Neural Reorganization and Compensation in Aging

According to prominent theories of aging, the brain may reorganize to compensate for neural deterioration and prevent or offset cognitive decline. A frequent and striking finding in functional imaging studies is that older adults recruit additional regions relative to young adults performing the same task. This is often interpreted as evidence for functional reorganization, suggesting that, as people age, different regions or networks may support the same cognitive functions. Associations between additional recruitment and better performance in older adults have led to the suggestion that the additional recruitment may contribute to preserved cognitive function in old age and may explain some of the variation among individuals in preservation of function. However, many alternative explanations are possible, and recent findings and methodological developments have highlighted the need for more systematic approaches to determine whether reorganization occurs with age and whether it benefits performance. We reevaluate current evidence for compensatory functional reorganization in the light of recent moves to address these challenges.

[1]  M. Andersson,et al.  Longitudinal evidence for diminished frontal cortex function in aging , 2010, Proceedings of the National Academy of Sciences.

[2]  Linda Geerligs,et al.  Reduced specificity of functional connectivity in the aging brain during task performance , 2014, Human brain mapping.

[3]  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.

[4]  Menno P. Witter,et al.  A pathophysiological framework of hippocampal dysfunction in ageing and disease , 2011, Nature Reviews Neuroscience.

[5]  T G Turkington,et al.  Selective and divided visual attention: Age‐related changes in regional cerebral blood flow measured by H215O PET , 1997, Human brain mapping.

[6]  L. Nyberg,et al.  Brain Characteristics of Individuals Resisting Age-Related Cognitive Decline over Two Decades , 2013, The Journal of Neuroscience.

[7]  Bradley P. Sutton,et al.  Span, CRUNCH, and Beyond: Working Memory Capacity and the Aging Brain , 2010, Journal of Cognitive Neuroscience.

[8]  C. Miniussi,et al.  Successful physiological aging and episodic memory: A brain stimulation study , 2011, Behavioural Brain Research.

[9]  Hans-Jochen Heinze,et al.  Functional phenotyping of successful aging in long‐term memory: Preserved performance in the absence of neural compensation , 2010, Hippocampus.

[10]  C. Frith,et al.  The functional neuroanatomy of episodic memory , 1997, Trends in Neurosciences.

[11]  L Tugan Muftuler,et al.  The effects of age, memory performance, and callosal integrity on the neural correlates of successful associative encoding. , 2011, Cerebral cortex.

[12]  P. Baltes,et al.  Selection, optimization, and compensation as strategies of life management: correlations with subjective indicators of successful aging. , 1998, Psychology and aging.

[13]  L. Nyberg,et al.  Memory aging and brain maintenance , 2012, Trends in Cognitive Sciences.

[14]  Richard Henson,et al.  Forward inference using functional neuroimaging: dissociations versus associations , 2006, Trends in Cognitive Sciences.

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

[16]  J. Rohrbaugh,et al.  Electrocortical signs of levels of processing: perceptual analysis and recognition memory. , 1980, Psychophysiology.

[17]  Ian J. Deary,et al.  Is retaining the youthful functional anatomy underlying speed of information processing a signature of successful cognitive ageing? An event-related fMRI study of inspection time performance , 2008, NeuroImage.

[18]  M. Rajah,et al.  Age-related differences in brain activity in the subsequent memory paradigm: A meta-analysis , 2014, Neuroscience & Biobehavioral Reviews.

[19]  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.

[20]  R. Cabeza,et al.  Effects of aging on true and false memory formation: An fMRI study , 2007, Neuropsychologia.

[21]  William Meredith,et al.  Latent curve analysis , 1990 .

[22]  R. Marioni,et al.  Age-associated cognitive decline. , 2009, British medical bulletin.

[23]  Jonas Persson,et al.  Longitudinal structure-function correlates in elderly reveal MTL dysfunction with cognitive decline. , 2012, Cerebral cortex.

[24]  J. Logan,et al.  Under-Recruitment and Nonselective Recruitment Dissociable Neural Mechanisms Associated with Aging , 2002, Neuron.

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

[26]  M. Rugg,et al.  The relationship between aging, performance, and the neural correlates of successful memory encoding. , 2009, Cerebral cortex.

[27]  M. Rugg,et al.  The Relationship Between Brain Activity, Cognitive Performance, and Aging: The Case of Memory , 2009 .

