of the limbic lobe were an almost unmitigated mystery. For years, a popular view based on studying a few anosmic patients—people unable to detect odors—held that the sole function of the limbic lobes was to enable our sense of smell. (An alternative name for the limbic lobes, in fact, was the olfactory cortex.) In the decade before Milner's arrival at the Neuro, however, that view had begun to change. Critically, the studies conducted by Paul Bucy and Heinrich Klüver at the University of Chicago, where chimpanzees tripping on mescaline had their temporal lobes removed bilaterally, seemed to indicate that more important functions than smell were at stake in the region.

Wilder Penfield, for one, had a feeling that the limbic lobe, and in particular its central and largest organ, the hippocampus, must serve an important purpose. This was based in large part on aesthetic reasons: He found it hard to believe that such a delicately formed, and in his view beautiful, structure—a structure that he'd noticed seemed to be directly connected by neural tracts to most of the other major structures in the brain—would be useless. The hippocampus didn't look like some sort of vestigial, peripheral throwback, a cerebral appendix. Nestled there in the center of our heads, enigmatic but interconnected, it looked crucial.

Brenda Milner reviewed the existing literature on the temporal lobes. Two things were clear to her.

One, the purpose of the hippocampus and its limbic brethren remained a mystery.

Two, she was in as good a position as anyone in the world to solve it.

—

She began working with Penfield's patients.

She would spend time with them before their operations, getting to know them, conducting long interviews, and writing up detailed impressions of everything she could think of, from their style of dress to their sense of humor. She would complement these subjective notes with extensive batteries of tests, measuring their intelligence, their memories, their problem-solving abilities, their temperaments.

On the day of the operation, she would often watch Penfield in action. There was no particular reason she had to be in the OR; she simply found it fascinating. She would squeeze down a narrow hallway that led to the spectators' gallery of operating room 2, Penfield's preferred arena, on the second floor. The gallery was cramped, with three rows of wooden benches fronting a large glass window overlooking the so-called operating theater. The gallery was almost always crowded with residents and visiting doctors coming to see the master at work. Another fixture there was the electrophysiologist Herbert Jasper, whose EEG (electroencephalograph) machine was installed front and center in the gallery, receiving electrical information from the sensors Penfield placed on the surface of his patients' brains. Jasper interpreted the signals and relayed those interpretations back to Penfield out loud to help guide the knife. In addition, there was always a secretary present to transcribe Penfield's observations as well as any comments made by the patient. And that was the most fascinating part for Milner: watching and listening to the patients as they responded to the direct manipulation of their brains.

Penfield quickly and deftly used his electrode, and the reactions it provoked, to orient himself so that he always had a sense of where the motor and somatosensory cortices were, ensuring that he wouldn't inadvertently cause paralysis or permanent numbness. In a similar way, he mapped out and identified all the other critical landmarks, like the auditory cortex, so that he wouldn't leave deafness or other deficits in his wake. Then he dug in, finding the area that intuition and electricity told him was responsible for his patient's disease and destroying it. The spectators in the gallery usually applauded at the operation's conclusion, before Penfield cleaned up and the nurses wheeled the patient off to the recovery room.

A few days later, once the swelling had subsided, Milner would meet with the patient again, pull out her notebook, and resume her testing.

—

For months, she came up empty.

She met and tested dozens of patients, watched them go under the knife, then retested them afterward. Almost all were helped by the operations: During the preoperative testing, Milner grew accustomed to the sessions being interrupted by seizures, which would manifest themselves as verbal tics or physical movements or momentary, blank-eyed absences. After the operations, these seizures came less frequently or not at all. As for whatever other changes Penfield's operations were causing—the changes she had come to the Neuro to ferret out—they appeared to be either too small to perceive or not testable by the methods she was employing. Or maybe they didn't exist at all? Was that possible? Could the removal of such an extensive portion of central structures in the brain truly have a negligible effect?

One of Milner's problems was that Penfield's operations were unilateral. In other words, he was removing only half of his patients' limbic lobes. The opposite hemisphere was no doubt compensating for most of the loss, which made finding deficits more challenging. There was no way around this. Penfield wasn't going to bilaterally lesion brain structures whose functions were unknown. To do so, he believed, would be a terrible thing, analogous to playing Russian roulette with his patients. Maybe they would only lose something minor, such as their sense of smell. But could he justify the risk?

