Subsequent functional MRI studies supported our hunch about Henry’s sense of familiarity for the complex pictures we had shown him. In 2003, a team of cognitive neuroscientists in California showed that familiarity and recollection depend on different anatomical areas within the medial temporal lobes. Inside the MRI scanner, their research participants encoded words such as NICKEL displayed in red letters and other words such as DEER displayed in green letters. After the scan, participants took a recognition memory test in which they viewed a random mix of studied words and unstudied words, and gave two responses. They first rated how confident they were that they had seen, or not seen, each word before. They then decided whether the letters in each word had been red or green when they first saw them in the scanner, a measure of their source memory. The ability to remember the color of the letters, source accuracy, assessed recollection—consciously associating each word with its color. Source memory judgments could not be based on familiarity because the study list contained red words intermixed with green words, making them equally familiar or unfamiliar at the time of the test.49
The researchers analyzed each participant’s functional MRI images individually. They distinguished brain circuits that showed increased activation when participants encoded words they later recognized based on recollection, versus brain circuits that showed increased activation when participants encoded words they later recognized based on familiarity. The contribution of familiarity increased gradually as recognition confidence increased. The more confident the participants were that they had seen a particular word before, the greater the familiarity effect.50
Consistent with the theory that the perirhinal cortex and hippocampus play different roles in recognition memory, the functional MRI analyses uncovered two distinct circuits, one for each kind of recognition memory. The researchers found a circuit dedicated to the feeling of familiarity in two contiguous areas, the entorhinal and perirhinal cortex. Here, brain activity increased as familiarity increased. Two other areas showed heightened activity when participants correctly remembered the color of the letters, indicating accurate memory for source information—the color—an index of recollection memory. This hotspot was in the back of the hippocampus and in the cortex next to it, the parahippocampal cortex.51
These findings indicate that the hippocampus and parahippocampal cortex specialize in recollection, whereas the perirhinal and entorhinal cortices specialize in familiarity. Henry’s anatomical MRI scans showed that he had some perirhinal tissue remaining on both sides of his brain. We reasoned that his residual perirhinal areas jumped into action when we asked him to remember the complex magazine pictures, enabling him later on to select the ones he had seen before, based on whether they seemed familiar.
Henry’s case proved that hippocampal lesions cause profound difficulty with recollection, and a parallel question arose with respect to the perirhinal cortex and familiarity. Would another person with a lesion restricted to the perirhinal cortex exhibit a deficit in familiarity? The answer came in 2007 from a patient who showed impaired familiarity and preserved recollection after she sustained damage to her perirhinal cortex but not her hippocampus. A group of Canadian researchers examined recognition memory in this patient, N.B., who had undergone a left anterior temporal lobectomy to relieve intractable epilepsy. Her operation was atypical because, unlike F.C., P.B., and Henry’s, it spared her hippocampus while excising a large portion of her perirhinal cortex. N.B.’s performance on recognition memory tests was the opposite of Henry’s—recollection was normal, while familiarity was impaired. This striking case report adds weight to the theory that separate circuits in the medial temporal-lobe region support recollection and familiarity. Still, researchers continue to debate the precise localization of recollection and familiarity processes and have deemed it a topic worthy of further study.52
Henry’s declarative memory was broken, and he was left with only vague feelings of familiarity. He could not evaluate whether these mental impressions were trustworthy, but perhaps that did not matter because they provided content in his life. Henry’s preserved capacity for familiarity helped him during his twenty-eight years at Bickford. He felt comfortable in the homey atmosphere, and one staff member described him as “the mainstay of the lounge.” He was very popular with the other patients, and some of them asked for him by name. His kind heart and polite demeanor helped him to be tolerant of the demented people who surrounded him. As his cordial interactions with them clearly showed, Henry certainly did not regard his fellow patients and the Bickford staff members as strangers.
One advantage I had in my interactions with Henry was that my face was familiar to him. He believed we went to high school together, so I was not an outsider. He made the same association with a few of the female staff members at Bickford with whom he regularly interacted, and this repeated exposure over time strengthened the feeling that he knew some of these people. Even though the faces, objects, and technology in his environment changed dramatically decade by decade, Henry accepted these changes without question, incorporating them into his universe. Before his operation, he had watched television programs in black and white; after his operation, when color television became available, he did not comment on the dramatic difference. Likewise, in our lab, he was so comfortable sitting in front of computers to perform tests that it seemed like they had always been part of his life. The sense of familiarity that permeated Henry’s world helped him cope with his disabling amnesia by grounding him and giving him the feeling that he was among family at Bickford and MIT.
Eight
Memory without Remembering I
Motor-skill Learning
Henry’s brain damage was restricted to his medial temporal-lobe structures, and the remaining areas, except for his cerebellum, still operated normally. These other regions supported several kinds of unconscious learning. In everyday life, he could acquire new skills and remember how to perform them.
