Aging, Brain Plasticity and Motor Learning

Highlights

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Despite poorer motor performance, older adults preserve the capacity for motor learning.

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Older adults demonstrate training-induced changes in brain structure and function.

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Motor skill learning may help to counteract age-related loss of brain structure.

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Training-induced neurotransmitter modulation is evident, also in older adults.

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Non-invasive brain stimulation techniques can be used for optimizing motor learning.

Abstract

Motor skill learning, the process of acquiring new motor skills, is critically important across the lifespan, from early development through adulthood and into older age, as well as in pathological conditions (i.e., rehabilitation). Extensive research has demonstrated that motor skill acquisition in young adults is accompanied by significant neuroplastic changes, including alterations in brain structure (gray and white matter), function (i.e., activity and connectivity), and neurochemistry (i.e., levels of neurotransmitters). In the aging population, motor performance typically declines, characterized by slower and less accurate movements. However, despite these age-related changes, older adults maintain the capacity for skill improvement through training. In this review, we explore the extent to which the aging brain retains the ability to adapt in response to motor learning, specifically whether skill acquisition is accompanied by neural changes. Furthermore, we discuss the associations between inter-individual variability in brain structure and function and the potential for future learning in older adults. Finally, we consider the use of non-invasive brain stimulation techniques aimed at optimizing motor learning in this population. Our review provides insights into the neurobiological underpinnings of motor learning in older adults and emphasizes strategies to enhance their motor skill acquisition.

Introduction

For a long time, brain plasticity (or neuroplasticity), i.e., “the ability of the nervous system to change its activity in response to intrinsic or extrinsic stimuli by reorganizing its structure, functions, or connections” (Mateos-Aparicio et al., 2019), was assumed to reach its peak during young age and then gradually decline with advancing age. The popular saying "you can't teach an old dog new tricks" has perpetuated the idea that individuals, as they grow older, may find it challenging to learn new behaviors.

However, recent times have witnessed remarkable strides in medical imaging technologies such as functional magnetic resonance imaging (fMRI), diffusion weighted imaging (DWI), magnetic resonance spectroscopy (MRS) as well as (neuronavigated) brain stimulation techniques like transcranial magnetic stimulation (TMS) and various transcranial (direct or alternating) current stimulation techniques (tDCS, tACS). These advancements have enabled researchers to better understand brain-behavior relationships. Interestingly, this progress has also led to the emergence of mounting evidence challenging the traditional notion of limited brain plasticity at older age. Instead, an increasing amount of research supports the existence of lifelong brain plasticity, indicating that the brain preserve its capacity for change throughout the entire lifespan.

Aging is marked by a continuing decline in motor function that can start as early as the age of 30 (e.g., Serbruyns et al., 2015). These declines become more pronounced at older age, leading to reduced motor functioning in older adults (Bartzokis et al., 2010, Heuninckx et al., 2004, Heuninckx et al., 2005, Heuninckx et al., 2008, Serbruyns et al., 2015, Serrien et al., 2000, Voelcker-Rehage, 2008). Nevertheless, older adults have plasticity potential and have the ability to learn new motor skills, be it at similar or reduced rates of learning as compared with young adults (for reviews, see Maes et al. (2017) and Voelcker-Rehage (2008)). The extent to which motor skills can be learned in healthy older adults through practice depends on multiple aspects such as context, difficulty of as well as the familiarity level with the to-be-learned task (Voelcker-Rehage, 2008).

The newfound understanding of lifelong brain plasticity, along with the insights from behavioral research incorporating motor learning paradigms, has profound implications for our estimation of aging and the brain's capacity for learning and neuroplasticity. Considering these discoveries, the notion of age-related motor decline as an inevitable and irreversible process is being reconsidered. Instead, a more optimistic perspective on brain plasticity and its enduring potential for behavioral change is gaining traction. Even at age 60 or beyond, the brain possesses a remarkable ability to reorganize neural circuits and adapt to new experiences, challenges, and learning tasks. As we continue to delve deeper into how the brain adapts, we uncover many ways to optimize motor function across the entire human lifespan. This insight opens exciting possibilities for interventions and therapies aimed at harnessing the brain's inherent plasticity to promote healthy aging, enhance motor and/or cognitive abilities, and facilitate recovery after injury or neurological disorders. The ultimate goal is not only to increase lifespan but also healthspan in aging adults.

To advance our understanding of training-induced neuroplasticity in the context of healthy aging, this literature review will encompass the following central topics. First, we will introduce basic principles of motor skill learning and motor memory processes. Second, we will explore the impact of age on motor skill learning and neuroplasticity, drawing insights from studies examining brain structure and function. Additionally, we will examine the role of neurochemicals (particularly γ-aminobutyric acid, GABA) in motor performance and learning. Third, we will discuss the optimization of motor skill acquisition and the underlying neural mechanisms in older adults using non-invasive brain stimulation (NIBS). Lastly, we will conclude this review with a synthesis including comprehensive remarks and perspectives for future directions in this fascinating and evolving field of research. Our most critical objective is to inform the scientific community about the potential for brain plasticity across the whole lifespan and to strongly encourage older citizens to actively promote the utilization of this potential for increasing healthspan and quality of life.

Section snippets

Basic principles of motor skill learning: motor memory processes

Here, we will discuss the basic principles of motor skill learning, which is essential for a comprehensive understanding of the remainder of this literature review. The primary aim of behavioral motor learning research is to explore how to enhance the execution of a motor skill as effectively as possible and, crucially, how to maintain these improvements over time. Motor skills fall into the broad category of procedural knowledge and are thus acquired through a procedural learning process.

Effects of motor task practice on neuroplasticity in aging

Neuroplasticity can be studied through brain structural, functional, connectivity, and neurochemical processes, offering complementary insights into the dynamic neural mechanisms underlying motor skill learning. Using anatomical and diffusion magnetic resonance imaging (MRI), investigating training-induced neuroplasticity in terms of brain structure allows us to gain valuable knowledge about the gray and white matter changes that occur in response to motor training. Complementary to research on

Conclusions and future directions

The present review aims to deepen the understanding of motor training-induced neuroplasticity in the context of healthy aging (see Fig. 1 for conceptual overview). Previous research indicated that aging generally affects motor performance, resulting in slower movements and/or reduced accuracy. Nevertheless, most studies show that older adults can improve their motor performance similarly to younger adults.

Concluding statements

Older adults typically perform worse on motor tasks than younger adults but still show clear training-induced improvements, though sometimes at a different rate. This demonstrates that the capacity for motor learning is preserved across the lifespan.

In both older and younger adults, motor training-induced performance improvements are linked to inter-individual variations in macro- and microstructural brain characteristics, with greater volume (gray matter) and higher fractional anisotropy