What if they lost something more important?

Milner understood this. The humans she was studying weren't lab rats or chimpanzees, to be sacrificed at will. They were, above all, patients, and the mandate of the Montreal Neurological Institute was to make them better. Their role as research subjects was strictly secondary, and Milner believed that the lure of making scientific discoveries should never trump their safety.

Nevertheless, it was frustrating. Patient after patient, test after test, day after day, very little discernible change. This didn't mean that the patients weren't each interesting in their own right, or that there weren't minor breakthroughs along the way. They were, and there were. Everyone had their own story, and she took satisfaction in getting to know them all. There was the twenty-three-year-old bank clerk from Ann Arbor, Michigan, for example, whose physician had sent him to Montreal after nine years of chronic psychomotor epilepsy. The origin of his disease was unclear, though it may have had something to do with a case of the measles he'd contracted at the age of ten. His seizure pattern was odd: Suddenly, at unpredictable times, he would stop whatever he was doing and then say the word
yes
. Then he would turn his head slowly to the left and contort his face in that direction as well, while staring into space. “This would be followed,” Brenda Milner noted, “by symmetrical licking movements.”

Milner ran her gamut of tests on the bank clerk preoperatively, watched the operation, and then reran the tests afterward. Two days after the operation, the patient became aphasic, unable to speak, and the lower portion of one side of his face sagged, as though he'd been stricken with Bell's palsy. Both the aphasia and the facial paralysis were, as Milner recorded, “transient,” likely just the result of the intracranial swelling that occurs after any brain operation. Those negative symptoms soon disappeared, and three days after the operation he seemed to recover most of his faculties. One of the tests she ran that day involved asking him to reproduce, from memory, a series of four geometric drawings that she'd shown him six days earlier, three days prior to the operation. He reproduced three of the four drawings perfectly, an accomplishment that would have been impressive for anyone, even a person who had not just experienced a procedure in which “the anterior portion of the left temporal lobe was removed, going back 5 cm along the lateral surface and 6.5 cm along the base.”

Then, more than a year into Milner's study of Penfield's patients, she sat down with Patient P.B., the civil engineer who'd received the same operation. She told him those stories about a mugging victim named Anna Thompson and a boat trip across perilous seas, and found that the stories slipped almost immediately out of his mind. She struggled to understand it. Why had the operation had an effect on him that it hadn't on anyone else? Why had it seemingly left him amnesic, while it left the memory systems of other patients, who'd undergone almost identical procedures, intact?

Soon afterward, she sat down with another patient, a twenty-eight-year-old man, Patient F.C., who worked as a glove cutter in a factory. He'd suffered from epilepsy since a young age, and after several years of treatment with antiseizure medications, he decided to undergo Penfield's operation at the Neuro. The operation took place on October 21, 1952, and by the time Milner reexamined him weeks later, the swelling had subsided, although there was a large reddish crescent-shaped scar slightly visible on the right side of his cranium, under his lengthening hair. Milner told him the first story, the one about the mugging victim in South Boston, and asked him to repeat it back to her.

“Anna Thompson,” he said tentatively, looking at her for support. “She robbed fifteen dollars. She had four children.”

When working with patients, Milner tried to keep her face composed and not betray anything she was thinking, so as not to give them clues as to how they were doing or cues that might influence their answers. She nodded, made some notes, then told him the next story, reading it out, as always, clearly and carefully.

“The American liner
New York,
” she said, “struck a mine near Liverpool Monday evening. In spite of a blinding snowstorm and darkness the sixty passengers, including eighteen women, were all rescued, though the boats were tossed about like corks in the heavy sea. They were brought into port the next day by a British steamer.”

As soon as she finished, she asked him to repeat it back to her.

“They were brought into port by a steamer,” he said, echoing the last line he had heard. Then he stopped. He was unable to add any more detail.

Milner asked him to recall the first story.

“It seems to me you mentioned Anna Thompson,” he said. “It was brought into the sea.”

She made some additional notes, administered some additional tests. About an hour and a half later, before the patient left for the day, she asked him to recount anything he could remember about the two stories she had told him.

