Brain Atrophy in Old Age Disrupts Sleep and Its Influence on Motor Memory
Material below summarizes the article White Matter Structure in Older Adults Moderates the Benefit of Sleep Spindles on Motor Memory Consolidation, published on October 30, 2017, in JNeurosci and authored by Bryce A. Mander, Alyssa H. Zhu, John R. Lindquist, Sylvia Villeneuve, Vikram Rao, Brandon Lu, Jared M. Saletin, Sonia Ancoli-Israel, William J. Jagust, and Matthew P. Walker.
Best described by the classic adage “practice makes perfect,” procedural memory encapsulates the ability to acquire new skills through repeated training. This training alters how our brains and bodies process information and perform specific behaviors, so when we carry out the same actions in the future, it will be “like riding a bike.”
Many studies show older adults are less able to learn new motor skills. Why this is so remains unclear, but recent findings suggest how well an older individual sleeps may matter.
Established literature has demonstrated sleep critically supports the consolidation of motor skills and this sleep benefit appears to be absent in older adults. The loss of this sleep benefit parallels a decline in sleep quality, with sleep being less rich in the brain oscillations known to support motor memory.
One such oscillation, called the sleep spindle, is generated in a specific nucleus in the thalamus that governs how sensory and motor information are relayed between the brain and the body. Through their expression, sleep spindles selectively modify connections within brain circuits, ultimately cementing learned skills into the brain to support adaptive behavior in the future.
Following training on a motor skill task, the number and physiological intensity of sleep spindles occurring during sleep predicts how well an individual performs that skill the next day. The first evidence supporting a causal role for sleep spindles in motor memory in humans was recently obtained in a study that showed brain stimulation to enhance sleep spindles also improved motor memory. In contrast, sleep spindles are less predictive of motor memory in older adults.
Why do older adults have fewer sleep spindles during sleep? Why does sleep benefit motor memory in young adults, but not older adults? These are the central questions we addressed in our study. To examine these questions, the study employed a motor skill task having shown to depend on sleep.
This task was performed by groups of young (ages 18-30) and older (ages 61-85) adults who either trained on the task prior to sleep and retested after sleep, or trained and retested across a wake period without sleep.
We combined measures of performance on this task with high resolution sleep recordings and a structural magnetic resonance imaging (MRI) technique, called diffusion tensor imaging, which measures white matter connections in the brain.
We first demonstrated older adults, relative to young adults, had far fewer sleep spindles. We next showed older adults performed more poorly on the motor skill task, gaining no benefit from sleep. In contrast, young adults who slept showed the normal overnight sleep benefit on motor skill performance relative to those with no sleep. Moreover, the degree of sleep benefit on motor memory positively correlated with how many sleep spindles were observed, and this relationship was specific to young adults.
These findings are all consistent with the prior literature, reproducing the core findings that older adults have fewer sleep spindles than young adults, and sleep spindles benefit motor memory in young but not older adults.
We next sought to understand why older adults had fewer sleep spindles than young adults, and why sleep spindles were less associated with motor memory in older relative to young adults.
We first found the strength of specific white matter connections predicted how many sleep spindles were observed during sleep, and these connections were significantly weaker in older adults.
The specific white matter connections predicted sleep spindle expression were similar to those identified in a prior study in young adults, including portions of white matter connecting the thalamus, basal ganglia, and motor cortex, as well as the corpus callosum, which connects the two hemispheres.
Our first core novel finding thus revealed erosion of specific white matter connections is one reason older adults have fewer sleep spindles.
Our second core novel finding was that specific portions of white matter connections that were more atrophied in older adults governed the ability of sleep spindles to support motor memory. Specifically, the magnitude of atrophy of white matter in the corpus callosum, a white matter pathway in the brain connects sensory, motor, and memory brain regions across hemispheres, determined the degree to which sleep spindles predicted motor memory.
Individuals with weaker corpus callosum connections showed a weaker association between sleep spindles and motor memory than those with stronger corpus callosum connections. While this is not a region of white matter we originally expected would impact motor learning, this finding is consistent with a rodent study that showed blocking myelination in the corpus callosum after novel motor learning abolished the long-term retention of motor learning.
This finding therefore reveals atrophy of white matter connections in the human brain is one reason memory benefits less from sleep in older adults.
Together, these findings establish the critical importance of white matter connections in the brain for the expression of sleep spindles and motor memory. These findings have several relevant implications for future studies.
First, individuals with more robust white matter connections may be more resilient to age-related decline in motor memory, while those with degenerative diseases targeting white matter may be more vulnerable.
Second, interventions to enhance sleep spindles may not aid motor memory to the same degree in older adults with more significant erosion of white matter connections.
Third, rehabilitation of motor skills following stroke or brain injury may be less robust in older adults with greater erosion of white matter connections.
Beyond aging, these findings also imply the development of white matter connections across childhood and adolescence may influence the role of sleep spindles in motor memory in children.
Overall, our findings demonstrate individual differences in the strength of white matter connections interact with sleep physiology to govern the retention of motor memory.
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White Matter Structure in Older Adults Moderates the Benefit of Sleep Spindles on Motor Memory Consolidation. Bryce A. Mander, Alyssa H. Zhu, John R. Lindquist, Sylvia Villeneuve, Vikram Rao, Brandon Lu, Jared M. Saletin, Sonia Ancoli-Israel, William J. Jagust, Matthew P. Walker. JNeurosci Oct 2017, DOI: https://doi.org/10.1523/JNEUROSCI.3033-16.2017
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