Training-induced plasticity in older adults: Effects of training on hemispheric asymmetry

doi:10.1016/j.neurobiolaging.2005.12.012

Neurobiology of Aging

Volume 28, Issue 2, February 2007, Pages 272-283

https://doi.org/10.1016/j.neurobiolaging.2005.12.012 Get rights and content

Abstract

The extent to which cortical plasticity is retained in old age remains an understudied question, despite large social and scientific implications of such a result. Neuroimaging research reports individual differences in age-related activation, thereby educing speculation that some degree of plasticity may remain throughout life. We conducted a randomized longitudinal dual-task training study to investigate if performance improvements (a) change the magnitude or pattern of fMRI activation, thereby suggesting some plasticity retention in old age and (b) result in a reduction in asymmetry and an increase in age differences in fMRI activation as a compensatory model of performance-related activation predicts. Performance improvements were correlated with an increase in hemispheric asymmetry and a reduction in age differences in ventral and dorsal prefrontal activation. These results provide evidence for plasticity in old age and are discussed in relation to an alternative argument for the role of reduced asymmetry in performance improvements.

Section snippets

Participants

We recruited 34 older adults between the ages of 55 and 80 (mean = 66.11; range = 55–76). All participants were screened for claustrophobia, metallic implants, previous head surgery, psychiatric and neurological illnesses and were excluded from the study based on these criteria. All participants were required to score above a 51 on a modified version of the mini-mental status examination (mMMSE; highest score = 57) for inclusion in the study. Participants were randomly placed into either a control

Results

The analyses described here are primarily for older adults in the control and training groups. A complete report of results from younger adults in this task and training protocol has been previously described [18]. However, we include a subset of results from younger adults reported in Erickson et al. [18] here in order to assess age-related differences in performance and brain activation.

Discussion

We conducted a dual-task training study to examine: (a) the degree of plasticity in regions involved in the management and coordination of performing multiple tasks in older adults and (b) whether training-induced dual-task performance improvements results in increased or reduced age differences in activity and hemispheric asymmetry. In short, our results provide evidence inconsistent with current views of compensation models of reduced asymmetry, but consistent with the complementary

Acknowledgments

We would like to thank the National Institute on Aging (R01 AG025667 and R01 AG025032) for supporting this research. The research reported in this manuscript was carried out with the approval of the Institutional Review Board at the University of Illinois.

References (50)

T. Braver et al.
Neural mechanisms of transient and sustained cognitive control during task switching
Neuron
(2003)
R. Cabeza et al.
Aging gracefully: compensatory brain activity in high-performing older adults
NeuroImage
(2002)
K.I. Erickson et al.
Selective sparing of brain tissue in postmenopausal women receiving hormone replacement therapy
Neurobiol Aging
(2005)
K.I. Erickson et al.
The neural correlates of dual-task performance and task-preparation
NeuroImage
(2005)
O. Gruber et al.
Executive control emerging from dynamic interactions between brain systems mediating language, working memory and attentional processes
Acta Psychol
(2004)
C. Lustig et al.
Preserved neural correlates of priming in old age and dementia
Neuron
(2004)
M.P. Milham et al.
The relative involvement of anterior cingulate and prefrontal cortex in attentional control depends on nature of conflict
Cogn Brain Res
(2001)
P. Reuter-Lorenz
New visions of the aging mind and brain
Trends Cogn Sci
(2002)
M.D. Rugg et al.
The role of the prefrontal cortex in recognition memory and memory for source: an fMRI study
NeuroImage
(1999)
M.D. Rugg et al.
Neural correlates of retrieval processing in the prefrontal cortex during recognition and exclusion tasks
Neuropsychologia
(2003)

K. Ball et al.

Effects of cognitive training interventions with older adults—a randomized controlled trial

JAMA

(2002)

P.J. Batsakes et al.

Age-related differences in dual-task visual search: are performance gains retained?

J Gerontol: Psychol Sci

(2000)

T.E. Behrens et al.

Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging

Nat Neurosci

(2003)

L. Bherer et al.

Training effects on dual-task performace: are there age-related differences in plasticity of attentional control?

Psychol Aging

(2005)

R.L. Buckner

Functional-anatomic correlates of control processes in memory

J Neurosci

(2003)

S.A. Bunge et al.

