The adaptive brain: aging and neurocognitive scaffolding.

There are declines with age in speed of processing, working memory, inhibitory function, and long-term memory, as well as decreases in brain structure size and white matter integrity. In the face of these decreases, functional imaging studies have demonstrated, somewhat surprisingly, reliable increases in prefrontal activation. To account for these joint phenomena, we propose the scaffolding theory of aging and cognition (STAC). STAC provides an integrative view of the aging mind, suggesting that pervasive increased frontal activation with age is a marker of an adaptive brain that engages in compensatory scaffolding in response to the challenges posed by declining neural structures and function. Scaffolding is a normal process present across the lifespan that involves use and development of complementary, alternative neural circuits to achieve a particular cognitive goal. Scaffolding is protective of cognitive function in the aging brain, and available evidence suggests that the ability to use this mechanism is strengthened by cognitive engagement, exercise, and low levels of default network engagement.

[1]  L. Hasher,et al.  Automatic and effortful processes in memory. , 1979 .

[2]  A Wingfield,et al.  Does the capacity of working memory change with age? , 1988, Experimental aging research.

[3]  Lynn Hasher,et al.  Working Memory, Comprehension, and Aging: A Review and a New View , 1988 .

[4]  Marcia K. Johnson,et al.  Aging and source monitoring. , 1989, Psychology and aging.

[5]  Timothy A. Salthouse,et al.  Theoretical Perspectives on Cognitive Aging , 1991 .

[6]  Morris Moscovitch,et al.  The neuropsychology of memory and aging. , 1992 .

[7]  Larry L. Jacoby,et al.  Automatic versus intentional uses of memory: aging, attention, and control. , 1993 .

[8]  P. Baltes,et al.  Sensory functioning and intelligence in old age: A strong connection , 1994 .

[9]  R. Mayeux,et al.  Influence of education and occupation on the incidence of Alzheimer's disease. , 1994, JAMA.

[10]  R. Malach,et al.  Object-related activity revealed by functional magnetic resonance imaging in human occipital cortex. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[11]  R. West,et al.  An application of prefrontal cortex function theory to cognitive aging. , 1996, Psychological bulletin.

[12]  Marcia K. Johnson,et al.  Feature memory and binding in young and older adults , 1996, Memory & cognition.

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

[14]  T. Salthouse The processing-speed theory of adult age differences in cognition. , 1996, Psychological review.

[15]  T. Allison,et al.  Differential Sensitivity of Human Visual Cortex to Faces, Letterstrings, and Textures: A Functional Magnetic Resonance Imaging Study , 1996, The Journal of Neuroscience.

[16]  P. Baltes,et al.  Emergence of a Powerful Connection Between Sensory and Cognitive Functions Across the Adult Life Span: A New Window to the Study of Cognitive Aging? , 1997 .

[17]  Anthony R. McIntosh,et al.  Age-Related Differences in Neural Activity during Memory Encoding and Retrieval: A Positron Emission Tomography Study , 1997, The Journal of Neuroscience.

[18]  C. Meltzer,et al.  Quantification of Neuroreceptors in the Living Human Brain: III. D2-Like Dopamine Receptors: Theory, Validation, and Changes during Normal Aging , 1997, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[19]  D. Schacter,et al.  Gist-Based False Recognition of Pictures in Older and Younger Adults , 1997 .

[20]  Daniel L. Schacter,et al.  False recognition in younger and older adults: Exploring the characteristics of illusory memories , 1997, Memory & cognition.

[21]  N. Kanwisher,et al.  The Fusiform Face Area: A Module in Human Extrastriate Cortex Specialized for Face Perception , 1997, The Journal of Neuroscience.

[22]  Nancy Kanwisher,et al.  A cortical representation of the local visual environment , 1998, Nature.

[23]  Paul B. Baltes,et al.  The Berlin aging study : aging from 70 to 100 , 1998 .

[24]  M. Banich The Missing Link: The Role of Interhemispheric Interaction in Attentional Processing , 1998, Brain and Cognition.

[25]  Gerd Kempermann,et al.  Experience-Induced Neurogenesis in the Senescent Dentate Gyrus , 1998, The Journal of Neuroscience.

[26]  S. Petersen,et al.  The effects of practice on the functional anatomy of task performance. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[27]  C. Schooler,et al.  The continuing effects of substantively complex work on the intellectual functioning of older workers. , 1999, Psychology and aging.

[28]  F. Craik,et al.  The effects of age on the neural correlates of episodic encoding. , 1999, Cerebral cortex.

[29]  Louise Stanczak,et al.  Neural Recruitment and Cognitive Aging: Two Hemispheres Are Better Than One, Especially as You Age , 1999 .

