Age-related differences in medial temporal lobe involvement during conceptual fluency

Not all memory processes are equally affected by aging. A widely accepted hypothesis is that older adults rely more on familiarity-based processing, typically linked with the perirhinal cortex (PRC), in the context of impaired recollection, linked with the hippocampus (HC). However, according to the dedifferentiation hypothesis, healthy aging reduces the specialization of MTL memory subregions so that they may mediate different memory processes than in young adults. Using fMRI, we tested this possibility using a conceptual fluency manipulation known to induce familiarity-related PRC activity. The study yielded two main findings. First, although fluency equivalently affected PRC in both young (18-28; N=14) and older (62-80; N=15) adults, it also uniquely affected HC activity in older adults. Second, the fluency manipulation reduced functional connectivity between HC and PRC in young adults, but it increased it in older adults. Taken together, the results suggest that aging may result in reduced specialization of the HC for recollection, such that the HC may be recruited when fluency increases familiarity-based responding. This article is part of a Special Issue entitled SI: Memory & Aging.

[1]  Jason D. Ozubko,et al.  The disruptive effects of processing fluency on familiarity-based recognition in amnesia , 2014, Neuropsychologia.

[2]  Larry L. Jacoby,et al.  An illusion of memory: false recognition influenced by unconscious perception , 1989 .

[3]  Angela D. Friederici,et al.  On the Processing of Semantic Aspects of Experience in the Anterior Medial Temporal Lobe: An Event-related fMRI Study , 2010, Journal of Cognitive Neuroscience.

[4]  L. Jacoby,et al.  On the relationship between autobiographical memory and perceptual learning. , 1981, Journal of experimental psychology. General.

[5]  A. Yonelinas,et al.  Memory variability is due to the contribution of recollection and familiarity, not to encoding variability. , 2010, Journal of experimental psychology. Learning, memory, and cognition.

[6]  D. Montaldi,et al.  The neural system that mediates familiarity memory , 2006, Hippocampus.

[7]  Joel L. Voss,et al.  The impact of fluency on explicit memory tasks in amnesia , 2012, Cognitive neuroscience.

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

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

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

[11]  Paul M. Matthews,et al.  Regional White Matter Integrity Differentiates Between Vascular Dementia and Alzheimer Disease , 2009, Stroke.

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

[13]  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.

[14]  D. Schacter,et al.  Associative recognition in Alzheimer's disease: evidence for impaired recall-to-reject. , 2004, Neuropsychology.

[15]  Ramona O Hopkins,et al.  Semantic Memory and the Human Hippocampus , 2003, Neuron.

[16]  Denise C. Park,et al.  Neural Broadening or Neural Attenuation? Investigating Age-Related Dedifferentiation in the Face Network in a Large Lifespan Sample , 2012, The Journal of Neuroscience.

[17]  Richard N. Henson,et al.  Behavioral and neural evidence for masked conceptual priming of recollection , 2013, Cortex.

[18]  Thomas A. Schreiber,et al.  The University of South Florida free association, rhyme, and word fragment norms , 2004, Behavior research methods, instruments, & computers : a journal of the Psychonomic Society, Inc.

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

[20]  M. D. Rugg,et al.  Regional specificity of age effects on the neural correlates of episodic retrieval , 2008, Neurobiology of Aging.

[21]  D. Schacter,et al.  Medial temporal lobe activations in fMRI and PET studies of episodic encoding and retrieval , 1999, Hippocampus.

[22]  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.

[23]  Adam Gazzaley,et al.  Measuring functional connectivity during distinct stages of a cognitive task , 2004, NeuroImage.

[24]  Regine Bader,et al.  Is a novel conceptual unit more than the sum of its parts?: FMRI evidence from an associative recognition memory study , 2014, Neuropsychologia.

[25]  Stephen M. Smith,et al.  Age-related changes in grey and white matter structure throughout adulthood , 2010, NeuroImage.

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

[27]  Roberto Cabeza,et al.  A Broader View of Perirhinal Function: From Recognition Memory to Fluency-Based Decisions , 2013, The Journal of Neuroscience.

[28]  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.

[29]  Vijeth Iyengar,et al.  Less wiring, more firing: low-performing older adults compensate for impaired white matter with greater neural activity. , 2015, Cerebral cortex.

[30]  T. Salthouse Adult cognition : an experimental psychology of human aging / Timothy A. Salthouse , 1982 .

[31]  Simon J Graham,et al.  Recollection- and familiarity-based memory in healthy aging and amnestic mild cognitive impairment. , 2008, Neuropsychology.

[32]  David G. Gadian,et al.  A Rapid, Hippocampus-Dependent, Item-Memory Signal that Initiates Context Memory in Humans , 2012, Current Biology.

[33]  Richard N. A. Henson,et al.  Event-related Potentials Associated with Masked Priming of Test Cues Reveal Multiple Potential Contributions to Recognition Memory , 2008, Journal of Cognitive Neuroscience.

[34]  R. Cabeza,et al.  Triple dissociation in the medial temporal lobes: recollection, familiarity, and novelty. , 2006, Journal of neurophysiology.

[35]  D. Schacter,et al.  Patients with mild Alzheimer's disease attribute conceptual fluency to prior experience , 2005, Neuropsychologia.

[36]  Morris Moscovitch,et al.  The nature and time‐course of medial temporal lobe contributions to semantic retrieval: An fMRI study on verbal fluency , 2012, Hippocampus.

[37]  L L Jacoby,et al.  Ironic effects of repetition: measuring age-related differences in memory. , 1999, Journal of experimental psychology. Learning, memory, and cognition.

