Age-related differences in the neural correlates of vivid remembering

When recollecting events, older adults typically report similar memory vividness levels as young adults, while they actually retrieve fewer episodic details. This suggests that young and older adults use episodic details differently to calibrate their vividness judgements. Capitalizing on the idea that remembering reactivates brain regions that initially processed details at encoding, the current fMRI study sought to examine these age-related changes in the basis of vivid recollection. At encoding, young and older adults saw pictures associated with labels and these labels were then used as retrieval cues for recalling the associated pictures and making memory vividness judgments. Results showed that highly vivid memories were associated with greater activity in the precuneus in young than older adults. Furthermore, the direct comparison between encoding and retrieval patterns of activity using Representational Similarity Analyses revealed stronger item-specific reactivation in the posterior cingulate/retrosplenial cortex in young than older adults. Taken together, these results provide new evidence that aging is associated with reduced reinstatement of activity in brain regions that processed the encoding of complex stimuli, but older individuals judge these impoverished memory representations as subjectively vivid.

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

[2]  Roberto Cabeza,et al.  Reinstatement of Individual Past Events Revealed by the Similarity of Distributed Activation Patterns during Encoding and Retrieval , 2015, Journal of Cognitive Neuroscience.

[3]  Charan Ranganath,et al.  Representational Similarity Analyses: A Practical Guide for Functional MRI Applications , 2018 .

[4]  Cinthya Estrada-Manilla,et al.  Brain activity during source memory retrieval in young, middle-aged and old adults , 2015, Brain Research.

[5]  Benjamin J. Shannon,et al.  Parietal lobe contributions to episodic memory retrieval , 2005, Trends in Cognitive Sciences.

[6]  A. Zeman,et al.  The neural correlates of visual imagery: A co-ordinate-based meta-analysis , 2018, Cortex.

[7]  N. Raz,et al.  Extrahippocampal contributions to age differences in human spatial navigation. , 2007, Cerebral cortex.

[8]  K. Mitchell,et al.  The Impact of Focusing on Different Features During Encoding on Young and Older Adults’ Source Memory , 2019, Open Psychology.

[9]  Arnaud D'Argembeau,et al.  PHENOMENAL CHARACTERISTICS OF AUTOBIOGRAPHICAL MEMORIES FOR EMOTIONAL AND NEUTRAL EVENTS IN OLDER AND YOUNGER ADULTS , 2005, Experimental aging research.

[10]  Robert Turner,et al.  Image Distortion Correction in fMRI: A Quantitative Evaluation , 2002, NeuroImage.

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

[12]  Ingrid R. Olson,et al.  Dissociation Between Memory Accuracy and Memory Confidence Following Bilateral Parietal Lesions , 2009, Cerebral cortex.

[13]  L. Bellak,et al.  Geriatric psychiatry : a handbook for psychiatrists and primary care physicians , 1976 .

[14]  Karl K. Szpunar,et al.  Shifting visual perspective during retrieval shapes autobiographical memories , 2017, NeuroImage.

[15]  James L. Keidel,et al.  Reinstatement of memory representations for lifelike events over the course of a week , 2017, Scientific Reports.

[16]  Michael D. Rugg,et al.  Effects of age on across-participant variability of cortical reinstatement effects , 2019, NeuroImage.

[17]  James L. Keidel,et al.  Consolidation of Complex Events via Reinstatement in Posterior Cingulate Cortex , 2015, The Journal of Neuroscience.

[18]  Gaoyan Zhang,et al.  Revealing the Semantic Association between Perception of Scenes and Significant Objects by Representational Similarity Analysis , 2017, Neuroscience.

[19]  Wil Dijkstra,et al.  Using Social Desirability Scales in Research among the Elderly , 2001 .

[20]  Y. Hu,et al.  Causal Evidence for Mnemonic Metacognition in Human Precuneus , 2018, The Journal of Neuroscience.

[21]  R. Henson,et al.  Neural evidence for age-related differences in representational quality and strategic retrieval processes , 2019, Neurobiology of Aging.

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

[23]  Franziska R. Richter,et al.  Distinct neural mechanisms underlie the success, precision, and vividness of episodic memory , 2016, eLife.