[30]  N. Cohen,et al.  Hippocampal system and declarative (relational) memory: Summarizing the data from functional neuroimaging studies , 1999, Hippocampus.

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

[32]  R. Dixon,et al.  Age-related cognitive deficits mediated by changes in the striatal dopamine system. , 2000, The American journal of psychiatry.

[33]  S A Small,et al.  Evaluating the function of hippocampal subregions with high‐resolution MRI in Alzheimer's disease and aging , 2000, Microscopy research and technique.

[34]  J. Jolles,et al.  The relation between global and limbic brain volumes on MRI and cognitive performance in healthy individuals across the age range , 2000, Neurobiology of Aging.

[35]  Edward E. Smith,et al.  Age Differences in the Frontal Lateralization of Verbal and Spatial Working Memory Revealed by PET , 2000, Journal of Cognitive Neuroscience.

[36]  Richard S. J. Frackowiak,et al.  Navigation-related structural change in the hippocampi of taxi drivers. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[37]  D. Bennett,et al.  Person-specific paths of cognitive decline in Alzheimer's disease and their relation to age. , 2000, Psychology and aging.

[38]  N. Raz Aging of the brain and its impact on cognitive performance: Integration of structural and functional findings. , 2000 .

[39]  Marcia K. Johnson,et al.  fMRI evidence of age-related hippocampal dysfunction in feature binding in working memory. , 2000, Brain research. Cognitive brain research.

[40]  Karl J. Friston,et al.  A Voxel-Based Morphometric Study of Ageing in 465 Normal Adult Human Brains , 2001, NeuroImage.

[41]  Robert A. Koeppe,et al.  Neurocognitive ageing of storage and executive processes , 2001 .

[42]  G L Shulman,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:A default mode of brain function , 2001 .

[43]  Mark D'Esposito,et al.  Age-related changes in brain–behaviour relationships: Evidence from event-related functional MRI studies , 2001 .

[44]  Stephan F. Taylor,et al.  Cerebral aging: integration of brain and behavioral models of cognitive function , 2001, Dialogues in clinical neuroscience.

[45]  S. Sikström,et al.  Aging cognition: from neuromodulation to representation , 2001, Trends in Cognitive Sciences.

[46]  J. Jonides,et al.  The neural basis of task-switching in working memory: effects of performance and aging. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[47]  Vinod Menon,et al.  Functional connectivity in the resting brain: A network analysis of the default mode hypothesis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[48]  Satoru Kobayashi,et al.  Effects of enriched environments with different durations and starting times on learning capacity during aging in rats assessed by a refined procedure of the Hebb‐Williams maze task , 2002, Journal of neuroscience research.

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

[50]  J. Schneider,et al.  Parahippocampal tau pathology in healthy aging, mild cognitive impairment, and early Alzheimer's disease , 2002, Annals of neurology.

[51]  C. Cotman,et al.  Exercise: a behavioral intervention to enhance brain health and plasticity , 2002, Trends in Neurosciences.

[52]  P. Reuter-Lorenz New visions of the aging mind and brain , 2002, Trends in Cognitive Sciences.

[53]  Roberto Cabeza,et al.  Aging Gracefully: Compensatory Brain Activity in High-Performing Older Adults , 2002, NeuroImage.

[54]  M. Farah,et al.  Neural Specialization for Letter Recognition , 2002, Journal of Cognitive Neuroscience.

[55]  T. Braver,et al.  A theory of cognitive control, aging cognition, and neuromodulation , 2002, Neuroscience & Biobehavioral Reviews.

[56]  G. Kempermann,et al.  Neuroplasticity in old age: Sustained fivefold induction of hippocampal neurogenesis by long‐term environmental enrichment , 2002, Annals of neurology.

[57]  D. Salat,et al.  Greater orbital prefrontal volume selectively predicts worse working memory performance in older adults. , 2002, Cerebral cortex.

[58]  Daniel L Schacter,et al.  Aging and strategic retrieval processes: reducing false memories with a distinctiveness heuristic. , 2002, Psychology and aging.

[59]  R. Cabeza Hemispheric asymmetry reduction in older adults: the HAROLD model. , 2002, Psychology and aging.

[60]  Y. Stern What is cognitive reserve? Theory and research application of the reserve concept , 2002, Journal of the International Neuropsychological Society.

[61]  D. Bennett,et al.  Cognitive Activity and Risk of Alzheimer's Disease , 2003 .

[62]  J. Morris,et al.  Functional deactivations: Change with age and dementia of the Alzheimer type , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[63]  D. Bennett,et al.  Alzheimer disease in the US population: prevalence estimates using the 2000 census. , 2003, Archives of neurology.