One skill Henry needed to learn as an older man was how to use a walking frame, which he came to depend on due to the side effects of his antiseizure medication. Although his operation had the desired result of markedly reducing the number of grand mal seizures he experienced, Henry still had to take epilepsy drugs. He had been taking high doses of Dilantin before his operation and continued to take therapeutic doses until 1984, when a neurologist recommended that he switch to a different antiseizure drug. By that time, Dilantin had caused several damaging side effects, including osteoporosis, which led to several bone fractures. Dilantin also resulted in significant withering of his cerebellum, the large structure at the back of the brain responsible for maintaining balance and coordination. As a result of this brain shrinkage, Henry was unsteady on his feet and moved slowly. Another of his seizure medications, Phenobarbital, is a sedative and likely contributed to his overall slowness.
Henry’s osteoporosis progressed to the point that it was unsafe for him to walk on his own. In 1985, he fractured his right ankle, and in 1986, had his left hip replaced. During his recovery, his doctor prescribed a walking frame to keep him physically active and safe when on his feet. Once he received this new tool, he had to learn several new procedures to use it properly. With practice, Henry acquired the technique for walking, transferring his body from a chair to his walker, and returning to a chair. When I asked him why he used the walker, he replied, “So I won’t fall down.” He had no conscious, declarative knowledge that he developed osteoporosis as a result of taking Dilantin; nor did he remember that he’d had several fractures that had required hospitalization and rehabilitation. But Henry did retain the new motor skills from day to day and month to month, a striking example of his ability to obtain and hang onto procedural knowledge.
In the lab, formal demonstrations of his motor-learning ability echoed these everyday achievements. Henry recruited areas in his brain that were spared, and he could learn and remember without knowing that he was doing so. The use of the term memory in this situation underscores the
point that we possess more than one kind of memory—we engage our conscious, declarative memory processes when we recall what we need to buy at the grocery store, whereas we rely on our unconscious, nondeclarative memory when we can still ride a bicycle after not having done so for ten years.
Recognizing that learning can take place without awareness was one of the most significant advances in human memory research. In the twentieth century, much of the scientific research on amnesia focused on declarative learning and memory, but a parallel story unfolded, revealing a different kind of memory, nondeclarative learning, by which amnesic patients could perform new tasks despite the inability to explicitly describe their learning experience. Nondeclarative learning is sometimes referred to as procedural or implicit. A broad range of preserved learning capacities is covered under the nondeclarative umbrella—motor-skill learning, classical conditioning, perceptual learning, and repetition priming. These procedures differ in several ways, including the number of trials required for acquisition, the critical brain substrate, and the durability of the knowledge.1
The first account suggesting that learning could occur in an amnesic patient appeared in 1911. Édouard Claparède, a psychologist at the University of Geneva, related a remarkable clinical anecdote about a forty-seven-year-old woman whose memory was impaired due to Korsakoff syndrome, amnesia attributed to thiamine deficiency. Like Henry, she retained the general knowledge of the world she had acquired before the onset of her illness; for example, she could name all the European capital cities and do simple arithmetic in her head. She could not, however, remember a list of words or stories read to her and did not recognize the doctors who cared for her.
To explore her capacity for learning, Claparède shook his patient’s hand one day with a pin hidden in his palm. She felt the pinprick and recoiled. When he approached her the next day with his hand outstretched, she declined to shake his hand but had no idea why. Clearly, she took in information at the time of the handshake, but the next day she could not bring to mind her unconscious memory of the painful experience that guided her response. She could not state her fear, demonstrating that her declarative memory was impaired. But at the same time, she witheld her handshake, indicating that her nondeclarative memory was still functioning.2
Four decades later, Brenda Milner provided the first formal experimental demonstration of preserved learning in amnesia. In 1955, when she first evaluated Henry at Scoville’s office in Hartford, she tried to unearth any evidence of new learning using many different kinds of behavioral tasks. Her tests were not driven by any particular hypothesis, but the payoff was tremendous: on one of the tasks, Henry’s performance improved measurably during three days of practice. This exciting, serendipitous finding suggested that the structures removed from Henry’s medial temporal lobes were not necessary for this kind of learning. Milner’s experiment suggested that the brain houses two different kinds of long-term memory, one on which Henry failed and another on which he succeeded. The ensuing decades witnessed the publication of thousands of investigations of nondeclarative memory inspired by Milner’s discovery (see Fig. 9).
