In 1983, the Nobel Laureate Francis Crick, who discovered the helical structure of DNA, decided to turn his theoretical mind toward the topic of sleep. He suggested that the function of REM-sleep dreaming was to remove unwanted or overlapping copies of information in the brain: what he termed “parasitic memories.” It was a fascinating idea, but it remained just that—an idea—for almost thirty years, receiving no formal examination. In 2009, a young graduate student and I put the hypothesis to the test. The results brought more than a few surprises.
We designed an experiment that again used daytime naps. At midday, our research subjects studied a long list of words presented one at a time on a computer screen. After each word had been presented on the screen, however, a large green “R” or a large red “F” was displayed, indicating to the participant that they should remember the prior word (R) or forget the prior word (F). It is not dissimilar to being in a class and, after having been told a fact, the teacher impresses upon you that it is especially important to remember that information for the exam, or instead that they made an error and the fact was incorrect, or the fact will not be tested on the exam, so you don’t need to worry about remembering it for the test. We were effectively doing the same thing for each word right after learning, tagging it with the label “to be remembered” or “to be forgotten.”
Half of the participants were then allowed a ninety-minute afternoon nap, while the other half remained awake. At six p.m. we tested everyone’s memory for all of the words. We told participants that regardless of the tag previously associated with a word—to be remembered or to be forgotten—they should try to recall as many words as possible. Our question was this: Does sleep improve the retention of all words equally, or does sleep obey the waking command only to remember some items while forgetting others, based on the tags we had connected to each?
The results were clear. Sleep powerfully, yet very selectively, boosted the retention of those words previously tagged for “remembering,” yet actively avoided the strengthening of those memories tagged for “forgetting.” Participants who did not sleep showed no such impressive parsing and differential saving of the memories.fn9
We had learned a subtle, but important, lesson: sleep was far more intelligent than we had once imagined. Counter to earlier assumptions in the twentieth and twenty-first centuries, sleep does not offer a general, nonspecific (and hence verbose) preservation of all the information you learn during the day. Instead, sleep is able to offer a far more discerning hand in memory improvement: one that preferentially picks and chooses what information is, and is not, ultimately strengthened. Sleep accomplishes this by using meaningful tags that have been hung onto those memories during initial learning, or potentially identified during sleep itself. Numerous studies have shown a similarly intelligent form of sleep-dependent memory selection across both daytime naps and a full night of sleep.
When we analyzed the sleep records of those individuals who napped, we gained another insight. Contrary to Francis Crick’s prediction, it was not REM sleep that was sifting through the list of prior words, separating out those that should be retained and those that should be removed. Rather, it was NREM sleep, and especially the very quickest of the sleep spindles that helped bend apart the curves of remembering and forgetting. The more of those spindles a participant had during a nap, the greater the efficiency with which they strengthened items tagged for remembering and actively eliminated those designated for forgetting.
Exactly how sleep spindles accomplish this clever memory trick remains unclear. What we have at least discovered is a rather telling pattern of looping activity in the brain that coincides with these speedy sleep spindles. The activity circles between the memory storage site (the hippocampus) and those regions that program the decision of intentionality (in the frontal lobe), such as “This is important” or “This is irrelevant.” The recursive cycle of activity between these two areas (memory and intentionality), which happens ten to fifteen times per second during the spindles, may help explain NREM sleep’s discerning memory influence. Much like selecting intentional filters on an Internet search or a shopping app, spindles offer a refining benefit to memory by allowing the storage site of your hippocampus to check in with the intentional filters carried in your astute frontal lobes, allowing selection only of that which you need to save, while discarding that which you do not.
We are now exploring ways of harnessing this remarkably intelligent service of selective remembering and forgetting with painful or problematic memories. The idea may invoke the premise of the Oscar-winning movie Eternal Sunshine of the Spotless Mind, in which individuals can have unwanted memories deleted by a special brain-scanning machine. In contrast, my real-world hope is to develop accurate methods for selectively weakening or erasing certain memories from an individual’s memory library when there is a confirmed clinical need, such as in trauma, drug addiction, or substance abuse.
SLEEP FOR OTHER TYPES OF MEMORY
All of the studies I have described so far deal with one type of memory—that for facts, which we associate with textbooks or remembering someone’s name. There are, however, many other types of memory within the brain, including skill memory. Take riding a bike, for example. As a child, your parents did not give you a textbook called How to Ride a Bike, ask you to study it, and then expect you to immediately begin riding your bike with skilled aplomb. Nobody can tell you how to ride a bike. Well, they can try, but it will do them—and more importantly you—no good. You can only learn how to ride a bike by doing rather than reading. Which is to say by practicing. The same is true for all motor skills, whether you are learning a musical instrument, an athletic sport, a surgical procedure, or how to fly a plane.