[64]  Alex Burdorf,et al.  Mental Work Demands Protect Against Cognitive Impairment: MAAS Prospective Cohort Study , 2003, Experimental aging research.

[65]  J. Yesavage,et al.  Differential associations between entorhinal and hippocampal volumes and memory performance in older adults. , 2003, Behavioral neuroscience.

[66]  Faith M. Gunning-Dixon,et al.  Neuroanatomical correlates of selected executive functions in middle-aged and older adults: a prospective MRI study , 2003, Neuropsychologia.

[67]  Richard S. J. Frackowiak,et al.  Age effects on the neural correlates of successful memory encoding. , 2003, Brain : a journal of neurology.

[68]  Douglas C. Noll,et al.  Working Memory for Complex Scenes: Age Differences in Frontal and Hippocampal Activations , 2003, Journal of Cognitive Neuroscience.

[69]  Joel E. Cohen,et al.  Human Population: The Next Half Century , 2003, Science.

[70]  R. Sutherland,et al.  The aging hippocampus: cognitive, biochemical and structural findings. , 2003, Cerebral cortex.

[71]  I. Lee,et al.  Correlation between fine motor activity and striatal dopamine D2 receptor density in patients with schizophrenia and healthy controls , 2003, Psychiatry Research: Neuroimaging.

[72]  S. Resnick,et al.  Longitudinal Magnetic Resonance Imaging Studies of Older Adults: A Shrinking Brain , 2003, The Journal of Neuroscience.

[73]  S. Tsai Brain-derived neurotrophic factor: a bridge between major depression and Alzheimer's disease? , 2003, Medical hypotheses.

[74]  J. Schneider,et al.  Education modifies the relation of AD pathology to level of cognitive function in older persons , 2003, Neurology.

[75]  Dick J. Veltman,et al.  Deep processing activates the medial temporal lobe in young but not in old adults , 2003, Neurobiology of Aging.

[76]  Richard J. Caselli,et al.  Hippocampal adaptation to face repetition in healthy elderly and mild cognitive impairment , 2004, Neuropsychologia.

[77]  Claudio Babiloni,et al.  Age-Related Functional Changes of Prefrontal Cortex in Long-Term Memory: A Repetitive Transcranial Magnetic Stimulation Study , 2004, The Journal of Neuroscience.

[78]  N. Raz,et al.  Shrinkage of the Entorhinal Cortex over Five Years Predicts Memory Performance in Healthy Adults , 2004, The Journal of Neuroscience.

[79]  Wei Wen,et al.  The topography of white matter hyperintensities on brain MRI in healthy 60- to 64-year-old individuals , 2004, NeuroImage.

[80]  R. Buckner Memory and Executive Function in Aging and AD Multiple Factors that Cause Decline and Reserve Factors that Compensate , 2004, Neuron.

[81]  M. Albert,et al.  Medial temporal lobe function and structure in mild cognitive impairment , 2004, Annals of neurology.

[82]  Denise C. Park,et al.  Aging reduces neural specialization in ventral visual cortex. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[83]  R. Cabeza,et al.  Task-independent and task-specific age effects on brain activity during working memory, visual attention and episodic retrieval. , 2004, Cerebral cortex.

[84]  D. Head,et al.  Differential aging of the medial temporal lobe , 2004, Neurology.

[85]  Stuart Maudsley,et al.  BDNF and 5-HT: a dynamic duo in age-related neuronal plasticity and neurodegenerative disorders , 2004, Trends in Neurosciences.

[86]  D. Head,et al.  Differential vulnerability of anterior white matter in nondemented aging with minimal acceleration in dementia of the Alzheimer type: evidence from diffusion tensor imaging. , 2004, Cerebral cortex.

[87]  A. Dale,et al.  Thinning of the cerebral cortex in aging. , 2004, Cerebral cortex.

[88]  W. Greenough,et al.  Environmental influences on cognitive and brain plasticity during aging. , 2004, The journals of gerontology. Series A, Biological sciences and medical sciences.

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

[90]  Gregory G. Brown,et al.  Increasing task difficulty facilitates the cerebral compensatory response to total sleep deprivation. , 2004, Sleep.

[91]  Randall R. Benson,et al.  Accrual of MRI white matter abnormalities in elderly with normal and impaired mobility , 2005, Journal of the Neurological Sciences.

[92]  D. Dagenbach,et al.  Recollection Training and Transfer Effects in Older Adults: Successful Use of a Repetition-Lag Procedure , 2005, Neuropsychology, development, and cognition. Section B, Aging, neuropsychology and cognition.

