Age-associated reduction of asymmetry in prefrontal function and preservation of conceptual repetition priming

Older adults often show bilateral brain activation, compared to unilateral activation in younger adults, when performing tasks in domains of age-associated cognitive impairment, such as episodic and working memory. Less is known about activation associated with performance in cognitive domains that are typically unaffected by healthy aging. We used event-related functional magnetic resonance imaging to examine age-related patterns in brain activation associated with a form of implicit memory, repetition priming, which is typically preserved in healthy aging. Sixteen younger adults and 15 nondemented older adults performed semantic judgments (abstract/concrete) on single words in a study phase. In a test phase, identical judgments were made for repeated and new words. Younger and older adults showed similar response-time benefits (repetition priming) from repeated semantic classification. Repetition priming was associated with repetition-related reductions of prefrontal activation in both groups, but the patterns of activation differed between groups. Both groups showed similar activation reductions in dorsal left inferior prefrontal cortex (LIPFC), but older adults showed less reduction than younger adults in ventral and anterior LIPFC. Activation reductions were exclusively left-lateralized for younger adults, whereas older adults showed additional reductions in multiple regions of right frontal cortices. Right prefrontal activation reductions in older adults correlated with better repetition priming and better performance on independent tests of semantic processing. Thus, reduced asymmetry of prefrontal activation reductions in healthy aging was related to conceptual repetition priming, a form of learning that is spared in aging, and with the sparing of semantic memory.

[1]  S. Black,et al.  Evidence from Functional Neuroimaging of a Compensatory Prefrontal Network in Alzheimer's Disease , 2003, The Journal of Neuroscience.

[2]  Dick J. Veltman,et al.  Aging affects both perceptual and lexical/semantic components of word stem priming: An event-related fMRI study , 2005, Neurobiology of Learning and Memory.

[3]  Tor D. Wager,et al.  Common and unique components of response inhibition revealed by fMRI , 2005, NeuroImage.

[4]  A. Dale,et al.  Selective averaging of rapidly presented individual trials using fMRI , 1997, Human brain mapping.

[5]  Cindy Lustig,et al.  Preserved Neural Correlates of Priming in Old Age and Dementia , 2004, Neuron.

[6]  J. Morris,et al.  The Consortium to Establish a Registry for Alzheimer's Disease (CERAD). Part XIII. , 1996, Neurology.

[7]  J. Desmond,et al.  The role of left prefrontal cortex in language and memory. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[8]  B. Winblad,et al.  Brain Activation in Young and Older Adults During Implicit and Explicit Retrieval , 1997, Journal of Cognitive Neuroscience.

[9]  Matthew H. Davis,et al.  Neural Response Suppression Predicts Repetition Priming of Spoken Words and Pseudowords , 2006, Journal of Cognitive Neuroscience.

[10]  J. Morris,et al.  The Consortium to Establish a Registry for Alzheimer's Disease (CERAD). Part I. Clinical and neuropsychological assesment of Alzheimer's disease , 1989, Neurology.

[11]  Gary Glover,et al.  Aging effects on memory encoding in the frontal lobes. , 2002, Psychology and aging.

[12]  H. Roediger Implicit memory in normal human subjects , 1993 .

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

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

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

[16]  T. Bussey,et al.  The cognitive neuroscience of memory : encoding and retrieval , 2002 .

[17]  Lisa Barnes,et al.  Assessment of Lifetime Participation in Cognitively Stimulating Activities , 2003, Journal of clinical and experimental neuropsychology.

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

[20]  J. Raven,et al.  Manual for Raven's progressive matrices and vocabulary scales , 1962 .

[21]  L L Light,et al.  Divided attention, aging, and priming in exemplar generation and category verification , 2000, Memory & cognition.

[22]  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.

[23]  Karl J. Friston,et al.  Multisubject fMRI Studies and Conjunction Analyses , 1999, NeuroImage.

[24]  E. Kaplan,et al.  The assessment of aphasia and related disorders , 1972 .

[25]  R. Buckner,et al.  Dissociating Memory Retrieval Processes Using fMRI Evidence that Priming Does Not Support Recognition Memory , 2001, Neuron.

[26]  D. Schacter,et al.  Functional MRI evidence for a role of frontal and inferior temporal cortex in amodal components of priming. , 2000, Brain : a journal of neurology.

[27]  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.

[28]  Karl J. Friston,et al.  Analysis of functional MRI time‐series , 1994, Human Brain Mapping.

[29]  M. Folstein,et al.  Clinical diagnosis of Alzheimer's disease , 1984, Neurology.

[30]  Matthew Flatt,et al.  PsyScope: An interactive graphic system for designing and controlling experiments in the psychology laboratory using Macintosh computers , 1993 .

[31]  E Tulving,et al.  Neuroanatomical correlates of retrieval in episodic memory: auditory sentence recognition. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[32]  Leah L. Light,et al.  Dual-process theories of memory in old age: An update , 2012 .

[33]  H J Sagar,et al.  Incidental and intentional recall in Parkinson's disease: an account based on diminished attentional resources. , 1993, Journal of clinical and experimental neuropsychology.