The term “muscle memory” is a misnomer. Muscles themselves have no such memory: a muscle that is not connected to a brain cannot perform any skilled actions, nor does a muscle store skilled routines. Muscle memory is, in fact, brain memory. Training and strengthening muscles can help you better execute a skilled memory routine. But the routine itself—the memory program—resides firmly and exclusively within the brain.
Years before I explored the effects of sleep on fact-based, textbook-like learning, I examined motor skill memory. Two experiences shaped my decision to perform these studies. The first was given to me as a young student at the Queen’s Medical Center—a large teaching hospital in Nottingham, England. Here, I performed research on the topic of movement disorders, specifically spinal-cord injury. I was trying to discover ways of reconnecting spinal cords that had been severed, with the ultimate goal of reuniting the brain with the body. Sadly, my research was a failure. But during that time, I learned about patients with varied forms of motor disorders, including stroke. What struck me about so many of these patients was an iterative, step-by-step recovery of their motor function after the stroke, be it legs, arms, fingers, or speech. Rarely was the recovery complete, but day by day, month by month, they all showed some improvement.
The second transformative experience happened some years later while I was obtaining my PhD. It was 2000, and the scientific community had proclaimed that the next ten years would be “The Decade of the Brain,” forecasting (accurately, as it turned out) what would be remarkable progress within the neurosciences. I had been asked to give a public lecture on the topic of sleep at a celebratory event. At the time, we still knew relatively little about the effects of sleep on memory, though I made brief mention of the embryonic findings that were available.
After my lecture, a distinguished-looking gentleman with a kindly affect, dressed in a tweed suit jacket with a subtle yellow-green hue that I still vividly recall to this day, approached me. It was a brief conversation, but one of the most scientifically important of my life. He thanked me for the presentation, and told me that he was a pianist. He said he was intrigued by my description of sleep as an active brain state, one in which we may review and even strengthen those things we have previously learned. Then came a comment that would leav
e me reeling, and trigger a major focus of my research for years to come. “As a pianist,” he said, “I have an experience that seems far too frequent to be chance. I will be practicing a particular piece, even late into the evening, and I cannot seem to master it. Often, I make the same mistake at the same place in a particular movement. I go to bed frustrated. But when I wake up the next morning and sit back down at the piano, I can just play, perfectly.”
“I can just play.” The words reverberated in my mind as I tried to compose a response. I told the gentleman that it was a fascinating idea, and it was certainly possible that sleep assisted musicianship and led to error-free performance, but that I knew of no scientific evidence to support the claim. He smiled, seeming unfazed by the absence of empirical affirmation, thanked me again for my lecture, and walked toward the reception hall. I, on the other hand, remained in the auditorium, realizing that this gentleman had just told me something that violated the most repeated and entrusted teaching edict: practice makes perfect. Not so, it seemed. Perhaps it was practice, with sleep, that makes perfect?
After three years of subsequent research, I published a paper with a similar title, and in the studies that followed gathered evidence that ultimately confirmed all of the pianist’s wonderful intuitions about sleep. The findings also shed light on how the brain, after injury or damage by a stroke, gradually regains some ability to guide skill movements day by day—or should I say, night by night.
By that time, I had taken a position at Harvard Medical School, and with Robert Stickgold, a mentor and now a longtime collaborator and friend, we set about trying to determine if and how the brain continues to learn in the absence of any further practice. Time was clearly doing something. But it seemed that there were, in fact, three distinct possibilities to discriminate among. Was it (1) time, (2) time awake, or (3) time asleep that incubated skilled memory perfection?
I took a large group of right-handed individuals and had them learn to type a number sequence on a keyboard with their left hand, such as 4-1-3-2-4, as quickly and as accurately as possible. Like learning a piano scale, subjects practiced the motor skill sequence over and over again, for a total of twelve minutes, taking short breaks throughout. Unsurprisingly, the participants improved in their performance across the training session; practice, after all, is supposed to make perfect. We then tested the participants twelve hours later. Half of the participants had learned the sequence in the morning and were tested later that evening after remaining awake across the day. The other half of the subjects learned the sequence in the evening and we retested them the next morning after a similar twelve-hour delay, but one that contained a full eight-hour night of sleep.
Those who remained awake across the day showed no evidence of a significant improvement in performance. However, fitting with the pianist’s original description, those who were tested after the very same time delay of twelve hours, but that spanned a night of sleep, showed a striking 20 percent jump in performance speed and a near 35 percent improvement in accuracy. Importantly, those participants who learned the motor skill in the morning—and who showed no improvement that evening—did go on to show an identical bump up in performance when retested after a further twelve hours, now after they, too, had had a full night’s sleep.
In other words, your brain will continue to improve skill memories in the absence of any further practice. It is really quite magical. Yet, that delayed, “offline” learning occurs exclusively across a period of sleep, and not across equivalent time periods spent awake, regardless of whether the time awake or time asleep comes first. Practice does not make perfect. It is practice, followed by a night of sleep, that leads to perfection. We went on to show that these memory-boosting benefits occur no matter whether you learn a short or a very long motor sequence (e.g., 4-3-1-2 versus 4-2-3-4-2-3-1-4-3-4-1-4), or when using one hand (unimanual) or both (bimanual, similar to a pianist).
