Neural correlates of training-related working-memory gains in old age

Working memory (WM) functioning declines in old age. Due to its impact on many higher-order cognitive functions, investigating whether training can modify WM performance has recently been of great interest. We examined the relationship between behavioral performance and neural activity following five weeks of intensive WM training in 23 healthy older adults (M=63.7 years). 12 participants received adaptive training (i.e. individually adjusted task difficulty to bring individuals to their performance maximum), whereas the others served as active controls (i.e. fixed low-level practice). Brain activity was measured before and after training, using fMRI, while subjects performed a WM task under two difficulty conditions. Although there were no training-related changes in WM during scanning, neocortical brain activity decreased post training and these decreases were larger in the adaptive training group than in the controls under high WM load. This pattern suggests intervention-related increases in neural efficiency. Further, there were disproportionate gains in the adaptive training group in trained as well as in non-trained (i.e. attention, episodic memory) tasks assessed outside the scanner, indicating the efficacy of the training regimen. Critically, the degree of training-related changes in brain activity (i.e. neocortical decreases and subcortical increases) was related to the maximum gain score achieved during the intervention period. This relationship suggests that the decreased activity, but also specific activity increases, observed were functionally relevant.

[1]  Raymond J Dolan,et al.  Maintenance versus manipulation in verbal working memory revisited: an fMRI study , 2003, NeuroImage.

[2]  M. H Beauchamp,et al.  Dynamic functional changes associated with cognitive skill learning of an adapted version of the Tower of London task , 2003, NeuroImage.

[3]  J C Gore,et al.  Preliminary evidence of improved verbal working memory performance and normalization of task-related frontal lobe activation in schizophrenia following cognitive exercises. , 2000, The American journal of psychiatry.

[4]  Lars Nyberg,et al.  Brain imaging of human memory systems: between-systems similarities and within-system differences. , 2002, Brain research. Cognitive brain research.

[5]  Priti Shah,et al.  Aging, Training, and the Brain: A Review and Future Directions , 2009, Neuropsychology Review.

[6]  Lars Nyberg,et al.  Neural correlates of training-related memory improvement in adulthood and aging , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[7]  N. Raz The Aging Brain Observed in Vivo: Differential Changes and Their Modifiers. , 2005 .

[8]  D. Linden,et al.  The Working Memory Networks of the Human Brain , 2007, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[9]  D. Gronwall,et al.  Paced Auditory Serial Addition Task , 2013 .

[10]  Anthony R. McIntosh,et al.  Age-Related Changes in Regional Cerebral Blood Flow during Working Memory for Faces , 1998, NeuroImage.

[11]  T. Klingberg,et al.  Computerized working memory training after stroke–A pilot study , 2007, Brain injury.

[12]  B. Postle,et al.  Maintenance versus Manipulation of Information Held in Working Memory: An Event-Related fMRI Study , 1999, Brain and Cognition.

[13]  Todd S. Braver,et al.  Age-related changes in neural activity during performance matched working memory manipulation , 2008, NeuroImage.

[14]  Michael Brady,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[15]  Mark W. Woolrich,et al.  Advances in functional and structural MR image analysis and implementation as FSL , 2004, NeuroImage.

[16]  P. Reuter-Lorenz Cognitive neuropsychology of the aging brain. , 2000 .

[17]  Lars Bäckman,et al.  Transfer of Learning After Updating Training Mediated by the Striatum , 2008, Science.

[18]  Frederik L Giesel,et al.  Plasticity of cortical activation related to working memory during training. , 2004, The American journal of psychiatry.

[19]  R. Engle,et al.  Individual differences in working memory capacity and what they tell us about controlled attention, general fluid intelligence, and functions of the prefrontal cortex. , 1999 .

[20]  A. Kelly,et al.  Human functional neuroimaging of brain changes associated with practice. , 2005, Cerebral cortex.

[21]  T. Klingberg,et al.  Increased prefrontal and parietal activity after training of working memory , 2004, Nature Neuroscience.

[22]  Jonas Persson,et al.  Common prefrontal activations during working memory, episodic memory, and semantic memory , 2003, Neuropsychologia.