He looked at her blankly.

SEVENTEEN
PROUST ON THE OPERATING TABLE

A
few years ago two friends of mine got married on Sifnos, a beautiful Greek island. I rented a small apartment right on the beach, and my daughter, Anwyn, and I flew and ferried there from our home in Whitehorse, in Canada's Yukon Territory. We stayed for a week. Anwyn was five years old, and Sifnos was the greatest playground she'd ever seen. Turquoise water, bright sun, breakfasts of fresh yogurt and honey; goats and cats roaming down whitewashed ancient alleys. Countless scenes of wonderful strangeness imprinted themselves indelibly upon her memory, like the potbellied man we saw some mornings down by the water, holding a cellphone to his ear with one hand while using a broomstick in the other to swish a huge, fresh-caught octopus back and forth along the ground, tenderizing it.

At night, sandy and sunburned and exhausted, we read stories from
D'Aulaires' Book of Greek Myths,
which I had bought for the trip. Anwyn loved the story of Hermes most, loved his mischievousness, his cleverness, his cheekiness. When Hermes's mother accused him of stealing a herd of cows from Apollo, Hermes feigned innocence, saying, “But I'm just an innocent baby.” When I read that line to Anwyn I'd stretch the word
baby
out like taffy, amping up the whininess. The line quickly became one of Anwyn's own catchphrases, and she started lobbing it back at me anytime she could.

“But I'm just an innocent baaaaa­aaaaa­by!”

She loved the story of Artemis the Huntress, too, and Hercules, and blustering, trident-waving Poseidon. She loved that near the front of the book there was a map of Greece and its islands and that it wasn't hard to imagine these tales we were reading taking place somewhere that looked very much like Sifnos. One afternoon, exploring some steep, thorny hills high above a rocky beach, we found some old stone walls in front of a small, empty cave. She wondered about the history of the cave and whether any gods had ever visited it.

Toward the end of the week, we came to a scene in the book that was a pleasing mirror to the scene we were living. It was a Greek myth about a parent telling the Greek myths to her children.

“The nine muses were the daughters of Zeus and the Titaness Mnemosyne,” it read. “Their mother's memory was as long as her beautiful hair, for she was the goddess of memory and knew all that had happened since the beginning of time. She gathered her nine daughters around her and told them wondrous tales. She told them about the creation of earth and the fall of the Titans, about the glorious Olympians and their rise to power, about Prometheus, who stole the heavenly fire, about the sun and the stars….The nine muses listened to her with wide, sparkling eyes and turned her stories into poems and songs so they would never be forgotten.”

Anwyn listened closely, looking at the colorful drawing of the nine muses and their beautiful, long-tressed mother. Then her eyes grew heavier and heavier until they finally closed.

—

Sometimes strange things happened in Wilder Penfield's operating room.

Once, while he was in the preliminary stages of operating on an epileptic patient with the initials S.B., Penfield determined that S.B.'s epileptogenic focus was somewhere in his right medial temporal lobe, then opened up that side of his skull and began seeking out the culprit. To avoid inadvertently destroying something he shouldn't, he first probed with his electrode to locate the borders of the auditory, motor, speech, and visual cortices, getting a feel for his patient's neural landscape. As Penfield probed near a large vein that rose upward from a portion of the surface of the brain known as the fissure of Sylvius, S.B. began to speak.

“There was a piano there and somebody playing! I could hear the song.”

Penfield paused. He removed the electrode, waited a beat, then placed it in exactly the same place. This time, the song came into focus. “Yes,” S.B. said. “ ‘Oh Marie, Oh Marie!' Someone is singing it.” Again Penfield stimulated the point, and again S.B. heard the song. This time, S.B. explained that it was the theme song to a radio program he listened to.

Penfield removed the electrode and touched it to another spot nearby.

“Something brings back a memory,” S.B. said. “I can see Seven-Up Bottling Company…Harrison Bakery.”

Penfield was puzzled. He wondered if the patient was inventing these visions, making things up because he knew he was being stimulated. He decided to test this. He told the patient that he was about to place the electrode on his brain again. But, instead of placing it, he simply held it above the surface of the cortex, not touching it.

“Nothing,” S.B. said.

