Aerobic exercise enhances neural correlates of motor skill learning

Highlights

• A preceding bout of aerobic exercise augments the cortical response to motor training.

• Excitability of trained muscles is enhanced although performance is unaffected.

• Acute exercise may be a useful adjunct to motor learning tasks.

Abstract

Introduction

Repetitive, in-phase bimanual motor training tasks can expand the excitable cortical area of the trained muscles. Recent evidence suggests that an acute bout of moderate-intensity aerobic exercise can enhance the induction of rapid motor plasticity at the motor hotspot. However, these changes have not been investigated throughout the entire cortical representation. Furthermore, it is unclear how exercise-induced changes in excitability may relate to motor performance. We investigated whether aerobic exercise could enhance the neural correlates of motor learning. We hypothesized that the combination of exercise and training would increase the excitable cortical area to a greater extent than either exercise or training alone, and that the addition of exercise would enhance performance on a motor training task.

Methods

25 young, healthy, right-handed individuals were recruited and divided into two groups and three experimental conditions. The exercise group performed exercise alone (EX) and exercise followed by training (EXTR) while the training group performed training alone (TR).

Results

The combination of exercise and training increased excitability within the cortical map of the trained muscle to a greater extent than training alone. However, there was no difference in performance between the two groups. These results indicate that exercise may enhance the cortical adaptations to motor skill learning.

Introduction

There is growing interest in the potential ability of aerobic exercise to enhance cortical excitability. A single session of moderate-intensity exercise has been shown to transiently increase cortical activity and cognitive function in frontal and motor regions, changes that persist following exercise cessation. Given its role in movement execution, it is not surprising that excitability in the primary motor cortex (M1) may be enhanced following an acute exercise bout. Although little is known about the direct effects of aerobic exercise on motor cortical neurons, emerging evidence suggests that a single session of moderate-intensity cycling activity can suppress short-interval intracortical inhibition (SICI) and enhance intracortical facilitation (ICF) for at least 30 min following exercise completion [1], [2], suggesting that the post-exercise environment may be ideal for inducing experience-dependent plasticity. Indeed, early markers of long-term potentiation (LTP) are enhanced when induction is preceded by acute exercise. Exercise has been shown to enhance the response to paired-associative stimulation (PAS), a technique thought to induce LTP-like plasticity in the motor cortex, and this effect is observed following both moderate and high-intensity exercise [3], [4].

One limitation of these studies is that excitability changes have only been examined at the motor hotspot. Motor learning often involves not only changes at the central site, but an outward expansion of the excitable area [5], [6], [7], [8], [9]. Whether and to what extent exercise affects the overall M1 representation is unclear. Additionally, it is not known whether this benefit extends beyond passive stimulation to tasks involving active motor learning. Although the retention of motor skills appears to be enhanced by subsequent aerobic activity [10], and neurorehabilitation outcomes are improved by the addition of aerobic exercise [11], [12], enhancements in motor performance following acute exercise in healthy individuals have not yet been investigated. Such investigations are critical for determining the potential mechanisms and clinical utility of aerobic exercise as an adjunct therapy to improve motor function and motor skill training in neurological patient populations. In-phase bimanual movements can increase both cortical excitability and the spatial representation of target muscles [5], [13]. Such movements can exploit interhemispheric connections between corresponding M1 representations in order to enhance learning effects. Specifically, in-phase bimanual movements promote disinhibition of M1 and facilitate interhemispheric communication between homologous regions [14], [15]. Bimanual training tasks have been shown to increase the size of the motor map of the target muscle following training [5], [6], [7], and the neural substrates underlying this expansion are also thought to mediate the functional reorganization of M1 [16], [17]. Short-term learning (<1 h) is associated with increased bilateral M1 activity [18] and increased functional connectivity between M1 and premotor regions [19]. While the consolidation of motor skills is related to a decrease in motor map size, early motor skill learning is associated with an increased cortical representation of the trained muscles [20].

Motor learning comprises skill acquisition and motor adaptation [21] and requires a cortical environment that is receptive to experience-dependent plasticity. Facilitatory interventions that target the motor cortex, such as intermittent theta-burst stimulation, or anodal transcranial direct current stimulation, have been shown to effectively prime the brain for subsequent motor learning [22], [23], [24]. In the current study, we investigate whether exercise may have a similar effect when performed prior to a bimanual visuomotor learning task. We used single-pulse transcranial magnetic stimulation to generate a cortical map of the extensor carpi radialis (ECR) muscle representation before and after training. We hypothesized that (a) exercise would enhance the cortical response to training, both in terms of the spatial extent of the cortical map and the excitability changes within the map; and (b) that a single-session of visuomotor training would induce motor learning as measured by response time, accuracy and movement trajectory on the motor task.