[24]  Karl Magnus Petersson,et al.  The role of precuneus and left inferior frontal cortex during source memory episodic retrieval , 2005, NeuroImage.

[25]  Tracy H. Wang,et al.  The Effects of Age on the Neural Correlates of Recollection Success, Recollection-Related Cortical Reinstatement, and Post-Retrieval Monitoring. , 2016, Cerebral cortex.

[26]  Troy A. Smith,et al.  The experience of vivid autobiographical reminiscence is supported by subjective content representations in the precuneus , 2018, Scientific Reports.

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

[28]  A. Grabowska,et al.  The Nencki Affective Picture System (NAPS): Introduction to a novel, standardized, wide-range, high-quality, realistic picture database , 2013, Behavior research methods.

[29]  Krzysztof J. Gorgolewski,et al.  Medial and Lateral Networks in Anterior Prefrontal Cortex Support Metacognitive Ability for Memory and Perception , 2013, The Journal of Neuroscience.

[30]  E. Kensinger,et al.  Effects of internal and external vividness on hippocampal connectivity during memory retrieval , 2016, Neurobiology of Learning and Memory.

[31]  Brice A. Kuhl,et al.  Age-related differences in the neural basis of the subjective vividness of memories: evidence from multivoxel pattern classification , 2015, Cognitive, Affective, & Behavioral Neuroscience.

[32]  R. N. Spreng,et al.  Characterizing the subjective experience of episodic past, future, and counterfactual thinking in healthy younger and older adults , 2016, Quarterly journal of experimental psychology.

[33]  Cheryl L. Grady,et al.  Influence of Aging on the Neural Correlates of Autobiographical, Episodic, and Semantic Memory Retrieval , 2011, Journal of Cognitive Neuroscience.

[34]  Donna Rose Addis,et al.  Neural Mechanisms of Episodic Retrieval Support Divergent Creative Thinking , 2019, Cerebral cortex.

[35]  Marcia K. Johnson,et al.  Source monitoring 15 years later: what have we learned from fMRI about the neural mechanisms of source memory? , 2009, Psychological bulletin.

[36]  Nikolaus Kriegeskorte,et al.  Frontiers in Systems Neuroscience Systems Neuroscience , 2022 .

[37]  Ian M. McDonough,et al.  Memory's aging echo: Age-related decline in neural reactivation of perceptual details during recollection , 2014, NeuroImage.

[38]  C. Ranganath,et al.  Two cortical systems for memory-guided behaviour , 2012, Nature Reviews Neuroscience.

[39]  A. Marchewka,et al.  The Set of Fear Inducing Pictures (SFIP): Development and validation in fearful and nonfearful individuals , 2016, Behavior Research Methods.

[40]  Michael D. Rugg,et al.  Decoding the content of recollection within the core recollection network and beyond , 2017, Cortex.

[41]  M. Bar,et al.  Cortical Analysis of Visual Context , 2003, Neuron.

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

[43]  S. Lehéricy,et al.  The eye of the self: precuneus volume and visual perspective during autobiographical memory retrieval , 2013, Brain Structure and Function.

[44]  Rossana de Beni,et al.  Left mediotemporal structures mediate the retrieval of episodic autobiographical mental images , 2006, NeuroImage.

[45]  S. Petersen,et al.  Memory's echo: vivid remembering reactivates sensory-specific cortex. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[46]  E. Tulving,et al.  Reactivation of encoding-related brain activity during memory retrieval. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

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

[48]  E. Balteau,et al.  Differential effects of aging on the neural correlates of recollection and familiarity , 2013, Cortex.

[49]  Marcia K. Johnson,et al.  Phenomenal characteristics of memories for perceived and imagined autobiographical events. , 1988, Journal of experimental psychology. General.

[50]  L. Bieliauskas,et al.  Contemporary Review 2009: Cognitive Aging , 2010, Journal of geriatric psychiatry and neurology.

[51]  Sabrina M. Tom,et al.  Dissociable correlates of recollection and familiarity within the medial temporal lobes , 2004, Neuropsychologia.

[52]  M. Bar Visual objects in context , 2004, Nature Reviews Neuroscience.

