Thinking While Moving or Moving While Thinking – Concepts of Motor-Cognitive Training for Cognitive Performance Enhancement

1A crucial aspect of human living is motion. While the control of movements requires cognitive processes, moving probably influences cognition and its underlying processes (structures), too. Cognition is a term covering a wide range of mental abilities that are necessary to percept, process, and interact with our environment. Therefore, intact cognitive processes are fundamental for human living. Across the life span, cognitive performance is influenced and changed by many factors. Normal aging is associated with a decline of cognitive functions such as processing speed and memory. Moreover, old age is also a risk factor for developing neurological diseases like dementia. Dementia has a negative impact on the cognitive performance of an individual and reduces the autonomy as well as the quality of life. Remarkably, dementia is a major contributor to health care costs, and it is expected that the number of those affected by dementia will almost double every 20 years. Furthermore, the neuropathological signs of dementia aggravate with physical inactivity. Physical inactivity and sedentary behavior are associated with reduced cognitive functions and increased welfare costs, too. Unfortunately, the average time people are physically inactive in daily life has increased substantially in the last decades in western countries. Taken together, the proportion of individuals with poorer cognitive capacities will increase in the next years, which makes it necessary to develop effective cognitive enhancement strategies that serve to enhance the cognitive reserve [defined as individual differences in how people process tasks; detailed description of term and concept could be found in, )] and the resilience against neurodegeneration.

2Apart from a healthy diet and cognitive stimulation, (I) physical activity which is defined as any bodily, muscle-produced movement that increases the energy expenditure above ∼1.5 metabolic equivalent of task [1 MET = 1 kcal (4,184 kJ) × kg-1 × h-1] and (II) physical exercise (training), which is defined as a planned, structured (repetitive) form of distinct physical activities are proposed crucial for the preservation of cognitive functions and the enhancement of the cognitive reserve. For instance, physical activity and/or exercise were shown to improve cognition in children, in adolescents, in young and middle-aged adults, in older adults, and in persons suffering from neurocognitive disorders such as dementia or mild cognitive impairment. Moreover, regardless of whether physical exercise is conducted in a single (acute) exercise bout and/or in form of multiple (chronic) exercise bouts, it has been demonstrated to enhance cognitive performance. Furthermore, it is speculated that regular physical activity and physical exercising prevent cognitive decline and neurological diseases. However, which exact prerequisites (e.g., intensity, duration, frequency, type of exercise) make an exercise optimal for effectively enhancing cognition are largely unknown. Often, aerobic (cardiovascular) exercises like cycling, walking, or running are used in interventions to enhance cognitive fitness, especially in the elderly. For instance, a 6-month walking intervention leads to an increased hippocampal volume and improved memory performance in seniors. Remarkably, preceding aerobic exercises boost performance in an alter reaction-time test but not in executive functions when compared to preceding resistance exercises.

3Interestingly, physical and motor fitness (coordinative abilities) are both related to cognitive performance in older individuals but do evoke differential structural adaptions or correlate only with distinct cognitive functions. For instance, a 12-month aerobic exercise intervention led to increased activation in sensori-motor networks while coordinative training increased activation in the visual–spatial network during an executive function test.

4An exercise type that demands a high level of coordinative abilities is dancing. Participating in a 6-month dancing intervention enhanced attentional performance to a higher degree than participating in a fall prevention or Tai Chi Chuan program. Additionally, in Parkinson disease dancing led to higher improvements in physical and cognitive functions than aerobic exercise. Regular dancing has been associated with a lower risk of dementia presumably because it induces a larger increase in gray matter volume in frontal regions and the hippocampus.

5Similar to chronic exercise, acute bouts of different exercise types have divergent effects on cognitive performance. Acute physical exercise with a high coordinative demand leads, in comparison to a purely aerobic exercise, to higher scores in attention tests, in working memory tests, and in cognitive flexibility measures. Taken together, acute and chronic physical exercises with high cognitive (coordinative) demands enhance cognitive performance. The beneficial effect of cognitively demanding exercises supports the recommendation of who proposes to shift the focus of exercise–cognition research from quantitative (e.g., exercise duration or intensity) to qualitative aspects (e.g., type of exercise).