[28]  Leslie G. Ungerleider,et al.  Age-related reductions in human recognition memory due to impaired encoding. , 1995, Science.

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

[30]  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.

[31]  Paul Wright,et al.  Age-related Neural Reorganization during Spoken Word Recognition: The Interaction of Form and Meaning , 2012, Journal of Cognitive Neuroscience.

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

[33]  Gary H. Glover,et al.  Variable effects of aging on frontal lobe contributions to memory , 2002, Neuroreport.

[34]  Karl J. Friston,et al.  Characterizing the Response of PET and fMRI Data Using Multivariate Linear Models , 1997, NeuroImage.

[35]  Ian J Deary,et al.  The impact of childhood intelligence on later life: following up the Scottish mental surveys of 1932 and 1947. , 2004, Journal of personality and social psychology.

[36]  R. Gur,et al.  Laterality in functional brain imaging studies of schizophrenia. , 1999, Schizophrenia bulletin.

[37]  Lorraine K. Tyler,et al.  Age-related functional reorganization, structural changes, and preserved cognition , 2014, Neurobiology of Aging.

[38]  R. Dixon,et al.  Psychological compensation: a theoretical framework. , 1992, Psychological bulletin.

[39]  Edward T. Bullmore,et al.  Age-related changes in modular organization of human brain functional networks , 2009, NeuroImage.

[40]  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.

[41]  Jonas Persson,et al.  Age-related and Genetic Modulation of Frontal Cortex Efficiency , 2014, Journal of Cognitive Neuroscience.

[42]  R. V. Van Heertum,et al.  Brain networks associated with cognitive reserve in healthy young and old adults. , 2005, Cerebral cortex.

[43]  C. Depp,et al.  Definitions and predictors of successful aging: a comprehensive review of larger quantitative studies. , 2006, The American journal of geriatric psychiatry : official journal of the American Association for Geriatric Psychiatry.

[44]  Lisa T. Eyler,et al.  A Review of Functional Brain Imaging Correlates of Successful Cognitive Aging , 2011, Biological Psychiatry.

[45]  A. McNeil,et al.  Latent Curve Models: A Structural Equation Approach , 2007 .

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

[47]  R. Sperling,et al.  Age-related memory impairment associated with loss of parietal deactivation but preserved hippocampal activation , 2008, Proceedings of the National Academy of Sciences.

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

[49]  J. Ware,et al.  Applied Longitudinal Analysis , 2004 .

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

[51]  K. Schaie A GENERAL MODEL FOR THE STUDY OF DEVELOPMENTAL PROBLEMS. , 1965, Psychological bulletin.

[52]  C. Grady Functional brain imaging and age-related changes in cognition , 2000, Biological Psychology.

[53]  Yaakov Stern,et al.  Age-related changes in brain activation during a delayed item recognition task , 2007, Neurobiology of Aging.

[54]  R. N. Spreng,et al.  Reliable differences in brain activity between young and old adults: A quantitative meta-analysis across multiple cognitive domains , 2010, Neuroscience & Biobehavioral Reviews.

[55]  Anthony Randal McIntosh,et al.  Partial Least Squares (PLS) methods for neuroimaging: A tutorial and review , 2011, NeuroImage.

[56]  Karl J. Friston,et al.  Decoding episodic memory in ageing: A Bayesian analysis of activity patterns predicting memory , 2012, NeuroImage.

[57]  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.

[58]  M. Cotelli,et al.  Better together: Left and right hemisphere engagement to reduce age-related memory loss , 2015, Behavioural Brain Research.

[59]  Denise C. Park,et al.  Both left and right posterior parietal activations contribute to compensatory processes in normal aging , 2012, Neuropsychologia.

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

[61]  B. Miller,et al.  Neural Correlates of Syntactic Processing in the Nonfluent Variant of Primary Progressive Aphasia , 2010, The Journal of Neuroscience.

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

[63]  Ulman Lindenberger,et al.  Cognitive aging: is there a dark side to environmental support? , 2014, Trends in Cognitive Sciences.

[64]  Denise C. Park,et al.  The adaptive brain: aging and neurocognitive scaffolding. , 2009, Annual review of psychology.

[65]  Christian Büchel,et al.  Structure–function interactions of correct retrieval in healthy elderly women , 2009, Neurobiology of Aging.

[66]  L. Nyberg,et al.  Memory Changes and the Aging Brain: A Multimodal Imaging Approach , 2010 .