[53]  Rolf A. Zwaan,et al.  Situation models in language comprehension and memory. , 1998, Psychological bulletin.

[54]  R. Petersen,et al.  Robust and expanded norms for the Dementia Rating Scale. , 2010, Archives of clinical neuropsychology : the official journal of the National Academy of Neuropsychologists.

[55]  D. F. Marks,et al.  Visual imagery differences in the recall of pictures. , 1973, British journal of psychology.

[56]  R. Henson,et al.  Episodic Reinstatement in the Medial Temporal Lobe , 2012, The Journal of Neuroscience.

[57]  J. Hart,et al.  Distinct prefrontal cortex activity associated with item memory and source memory for visual shapes. , 2003, Brain research. Cognitive brain research.

[58]  S. Moffat Aging and Spatial Navigation: What Do We Know and Where Do We Go? , 2009, Neuropsychology Review.

[59]  Hervé Abdi,et al.  Distributed Patterns of Reactivation Predict Vividness of Recollection , 2015, Journal of Cognitive Neuroscience.

[60]  Karl J. Friston,et al.  Modelling Geometric Deformations in Epi Time Series , 2022 .

[61]  Kate Jeffery,et al.  Retrosplenial cortex and its role in spatial cognition , 2017 .

[62]  Christine Bastin,et al.  Associative memory in aging: the effect of unitization on source memory. , 2013, Psychology and aging.

[63]  M. Johnson,et al.  Aging and qualitative characteristics of memories for perceived and imagined complex events. , 1990, Psychology and aging.

[64]  M. Husain,et al.  Association between precuneus volume and autobiographical memory impairment in posterior cortical atrophy: Beyond the visual syndrome , 2018, NeuroImage: Clinical.

[65]  Maria Pietronilla Penna,et al.  Does Social Desirability Confound the Assessment of Self-Reported Measures of Well-Being and Metacognitive Efficiency in Young and Older Adults? , 2012 .

[66]  Marco Bozzali,et al.  TMS evidence for a selective role of the precuneus in source memory retrieval , 2015, Behavioural Brain Research.

[67]  Morris Moscovitch,et al.  Familiar Real-World Spatial Cues Provide Memory Benefits in Older and Younger Adults , 2017, Psychology and aging.

[68]  Tracy H. Wang,et al.  Recollection-Related Increases in Functional Connectivity Predict Individual Differences in Memory Accuracy , 2015, The Journal of Neuroscience.

[69]  M. Naveh-Benjamin Adult age differences in memory performance: tests of an associative deficit hypothesis. , 2000, Journal of experimental psychology. Learning, memory, and cognition.

[70]  Kaia L. Vilberg,et al.  Brain Networks Underlying Episodic Memory Retrieval This Review Comes from a Themed Issue on Macrocircuits Memory Signals within the Mtl , 2022 .

[71]  Erik A. Wing,et al.  Neural similarity between encoding and retrieval is related to memory via hippocampal interactions. , 2013, Cerebral cortex.

[72]  A. Dufour,et al.  What do we know about aging and spatial cognition? Reviews and perspectives , 2012, Ageing Research Reviews.

[73]  A. D'Argembeau,et al.  Deciphering the relationship between objective and subjective aspects of recollection in healthy aging , 2020, Memory.

[74]  Daniel L. Schacter,et al.  Neural Correlates of Metamemory: A Comparison of Feeling-of-Knowing and Retrospective Confidence Judgments , 2009, Journal of Cognitive Neuroscience.

[75]  Nikolaas N. Oosterhof,et al.  CoSMoMVPA: multi-modal multivariate pattern analysis of neuroimaging data in Matlab/GNU Octave , 2016 .

[76]  G. Xue,et al.  Reduced Fidelity of Neural Representation Underlies Episodic Memory Decline in Normal Aging , 2018, Cerebral cortex.

[77]  D. Schacter,et al.  Characterizing Age-related Changes in Remembering the past and Imagining the Future Experiment 1 , 2022 .

[78]  Hervé Abdi,et al.  Memory Reactivation in Healthy Aging: Evidence of Stimulus-Specific Dedifferentiation , 2014, The Journal of Neuroscience.