A second, similar episode involved a woman with the initials D.F. That time, the point that elicited the response was within the fissure of Sylvius itself. In her case, the patient began hearing music, an orchestral arrangement of a popular song. Whenever Penfield stimulated this particular spot, D.F. reported that the same piece of music leapt into her mind. She even hummed along, accompanying the song for a full chorus and verse.

Whenever one of these odd, electrode-provoked delusions happened, a secretary in the gallery overlooking the OR made sure to record every detail. In one patient, Penfield's probing triggered a vision of a dog walking along a country road. Another time, a female patient began to hear a voice speaking faintly, indecipherably. Penfield moved the electrode slightly to a different part of her brain, and the voice came into focus: Somebody was calling out a single name, over and over: “Jimmie, Jimmie, Jimmie…” Jimmie was the name of the patient's husband. And once, when Penfield stimulated a point near the top of a twelve-year-old boy's right temporal lobe, the boy announced that he could hear a telephone conversation between his mother and his aunt. Penfield removed the electrode, and the conversation stopped. As soon as he reapplied it, the conversation resumed. “The same as before,” the boy said. “My mother telling my aunt to come up and visit us tonight.” Penfield asked the boy how he knew the conversation was taking place over the telephone, and the boy said that he could tell by the way the conversation sounded, and he knew his mother was on the line with his aunt because he recognized the tone of voice she used when speaking with her sister. Penfield tried again to determine if the patient was just making things up and concluded that the boy was an accurate witness. “Every effort was made to mislead him by stimulations without warnings and warnings without stimulation, but at no time could he be deceived. When in doubt, he asked thoughtfully to have the stimulation repeated before committing himself to a reply!”

To Penfield, it was clear that these unexpected responses he was getting by stimulating the medial temporal lobes differed fundamentally from the responses produced by stimulation of other parts of the brain. The response of his patients to the jolting of other areas might be marked by “a tingling feeling, an absence of feeling called numbness, a sense of movement; olfactory sensation, by a disagreeable odor; gustatory, by a strong taste,” but all of those sensations had one thing in common: They were generalized, not tied to any particular moment in time. The responses he was triggering by stimulating the medial temporal lobes were, Penfield noted, “of an entirely different order. They are made up of the acquired experience of that particular individual. It is the difference between a simple sound and a conversation or a symphony. It is the difference between the sight of colored squares and the moving spectacle of friends who walk and talk and laugh with you. The one is a simple element of sensation. The other is a recollective hallucination.”

A recollective hallucination.

In other words, a memory.

Penfield wrestled with the implications of what he'd observed. In his famous homunculus illustrations, he'd already mapped out the human brain's sensory and somatosensory cortices. Now he'd stumbled into an entirely new domain: the memory cortex.

But how was this possible?

What made a spark of electricity spark the past?

“The answers to those questions are of great psychological importance,” Penfield wrote, before admitting that he was going to have to “venture from the firm ground of observation onto the dizzying scaffolding of hypothesis.” His patients' experiences in the OR led him to believe that the human brain retained absolutely every experience that ever crossed its synapses. Every moment, every waking hour, even every dream. Anything that it had seen or heard or tasted or smelled or thought. Anything and everything, so long as during the moment of raw experience some attention had been paid to it. “Whenever a normal person is paying conscious attention to something,” Penfield wrote, “he is simultaneously recording it in the temporal cortex of each hemisphere. Every conscious aspect of the experience seems to be included in these records.” It was, as Penfield would later describe it to
Time,
as though there were a “tape recorder” in the brain, activated at the moment of birth and stopping only at death. Each event of a person's life was stored away as a distinct “neurone pathway.” Even events that people might later have no ability to recall of their own volition, the ephemera of the everyday, were all carefully preserved. “It would appear,” Penfield said, “that the memory record continues intact even after the subject's ability to recall it disappears.”

Penfield further speculated that when people engaged in an act of normal remembering, without the aid of an external electrode, they were still doing exactly what Penfield was doing to his patients on the operating table. That is, a self-generated electrical jolt to the medial temporal lobe's “memory cortex” was triggering the playback of particular memories. “This would seem to be absurdly simple,” Penfield wrote, “and yet the new evidence is inescapable.”