[38]  A P Yonelinas,et al.  Consciousness, control, and confidence: the 3 Cs of recognition memory. , 2001, Journal of experimental psychology. General.

[39]  Michael W Weiner,et al.  Memory in the aging brain: Doubly dissociating the contribution of the hippocampus and entorhinal cortex , 2007, Hippocampus.

[40]  Cheryl Grady,et al.  Faculty Opinions recommendation of Memory signals are temporally dissociated in and across human hippocampus and perirhinal cortex. , 2013 .

[41]  Deborah M. Burke,et al.  Language, memory, and aging: Patterns of language and memory in old age , 1988 .

[42]  M. Verfaellie,et al.  Increasing the salience of fluency cues reduces the recognition memory impairment in amnesia , 2006, Neuropsychologia.

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

[44]  Shauna M. Stark,et al.  Pattern separation deficits associated with increased hippocampal CA3 and dentate gyrus activity in nondemented older adults , 2010, Hippocampus.

[45]  Yee Lee Shing,et al.  Neuromodulation of associative and organizational plasticity across the life span: Empirical evidence and neurocomputational modeling , 2006, Neuroscience & Biobehavioral Reviews.

[46]  L. Nyberg,et al.  Preserved hippocampus activation in normal aging as revealed by fMRI , 2011, Hippocampus.

[47]  John T Wixted,et al.  The Hippocampus Supports Both Recollection and Familiarity When Memories Are Strong , 2011, The Journal of Neuroscience.

[48]  D. Schacter,et al.  Conceptual fluency at test shifts recognition response bias in Alzheimer's disease: Implications for increased false recognition , 2007, Neuropsychologia.

[49]  Jason R. Taylor,et al.  Could masked conceptual primes increase recollection? The subtleties of measuring recollection and familiarity in recognition memory , 2012, Neuropsychologia.

[50]  Roberto Cabeza,et al.  Age-related Differences in Brain Activity during True and False Memory Retrieval , 2008, Journal of Cognitive Neuroscience.

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

[52]  Deborah M. Burke,et al.  Language, memory, and aging: Subject index , 1988 .

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

[54]  H. Eichenbaum,et al.  The medial temporal lobe and recognition memory. , 2007, Annual review of neuroscience.

[55]  Brian P. Kurilla,et al.  Processing fluency affects subjective claims of recollection , 2008, Memory & cognition.

[56]  Andrew P. Yonelinas,et al.  Activity reductions in perirhinal cortex predict conceptual priming and familiarity-based recognition , 2014, Neuropsychologia.

[57]  W. C. Shipley A Self-Administering Scale for Measuring Intellectual Impairment and Deterioration , 1940 .

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

[59]  G. Glover,et al.  Spiral‐in/out BOLD fMRI for increased SNR and reduced susceptibility artifacts , 2001, Magnetic resonance in medicine.

[60]  Sverker Sikström,et al.  Integrative neurocomputational perspectives on cognitive aging, neuromodulation, and representation , 2002, Neuroscience & Biobehavioral Reviews.

[61]  H. Kucera,et al.  Computational analysis of present-day American English , 1967 .

[62]  Andrew P. Yonelinas,et al.  Medial Temporal Lobe Activity during Source Retrieval Reflects Information Type, not Memory Strength , 2010, Journal of Cognitive Neuroscience.

[63]  D. Wolk,et al.  Discrimination and reliance on conceptual fluency cues are inversely related in patients with mild Alzheimer's disease , 2009, Neuropsychologia.

[64]  Shu-Chen Li,et al.  Neurocomputational perspectives linking neuromodulation, processing noise, representational distinctiveness, and cognitive aging , 2005 .

[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]  A P Yonelinas,et al.  The contribution of recollection and familiarity to recognition and source-memory judgments: a formal dual-process model and an analysis of receiver operating characteristics. , 1999, Journal of experimental psychology. Learning, memory, and cognition.

[67]  Christian Unkelbach,et al.  The Learned Interpretation of Cognitive Fluency , 2006, Psychological science.

[68]  Silvia A. Bunge,et al.  Developmental Cognitive Neuroscience Neural changes underlying the development of episodic memory during middle childhood , 2022 .

[69]  C B Cave,et al.  Memory: organization of brain systems and cognition. , 1993, Cold Spring Harbor symposia on quantitative biology.

[70]  Kevin J. Hawley,et al.  Contribution of perceptual fluency to recognition judgments. , 1991, Journal of experimental psychology. Learning, memory, and cognition.

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

[72]  Larry L. Jacoby,et al.  Subjective reports and process dissociation: Fluency, knowing, and feeling , 1998 .

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

[74]  Dana M. DeMaster,et al.  Developmental Differences in Medial Temporal Lobe Function during Memory Encoding , 2010, The Journal of Neuroscience.

[75]  E. Salmon,et al.  Patients with Alzheimer's disease use metamemory to attenuate the Jacoby–Whitehouse illusion , 2009, Neuropsychologia.

[76]  T. Tombaugh,et al.  The Mini‐Mental State Examination: A Comprehensive Review , 1992, Journal of the American Geriatrics Society.

[77]  A. Thapar,et al.  Aging and fluency-based illusions in recognition memory. , 2009, Psychology and aging.

[78]  Steven E. Prince,et al.  The Medial Temporal Lobe Distinguishes Old from New Independently of Consciousness , 2006, The Journal of Neuroscience.

[79]  S. Rajaram,et al.  Conceptual fluency selectively influences knowing. , 2000, Journal of experimental psychology. Learning, memory, and cognition.

[80]  D L Schacter,et al.  When false recognition is unopposed by true recognition: gist-based memory distortion in Alzheimer's disease. , 2000, Neuropsychology.

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