[23]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

[24]  L. Nyberg,et al.  Neural correlates of variable working memory load across adult age and skill: dissociative patterns within the fronto-parietal network. , 2009, Scandinavian journal of psychology.

[25]  L. Bäckman,et al.  The role of the striatal dopamine transporter in cognitive aging , 2005, Psychiatry Research: Neuroimaging.

[26]  C. Dodrill A Neuropsychological Battery for Epilepsy , 1978, Epilepsia.

[27]  G. Lautenschlager,et al.  Mediators of long-term memory performance across the life span. , 1996, Psychology and aging.

[28]  S. Petersen,et al.  Direct Comparison of Prefrontal Cortex Regions Engaged by Working and Long-Term Memory Tasks , 2001, NeuroImage.

[29]  Arthur F Kramer,et al.  Testing the limits of cognitive plasticity in older adults: application to attentional control. , 2006, Acta psychologica.

[30]  Lars Nyberg,et al.  Cognitive neuroscience of aging : linking cognitive and cerebral aging , 2004 .

[31]  Ching-Yune C. Sylvester,et al.  The Cognitive Neuroscience of Working Memory and Aging , 2005 .

[32]  Michelle Hampson,et al.  Functional connectivity between task-positive and task-negative brain areas and its relation to working memory performance. , 2010, Magnetic resonance imaging.

[33]  Paige E. Scalf,et al.  Training-induced plasticity in older adults: Effects of training on hemispheric asymmetry , 2007, Neurobiology of Aging.

[34]  R I Grossman,et al.  Brain imaging , 1999, Current Biology.

[35]  Mark D'Esposito,et al.  Region-specific changes in prefrontal function with age: a review of PET and fMRI studies on working and episodic memory. , 2005, Brain : a journal of neurology.

[36]  L. Nyberg,et al.  The correlative triad among aging, dopamine, and cognition: Current status and future prospects , 2006, Neuroscience & Biobehavioral Reviews.

[37]  Sharona M. Atkins,et al.  Memory enhancement in healthy older adults using a brain plasticity-based training program: A randomized, controlled study , 2006, Proceedings of the National Academy of Sciences.

[38]  Mike Martin,et al.  Memory training effects in old age as markers of plasticity: a meta-analysis. , 2009, Restorative neurology and neuroscience.

[39]  Paige E. Scalf,et al.  Cardiovascular fitness, cortical plasticity, and aging. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[40]  Torkel Klingberg,et al.  Training and transfer effects of executive functions in preschool children. , 2009, Developmental science.

[41]  Thomas S. Redick,et al.  Does working memory training generalize , 2010 .

[42]  A. Miyake,et al.  Models of Working Memory: Mechanisms of Active Maintenance and Executive Control , 1999 .

[43]  Bradley T. Christian,et al.  Measuring dopamine neuromodulation in the thalamus: Using [F-18]fallypride PET to study dopamine release during a spatial attention task , 2006, NeuroImage.

[44]  R. O’Reilly Biologically Based Computational Models of High-Level Cognition , 2006, Science.

[45]  Lars Nyberg,et al.  Plasticity of executive functioning in young and older adults: immediate training gains, transfer, and long-term maintenance. , 2008, Psychology and aging.

[46]  Joni Holmes,et al.  Adaptive training leads to sustained enhancement of poor working memory in children. , 2009, Developmental science.

[47]  Edward E. Smith,et al.  Neuroimaging studies of working memory: , 2003, Cognitive, affective & behavioral neuroscience.

[48]  Pamela K. Smith,et al.  Models of visuospatial and verbal memory across the adult life span. , 2002, Psychology and aging.

[49]  T. Klingberg Training and plasticity of working memory , 2010, Trends in Cognitive Sciences.

[50]  Serge A. R. B. Rombouts,et al.  Practice effects in the brain: Changes in cerebral activation after working memory practice depend on task demands , 2010, NeuroImage.

[51]  Nick F. Ramsey,et al.  Functional Anatomical Correlates of Controlled and Automatic Processing , 2001, Journal of Cognitive Neuroscience.

[52]  J. Callicott,et al.  Age-related alterations in default mode network: Impact on working memory performance , 2010, Neurobiology of Aging.

