Influence of Aging on the Neural Correlates of Autobiographical, Episodic, and Semantic Memory Retrieval

We used fMRI to assess the neural correlates of autobiographical, semantic, and episodic memory retrieval in healthy young and older adults. Participants were tested with an event-related paradigm in which retrieval demand was the only factor varying between trials. A spatio-temporal partial least square analysis was conducted to identify the main patterns of activity characterizing the groups across conditions. We identified brain regions activated by all three memory conditions relative to a control condition. This pattern was expressed equally in both age groups and replicated previous findings obtained in a separate group of younger adults. We also identified regions whose activity differentiated among the different memory conditions. These patterns of differentiation were expressed less strongly in the older adults than in the young adults, a finding that was further confirmed by a barycentric discriminant analysis. This analysis showed an age-related dedifferentiation in autobiographical and episodic memory tasks but not in the semantic memory task or the control condition. These findings suggest that the activation of a common memory retrieval network is maintained with age, whereas the specific aspects of brain activity that differ with memory content are more vulnerable and less selectively engaged in older adults. Our results provide a potential neural mechanism for the well-known age differences in episodic/autobiographical memory, and preserved semantic memory, observed when older adults are compared with younger adults.

[1]  Roberto Cabeza,et al.  Effects of healthy aging on hippocampal and rhinal memory functions: an event-related fMRI study. , 2005, Cerebral cortex.

[2]  L. Light,et al.  Memory and aging: the role of retrieval processes. , 1981, Psychological bulletin.

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

[4]  M. Conway Sensory-perceptual episodic memory and its context: autobiographical memory. , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[5]  R. Buckner,et al.  Self-projection and the brain , 2007, Trends in Cognitive Sciences.

[6]  Hervé Abdi,et al.  The Neural Basis of Vivid Memory Is Patterned on Perception , 2012, Journal of Cognitive Neuroscience.

[7]  Asaf Gilboa,et al.  Autobiographical and episodic memory—one and the same? Evidence from prefrontal activation in neuroimaging studies , 2004, Neuropsychologia.

[8]  L. Nilsson Memory function in normal aging , 2003, Acta neurologica Scandinavica. Supplementum.

[9]  Anthony R. McIntosh,et al.  Age-related differences in brain activity during verbal recency memory , 2008, Brain Research.

[10]  Richard S. J. Frackowiak,et al.  The Mind's Eye—Precuneus Activation in Memory-Related Imagery , 1995, NeuroImage.

[11]  Christophe Destrieux,et al.  [Aging and hemispheric cerebral lateralization]. , 2008, Psychologie & neuropsychiatrie du vieillissement.

[12]  D. Burke,et al.  Why do semantic priming effects increase in old age? A meta-analysis. , 1993, Psychology and aging.

[13]  D. B. Mitchell,et al.  The handbook of aging and cognition , 2001 .

[14]  B. Desgranges,et al.  Autobiographical memory, autonoetic consciousness, and self-perspective in aging. , 2006, Psychology and aging.

[15]  E. Tulving,et al.  Episodic and semantic memory , 1972 .

[16]  M. Moscovitch,et al.  The parietal cortex and episodic memory: an attentional account , 2008, Nature Reviews Neuroscience.

[17]  N. Raz,et al.  Differential effects of aging on memory for content and context: a meta-analysis. , 1995, Psychology and aging.

[18]  E. Maguire,et al.  What does the retrosplenial cortex do? , 2009, Nature Reviews Neuroscience.

[19]  Morris Moscovitch,et al.  Recollective qualities modulate hippocampal activation during autobiographical memory retrieval , 2004, Hippocampus.

[20]  Richard A. Andersen,et al.  Separate body- and world-referenced representations of visual space in parietal cortex , 1998, Nature.

[21]  Gereon R. Fink,et al.  Recollections of one’s own past: the effects of aging and gender on the neural mechanisms of episodic autobiographical memory , 2005, Anatomy and Embryology.

[22]  Patrick S. R. Davidson,et al.  Neuropsychological correlates of recollection and familiarity in normal aging , 2002, Cognitive, affective & behavioral neuroscience.

[23]  Philip A Allen,et al.  Differential age effects in semantic and episodic memory. , 2002, The journals of gerontology. Series B, Psychological sciences and social sciences.

[24]  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.

[25]  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.

[26]  F. Craik,et al.  The handbook of aging and cognition , 1992 .

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

[28]  Justin L. Vincent,et al.  Disruption of Large-Scale Brain Systems in Advanced Aging , 2007, Neuron.

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

[30]  Anthony Randal McIntosh,et al.  A common functional brain network for autobiographical, episodic, and semantic memory retrieval , 2010, NeuroImage.

[31]  Hervé Abdi,et al.  A Tutorial on Multiblock Discriminant Correspondence Analysis ( MUDICA ) : A New Method for Analyzing Discourse Data From Clinical Populations , 2010 .

[32]  Pascale Piolino,et al.  Hippocampal activation for autobiographical memories over the entire lifetime in healthy aged subjects: an fMRI study. , 2007, Cerebral cortex.

