Decoding episodic memory in ageing: A Bayesian analysis of activity patterns predicting memory

Normal ageing is associated with a decline in episodic memory, and neuroimaging studies in older adults have shown reduced activity in prefrontal cortex and other regions critical for memory function in the young. However, older adults also activate additional regions, suggesting a degree of functional reorganisation that has been attributed variously to detrimental and adaptive changes. Evaluation of these competing hypotheses depends critically upon inferences about the relative location and distribution of activity that are not well supported by current univariate or multivariate analyses. Here, we employed a recently developed model-based multivariate ‘decoding’ approach (Friston et al., 2008) to re-analyse a rich episodic encoding dataset and examine directly how the patterns of activity change in ageing. We assessed which spatial activity patterns, within lateral prefrontal cortex, best predict successful memory formation. Bayesian model comparison showed that the older adults had more distributed and bilateral (fragmented) predictive patterns of activity in anterior inferior frontal gyrus and middle frontal gyrus. With this direct multivariate test for changes in patterns of activity, we replicate and extend earlier findings of reduced prefrontal lateralisation in ageing. These findings extend conclusions based on conventional analyses, and support the notion that ageing alters the spatial deployment of neuronal activity, to render it less spatially coherent and regionally specific. This greater distribution of activity in older adults was also linked to poorer individual memory performance, suggesting that it reflects neural ageing, rather than adaptive compensatory responses.

[1]  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.

[2]  M. D’Esposito,et al.  The Effect of Normal Aging on the Coupling of Neural Activity to the Bold Hemodynamic Response , 1999, NeuroImage.

[3]  Karl J. Friston,et al.  Classical and Bayesian Inference in Neuroimaging: Applications , 2002, NeuroImage.

[4]  K. Miller,et al.  Ocular dominance column development: analysis and simulation. , 1989, Science.

[5]  Christoph Kayser,et al.  Spatial Organization of Multisensory Responses in Temporal Association Cortex , 2009, The Journal of Neuroscience.

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

[7]  G. McCarthy,et al.  The Effects of Aging upon the Hemodynamic Response Measured by Functional MRI , 2001, NeuroImage.

[8]  M. Metz-Lutz Handbook of neuropsychology, Vol 6 et 7, Rapin I, Segalowitz SJ (Eds.). Elsevier (1992) , 1993 .

[9]  Karl J. Friston,et al.  Comparing Functional (PET) Images: The Assessment of Significant Change , 1991, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[10]  Y. Yamane,et al.  Complex objects are represented in macaque inferotemporal cortex by the combination of feature columns , 2001, Nature Neuroscience.

[11]  Stephan F. Taylor,et al.  Cerebral aging: integration of brain and behavioral models of cognitive function , 2001, Dialogues in clinical neuroscience.

[12]  Alan F. Murray,et al.  Synaptic rewiring for topographic mapping and receptive field development , 2010, Neural Networks.

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

[14]  B. Urbanc,et al.  Age-related reduction in microcolumnar structure correlates with cognitive decline in ventral but not dorsal area 46 of the rhesus monkey , 2009, Neuroscience.

[15]  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.

[16]  S. Petersen,et al.  Characterizing the Hemodynamic Response: Effects of Presentation Rate, Sampling Procedure, and the Possibility of Ordering Brain Activity Based on Relative Timing , 2000, NeuroImage.

[17]  R. Cabeza,et al.  Que PASA? The posterior-anterior shift in aging. , 2008, Cerebral cortex.

[18]  Patricia A. Reuter-Lorenz,et al.  Age differences in prefontal recruitment during verbal working memory maintenance depend on memory load , 2010, Cortex.

[19]  C. Spearman,et al.  "THE ABILITIES OF MAN". , 1928, Science.

[20]  Paul J. Laurienti,et al.  An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets , 2003, NeuroImage.

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

[22]  Shu-Chen Li,et al.  Aging Neuromodulation Impairs Associative Binding , 2005, Psychological science.

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

[24]  R. Henson What can Functional Neuroimaging Tell the Experimental Psychologist? , 2005, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[25]  Colin Blakemore,et al.  Vision: Coding and Efficiency , 1991 .