6Remarkably, it has been speculated that the combination of physical and cognitive exercise (also known as motor-cognitive training) could evoke a higher cognitive enhancement than cognitive or physical exercise alone. The reasons why combined physical and cognitive exercise may be more effective than physical or cognitive training alone as well as the underlying neurophysiological mechanism are elucidated in the next section.

7To understand the beneficial effects of combined physical and cognitive exercises, it is advisable to consider our evolutionary past. From an evolutionary perspective, the human body and its organic systems exhibit a high adaptability to environmental constraints. Moreover, over centuries the human physiology was adapted to an active lifestyle which ensured human survival, for example, through foraging, hunting, and fishing. In industrialized nations, an increasing sedentary lifestyle probably promotes negative adaptations which minimize energy consumption, but also cause a decline of the motor and cognitive systems. In contrast, the foraging activities (e.g., hunting) of our ancestors required a simultaneous use of cognitive and sensori-motor resources (e.g., walking and simultaneously scanning the environment for food). Such cognitive processes (e.g., detecting a deer in the landscape) were intertwined with related actions of the body (e.g., throwing a spear on a moving deer). The idea expressing that cognitive processes, bodily movements and interaction with the environment are interrelated is close to those theories known as “embodied cognition” and “embedded cognition”. These considerations suggest that the combination of physical and cognitive challenges are essential to preserve or enhance the neural capacity which, in turn, ensures that cognitive processes function well.

8According to the “guided plasticity facilitation” framework (see Figure 1), the combination of physical and cognitive activities has positive synergistic effects that exceed the pure addition of the positive effects of cognitive and physical exercises. These super additive synergistic effects emerge from (I) the “facilitation effects” of physical exercises and (II) the “guidance effects” of cognitive exercises (see Figure 1). The “facilitation effect” of physical exercises triggers neurophysiological mechanisms, which promote neuroplasticity. A possible physical exercise-induced mechanism, which promotes neuroplasticity is the enhanced release of neurotrophic factors such as the brain-derived neurotrophic factor (BDNF). BDNF is associated with synaptogenesis and neurogenesis which may foster improved cognition. Notably, an increased level of BDNF was observed during physical exercises and up to 60 min after cessation of the acute bout of physical exercises. Based on this observation, the “facilitation effects” of acute physical exercises seem transient and time-constrained. While physical exercises induce neurophysiological processes that are fundamental for transient neuroplasticity (e.g., neurogenesis, cognitive stimulation is assumed to “guide” these neuroplastic processes. The “guidance effects” of cognitive exercises probably initiate distinct survival mechanisms of newborn cells. These survival mechanisms are presumably part of a complex, multi-step mechanism that depends on the activation/stimulation of the newly generated synapses or neurons. The activation/stimulation of synapses and neurons occurs due to the execution of cognitive tasks and enables the functional integration of new neuronal structures in the respective brain circuits. The integration in functional brain circuits seems to be crucial in order to stabilize the (by motor-cognitive training) induced neuroplastic changes. In addition to neuroplasticity, the stabilization of central nervous structures is likewise important to ensure good brain function.

9As shown in the framework in Figure 2, motor and cognitive exercises can be combined in several ways. In the first stage, we categorize motor and cognitive exercises based on their temporal order, which is a key factor for the effectiveness of the intervention in (I) sequential (or subsequent) motor-cognitive training and (II) simultaneous motor-cognitive training (see Figure 2).

10In sequential (or subsequent) motor-cognitive training, both the motor training and the cognitive training are each conducted at separate time points on the same day (prior to or after a bout of physical exercises) or at separate days. Commonly, the motor component of simultaneous motor-cognitive exercises compromises aerobic, resistance, balance, flexibility training, or a combination of them (for review see; ). In sequential motor-cognitive training interventions, the cognitive training was mainly focused on attention, memory, or multiple cognitive domains (for review see; ). An advantage of sequential motor-cognitive training (compared to simultaneous motor-cognitive training) is the absence of (1) possible dual-task costs [performance decrements in the motor task, the cognitive task, or in both tasks that may occur when two tasks are solved simultaneously] and (2) prioritization effects (given a priority either to the motor task or the cognitive task), which vary individually and which might influence the results of the intervention. However, drawbacks of a sequential motor-cognitive training are the unknown appropriate load characteristics (frequency, length, duration, type of exercise, and the temporal order of the cognitive intervention and the motor intervention) for favorable cognitive outcomes. For instance, the best benefit of an acute bout of motor exercises on cognitive performance was observed 11–20 min after cessation of the motor exercises. In contrast, another study reported that performing motor exercises 4 h after learning resulted in higher cognitive performance as compared to learning immediately afterward. Hence, it remains unclear whether cognitive training should be performed prior to or after motor exercises.