A resource model of the neural basis of executive working memory

Proc Natl Acad Sci USA

(2000)

R. Cabeza et al.

Task-independent and task-specific age effects on brain activity during working memory, visual attention and episodic retrieval

Cereb Cortex

(2004)

S.J. Colcombe et al.

Aerobic fitness reduces brain tissue loss in aging humans

J Gerontol A Biol Sci Med Sci

(2003)

S.J. Colcombe et al.

Fitness effects on the cognitive function of older adults: a meta-analytic study

Psychol Sci

(2003)

S.J. Colcombe et al.

Cardiovascular fitness, cortical plasticity, and aging

Proc Natl Acad Sci USA

(2004)

S.J. Colcombe et al.

The implications of cortical recruitment and brain morphology for individual differences in inhibitory function in aging humans

Psychol Aging

(2005)

M. D’Esposito et al.

The neural basis of the central executive system of working memory

Nature

(1995)

Erickson KI, Colcombe SJ, Elavsky S, McAuley E, Korol DL, Scalf PE, Kramer AF. Interactive effects of fitness and...

Erickson KI, Colcombe SJ, Wadhwa R, Bherer L, Peterson M, Scalf P, et al. Training-induced changes in dual-task...

M. Fabiani et al.

Individual differences in P3 scalp distribution in older adults, and their relationship to frontal lobe function

Psychophysiology

(1998)

Cited by (191)

