Structural brain correlates of associative memory in older adults

Associative memory involves binding two or more items into a coherent memory episode. Relative to memory for single items, associative memory declines greatly in aging. However, older individuals vary substantially in their ability to memorize associative information. Although functional studies link associative memory to the medial temporal lobe (MTL) and prefrontal cortex (PFC), little is known about how volumetric differences in MTL and PFC might contribute to individual differences in associative memory. We investigated regional gray-matter volumes related to individual differences in associative memory in a sample of healthy older adults (n=54; age=60years). To differentiate item from associative memory, participants intentionally learned face-scene picture pairs before performing a recognition task that included single faces, scenes, and face-scene pairs. Gray-matter volumes were analyzed using voxel-based morphometry region-of-interest (ROI) analyses. To examine volumetric differences specifically for associative memory, item memory was controlled for in the analyses. Behavioral results revealed large variability in associative memory that mainly originated from differences in false-alarm rates. Moreover, associative memory was independent of individuals' ability to remember single items. Older adults with better associative memory showed larger gray-matter volumes primarily in regions of the left and right lateral PFC. These findings provide evidence for the importance of PFC in intentional learning of associations, likely because of its involvement in organizational and strategic processes that distinguish older adults with good from those with poor associative memory.

[1]  M. Jenkinson,et al.  Structural and functional bases of visuospatial associative memory in older adults , 2013, Neurobiology of Aging.

[2]  L L Jacoby,et al.  An opposition procedure for detecting age-related deficits in recollection: telling effects of repetition. , 1997, Psychology and aging.

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

[4]  M. Naveh-Benjamin,et al.  Journal of Experimental Psychology : Learning , Memory , and Cognition The Effects of Pure Pair Repetition on Younger and Older Adults ' Associative Memory , 2011 .

[5]  C K Morse Does variability increase with age? An archival study of cognitive measures. , 1993, Psychology and aging.

[6]  N. Raz,et al.  Prefrontal cortex and executive functions in healthy adults: A meta-analysis of structural neuroimaging studies , 2014, Neuroscience & Biobehavioral Reviews.

[7]  D. Schacter,et al.  Prefrontal Contributions to Executive Control: fMRI Evidence for Functional Distinctions within Lateral Prefrontal Cortex , 2001, NeuroImage.

[8]  Daniel L Schacter,et al.  Evidence for a specific role of the anterior hippocampal region in successful associative encoding , 2007, Hippocampus.

[9]  Moshe Naveh-Benjamin,et al.  Paying attention to binding: Further studies assessing the role of reduced attentional resources in the associative deficit of older adults , 2007, Memory & cognition.

[10]  Guillén Fernández,et al.  Probing the transformation of discontinuous associations into episodic memory: An event-related fMRI study , 2007, NeuroImage.

[11]  Anthony J. Lombardino The Cognitive Neuroscience of Memory: An Introduction.ByHoward Eichenbaum.Oxford and New York: Oxford University Press. $69.50 (hardcover); $39.50 (paper). xi + 370 p; ill.; index. ISBN: 0–19–514174–1 (hc); 0–19–514175–X (pb). 2002. , 2004 .

[12]  Brigitte Landeau,et al.  Structural and Metabolic Correlates of Episodic Memory in Relation to the Depth of Encoding in Normal Aging , 2009, Journal of Cognitive Neuroscience.

[13]  Lily Riggs,et al.  The hippocampus supports multiple cognitive processes through relational binding and comparison , 2012, Front. Hum. Neurosci..

[14]  Martin Lepage,et al.  Dorsolateral prefrontal cortex involvement in memory post-retrieval monitoring revealed in both item and associative recognition tests , 2005, NeuroImage.

[15]  Lila Davachi,et al.  Selective and Shared Contributions of the Hippocampus and Perirhinal Cortex to Episodic Item and Associative Encoding , 2008, Journal of Cognitive Neuroscience.

[16]  A. Yonelinas Recognition memory ROCs for item and associative information: The contribution of recollection and familiarity , 1997, Memory & cognition.

[17]  C. Van Petten,et al.  Relationship between hippocampal volume and memory ability in healthy individuals across the lifespan: review and meta-analysis. , 2004, Neuropsychologia.

[18]  M. Naveh-Benjamin,et al.  Assessing the associative deficit of older adults in long-term and short-term/working memory. , 2012, Psychology and aging.

[19]  Martin Lövdén,et al.  Genetic effects on old-age cognitive functioning: a population-based study. , 2013, Psychology and aging.

[20]  Yee Lee Shing,et al.  Aging Neuroscience , 2022 .

[21]  H. Eichenbaum The Cognitive Neuroscience of Memory , 2002 .

[22]  E. Glisky,et al.  Source memory in older adults: an encoding or retrieval problem? , 2001 .

[23]  Jing Luo,et al.  Dissecting medial temporal lobe contributions to item and associative memory formation , 2009, NeuroImage.

[24]  Roberto Cabeza,et al.  Prefrontal and medial temporal lobe contributions to relational memory in young and older adults , 2006, Handbook of Binding and Memory.

[25]  R. Buckner,et al.  Functional Dissociation among Components of Remembering: Control, Perceived Oldness, and Content , 2003, The Journal of Neuroscience.

[26]  Ellen M. Migo,et al.  Associative memory and the medial temporal lobes , 2007, Trends in Cognitive Sciences.

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

[28]  H. Spiers,et al.  Prefrontal and medial temporal lobe interactions in long-term memory , 2003, Nature Reviews Neuroscience.