Analyzing the individual elements of the motor sequence, such as 4-1-3-2-4, allowed me to discover how, precisely, sleep was perfecting skill. Even after a long period of initial training, participants would consistently struggle with particular transitions within the sequence. These problem points stuck out like a sore thumb when I looked at the speed of the keystrokes. There would be a far longer pause, or consistent error, at specific transitions. For example, rather than seamlessly typing 4-1-3-2-4, 4-1-3-2-4, a participant would instead type: 4-1-3 [pause] 2-4, 4-1-3 [pause] 2-4. They were chunking the motor routine into pieces, as if attempting the sequences all in one go was just too much. Different people had different pause problems at different points in the routine, but almost all people had one or two of these difficulties. I assessed so many participants that I could actually tell where their unique difficulties in the motor routine were just by listening to their typing during training.
When I tested participants after a night of sleep, however, my ears heard something very different. I knew what was happening even before I analyzed the data: mastery. Their typing, post-sleep, was now fluid and unbroken. Gone was the staccato performance, replaced by seamless automaticity, which is the ultimate goal of motor learning: 4-1-3-2-4, 4-1-3-2-4, 4-1-3-2-4, rapid and nearly perfect. Sleep had systematically identified where the difficult transitions were in the motor memory and smoothed them out. This finding rekindled the words of the pianist I’d met: “but when I wake up the next morning and sit back down at the piano, I can just play, perfectly.”
I went on to test participants inside a brain scanner after they had slept, and could see how this delightful skill benefit had been achieved. Sleep had again transferred the memories, but the results were different from that for textbook-like memory. Rather than a transfer from short- to long-term memory required for saving facts, the motor memories had been shifted over to brain circuits that operate below the level of consciousness. As a result, those skill actions were now instinctual habits. They flowed out of the body with ease, rather than feeling effortful and deliberate. Which is to say that sleep helped the brain automate the movement routines, making them second nature—effortless—precisely the goal of many an Olympic coach when perfecting the skills of their elite athletes.
My final discovery, in what spanned almost a decade of research, identified the type of sleep responsible for the overnight motor-skill enhancement, carrying with it societal and medical lessons. The increases in speed and accuracy, underpinned by efficient automaticity, were directly related to the amount of stage 2 NREM, especially in the last two hours of an eight-hour night of sleep (e.g., from five to seven a.m., should you have fallen asleep at eleven p.m.). Indeed, it was the number of those wonderful sleep spindles in the last two hours of the late morning—the time of night with the richest spindle bursts of brainwave activity—that were linked with the offline memory boost.
More striking was the fact that the increase of these spindles after learning was detected only in regions of the scalp that sit above the motor cortex (just in front of the crown of your head), and not in other areas. The greater the local increase in sleep spindles over the part of the brain we had forced to learn the motor skill exhaustively, the better the performance upon awakening. Many other groups have found a similar “local-sleep”-and-learning effect. When it comes to motor-skill memories, the brainwaves of sleep were acting like a good masseuse—you still get a full body massage, but they will place special focus on areas of the body that need the most help. In the same way, sleep spindles bathe all parts of the brain, but a disproportionate emphasis will be placed on those parts of the brain that have been worked hardest with learning during the day.
Perhaps more relevant to the modern world is the time-of-night effect we discovered. Those last two hours of sleep are precisely the window that many of us feel it is okay to cut short to get a jump start on the day. As a result, we miss out on this feast of late-morning sleep spindles. It also brings to mind the prototypical Olympic coach who stoically has her athletes practicing late into the day, only to have them wake in t
he early hours of the morning and return to practice. In doing so, coaches may be innocently but effectively denying an important phase of motor memory development within the brain—one that fine-tunes skilled athletic performance. When you consider that very small performance differences often separate winning a gold medal from a last-place finish in professional athletics, then any competitive advantage you can gain, such as that naturally offered by sleep, can help determine whether or not you will hear your national anthem echo around the stadium. Not without putting too fine a point on it, if you don’t snooze, you lose.
The 100-meter sprint superstar Usain Bolt has, on many occasions, taken naps in the hours before breaking the world record, and before Olympic finals in which he won gold. Our own studies support his wisdom: daytime naps that contain sufficient numbers of sleep spindles also offer significant motor skill memory improvement, together with a restoring benefit on perceived energy and reduced muscle fatigue.
In the years since our discovery, numerous studies have shown that sleep improves the motor skills of junior, amateur, and elite athletes across sports as diverse as tennis, basketball, football, soccer, and rowing. So much so that, in 2015, the International Olympic Committee published a consensus statement highlighting the critical importance of, and essential need for, sleep in athletic development across all sports for men and women.fn10
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