Review
A review of physical and cognitive interventions in aging

https://doi.org/10.1016/j.neubiorev.2014.03.019Get rights and content

Highlights

  • Cognitive and physical training is effective against age-related cognitive decline.

  • Neuropsychological, structural and functional neuroimaging evidence for aging brain neuroplasticity.

  • The role of functional brain connectivity in healthy aging.

  • Neuroscientific basis of new exergame designs, optimal training combinations.

  • Understanding/training the aging brain and associate impact with performance in daily routine settings.

Abstract

Maintaining a healthy brain is a critical factor for the quality of life of elderly individuals and the preservation of their independence. Challenging aging brains through cognitive training and physical exercises has shown to be effective against age-related cognitive decline and disease. But how effective are such training interventions? What is the optimal combination/strategy? Is there enough evidence from neuropsychological observations, animal studies, as well as, structural and functional neuroimaging investigations to interpret the underlying neurobiological mechanisms responsible for the observed neuroplasticity of the aging brain? This piece of work summarizes recent findings toward these questions, but also highlights the role of functional brain connectivity work, an emerging discipline for future research in healthy aging and the study of the underlying mechanisms across the life span. The ultimate aim is to conclude on recommended multimodal training, in light of contemporary trends in the design of exergaming interventions. The latter issue is discussed in conjunction with building up neuroscientific knowledge and envisaged future research challenges in mapping, understanding and training the aging brain.

Introduction

Growing older, may lead to wiser states of mind, but it may also lead to cognitive decline that interferes with our daily routines. Physical and cognitive interventions in elderly adults have challenged this deteriorating process and seem to be responsible for the induced neural change. These interventions target group (elderly individuals, aged > 60 years old) exhibits an augmented representation in the general population of western societies as a result of life expectancy increase along with a downwards trend in birth rates. The percentage of this group of people will reach 20% in 2025 and at least 30% in 2060 within the general population (Atchley and Barusch, 2004, FUTURAGE project, 2011). However, the physical and cognitive deterioration that occurs during aging poses challenges (social and financial) such as the need for social integration, as well as the financial burden resting on the public health systems which is associated to age-related disease, disability and dependency (Hertzog et al., 2008). Understanding age-associated changes in cognition is challenging and in proximity to the cognitive, mental and physical health issues of the elderly individuals.

Memory is probably the first of cognitive functions to exhibit various patterns of decline, i.e. episodic memory (Buckner, 2004, Grady, 2012, Hedden and Gabrieli, 2004), metamemory (Woodruff-Park, 1997), and the ability to retrieve both verbal and non-verbal material (Davis et al., 2003, Grady et al., 2006). Despite the fact that implicit memory is preserved in healthy older adults, in elders with Mild Cognitive Impairment (MCI) and even in Alzheimer's disease (AD) patients (Ballesteros and Reales, 2004, Ballesteros et al., 2012, Mitchell and Bruss, 2003, Wiggs et al., 2006), processing speed (Charness, 2008), as well as, attentional control and working memory, which fall under the umbrella term executive functions (Andrés and Van der Linden, 2000, Grady, 2012, Hahn and Kramer, 1995) exhibit robust declines. These deteriorations are associated to age-related changes at the neural (structural and functional) level as well. For instance, structural changes in the striatum and the prefrontal cortex such as reduced brain volume and thinning of the cortex are commonly observed in the aging brain (Haug and Eggers, 1991, Raz et al., 2004). Moreover, reduced connectivity between frontal and posterior areas of the human brain may account for the decline in attentional function observed with age (Grady, 2012). Nevertheless, it is plausible that the synaptic connectivity, and not the neural loss, is responsible for the age-related cognitive decline (Duan et al., 2003, Morrison and Baxter, 2012).

An adequate cognitive status and physical well-being play crucial roles in daily activities such as driving and managing finances, and adequate work performance (Callahan et al., 2003, Charness, 2008, Charness and Czaja, 2006, Drag and Bieliauskas, 2010, Wegman and McGee, 2004; for a meta-analysis of physical performance and daily functioning see Heyn et al., 2008). Consequently, the independent living promotion as well as the participation of senior citizens in the job market and society, call for evidence-based interventions focused on maintaining cognitive function and physical well-being during the silver ages (Ferri et al., 2005). At the same time, a greater integration between the cognitive functions and related brain areas should be envisaged in a multi-disciplinary way in view of emerging pilot studies and advances in structural and functional imaging, brain networks, electrophysiological evidence and multi-level modeling.