[26]  K. Svoboda,et al.  Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex , 2002, Nature.

[27]  Douglas C. Noll,et al.  Working Memory for Complex Scenes: Age Differences in Frontal and Hippocampal Activations , 2003, Journal of Cognitive Neuroscience.

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

[29]  R N Henson,et al.  Depth of processing effects on neural correlates of memory encoding: relationship between findings from across- and within-task comparisons. , 2001, Brain : a journal of neurology.

[30]  N. Kriegeskorte,et al.  The neuroscientific exploitation of high-resolution functional magnetic resonance imaging , 2006, 2006 International Conference of the IEEE Engineering in Medicine and Biology Society.

[31]  Antonino Vallesi,et al.  Overrecruitment in the Aging Brain as a Function of Task Demands: Evidence for a Compensatory View , 2011, Journal of Cognitive Neuroscience.

[32]  Bradley P. Sutton,et al.  Span, CRUNCH, and Beyond: Working Memory Capacity and the Aging Brain , 2010, Journal of Cognitive Neuroscience.

[33]  N. Kanwisher,et al.  Interpreting fMRI data: maps, modules and dimensions , 2008, Nature Reviews Neuroscience.

[34]  Karl J. Friston,et al.  Bayesian decoding of brain images , 2008, NeuroImage.

[35]  M. Albert,et al.  Changes in cerebral lateralization in aging? , 1984, Neuropsychologia.

[36]  Robert C. Welsh,et al.  Decreased neural specialization in old adults on a working memory task , 2006, Neuroreport.

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

[38]  Anna W. Roe Imaging the brain with optical methods , 2010 .

[39]  P. Reuter-Lorenz New visions of the aging mind and brain , 2002, Trends in Cognitive Sciences.

[40]  Rainer Goebel,et al.  Information-based functional brain mapping. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[41]  Anthony D Wagner,et al.  Assembling and encoding word representations: fMRI subsequent memory effects implicate a role for phonological control , 2003, Neuropsychologia.

[42]  M. Rugg,et al.  The relationship between aging, performance, and the neural correlates of successful memory encoding. , 2009, Cerebral cortex.

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

[44]  A. Dale,et al.  Building memories: remembering and forgetting of verbal experiences as predicted by brain activity. , 1998, Science.

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

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

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

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

[49]  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.

[50]  D. Hubel,et al.  Receptive fields and functional architecture of monkey striate cortex , 1968, The Journal of physiology.

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

[52]  William D. Penny,et al.  Bayesian model selection and averaging , 2007 .

[53]  John Harris,et al.  Vision: Coding and efficiency , 1994, Image Vis. Comput..

[54]  Daniel L Adams,et al.  The cortical column: a structure without a function , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[55]  David Willshaw Analysis of mouse EphA knockins and knockouts suggests that retinal axons programme target cells to form ordered retinotopic maps , 2006, Development.

[56]  A. Roe Optical Imaging of Short–Term Working Memory in Prefrontal Cortex of the Macaque Monkey , 2009 .

[57]  Karl J. Friston,et al.  Statistical parametric mapping , 2013 .

[58]  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.

[59]  Robert T. Knight,et al.  Altered prefrontal function with aging: Insights into age-associated performance decline , 2008, Brain Research.

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

[61]  J. Duncan An adaptive coding model of neural function in prefrontal cortex , 2001 .

[62]  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.

[63]  Morris Moscovitch,et al.  Neural correlates of auditory recognition under full and divided attention in younger and older adults , 2006, Neuropsychologia.

[64]  J. Ashburner,et al.  Nonlinear spatial normalization using basis functions , 1999, Human brain mapping.

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

[66]  Mark D'Esposito,et al.  Group comparisons: imaging the aging brain. , 2008, Social cognitive and affective neuroscience.

[67]  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.

[68]  S. Zeki Vision: The motion pathways of the visual cortex , 1991 .

[69]  C. Spence,et al.  Multisensory Integration: Space, Time and Superadditivity , 2005, Current Biology.

[70]  Karl J. Friston,et al.  Variational free energy and the Laplace approximation , 2007, NeuroImage.