Among the tests Milner chose was a motor-skill learning task, mirror tracing, which she administered on three consecutive days during one visit. Each day, Milner asked Henry to trace a five-pointed star, keeping his pencil inside its borders. This task was challenging because the star, printed on paper, was mounted on a horizontal wooden board hidden from Henry’s view by a near-vertical metal barrier that blocked direct vision of the star, his hand, and the pencil. He reached around the right side of the metal barrier and could see the star, his right hand, and the pencil in a mirror mounted on the far side of the wooden board. The entire image was reversed so that if he wanted the pencil to trace around the star away from his body, he had to move the pencil down toward his body. The normal visual cues we use to guide our movements were turned upside-down. The task required mastering a new motor skill—allowing this reversed visual image to dictate the movement of his hand. Every time Henry strayed outside the lines and had to return, it was counted as an error. Most people find the task difficult and frustrating at first but improve over time, and with practice, they gradually trace around the star faster and with fewer errors.3
As Henry performed the task over and over again, something remarkable happened. On the first day, his errors dropped steadily from trial to trial, and—unpredictably—he retained what he learned overnight. On the second day, his initial error scores were almost as good as they had been at the end of training the first day, and he continued to trace around the star with fewer and fewer mistakes. On the third day, he performed nearly perfectly—he traced around the star cleanly and rarely veered outside the lines.
Henry had learned a new skill. This learning, however, had taken place outside his conscious knowledge. On days two and three, he had no memory of having done the task before. Milner vividly remembers the last day of testing: after skillfully tracing the star in the mirror, Henry sat up straight and proudly observed, “Well, this is strange. I thought that that would be difficult, but it seems as though I’ve done it quite well.”
Milner speculated that motor skills, such as the one Henry had mastered, might be learned by recruiting a different memory circuit, one outside the hippocampal structures Henry lacked. This unforeseen discovery unlocked a treasure trove of learning processes that do not depend on the medial temporal-lobe circuits that were damaged during Henry’s operation, but instead are mediated by brain areas that were left behind.4
In 1962, I expanded on Milner’s amazing discovery while working in her lab at the Montreal Neurological Institute as a McGill University graduate student. Henry and his mother were in Montreal for a week of testing. By that time, scientists had vetted and verified his declarative memory impairment with tests that required him to remember information presented through vision and hearing. No one, however, had tested to see whether his memory deficit extended to his sense of touch, his somatosensory system. Taking on this project, I presented Henry with a task to learn the correct sequence of turns in a touch-guided maze that he traced with a pen. In Chapter 5, I described his failure to learn the correct route from the start to the finish. But even though his error scores did not decrease over the eighty trials, Henry had learned something new. In addition to recording how many errors he made on each trial, I noted how many seconds elapsed between his leaving the start point and reaching the finish. After he and his mother returned to East Hartford, I plotted these data on a graph, and found to my surprise that while his number of errors never changed, his time scores decreased steadily over the same eighty trials. From day to day, he moved more quickly through the alleys in the maze, even though he could not remember the route. This decrease in the time it took Henry to traverse the maze showed that he learned something—the procedure, the how to do it. He did not remember the route, but he became increasingly comfortable with the task. This experiment strengthened the view Milner had proposed: motor learning depends on a different memory circuit from the medial temporal-lobe area, which underlies the consolidation and storage of facts and experiences.
Henry’s contrasting error and time scores when he traced my tactual maze reinforced the view that free recall—declarative memory—depends on the hippocampal region, which he now lacked, whereas skill learning—procedural memory—engages different networks that were undamaged. To the best of my knowledge, this result from 1962 was the first quantitative demonstration, within a single experiment, of impaired declarative learning (failure to learn the correct route) with preserved procedural—nondeclarative—learning (improving the motor skill). Further research in patients and in healthy individuals went on to characterize the important distinctions between these two kinds of long-term memory.5
To learn a new motor skill, the task must be performed over and over again. Once attained, motor skills are enduring—hence the adage about never forgetting how to ride a bicycle. But as any tennis player can tell you, motor sk
ills are not perfected in a single practice session; instead, they evolve with experience, and performance progresses from the staccato execution of several actions to the integration of those actions into a smooth movement performed automatically. Consider, for example, the many steps required to execute the two-handed backhand. Begin by facing the net with your toes pointed forward and your racket and body in the ready position. When the ball approaches your backhand side, slide your hands to the two-handed backhand grip and then take your backswing away from the net with your shoulders and body turning in the same direction. Try to keep the racket head below your hands so that when you hit the ball, the strings of your racket brush up the backside of the ball, giving it topspin. Next, take a big step, moving your body forward and your arms up. As you execute the stroke, transfer your weight to your front leg, and then follow through with your racket ending up over your shoulder. From beginning to end, keep your eye on the ball and bend your knees.
That is a lot of information to juggle! To do so, you must engage your cognitive control processes—regulated by your prefrontal cortex—to keep the individual steps in mind, and to execute them in the proper order. As a novice, you consciously monitor your performance, second by second; this skill does not come easily, and you must practice until all the critical steps come together. During the learning process, your brain will chunk the many individual pieces of your backhand stroke into a single, fluent shot. When you retrieve them, the combined elements of your backhand act as a coherent, integrated group. Weeks, months, and even years later, you will make the shot automatically, without thinking, and then can direct your attention and cognitive control processes to the strategies needed to win the game, set, and match.6
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