Aerobic exercise is associated with region-specific changes in volumetric, tensor-based, and fixel-based measures of white matter integrity in healthy older adults
2023, Neuroimage: Reports
White matter integrity and cognition have been found to decline with advancing adult age. Aerobic exercise may be effective in counteracting these declines. Generally, white matter integrity has been quantified using a volumetric measure (WMV) and with tensor-based parameters, such as fractional anisotropy (FA) and mean diffusivity (MD), the validity of which appears to be compromised in the presence of crossing fibers. Fixel-based analysis techniques claim to overcome this problem by yielding estimates of fiber density (FD), cross-section (FC), and their product (FDC) in multiple directions per voxel. In a sample of 61 healthy older adults (63–76 years old), we quantified changes in white matter integrity following an aerobic exercise intervention with the commonly used volumetric and tensor-based metrics (WMV, FA, MD) and with fixel-based metrics (FD, FC, FDC). We investigated the associations of changes in these white matter parameters with changes in cardiovascular fitness and Digit Symbol Substitution task (DSST) performance, a marker of perceptual speed. In line with previous findings, we observed maintained WMV in the corpus callosum of exercisers, and positive change-change correlations between WMV and fitness, and between WMV and perceptual speed. For FA and MD, group differences in change opposite to those hypothesized were found in the corpus callosum, posterior corona radiata, and superior longitudinal fasciculus at an uncorrected significance threshold. Likewise, regions in superficial WM in the prefrontal cortex showed group differences in FD and FDC change, uncorrected, with more positive change in controls and more negative change in exercisers. Finally, changes in FD and FDC were found to be inversely correlated to changes in fitness and DSST performance. The present results corroborate previous findings of WMV changes, but cast doubt on current physiological interpretations of both tensor-based and fixel-based indicators of white matter properties in the context of exercise intervention studies.
The effect of acute exercise on cognitive and motor inhibition – Does fitness moderate this effect?
2023, Psychology of Sport and Exercise
Given the extensive evidence on improvements in cognitive inhibition immediately following exercise, and the literature indicating that cognitive and motor inhibitory functions are mediated by overlapping brain networks, the aim of this study was to assess, for the first time, the effect of moderate intensity acute aerobic exercise on multi-limb motor inhibition, as compared to cognitive inhibition.
Participants were 36 healthy adults aged 40–60 years old (mean age 46.8 ± 5.7), who were randomly assigned to experimental or control groups. One-to-two weeks following baseline assessment, participants were asked to perform a three-limb (3-Limb) inhibition task and a vocal version of the Stroop before and after either acute moderate-intense aerobic exercise (experimental group) or rest (control).
Similar rates of improvement were observed among both groups from baseline to the pre-test. Conversely, a meaningful, yet non-significant trend was seen among the experimental group in their pretest to posttest improvement in both cognitive and motor tasks. In addition, exploratory analysis revealed significant group differences in favor of the experimental group among highly fit participants on the 3-Limb task. A significant correlation was indicated between the inhibition conditions, i.e., choice in the motor inhibition and color/word (incongruent) in the cognitive inhibition, especially in the improvement observed following the exercise.
Moderate-intensity acute aerobic exercise is a potential stimulator of both multi-limb motor inhibition and cognitive inhibition. It appears that high-fit participants benefit from exercise more than low-fit people. Additionally, performance on behavioral tasks that represent motor and cognitive inhibition is related. This observation suggests that fitness levels and acute exercise contribute to the coupling between cognitive and motor inhibition. Neuroimaging methods would allow examining brain-behavior associations of exercise-induced changes in the brain.
Targeting disrupted rich-club network organization with neuroplasticity-based computerized cognitive remediation in major depressive disorder patients
2022, Psychiatry Research
Disrupted rich-club organization has been extensively studied in major depressive disorder (MDD) patients. Although data indicate that neuroplasticity-based computerized cognitive remediation (nCCR) can accelerate clinical responses in MDD patients, the mechanisms underlying its antidepressant efficacy are unknown. In this study, all MDD patients underwent two (baseline and week 4) neuropsychological assessments and DTI imaging. Additionally, 17 MDD patients did nCCR for 30 hours spread across 4 weeks. Rich-club organization was calculated with a graph-theoretical approach, and SC-FC coupling was explored. After 4 weeks of treatment, the number of rich-club connections, global efficiency, and SC-FC coupling strength increased significantly and were negatively associated with TMT-B scores. The effects of nCCR on disrupted rich-club organization may partly underlie its efficacy in improving the executive function of patients with MDD. Effects of nCCR on disrupted rich-club organization may partly underlie its efficacy in improving the executive function of patients with MDD.
The Effect of Convergence Gamification Training in Community-Dwelling Older People: A Multicenter, Randomized Controlled Trial
2022, Journal of the American Medical Directors Association
It is necessary to improve the health of older adults through exercise, but there is no concrete way to implement it or an environment in which they can exercise continuously. Our objective was to confirm the safety and efficacy of information technology (IT) convergence gamification exercise equipment for older adults. We tried to demonstrate equivalence to conventional exercise by comparing the functional improvement.
Randomized controlled trial, with 8-week-long IT convergence exercises 3 times a week vs conventional exercise.
40 community-dwelling participants aged 60-85 years.
Participants were randomly divided into a conventional exercise group (group 1) and an IT convergence exercise group (group 2). Both groups were trained for 8 weeks, and functional assessment was performed before training (pre-evaluation), after training, and after 4 weeks of rest.
There were functional improvements in both groups. A comparison of the differences in the functional assessment between pre-evaluation and after 8 weeks of training yielded the following results. In group 1, the mean Five Times Sit to Stand Test–30 seconds was scored as 3.60 ± 2.56 (P < .015); Five Times Sit to Stand Test–5 times, −1.75 ± 2.04 s (P < .015); Berg Balance Scale, 1.05 ± 1.39 (P < .015); Timed Up-and-Go test, −0.64 ± 0.64 s (P < .015); and 10-m Walking Test, −0.35 ± 0.47 s (P < .015). And in group 2, the mean Five Times Sit to Stand Test–30 seconds (s) was scored as 3.70 ± 2.62 (P < .015), Five Times Sit to Stand Test–5 times, −1.65 ± 1.59 s (P < .015); Berg Balance Scale, 1.05 ± 1.00 (P < .015); Timed Up-and-Go test, −0.93 ± 0.68 s (P < .015); 10-m Walking Test, −0.41 ± 0.489 s (P < .015); Chair Sit and Reach test, 2.23 ± 3.19 cm (P < .015); and Korean version of the Falls Efficacy Scale–International, −1.05 ± 1.43 (P < .015).
The results of this study suggest that the IT convergence gamification exercise equipment such as balpro110 has exercise effects similar to conventional exercise and also has advantages as an alternative to exercise for older adults in the next generation.
Age-related differences in the role of the prefrontal cortex in sensory-motor training gains: A tDCS study
2021, Neuropsychologia
The ability to process multiple sources of information concurrently is particularly impaired as individuals age and such age-related increases in multitasking costs have been linked to impairments in response selection. Previous neuroimaging studies with young adults have implicated the left hemisphere prefrontal cortex (PFC) as a key neural substrate of response selection. In addition, several transcranial direct current stimulation (tDCS) studies have provided causal evidence implicating this region in response selection and multitasking operations. For example, Filmer et al. (2013b) demonstrated that typically observed response selection learning/training gains in young adults were disrupted via offline tDCS of left, but not right, PFC. Here, considering evidence of age-related structural and functional changes in the brains of older adults, we assessed if this pattern of response selection learning disruption via tDCS to the left PFC is observed in older adults, testing if this region remains a key response selection node as individuals age. In a pre-registered study with 58 older adults, we applied anodal, cathodal, and sham stimulation to left and right PFC, and measured performance as participants trained on low- and high-response selection load tasks. Active stimulation did not disrupt training in older adults as compared to younger adults from our previous study. The results highlight age-related differences in the casual neural substrates that subserve response selection and learning.
Asymmetrical Brain Plasticity: Physiology and Pathology
2021, Neuroscience
Citation Excerpt :
In a study from our lab, we observed that older subjects performing a working memory task showed mainly symmetrical activation, while higher accuracy was seen to be associated with increased (leftward) functional asymmetry of the superior parietal lobule (Esteves et al., 2018). Similarly, training aged subjects to perform a dual task was demonstrated to improve performance, and was accompanied by an increase in (leftward) asymmetry in ventral PFC activation (Erickson et al., 2007). In a series of manipulation studies, rTMS interferent modulation of the left dorsolateral PFC affected encoding of episodic memory in aged low performers, but no differences were found in aged high performers when this was applied to either hemisphere (Manenti et al., 2011).
The brain is inherently asymmetrical. How that attribute, manifest both structurally (volumetric, cytological, molecular) as well as functionally, relates to cognitive function, is not fully understood. Since the early descriptions of Paul Broca and Marc Dax it has been known that the processing of language in the brain is fundamentally asymmetrical. Contemporary imaging studies have corroborated early observations, and have also revealed significant functional links to multiple other systems, such as those sub serving memory or emotion.
Recent studies have demonstrated that laterality is both plastic and adaptive. Learning and training have shown to affect regional changes in asymmetry, such as that observed in the volume of the planum temporale associated with musical practice. Increasing task complexity has been demonstrated to induce recruitment of contralateral regions, suggesting that laterality is a manifestation of functional reserve. Indeed, in terms of cognitive function, successful aging is often associated with a reduction of asymmetrical activity.
The goal of this review is to survey and critically appraise the current literature addressing brain laterality, both morphological and functional, with particular emphasis on the asymmetrical plasticity associated with environmental factors and training. The plastic recruitment of contralateral areas associated with aging and unilateral lesions will be discussed in the context of the loss of asymmetry as a compensatory mechanism, and specific instances of maladaptive plasticity will be explored.