11Interestingly, a recent review that compared the effects of sequential with simultaneous motor-cognitive training, reported that the simultaneous training significantly improved cognitive performance in various populations, whereas the sequential training yield inconclusive results. The latter finding may be explained by the fact that up to day it is unknown what time interval between motor and cognitive exercises is optimal (see Figure 1). Different time intervals may activate different neurobiological pathways. Based on these findings, simultaneous motor-cognitive training seems a more promising and time-efficient approach to foster cognitive functions than sequential training regimens.

12Simultaneous motor-cognitive training or motor-cognitive dual-task training is defined as training where both motor training and cognitive training are performed at the same time. Simultaneous motor-cognitive training can be further classified regarding the supposed demands of the cognitive task (see Figure 2). We suggest to differentiate the two types of the supposed demands of cognitive tasks in simultaneous motor-cognitive training, which are presented in the following.

13A motor-cognitive training with additional cognitive task is similar to the “classical” dual-task approaches where, the secondary cognitive task is typically used as a distractor of the motor task. Distractor means that the additional cognitive task is not a relevant prerequisite to successfully complete the motor-cognitive task (task nonrelevant; e.g., walking and solving an arithmetic task or stationary cycling while citing alternate letters) and can be described as Thinking while Moving.

14When the cognitive task is “incorporated” into the motor task, the cognitive task is a relevant prerequisite to successfully solve the motor-cognitive task (e.g., walking to certain cones in a predefined order or dancing; see Figure 2). Hence, this form of motor cognitive training can be described as Moving while Thinking.

15We argue that incorporating the cognitive task(s) into the motor task(s) is more beneficial in terms of stabilizing neuroplasticity effects than using the cognition task as a distractor. Below, we will outline several reasons why this might be the case:

16Several studies suggest that the incorporation of a cognitive task into the motor task combines the advantageous effects of cognitive and motor training and leads to greater (motor-) cognitive improvements. For example, it was observed that the integration of the cognitive task into physical activity enhanced cognitive learning in children more than performing physical activity unrelated to the cognitive task.

17A training form that incorporates the cognitive task(s) into the motor task(s) is closer to daily life situations. For example, it is unlikely that an older person habitually solves an arithmetic task during walking, but it is likely that he/she walks through the supermarket while remembering what goods to buy and where to find those.

18Exercise benefits are moderated by expectations (beliefs toward the effectiveness of the intervention) and preferences. Given that even neurophysiological parameters are affected by individual preferences and expectations regarding the exercise intervention, it can be assumed that the exercise-induced neural adaption processes and, in turn, the cognitive outcomes are influenced by those factors, too. For example, for an intervention to be effective, the adherence rate (compliance) to the training must be high. The latter is largely influenced by the subjectively experienced meaningfulness (perceived importance of the intervention with respect to individual situation) of the training. As a cognitive task that is incorporated into a motor task closely resembles real-life situations, it is likely that such a combination is regarded as meaningful and, therefore, results in a high degree of adherence and in training success.

19Older adults and persons with dementia, for instance, exhibit impaired visuospatial abilities (e.g., remembering the location of a certain product in the supermarket). As physical fitness effectively enhances cognitive functions, an intervention, that targets the deficit in visuospatial memory, should, in our opinion, not only include a training of cognitive functions but also one of physical fitness. Moreover, given that the adaptions of the brain are task-specific, we propose that the ideal (motor-) cognitive training should also be specific (e.g., related to spatial memory) and should induce substantial transfer effects to everyday cognitive functions (e.g., remembering shopping list) as well as to activities of daily living (e.g., walking). These considerations suggest that the cognitive task should be incorporated into the motor task. In the context of our supermarket example remembering and walking to the respective goods can be combined. This approach is schematically depicted in Figure 2.