[93]  Robert C. Welsh,et al.  Aging and the Neural Correlates of Successful Picture Encoding: Frontal Activations Compensate for Decreased Medial-Temporal Activity , 2005, Journal of Cognitive Neuroscience.

[94]  L. Cohen,et al.  Mechanisms underlying recovery of motor function after stroke , 2005, Postgraduate Medical Journal.

[95]  Benjamin J. Shannon,et al.  Molecular, Structural, and Functional Characterization of Alzheimer's Disease: Evidence for a Relationship between Default Activity, Amyloid, and Memory , 2005, The Journal of Neuroscience.

[96]  N. Kanwisher,et al.  Reorganization of Visual Processing in Macular Degeneration , 2005, The Journal of Neuroscience.

[97]  Cindy Lustig,et al.  Brain aging: reorganizing discoveries about the aging mind , 2005, Current Opinion in Neurobiology.

[98]  M. Gluck,et al.  Neural Mechanisms Underlying Probabilistic Category Learning in Normal Aging , 2005, The Journal of Neuroscience.

[99]  J. Hellige,et al.  Aging and Individual Variation in Interhemispheric Collaboration and Hemispheric Asymmetry , 2005, Neuropsychology, development, and cognition. Section B, Aging, neuropsychology and cognition.

[100]  Cheryl L. Dahle,et al.  Regional brain changes in aging healthy adults: general trends, individual differences and modifiers. , 2005, Cerebral cortex.

[101]  Bart Rypma,et al.  Prefrontal modulation of working memory performance in brain injury and disease , 2006, Human brain mapping.

[102]  Jonas Persson,et al.  Structure-function correlates of cognitive decline in aging. , 2006, Cerebral cortex.

[103]  D. Blazer Cognitive Neuroscience of Aging: Linking Cognitive and Cerebral Aging , 2006 .

[104]  Anthony R. McIntosh,et al.  Age-related Changes in Brain Activity across the Adult Lifespan , 2006 .

[105]  Carles Falcón,et al.  Repetitive transcranial magnetic stimulation effects on brain function and cognition among elders with memory dysfunction. A randomized sham-controlled study. , 2006, Cerebral cortex.

[106]  Robert C. Welsh,et al.  Decreased neural specialization in old adults on a working memory task , 2006, Neuroreport.

[107]  C. Barnes,et al.  Neural plasticity in the ageing brain , 2006, Nature Reviews Neuroscience.

[108]  Jeffrey P. Toth,et al.  The Aging of Executive Functions. , 2006 .

[109]  Michael W. L. Chee,et al.  Age-related Changes in Object Processing and Contextual Binding Revealed Using fMR Adaptation , 2006, Journal of Cognitive Neuroscience.

[110]  C. Weiller,et al.  Dynamics of language reorganization after stroke. , 2006, Brain : a journal of neurology.

[111]  P. Greenwood Functional plasticity in cognitive aging: review and hypothesis. , 2007, Neuropsychology.

[112]  James K. Nelson,et al.  Age Differences in Deactivation: A Link to Cognitive Control? , 2007, Journal of Cognitive Neuroscience.

[113]  C. Lustig,et al.  Inhibitory Mechanisms and the Control of Attention , 2007 .

[114]  Michael M Merzenich,et al.  Intensive training in adults refines A1 representations degraded in an early postnatal critical period , 2007, Proceedings of the National Academy of Sciences.

[115]  R. Cabeza,et al.  Que PASA? The posterior-anterior shift in aging. , 2008, Cerebral cortex.

[116]  S. Petersen,et al.  A developmental fMRI study of reading and repetition reveals changes in phonological and visual mechanisms over age. , 2008, Cerebral cortex.

[117]  Scott T. Grafton,et al.  Structural Organization of the Corpus Callosum Predicts the Extent and Impact of Cortical Activity in the Nondominant Hemisphere , 2008, The Journal of Neuroscience.

[118]  S. Rombouts,et al.  Reduced resting-state brain activity in the "default network" in normal aging. , 2008, Cerebral cortex.

[119]  P. Reuter-Lorenz,et al.  Neurocognitive Aging and the Compensation Hypothesis , 2008 .

[120]  S. Gelman Learning from others: children's construction of concepts. , 2009, Annual review of psychology.

[121]  Jaime L. Napier,et al.  A tale of two systems: co-occurring mental health and substance abuse disorders treatment for adolescents. , 2009, Annual review of psychology.

[122]  Denise C. Park,et al.  Long-Term Memory and Aging: A Cognitive Neuroscience Perspective , 2009 .