This review summarizes recent work in the efficacy of non-pharmaceutical interventions to enhance cognitive performance and prevent or at least slow down the age-related cognitive decline. We discuss several of the most pressing issues with respect to the use of cognitive and physical training to promote healthy aging, in an attempt to summarize and sketch the likely neurobiological mechanisms responsible for the positive effects of such type of interventions. Evidence is drawn from studies focusing on neuropsychological evaluation, but also structural and functional neuroimaging approaches and associated interpretations. Our review also highlights recent approaches with functional brain connectivity work, which is considered as an emerging discipline for the forth-coming research agenda in healthy aging and the study of the underlying cognitive decline mechanisms across the life span. The emerging picture is complemented by evidences from electrophysiological recordings and neurobiological mechanisms. Based on all of these, the ultimate aim of this review is to focus on recommending combined cognitive and physical training, and the emergence of contemporary trends in the design of exergaming interventions. The phrase exergaming or exergames derives from the combination of ‘exercise’ and ‘games’ and relates to computer games that involve deliberate intense physical activity (Mueller et al., 2003). The latter issue is discussed in view of the aforementioned neuroscientific evidence and the envisaged future research challenges in mapping, understanding and training the aging brain.

The terms cognitive training, mental activity, cognitive stimulation, cognitive rehabilitation and cognitive exercise have interchangeably referred to the general notion of cognitive intervention (Buschert et al., 2010; for reviews see Clare and Woods, 2004, Gates and Valenzuela, 2010).

Clare and Woods (2004) have attempted to clarify the terminology associated with cognitive interventions, by proposing two main categories; cognitive stimulation/reality orientation and cognitive training/cognitive rehabilitation. The former category may include procedures designed to provide general cognitive stimulation and enhance people's social skills. This category of intervention usually consists of structured group activities and discussions, and is theoretically driven by the use-it-or-lose-it (Hultsch et al., 1999) and the cognitive-enrichment theories (Hertzog et al., 2008). Namely, this category does not target a specific cognitive process, but rather it involves activities that require general cognitive resources. The latter category refers to interventions designed to train specific cognitive processes (Clare and Woods, 2004), and are based on theories of neuroplasticity (Buschert et al., 2010, Mahncke et al., 2006b, Pascual-Leone et al., 2011).

There is an ongoing debate regarding the effectiveness of the aforementioned categories of cognitive interventions as a counter measure for cognitive decline (Hertzog et al., 2008, Salthouse, 2006). However, a common ground among most researchers is that the cognitive training/cognitive rehabilitation intervention exhibits positive effects with properly designed experimental controlled studies. In this review we will focus on this specific category (see Table 1). Cognitive rehabilitation can be precisely defined as a holistic biopsychosocial approach (McLellan, 1991) that takes into account the person's emotional, cognitive and social deficits which stem from disease or injury (Prigatano, 1999). This type of intervention improves daily functioning, and the patient's quality of life (Wilson, 1997). On the other hand, cognitive training, also termed as cognitive exercise (Gates and Valenzuela, 2010) can be defined as a standardized set of exercises (Clare and Woods, 2004, Martin et al., 2011), which involves repeated practice and increasing levels of difficulty, and taps into specific cognitive functions.

Cognitive rehabilitation is usually coined for interventions that target a pathological population with cognitive deficits; cognitive training/exercise is used in interventions that target both healthy people and patients with cognitive deficits (Clare and Woods, 2004). The level of individualization differentiates among these two types of intervention. The cognitive rehabilitation follows a highly individualized approach, which demands the involvement of health professionals, and care-givers (Wilson, 1997). In cognitive training, the only individualized aspect is the difficulty of the exercises, which is automatically adjusted according to the participants’ performance. Consequently, cognitive training is a more flexible approach with both individual (Bernhardt et al., 2002, Koltai et al., 2001, Moore et al., 2001) and group participation (Davis et al., 2001, Farina et al., 2002). The involvement of care-givers and health professionals in cognitive training is not a necessary condition/prerequisite (Quayhagen et al., 2000).