20If the cognitive task is incorporated into the motor task, no prioritization effects (which can be observed in motor-cognitive tasks with an additional cognitive task) would occur. Such prioritization effects (giving priority either to the cognitive or the motor task) are known to influence motor and cognitive performance as well as the activation of prefrontal structures. Theoretically, such prioritization-related effects could evoke distinct (undesired) adaptation processes.

21A further advantage of motor-cognitive training with incorporated cognitive tasks could be that multiple sensory systems are stimulated (due to the execution and control of the cognitive task and the motor task at the same point of time). Also, it is assumed that multisensory training environments better approximate all-day settings (which are ecologically more valid) and therefore provide an optimal basis for cognitive processes such as learning.

22Apart from a real-world setting as outlined for the proposed supermarket task, virtual reality environments offer the opportunity to combine cognitive and motor tasks without the need to construct a complex scenery. Respective approaches are the so-called “exergames”. Those video games, that are also a type of physical exercise task, can be classified within our proposed framework as simultaneous motor-cognitive training because they pose motor and cognitive demands simultaneously. However, as expectations always prove the rule, motor-cognitive tasks with an additional cognitive task are sometimes also common in a modern world [e.g., walking while texting or phoning]. Nevertheless, we argue that this circumstance does not challenge our proposed framework; however, one would have to adapt the training characteristics if the aim is to improve the use of a smartphone while walking.

23We conclude that further exercise-cognition research is strongly needed, and we recommend that the major goals of this research should be:

24The identification of optimal qualitative (e.g., type of exercise) and quantitative training characteristics (e.g., frequency, duration, intensity, and temporal proximity of cognitive and motor training), which effectively and sustainably enhance the individual cognitive reserve and show transfer to daily life activities. Thereto, future research should consider the concept of “personalized training (or personalized medicine, if exercise is seen as a “medicament”), which aims to understand the heterogeneity in (motor-cognitive) exercise responsiveness. “Personalized training” goes behind the “one-size-fits-all approach,” and the overall goal is to deliver tailored exercise prescriptions for the individual subject. Hence, participating subjects in future studies should be intensively screened and stratified into subgroups based on measures of physical fitness (e.g., cardiorespiratory fitness level or physical activity level assessed by questionnaires); motor fitness (e.g., coordinative abilities such as fine motor skills or hand/foot tapping speed); cognitive fitness (e.g., level of individual working memory performance); age, gender health status, and socioemotional status (e.g., measures of motivation, mood or stress). Furthermore, other potential moderators such as genotypic factors should be assessed if possible. In order to achieve a “personalized training,” the programming of (motor-cognitive) exercise training should not solely be based on external training load characteristics (work performed by the subject, e.g., 70 % of maximal oxygen uptake) but also on internal training load characteristics (physiological and/or psychological effects in response to the performed task; e.g., individual level of blood lactate), because the same external training loads could lead to varying internal training loads (e.g., metabolic response such as blood lactate level). For more detailed information on exercise prescriptions, we refer to the articles of,,,, and.

25In order to prove whether the incorporation of cognitive tasks into acute or chronic exercise interventions (as described, for example, in Figure 2) is more effective regarding the enhancement of cognitive performance than (I) a sole motor training, (II) a sole cognitive training, (III) a sequential motor-cognitive training, or (IV) simultaneous motor-cognitive training with a non-task-relevant secondary cognitive task and in order to verify (or identify further) underlying, causal mechanisms, future work should elaborate on detailed modeling of neurobehavioral effects of (motor-cognitive) exercise interventions. Since physical exercises influence cognitive performance on multiple levels and also trough diverse short- and long-term mechanisms, different behavioral proxies (e.g., neuropsychological clinical tests and/or gait analysis), neuroimaging modalities (e.g., functional magnetic resonance imaging and/or functional near-infrared spectroscopy) as well as molecular and cellular measures (e.g., BDNF and/or lactate) should be used to validate such a neurobehavioral model.

26FH and DH wrote the manuscript. LS and NM reviewed the drafted versions. All authors have read and approved the final version.

27The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.