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

[35]  Jesper Andersson,et al.  Valid conjunction inference with the minimum statistic , 2005, NeuroImage.

[36]  J. Gabrieli,et al.  Insights into the ageing mind: a view from cognitive neuroscience , 2004, Nature Reviews Neuroscience.

[37]  J. Gabrieli Cognitive neuroscience of human memory. , 1998, Annual review of psychology.

[38]  John D. E. Gabrieli,et al.  Neural Correlates of Auditory Repetition Priming: Reduced fMRI Activation in the Auditory Cortex , 2004, Journal of Cognitive Neuroscience.

[39]  M. Corbetta,et al.  Neural correlates of recovery from aphasia after damage to left inferior frontal cortex , 2000, Neurology.

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

[41]  Jordan Grafman,et al.  Handbook of Neuropsychology , 1991 .

[42]  J. Greene Contributions to Neuropsychological Assessment , 1995 .

[43]  D. Schacter,et al.  Task-specific repetition priming in left inferior prefrontal cortex. , 2000, Cerebral cortex.

[44]  Andrew Kirk,et al.  CONTRIBUTIONS TO NEUROPSYCHOLOGICAL ASSESSMENT. 2nd Edition. 1994. By Arthur L. Benton, Abigail B. Sivan, Kerry deS. Hamsher, Nils R. Varney and Otfried Spreen. Published by Oxford University Press. 159 pages. $C34.95 , 1996 .

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

[46]  D. Schacter,et al.  Priming and the Brain , 1998, Neuron.

[47]  J. B. Demb,et al.  Semantic Repetition Priming for Verbal and Pictorial Knowledge: A Functional MRI Study of Left Inferior Prefrontal Cortex , 1997, Journal of Cognitive Neuroscience.

[48]  James K. Nelson,et al.  Selection requirements during verb generation: differential recruitment in older and younger adults , 2004, NeuroImage.

[49]  Ruth B. Ekstrom,et al.  Manual for kit of factor-referenced cognitive tests , 1976 .

[50]  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.

[51]  J. B. Demb,et al.  Functional Magnetic Resonance Imaging of Semantic Memory Processes in the Frontal Lobes , 1996 .

[52]  D A Fleischman,et al.  Repetition priming in normal aging and Alzheimer's disease: a review of findings and theories. , 1998, Psychology and aging.

[53]  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.

[54]  Jemett L. Desmond,et al.  Semantic encoding and retrieval in the left inferior prefrontal cortex: a functional MRI study of task difficulty and process specificity , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[55]  Scott T. Grafton,et al.  Reductions in neural activity underlie behavioral components of repetition priming , 2005, Nature Neuroscience.

[56]  L. Light Memory and aging: four hypotheses in search of data. , 1991, Annual review of psychology.

[57]  Abraham Z. Snyder,et al.  Word Retrieval Learning Modulates Right Frontal Cortex in Patients with Left Frontal Damage , 2002, Neuron.

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

[59]  G. Glover,et al.  Self‐navigated spiral fMRI: Interleaved versus single‐shot , 1998, Magnetic resonance in medicine.

[60]  L L Light,et al.  Adult age differences in repetition priming: a meta-analysis. , 1994, Psychology and aging.

[61]  D. B. Mitchell,et al.  Age differences in implicit memory: conceptual, perceptual, or methodological? , 2003, Psychology and aging.

[62]  Karl J. Friston,et al.  Generalisability, Random Effects & Population Inference , 1998, NeuroImage.

[63]  R. L. Buckner and J.M. Logan,et al.  Frontal contributions to episodic memory encoding in the young and elderly , 2005 .

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

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

[66]  A. Dale,et al.  Functional-Anatomic Correlates of Object Priming in Humans Revealed by Rapid Presentation Event-Related fMRI , 1998, Neuron.

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

[68]  Debra A. Fleischman,et al.  Repetition Priming in Aging and Alzheimer's Disease: An Integrative Review and Future Directions , 2007, Cortex.

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

[70]  Randy L Buckner,et al.  Functional–Anatomic Correlates of Control Processes in Memory , 2003, The Journal of Neuroscience.

[71]  R. Henson Neuroimaging studies of priming , 2003, Progress in Neurobiology.

[72]  J. Rybash,et al.  Implicit memory and aging: A cognitive neuropsychological perspective , 1996 .

[73]  A. Paivio,et al.  Concreteness, imagery, and meaningfulness values for 925 nouns. , 1968, Journal of experimental psychology.

[74]  R. Buckner,et al.  Evidence for Neural Effects of Repetition that Directly Correlate with Behavioral Priming , 2004, Journal of Cognitive Neuroscience.

[75]  M. Albert,et al.  Use of brief cognitive tests to identify individuals in the community with clinically diagnosed Alzheimer's disease. , 1991, The International journal of neuroscience.

[76]  David A. Bennett,et al.  The Rush Memory and Aging Project: Study Design and Baseline Characteristics of the Study Cohort , 2005, Neuroepidemiology.

[77]  K. Grill-Spector,et al.  Object-selective cortex exhibits performance-independent repetition suppression. , 2006, Journal of neurophysiology.

[78]  E. Kaplan,et al.  The Boston naming test , 2001 .