Physical training interventions usually involve quite a wide range of activities (Colcombe and Kramer, 2003). For the World Health Organization (WHO), physical activity for elderly individuals includes “recreational or leisure-time physical activity, transportation (e.g. walking or cycling), occupational (if the person is still engaged in work), household chores, play, games, sports or planned exercise, in the context of daily, family, and community activities” (WHO, 2010). According to the definitions provided by the Institute of Medicine and the American College of Sports Medicine (ACSM) though, physical activity refers to “body movement that is produced by the contraction of skeletal muscles and that increases energy expenditure” while exercise “refers to planned, structured, and repetitive movement to improve or maintain one or more components of physical fitness” (Chodzko-Zajko et al., 2009). Table 1 familiarizes the reader with the utilized terminologies and summarizes the recommendations for each type of physical activity from the two aforementioned main sources, namely, the WHO and the ACSM.

The benefits of physical activity and exercise on the body have been well-established by research (Rooney, 1993) and are nowadays much promoted by associations and agencies working with elderly individuals, as well as, governments and world organizations (e.g. the World Health Organization (WHO), 2010). The relationship between physical activity and mental health or cognition has only recently been strongly emphasized (Fratiglioni et al., 2004, Van Gelder et al., 2004). The key question, which remains to be answered, is the causality of this relationship, namely whether decreased physical activity that precedes cognitive decline could be either the cause of the decline per se or be the result of the prodromal cognitive impairment (Eggermont et al., 2006). In order to explore this causality, but also intervene non-pharmacologically, intervention studies incorporating physical activity and exercise have been deployed in numerous settings and under different conditions. Most interventions execute one (e.g. aerobic when focusing on cardiovascular fitness) or combinations of more than one categories (see Table 2, e.g. aerobic exercise training (AET) and resistance exercise training (RET) plus balance). The main parameters to control within such an intervention are the duration of training (how long the actual training lasts), the length of exercise intervention (how many weeks/months) and the outcome measure tools (e.g. cardiovascular improvement, senior fitness test, etc., Colcombe and Kramer, 2003).

During the past decade though, a renewed interest was noticed in using technological assistance, including user interface feedback loops, so as to physically (but also mentally) train healthy elderly individuals. Researchers and practitioners in the field of aging introduced elderly audiences to cognitive training and stimulation games which are now enjoyed within the context of computer and/or game consoles; and in a further step toward mens sana in corpore sano, to provide physical stimulation or rehabilitation exercises in the relaxed form of exergaming (Bamidis et al., 2011, Billis et al., 2010). The games that assist in achieving and improving spiritual and physical fitness have shaped a newer type of interventions, the so-called Silver Gaming Interventions.

Numerous recent studies have investigated how exergaming/silvergaming can be specifically applied to the needs of seniors, and the impact of such programs on specific issues as diverse as intergenerational interactions (Khoo et al., 2010) and geriatric depression (Rosenberg et al., 2010). The majority of these studies though have yet featured very small numbers of participants, in focused pilot studies and focus group environments. This line of research is certainly growing though and has been the subject of recent meta-analyses (Powers et al., 2013) and systematic reviews (Kueider et al., 2012).

Section snippets

Neuropsychological evidence for benefits of cognitive and physical interventions on brain health

In this section, we revisit evidence for the beneficial effects of each intervention, i.e. cognitive and physical. In line with the Ancient Greek proverb Healthy mind in a healthy body, the combined physical and cognitive training researches the separate and the combined effects of this intervention on cognitive performance of healthy elderly individuals. Although a limited number of studies analytically compare the effects of each training type (i.e. cognitive or physical activity) with those

Neuroimaging evidence for benefits of cognitive and physical interventions on brain health

In this section we collect evidence for the likely benefits of cognitive and physical interventions as these are manifested in recent neuroimaging (structural and functional) studies. We aim to outline the likely neurobiological mechanisms that underlie the process of maintaining brain health and healthy aging. Emphasis is drawn on different study threads, namely, structural/functional neuroimaging, as well as, the more recent notion of functional brain connectivity, across different thematic