View all citing articles on Scopus

View full text

Training-induced plasticity in older adults: Effects of training on hemispheric asymmetry

Abstract

Section snippets

Participants

Results

Discussion

Acknowledgments

Neuron

NeuroImage

Neurobiol Aging

NeuroImage

Acta Psychol

Neuron

Cogn Brain Res

Trends Cogn Sci

NeuroImage

Neuropsychologia

Effects of cognitive training interventions with older adults—a randomized controlled trial

JAMA

Age-related differences in dual-task visual search: are performance gains retained?

J Gerontol: Psychol Sci

Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging

Nat Neurosci

Training effects on dual-task performace: are there age-related differences in plasticity of attentional control?

Psychol Aging

Functional-anatomic correlates of control processes in memory

J Neurosci

A resource model of the neural basis of executive working memory

Proc Natl Acad Sci USA

Task-independent and task-specific age effects on brain activity during working memory, visual attention and episodic retrieval

Cereb Cortex

Aerobic fitness reduces brain tissue loss in aging humans

J Gerontol A Biol Sci Med Sci

Fitness effects on the cognitive function of older adults: a meta-analytic study

Psychol Sci

Cardiovascular fitness, cortical plasticity, and aging

Proc Natl Acad Sci USA

The implications of cortical recruitment and brain morphology for individual differences in inhibitory function in aging humans

Psychol Aging

The neural basis of the central executive system of working memory

Nature

Individual differences in P3 scalp distribution in older adults, and their relationship to frontal lobe function

Psychophysiology