[53]  Hans Forssberg,et al.  Increased Brain Activity in Frontal and Parietal Cortex Underlies the Development of Visuospatial Working Memory Capacity during Childhood , 2002, Journal of Cognitive Neuroscience.

[54]  J. A. Pruszynski,et al.  Neural correlates , 2023 .

[55]  L. Nyberg,et al.  Linking cognitive aging to alterations in dopamine neurotransmitter functioning: Recent data and future avenues , 2010, Neuroscience & Biobehavioral Reviews.

[56]  A. Meyer-Lindenberg,et al.  Neurophysiological correlates of age-related changes in working memory capacity , 2006, Neuroscience Letters.

[57]  J. Kray,et al.  How useful is executive control training? Age differences in near and far transfer of task-switching training. , 2009, Developmental science.

[58]  Michael X. Cohen,et al.  Neural Mechanisms of Expert Skills in Visual Working Memory , 2006, The Journal of Neuroscience.

[59]  Joseph B. Sala,et al.  Increased neural efficiency with repeated performance of a working memory task is information-type dependent. , 2006, Cerebral cortex.

[60]  Susanne M. Jaeggi,et al.  Impact of working memory training on memory performance in old-old adults. , 2008, Psychology and aging.

[61]  M. McDaniel,et al.  The relationship between working memory capacity and executive functioning: evidence for a common executive attention construct. , 2010, Neuropsychology.

[62]  Susan M. Landau,et al.  Regional specificity and practice: Dynamic changes in object and spatial working memory , 2007, Brain Research.

[63]  R. Poldrack Imaging Brain Plasticity: Conceptual and Methodological Issues— A Theoretical Review , 2000, NeuroImage.

[64]  Florin Dolcos,et al.  Similarities and Differences in the Neural Correlates of Episodic Memory Retrieval and Working Memory , 2002, NeuroImage.

[65]  Ashley R. Morgan,et al.  A cognitive training intervention improves modality-specific attention in a randomized controlled trial of healthy older adults , 2011, Neurobiology of Aging.

[66]  Susanne M. Jaeggi,et al.  Improving fluid intelligence with training on working memory: a meta-analysis , 2008, Psychonomic Bulletin & Review.

[67]  Hauke R. Heekeren,et al.  Performance level modulates adult age differences in brain activation during spatial working memory , 2009, Proceedings of the National Academy of Sciences.

[68]  Terry E. Goldberg,et al.  Neurophysiological correlates of age-related changes in working memory updating , 2012, NeuroImage.

[69]  Jennifer L. Mozolic,et al.  Human Neuroscience , 2022 .

[70]  R. Coppola,et al.  Physiological characteristics of capacity constraints in working memory as revealed by functional MRI. , 1999, Cerebral cortex.

[71]  Hauke R. Heekeren,et al.  Load Modulation of BOLD Response and Connectivity Predicts Working Memory Performance in Younger and Older Adults , 2011, Journal of Cognitive Neuroscience.

[72]  Hugh Garavan,et al.  Practice‐related functional activation changes in a working memory task , 2000, Microscopy research and technique.

[73]  Shu-Chen Li,et al.  Working memory plasticity in old age: practice gain, transfer, and maintenance. , 2008, Psychology and aging.

[74]  J. Ashe,et al.  Cerebellum Activation Associated with Performance Change but Not Motor Learning , 2002, Science.

[75]  L. Nyberg,et al.  Learning by doing versus learning by thinking: An fMRI study of motor and mental training , 2006, Neuropsychologia.

[76]  S Hale,et al.  Converging evidence that visuospatial cognition is more age-sensitive than verbal cognition. , 2000, Psychology and aging.

[77]  A. Baddeley Working memory: looking back and looking forward , 2003, Nature Reviews Neuroscience.

[78]  Denise C. Park,et al.  Cognitive Aging: A Primer , 1999 .

[79]  Peter Fransson,et al.  Sustained and Transient Neural Modulations in Prefrontal Cortex Related to Declarative Long-Term Memory, Working Memory, and Attention , 2007, Cortex.

[80]  Edward E. Smith,et al.  Working Memory: A View from Neuroimaging , 1997, Cognitive Psychology.