Electrophysiological findings on brain health

Electrophysiological recordings are usually conducted by means of (resting-state) Electroencephalogram (EEG) or Event Related Potentials (ERPs), with subsequent analysis usually focusing on different brain signal frequency bands in connection with (or without) topographical/anatomical correlates. To this extent, it has been known for quite some time, that physiological aging is accompanied by EEG spectral slowing, since the amplitude of alpha oscillation decreases and gives rise to theta and

Models of neurobiological mechanisms in healthy aging and the case of combined physical and cognitive interventions

What might be the advantage of combined physical and cognitive exercise and can we use this knowledge to make the exercise protocols more effective? We postulate that the advantage is largely based on the brain's ability to adapt to new environmental challenges by plastic reorganization of the cortex. From an evolutionary perspective, physical and cognitive challenges were highly interwoven (Kempermann et al., 2010). The dissociation in current society (playing computer games or desk work) is a

Drawing the threads together and suggesting future research

The protective effects of cognitive training for cognitive decline and dementia which formed classical knowledge found in prospective observational studies have been lately enriched with more convincing neuroscientific evidence. However, in addition to that, the currently available knowledge is supportive of physical exercise having beneficial effects on cognition by enhancing neuroplasticity, thereby preventing cognitive decline and pathological aging and promoting healthy aging. Recent

Acknowledgments

This work has been partially funded by the European community's 7th framework programme (USEFIL, project no. 223920), the CIP-PSP program (LongLastingMemories, project no. 238904; and DISCOVER, project no. 297268). Authors would like to thank: P. Fissler and I T. Kollassa of Clinical and Biological Psychology, Institute of Psychology & Education, University of Ulm, Germany; F. Thurm of Lifespan Developmental Neuroscience Group, Department of Psychology, Technical University of Dresden, Germany;

References (200)

  • H.P. Davis et al.

    Acquisition, recall, and forgetting of verbal information in long-term memory by young, middle-aged, and elderly individuals

    Cortex

    (2003)
  • M.P. Deiber et al.

    Age-associated modulations of cerebral oscillatory patterns related to attention control

    Neuroimage

    (2013)
  • C. Eckerstrom et al.

    Small baseline volume of left hippocampus is associated with subsequent conversion of MCI into dementia: the Goteborg MCI study

    J. Neurol. Sci.

    (2008)
  • L. Eggermont et al.

    Exercise, cognition and Alzheimer's disease: more is not necessarily better

    Neurosci. Biobehav. Rev.

    (2006)
  • A. Engvig et al.

    Effects of memory training on cortical thickness in the elderly

    Neuroimage

    (2010)
  • C.P. Ferri et al.

    Global prevalence of dementia: a Delphi consensus study

    Lancet

    (2005)
  • P. Fissler et al.

    Novelty interventions to enhance broad cognitive abilities and prevent dementia: synergistic approaches for the facilitation of positive plastic change

    Prog. Brain Res.

    (2013)
  • L. Fratiglioni et al.

    An active and socially integrated lifestyle in late life might protect against dementia

    Lancet Neurol.

    (2004)
  • C.S. Geibig et al.

    Functional recruitment of newborn hippocampal neurons after experimental stroke

    Neurobiol. Dis.

    (2012)
  • H. Haug et al.

    Morphometry of the human cortex cerebri and corpus striatum during aging

    Neurobiol. Aging

    (1991)
  • P.C. Heyn et al.

    Endurance and strength training outcomes on cognitively impaired and cognitively intact older adults: a meta-analysis

    J. Nutr. Health Aging

    (2008)
  • M.C. Ho et al.

    Age-related changes of task-specific brain activity in normal aging

    Neurosci. Lett.

    (2012)
  • K. Holzschneider et al.

    Cardiovascular fitness modulates brain activation associated with spatial learning

    Neuroimage

    (2012)
  • K. Hötting et al.

    Beneficial effects of physical exercise on neuroplasticity and cognition

    Neurosci. Biobehav. Rev.

    (2013)
  • P.A. Adlard et al.

    Voluntary exercise decreases amyloid load in a transgenic model of Alzheimer's disease

    J. Neurosci.

    (2005)
  • D.M. Alexander et al.

    EEG markers for cognitive decline in elderly subjects with subjective memory complaints

    J. Integr. Neurosci.

    (2006)
  • P. Andrés et al.