[33]  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.

[34]  T G Turkington,et al.  Adult age differences in the functional neuroanatomy of verbal recognition memory , 1999, Human brain mapping.

[35]  D. B. Mitchell,et al.  How many memory systems? Evidence from aging. , 1989, Journal of experimental psychology. Learning, memory, and cognition.

[36]  Arthur F. Kramer,et al.  Dedifferentiation in the visual cortex: An fMRI investigation of individual differences in older adults , 2008, Brain Research.

[37]  Alana T. Wong,et al.  Age-Related Changes in the Episodic Simulation of Future Events , 2008, Psychological science.

[38]  Morris Moscovitch,et al.  Recollection versus strength as the primary determinant of hippocampal engagement at retrieval , 2009, Proceedings of the National Academy of Sciences.

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

[40]  Asaf Gilboa,et al.  Semantic memory recognition is supported by intrinsic recollection-like processes: “The butcher on the bus” revisited , 2012, Neuropsychologia.

[41]  Brian Levine,et al.  Ageing and autobiographical memory for emotional and neutral events , 2007, Memory.

[42]  David A. Balota,et al.  Lexical , Sublexical , and Implicit Memory Processes in Healthy Young and Healthy Older Adults and in Individuals With Dementia of the Alzheimer Type , 2004 .

[43]  A J Parkin,et al.  Recollective experience, normal aging, and frontal dysfunction. , 1992, Psychology and aging.

[44]  G. Winocur,et al.  Brain regions involved in the retrieval of spatial and episodic details associated with a familiar environment: An fMRI study , 2012, Neuropsychologia.

[45]  Richard N. Henson,et al.  Age-related changes in neural activity associated with familiarity, recollection and false recognition , 2010, Neurobiology of Aging.

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

[47]  Malcolm W. Brown,et al.  Recognition memory: What are the roles of the perirhinal cortex and hippocampus? , 2001, Nature Reviews Neuroscience.

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

[49]  D J Madden,et al.  Influence of age and processing stage on visual word recognition. , 1993, Psychology and aging.

[50]  Andreas Voss,et al.  A diffusion model analysis of adult age differences in episodic and semantic long-term memory retrieval. , 2006, Journal of experimental psychology. Learning, memory, and cognition.

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

[52]  E A Maguire,et al.  Neuroimaging studies of autobiographical event memory. , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

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

[54]  Gereon R Fink,et al.  Age-dependent differences in the neural mechanisms supporting long-term declarative memories. , 2010, Archives of clinical neuropsychology : the official journal of the National Academy of Neuropsychologists.

[55]  A. Parkin,et al.  Human memory , 1999, Current Biology.

[56]  J. Callicott,et al.  Normal aging modulates prefrontoparietal networks underlying multiple memory processes , 2012, The European journal of neuroscience.

[57]  Morris Moscovitch,et al.  Age-related Deficits in Associative Memory: the Influence of Impaired Strategic Retrieval Binding Hypothesis and Retrieval Failure , 2022 .

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

[59]  B. Levine,et al.  The functional neuroanatomy of autobiographical memory: A meta-analysis , 2006, Neuropsychologia.

[60]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[61]  David A. Balota,et al.  Lexical, Sublexical, and Implicit Memory Processes in Healthy Young and Healthy Older Adults and in Individuals With Dementia of the Alzheimer Type , 1996 .

[62]  R. Henson,et al.  A familiarity signal in human anterior medial temporal cortex? , 2003, Hippocampus.

[63]  S. Giaquinto,et al.  Stability of word comprehension with age An electrophysiological study , 2007, Mechanisms of Ageing and Development.

[64]  F. Bookstein,et al.  Neurobehavioral effects of prenatal alcohol: Part II. Partial least squares analysis. , 1989, Neurotoxicology and teratology.

[65]  R. N. Spreng,et al.  Default network modulation and large-scale network interactivity in healthy young and old adults. , 2012, Cerebral cortex.

[66]  Denise C Park,et al.  Neural Specificity Predicts Fluid Processing Ability in Older Adults , 2010, The Journal of Neuroscience.

[67]  G. Winocur,et al.  Aging and autobiographical memory: dissociating episodic from semantic retrieval. , 2002, Psychology and aging.

[68]  Piero Antuono,et al.  Age-related functional recruitment for famous name recognition: An event-related fMRI study , 2006, Neurobiology of Aging.

[69]  E. Maguire,et al.  A Temporoparietal and Prefrontal Network for Retrieving the Spatial Context of Lifelike Events , 2001, NeuroImage.

[70]  H. David Sheets,et al.  Partial least squares analysis , 2012 .

[71]  T. Paus,et al.  Functional coactivation map of the human brain. , 2008, Cerebral cortex.

[72]  Thad A. Polk,et al.  Age differences in neural distinctiveness revealed by multi-voxel pattern analysis , 2011, NeuroImage.

[73]  Roberto Cabeza,et al.  Age-related effects on the neural correlates of autobiographical memory retrieval , 2012, Neurobiology of Aging.