—

Penfield first presented his theory of memory during his presidential address at the seventy-sixth annual meeting of the American Neurological Association on June 18, 1951. The meeting took place in the grand ballroom of the tallest building in New Jersey, the twenty-four-story Claridge Hotel, high above the boardwalk in Atlantic City. His presentation caused a stir. The first audience member to comment was Lawrence Kubie, a psychiatrist and psychoanalyst who had acquired a sort of reflected fame by gathering an impressive collection of famous clients, including Vladimir Horowitz and Tennessee Williams.

“I am profoundly grateful for this opportunity to discuss Dr. Penfield's paper,” he said, describing how it had put him in a “state of ferment,” as though he were “watching pieces of a jigsaw puzzle fit into place and a picture emerge.” The address, he said, had “been as exciting a moment as I have spent in a scientific meeting in recent years. I can sense the shades of Harvey Cushing [the founder of modern neurosurgery] and Sigmund Freud shaking hands over this long-deferred meeting between psychoanalysis and modern neurology and neurosurgery, through the experimental work which Dr. Penfield has reported.”

Kubie then said that he hoped Penfield might begin adding dream studies and free association exercises to his battery of preoperative routines and wondered how many of the electrically stimulated memories might have been in fact the sorts of repressed memories that analysts such as himself trafficked in. Casting “a hopeful glance into the future,” Kubie imagined a day when even nonepileptics might have their brains “stimulated on the operating table” to “see whether the reliving of the past through electrical stimulation of the temporal cortex exercises any influence on preexisting neurotic symptoms and mechanisms, and on preexisting associative patterns and emotional storm centers”—a sort of open-brain psychoanalysis.

Penfield didn't comment on Kubie's suggestions, perhaps because he had always distrusted psychoanalysis and psychoanalysts. He was almost certainly pleased, however, by Kubie's memorable summation of his discoveries.

“This is Proust on the operating table,” Kubie declared. “An electrical
recherche aux temps perdu.
Yet is it
perdu
?”

Others in the audience were less impressed.

A neurologist named Karl Lashley, who was at the time the world's leading expert on the science of memory, was also in attendance. For the past two decades, working first at the University of Minnesota and then at his own laboratory in Orange Park, Florida, Lashley had conducted a series of experiments on rats, attempting to determine where their memories were stored. To do this, he would teach the rats a task, say, the proper way to navigate a maze, and then cut out various parts of their brains. What he found, to his surprise, was that no particular lesion would make the rats less able to remember how to navigate the maze. Instead the rat's navigational skills became muddled in proportion to how much of their brain tissue he removed, regardless of where exactly he removed that tissue from. Also, he was able to teach the rats new tasks, regardless of what parts of their brains he removed. The conclusions he drew from this were that no particular part of the brain stored memories and, likewise, that no particular part of the brain was responsible for the task of storing memories. Instead, he theorized, when it came to memory, if you removed a specific part of the brain, the remaining parts would attempt to pick up the slack, taking over the tasks the lost part had once been responsible for. He called this theory equipotentiality, to indicate his belief that every part of the brain had equal potential. And equipotentiality, or replaceability, as others often referred to it, became the prevailing view of how memory worked. Looking for the specific sites responsible for memory creation and storage, in this view, was pointless, since those sites could be anywhere, changing from brain to brain.

In Atlantic City, Lashley's critique of Penfield began somewhat obliquely, with a comment about the use of metaphor. This criticism was most likely directed toward Penfield's reference to the brain as a tape recorder, though he didn't say so specifically. Instead, Lashley simply dismissed “the analogies of various machines and neural activity” and pointed to “a curious parallel in the histories of neurological theories and of paranoid delusional systems. In Mesmer's day the paranoiac was persecuted by malicious animal magnetism; his successors, by galvanic shocks, by the telegraph, by radio, and by radar, keeping their delusional systems up-to-date with the latest fashions in physics. Descartes was impressed by the hydraulic figures in the royal gardens and developed a hydraulic theory of the action of the brain. We have since had telephone theories, electrical field theories and, now, theories based on the computing machines and automatic rudders. I suggest that we are more likely to find out how the brain works by studying the brain itself and the phenomena of behavior than by indulging in far-fetched physical analogies.”

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