    Age-related differences in supervisory attentional system functions

    J. Gerontol. Ser. B

    (2000)
  • J.A. Anguera et al.

    Video game training enhances cognitive control in older adults

    Nature

    (2013)
  • L. Astolfi et al.

    Comparison of different cortical connectivity estimators for high-resolution EEG recordings

    Hum. Brain Mapp.

    (2007)
  • R.C. Atchley et al.

    The demography of aging

  • K. Ball et al.

    The impact of speed of processing training on cognitive and everyday functions

    J. Gerontol. Ser. B

    (2007)
  • S. Ballesteros et al.

    Neural correlates of conceptual object priming in young and older adults: an event-related functional magnetic resonance imaging study

    Neurobiol. Aging

    (2012)
  • P.D. Bamidis et al.

    A Web services-based exergaming platform for senior citizens: the Long Lasting Memories project approach to e-health care

    Conf. Proc. IEEE Eng. Med. Biol. Soc.

    (2011)
  • D.E. Barnes et al.

    A longitudinal study of cardiorespiratory fitness and cognitive function in healthy older adults

    J. Am. Geriatr. Soc.

    (2003)
  • C. Basak et al.

    Can training in a real-time strategy video game attenuate cognitive decline in older adults?

    Psychol. Aging

    (2008)
  • O.M. Bazanova et al.

    Interpreting EEG alpha activity

    Neurosci. Biobehav. Rev.

    (2013)
  • T. Bernhardt et al.

    The influence of an everyday-related cognitive training on attention and memory performance of people with dementia

    Int. J. Gerontol. Geriatr.

    (2002)
  • L. Bezzola et al.

    Training-induced neural plasticity in golf novices

    J. Neurosci.

    (2011)
  • A.S. Billis et al.

    A game-like interface for training seniors’ dynamic balance and coordination

  • J. Boyke et al.

    Training-induced brain structure changes in the elderly

    J. Neurosci.

    (2008)
  • J.H. Burdette et al.

    Using network science to evaluate exercise-associated brain changes in older adults

    Front. Aging Neurosci.

    (2010)
  • V. Buschert et al.

    Cognitive intervention in Alzheimer disease

    Nat. Rev. Neurol.

    (2010)
  • M. Buschkuehl et al.

    Impact of working memory training on memory performance in old-old adults

    Psychol. Aging

    (2008)
  • S. Carroll et al.

    What is the relationship between exercise and metabolic abnormalities? A review of the metabolic syndrome

    Sports Med.

    (2004)
  • R.C. Cassilhas et al.

    The impact of resistance exercise on the cognitive function of the elderly

    Med. Sci. Sports Exerc.

    (2007)
  • N. Charness

    Aging and human performance

    Hum Factors

    (2008)
  • N. Charness et al.

    Older Worker Training: What We Know and Don’t Know

    (2006)
  • B. Cheeran et al.

    A common polymorphism in the brain-derived neurotrophic factor gene (BDNF) modulates human cortical plasticity and the response to rTMS

    J. Physiol.

    (2008)
  • J.M. Chein et al.

    Expanding the mind's workspace: training and transfer effects with a complex working memory span task

    Psychon. Bull. Rev.

    (2010)
  • D.B. Chklovskii et al.

    Cortical rewiring and information storage

    Nature

    (2004)
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      The age-related deterioration in cognitive performance most likely stems from structural changes in the brain, manifested as losses of grey and white matter volume especially in frontal cortical areas (Lupien et al., 1998; Penke et al., 2010) and less efficient synaptic transmission (Bäckman et al., 2010). Even though the impact of aging on cortical function remains poorly understood, increasing evidence point to notable aging-related changes in spontaneous cortical oscillatory activity measured by electroencephalography (EEG) and magnetoencephalography (MEG) (Bamidis et al., 2014; Berendse et al., 2000; Cummins & Finnigan, 2007; Finnigan & Robertson, 2011; Vlahou et al., 2014). The physiological changes in cortical structure and function may signify memory disorders, such as Alzheimer’s disease (Bäckman et al., 2005; Lupien et al., 1998), but the neurocognitive capacity as well as brain structure and function vary greatly also within healthy aging populations (Aine et al., 2011).

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