[67]  Y. Stern,et al.  Efficiency, capacity, compensation, maintenance, plasticity: emerging concepts in cognitive reserve , 2013, Trends in Cognitive Sciences.

[68]  C. Depp,et al.  Older adults' perspectives on successful aging: qualitative interviews. , 2010, The American journal of geriatric psychiatry : official journal of the American Association for Geriatric Psychiatry.

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

[70]  S. Petersen,et al.  Characterizing the Hemodynamic Response: Effects of Presentation Rate, Sampling Procedure, and the Possibility of Ordering Brain Activity Based on Relative Timing , 2000, NeuroImage.

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

[72]  R. Marioni,et al.  Reverse Causation in the Association Between C-Reactive Protein and Fibrinogen Levels and Cognitive Abilities in an Aging Sample , 2009, Psychosomatic medicine.

[73]  Patricia A. Reuter-Lorenz,et al.  Age differences in prefontal recruitment during verbal working memory maintenance depend on memory load , 2010, Cortex.

[74]  R. Cabeza,et al.  Age-related changes in hemispheric organization , 2005 .

[75]  Jack L. Gallant,et al.  Encoding and decoding in fMRI , 2011, NeuroImage.

[76]  C. Grady Cognitive Neuroscience of Aging , 2008, Annals of the New York Academy of Sciences.

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

[78]  E. Paulesu,et al.  Reassessing the HAROLD model: Is the hemispheric asymmetry reduction in older adults a special case of compensatory-related utilisation of neural circuits? , 2013, Experimental Brain Research.

[79]  Denise C. Park,et al.  Handbook of the Psychology of Aging , 1979 .

[80]  Roberto Cabeza,et al.  The architecture of cross-hemispheric communication in the aging brain: linking behavior to functional and structural connectivity. , 2012, Cerebral cortex.

[81]  Leslie G. Ungerleider,et al.  Age-related changes in cortical blood flow activation during visual processing of faces and location , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[83]  Ian M. McDonough,et al.  The Dynamic Aging Mind , 2013, Perspectives on psychological science : a journal of the Association for Psychological Science.

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

[85]  M. Rugg,et al.  Age effects on the neural correlates of episodic retrieval: increased cortical recruitment with matched performance. , 2007, Cerebral cortex.

[86]  C. Grady The cognitive neuroscience of ageing , 2012, Nature Reviews Neuroscience.

[87]  J J McArdle,et al.  Latent growth curves within developmental structural equation models. , 1987, Child development.

[88]  Audrey Duarte,et al.  The effects of aging on material-independent and material-dependent neural correlates of source memory retrieval. , 2012, Cerebral cortex.

[89]  Edward T. Bullmore,et al.  Dopamine and memory dedifferentiation in aging , 2017, NeuroImage.

[90]  M. Ho,et al.  Age-related differences in effective connectivity of brain regions involved in Japanese kanji processing with homophone judgment task , 2014, Brain and Language.

[91]  L. Bäckman Compensation and recoding: a framework for aging and memory research. , 1985, Scandinavian journal of psychology.

[92]  Morris Moscovitch,et al.  Face Processing Changes in Normal Aging Revealed by fMRI Adaptation , 2011, Journal of Cognitive Neuroscience.

[93]  R. Henson,et al.  The Effects of Aging on the Neural Correlates of Subjective and Objective Recollection , 2007, Cerebral cortex.

[94]  E. Tulving,et al.  Age‐related differences in effective neural connectivity during encoding and recall , 1997, Neuroreport.

[95]  A. Dale,et al.  Building memories: remembering and forgetting of verbal experiences as predicted by brain activity. , 1998, Science.

[96]  Scott Hershberger,et al.  Genes and environment in personality development , 1994 .

[97]  Klaus F. Riegel,et al.  Development, Drop, and Death. , 1972 .

[98]  S. M. Resnick,et al.  I. Longitudinal changes in aging brain function , 2008, Neurobiology of Aging.

[99]  U. Lindenberger,et al.  A theoretical framework for the study of adult cognitive plasticity. , 2010, Psychological bulletin.

[100]  M. D’Esposito,et al.  Isolating the neural mechanisms of age-related changes in human working memory , 2000, Nature Neuroscience.

[101]  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.

[102]  A. Yonelinas The Nature of Recollection and Familiarity: A Review of 30 Years of Research , 2002 .

[103]  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.