[74]  Marcia K. Johnson,et al.  An fMRI investigation of short-term source memory in young and older adults , 2006, NeuroImage.

[75]  A F Smith,et al.  Age differences in mental multiplication: evidence for peripheral but not central decrements. , 1997, The journals of gerontology. Series B, Psychological sciences and social sciences.

[76]  J. V. Haxby,et al.  Spatial Pattern Analysis of Functional Brain Images Using Partial Least Squares , 1996, NeuroImage.

[77]  John A. E. Anderson,et al.  A multivariate analysis of age-related differences in default mode and task-positive networks across multiple cognitive domains. , 2010, Cerebral cortex.

[78]  L Nyberg,et al.  Age differences in episodic memory, semantic memory, and priming: relationships to demographic, intellectual, and biological factors. , 1996, The journals of gerontology. Series B, Psychological sciences and social sciences.

[79]  Hervé Abdi,et al.  Barycentric Discriminant Analysis (BADIA) , 2009 .

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

[81]  Roberto Cabeza,et al.  Age-related dedifferentiation of learning systems: an fMRI study of implicit and explicit learning , 2011, Neurobiology of Aging.

[82]  D. Schacter,et al.  The Brain's Default Network , 2008, Annals of the New York Academy of Sciences.

[83]  William F. Brewer,et al.  What is autobiographical memory , 1986 .

[84]  Roberto Cabeza,et al.  Other Perspectives , 2015 .

[85]  E. Tulving Memory and consciousness. , 1985 .

[86]  Neil Salkind,et al.  Encyclopedia of research design , 2010 .

[87]  Pascale Piolino,et al.  Factors affecting medial temporal lobe engagement for past and future episodic events: An ALE meta-analysis of neuroimaging studies , 2012, Brain and Cognition.

[88]  Eleanor A Maguire,et al.  Aging affects the engagement of the hippocampus during autobiographical memory retrieval. , 2003, Brain : a journal of neurology.

[89]  R. Java,et al.  Effects of age on state of awareness following implicit and explicit word-association tasks. , 1996, Psychology and aging.

[90]  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.

[91]  A. R. McIntosh,et al.  Spatiotemporal analysis of event-related fMRI data using partial least squares , 2004, NeuroImage.

[92]  Christine Bastin,et al.  The contribution of recollection and familiarity to recognition memory: a study of the effects of test format and aging. , 2003, Neuropsychology.

[93]  Anthony R. McIntosh,et al.  Task-related activity in prefrontal cortex and its relation to recognition memory performance in young and old adults , 2005, Neuropsychologia.

[94]  Caroline Hommet,et al.  Influence de l’âge sur la latéralisation cérébrale , 2008 .

[95]  Cheryl L Grady,et al.  Age-related differences in face processing: a meta-analysis of three functional neuroimaging experiments. , 2002, Canadian journal of experimental psychology = Revue canadienne de psychologie experimentale.

[96]  G. Winocur,et al.  Functional neuroanatomy of remote episodic, semantic and spatial memory: a unified account based on multiple trace theory , 2005, Journal of anatomy.

[97]  Hervé Abdi,et al.  How to compute reliability estimates and display confidence and tolerance intervals for pattern classifiers using the Bootstrap and 3-way multidimensional scaling (DISTATIS) , 2009, NeuroImage.

[98]  E. Tulving,et al.  Toward a theory of episodic memory: the frontal lobes and autonoetic consciousness. , 1997, Psychological bulletin.

[99]  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.

[100]  Joshua Oon Soo Goh,et al.  Reduced neural selectivity increases fMRI adaptation with age during face discrimination , 2010, NeuroImage.

[101]  H. Abdi,et al.  The survey of autobiographical memory (SAM): A novel measure of trait mnemonics in everyday life , 2013, Cortex.

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

[103]  T. Mäntylä,et al.  Priming effects in prospective memory. , 1993, Memory.

[104]  F. Bookstein,et al.  Neurobehavioral effects of prenatal alcohol: Part I. Research strategy. , 1989, Neurotoxicology and teratology.

[105]  Hervé Abdi,et al.  Multiple Subject Barycentric Discriminant Analysis (MUSUBADA): How to Assign Scans to Categories without Using Spatial Normalization , 2012, Comput. Math. Methods Medicine.

[106]  Maurizio Corbetta,et al.  The human brain is intrinsically organized into dynamic, anticorrelated functional networks. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[107]  Cheryl L. Grady,et al.  Common and Unique Neural Activations in Autobiographical, Episodic, and Semantic Retrieval , 2007, Journal of Cognitive Neuroscience.

[108]  Denise C. Park,et al.  Human neuroscience and the aging mind: a new look at old problems. , 2010, The journals of gerontology. Series B, Psychological sciences and social sciences.

[109]  Robert Tibshirani,et al.  The Bootstrap Method for Assessing Statistical Accuracy , 1985 .

[110]  B. Knowlton,et al.  Remembering episodes: a selective role for the hippocampus during retrieval , 2000, Nature Neuroscience.