[71]  C. Carter,et al.  The BOLD Hemodynamic Response in Healthy Aging , 2004, Journal of Cognitive Neuroscience.

[72]  Patricia A. Reuter-Lorenz,et al.  Human Neuroscience , 2022 .

[73]  J. Haynes Brain Reading: Decoding Mental States From Brain Activity In Humans , 2011 .

[74]  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.

[75]  R. Sperling,et al.  Age-related memory impairment associated with loss of parietal deactivation but preserved hippocampal activation , 2008, Proceedings of the National Academy of Sciences.

[76]  Leslie G. Ungerleider,et al.  Age-related changes in cortical blood flow activation during visual processing of faces and location , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[78]  F. Craik,et al.  The effects of age on the neural correlates of episodic encoding. , 1999, Cerebral cortex.

[79]  R. Gur,et al.  Laterality in functional brain imaging studies of schizophrenia. , 1999, Schizophrenia bulletin.

[80]  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.

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

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

[83]  G. Hogben EARTHQUAKES IN AUSTRALASIA. , 1893, Science.

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

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

[86]  Karl J. Friston,et al.  Characterizing the Response of PET and fMRI Data Using Multivariate Linear Models , 1997, NeuroImage.

[87]  R. West,et al.  An application of prefrontal cortex function theory to cognitive aging. , 1996, Psychological bulletin.

[88]  D. Chklovskii,et al.  Maps in the brain: what can we learn from them? , 2004, Annual review of neuroscience.

[89]  Leila Reddy,et al.  Coding of visual objects in the ventral stream , 2006, Current Opinion in Neurobiology.

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

[91]  Cheryl L Grady,et al.  The effects of encoding task on age-related differences in the functional neuroanatomy of face memory. , 2002, Psychology and aging.

[92]  Anthony R. McIntosh,et al.  The Effects of Divided Attention on Encoding- and Retrieval-Related Brain Activity: A PET Study of Younger and Older Adults , 2000, Journal of Cognitive Neuroscience.

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

[94]  Yaakov Stern,et al.  Age-related changes in brain activation during a delayed item recognition task , 2007, Neurobiology of Aging.

[95]  Yaakov Stern,et al.  Cognitive Reserve: Implications for Assessment and Intervention , 2013, Folia Phoniatrica et Logopaedica.

[96]  Sean M. Polyn,et al.  Beyond mind-reading: multi-voxel pattern analysis of fMRI data , 2006, Trends in Cognitive Sciences.

[97]  Keiji Tanaka Columns for complex visual object features in the inferotemporal cortex: clustering of cells with similar but slightly different stimulus selectivities. , 2003, Cerebral cortex.

[98]  C. Malsburg,et al.  How patterned neural connections can be set up by self-organization , 1976, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[99]  F. Tong,et al.  Decoding the visual and subjective contents of the human brain , 2005, Nature Neuroscience.

[100]  D. Hubel,et al.  Receptive fields, binocular interaction and functional architecture in the cat's visual cortex , 1962, The Journal of physiology.

[101]  Ian J. Deary,et al.  Inter-individual Differences in fMRI Entropy Measurements in Old Age , 2011, IEEE Transactions on Biomedical Engineering.

[102]  J. G. Snodgrass,et al.  Pragmatics of measuring recognition memory: applications to dementia and amnesia. , 1988, Journal of experimental psychology. General.

[103]  S. Geisser,et al.  On methods in the analysis of profile data , 1959 .

[104]  Robert C. Welsh,et al.  Aging and the Neural Correlates of Successful Picture Encoding: Frontal Activations Compensate for Decreased Medial-Temporal Activity , 2005, Journal of Cognitive Neuroscience.

[105]  T. Salthouse The processing-speed theory of adult age differences in cognition. , 1996, Psychological review.

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

[107]  Kikumi K. Tatsuoka,et al.  Caution indices based on item response theory , 1984 .

[108]  John Duncan,et al.  Target Detection by Opponent Coding in Monkey Prefrontal Cortex , 2010, Journal of Cognitive Neuroscience.

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