[29]  R. Cabeza,et al.  Effects of aging on the neural correlates of successful item and source memory encoding. , 2008, Journal of experimental psychology. Learning, memory, and cognition.

[30]  S. Black,et al.  Memory impairments associated with hippocampal versus parahippocampal-gyrus atrophy: an MR volumetry study in Alzheimer’s disease , 1998, Neuropsychologia.

[31]  Claire Morse,et al.  Does variability increase with age? An archival study of cognitive measures. , 1993, Psychology and aging.

[32]  Yee Lee Shing,et al.  Adult age differences in memory for name–face associations: The effects of intentional and incidental learning , 2009, Memory.

[33]  S. Petersen,et al.  Frontal cortex contributes to human memory formation , 1999, Nature Neuroscience.

[34]  Karl J. Friston,et al.  Voxel-Based Morphometry—The Methods , 2000, NeuroImage.

[35]  M. N. Rajah,et al.  Group differences in anterior hippocampal volume and in the retrieval of spatial and temporal context memory in healthy young versus older adults , 2010, Neuropsychologia.

[36]  Andrew P. Yonelinas,et al.  Putting the Pieces Together: The Role of Dorsolateral Prefrontal Cortex in Relational Memory Encoding , 2011, Journal of Cognitive Neuroscience.

[37]  M. Brodeur,et al.  Prefrontal cortex contribution to associative recognition memory in humans: an event-related functional magnetic resonance imaging study , 2003, Neuroscience Letters.

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

[39]  Brenda A. Kirchhoff,et al.  Prefrontal gray matter volume mediates age effects on memory strategies , 2014, NeuroImage.

[40]  A. Wagner,et al.  Prefrontal and hippocampal contributions to visual associative recognition: Interactions between cognitive control and episodic retrieval , 2004, Brain and Cognition.

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

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

[43]  J. Dunlosky,et al.  Aging and deficits in associative memory: what is the role of strategy production? , 1998, Psychology and aging.

[44]  M. Rajah,et al.  Age-related changes in prefrontal cortex activity are associated with behavioural deficits in both temporal and spatial context memory retrieval in older adults , 2010, Cortex.

[45]  E. Miller,et al.  An integrative theory of prefrontal cortex function. , 2001, Annual review of neuroscience.

[46]  John Ashburner,et al.  A fast diffeomorphic image registration algorithm , 2007, NeuroImage.

[47]  C. Petten Relationship between hippocampal volume and memory ability in healthy individuals across the lifespan: review and meta-analysis , 2004, Neuropsychologia.

[48]  T. Shallice,et al.  “Sculpting the Response Space”—An Account of Left Prefrontal Activation at Encoding , 2000, NeuroImage.

[49]  H. Christensen,et al.  An analysis of diversity in the cognitive performance of elderly community dwellers: individual differences in change scores as a function of age. , 1999, Psychology and aging.

[50]  Tom den Heijer,et al.  Hippocampal Head Size Associated with Verbal Memory Performance in Nondemented Elderly , 2002, NeuroImage.

[51]  R. Buckner,et al.  Functional-Anatomic Correlates of Individual Differences in Memory , 2006, Neuron.

[52]  Yee Lee Shing,et al.  Associative and strategic components of episodic memory: a life-span dissociation. , 2008, Journal of experimental psychology. General.

[53]  Natalie C. Ebner,et al.  FACES—A database of facial expressions in young, middle-aged, and older women and men: Development and validation , 2010, Behavior research methods.

[54]  Mercedes Atienza,et al.  Associative memory deficits in mild cognitive impairment: The role of hippocampal formation , 2011, NeuroImage.

[55]  Matthew G. Rhodes,et al.  False Remembering in the Aged , 2006 .

[56]  J. Schneider,et al.  Individual differences in rates of change in cognitive abilities of older persons. , 2002, Psychology and aging.

[57]  L. Davachi Item, context and relational episodic encoding in humans , 2006, Current Opinion in Neurobiology.

[58]  Joel L. Voss,et al.  Medial temporal contributions to successful face‐name learning , 2012, Human brain mapping.

[59]  M. Naveh-Benjamin,et al.  Differential effects of age on item and associative measures of memory: a meta-analysis. , 2008, Psychology and aging.

[60]  H. Eichenbaum,et al.  The Episodic Memory System: Neurocircuitry and Disorders , 2010, Neuropsychopharmacology.

[61]  Ana M. Daugherty,et al.  Vascular Risk Moderates Associations between Hippocampal Subfield Volumes and Memory , 2013, Journal of Cognitive Neuroscience.

[62]  J. Whitwell Voxel-Based Morphometry: An Automated Technique for Assessing Structural Changes in the Brain , 2009, The Journal of Neuroscience.

[63]  Erika K. Fulton,et al.  Older adults show deficits in retrieving and decoding associative mediators generated at study. , 2013, Developmental psychology.

[64]  Ulman Lindenberger,et al.  Heterogeneity in frontal lobe aging , 2013 .

[65]  A. Yonelinas Receiver-operating characteristics in recognition memory: evidence for a dual-process model. , 1994, Journal of experimental psychology. Learning, memory, and cognition.

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

[67]  E. Heit,et al.  Associative Recognition: a Case of Recall-to-reject Processing , 2022 .

[68]  U. Lindenberger Human cognitive aging: Corriger la fortune? , 2014, Science.

[69]  M. Naveh-Benjamin,et al.  The associative memory deficit of older adults: the role of strategy utilization. , 2007, Psychology and aging.

[70]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

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