Hemispheric asymmetry reduction in older adults: the HAROLD model.

A model of the effects of aging on brain activity during cognitive performance is introduced. The model is called HAROLD (hemispheric asymmetry reduction in older adults), and it states that, under similar circumstances, prefrontal activity during cognitive performances tends to be less lateralized in older adults than in younger adults. The model is supported by functional neuroimaging and other evidence in the domains of episodic memory, semantic memory, working memory, perception, and inhibitory control. Age-related hemispheric asymmetry reductions may have a compensatory function or they may reflect a dedifferentiation process. They may have a cognitive or neural origin, and they may reflect regional or network mechanisms. The HAROLD model is a cognitive neuroscience model that integrates ideas and findings from psychology and neuroscience of aging.

[1]  Daniel L. Schacter,et al.  The role of hippocampus and frontal cortex in age‐ related memory changes: a PET study , 1996, Neuroreport.

[2]  J. Mortimer,et al.  Education and other socioeconomic determinants of dementia and Alzheimer's disease , 1993 .

[3]  Hiroshi Shibasaki,et al.  Age-related changes in cerebral blood flow activation during a Card Sorting Test , 1997, Experimental Brain Research.

[4]  Cheryl L. Grady,et al.  AGE-RELATED CHANGES IN THE NEURAL CORRELATES OF DEGRADED AND NONDEGRADED FACE PROCESSING , 2000, Cognitive neuropsychology.

[5]  G. Ratcliff,et al.  Sex differences in brain aging: a quantitative magnetic resonance imaging study. , 1998, Archives of neurology.

[6]  F. Craik,et al.  The attentional demands of encoding and retrieval in younger and older adults: 1. Evidence from divided attention costs. , 1998, Psychology and aging.

[7]  Marcia K. Johnson,et al.  The role of prefrontal cortex during tests of episodic memory , 1998, Trends in Cognitive Sciences.

[8]  F. Craik,et al.  On the Transfer of Information from Temporary to Permanent Memory [and Discussion] , 1983 .

[9]  K P George,et al.  Cortical language activation in stroke patients recovering from aphasia with functional MRI. , 1999, Stroke.

[10]  J. Papadimitriou,et al.  TaqI polymorphism of the epidermal growth factor receptor gene in Caucasoids and Japanese. , 1993, Human heredity.

[11]  P. Pietrini,et al.  Sex differences in human brain morphometry and metabolism: an in vivo quantitative magnetic resonance imaging and positron emission tomography study on the effect of aging. , 1996, Archives of general psychiatry.

[12]  Roberto Cabeza,et al.  Functional neuroimaging of cognitive aging , 2001 .

[13]  P. Baltes,et al.  Emergence of a powerful connection between sensory and cognitive functions across the adult life span: a new window to the study of cognitive aging? , 1997, Psychology and aging.

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

[15]  M. Kleban,et al.  Relationships between hearing loss and cognition in normally hearing aged persons. , 1976, Journal of gerontology.

[16]  B Horwitz,et al.  Age-related differences in volumes of subcortical nuclei, brain matter, and cerebrospinal fluid in healthy men as measured with magnetic resonance imaging. , 1992, Archives of neurology.

[17]  S. Roesch,et al.  A comparison of the factor structure of processing speed for younger and older adults: testing the assumption of measurement equivalence across age groups. , 1997, Psychology and aging.

[18]  Fergus I. M. Craik,et al.  A functional account of age differences in memory , 2016 .

[19]  Arthur P. Shimamura,et al.  Memory and frontal lobe function. , 1995 .

[20]  MasashiOhyama,et al.  Role of the Nondominant Hemisphere and Undamaged Area During Word Repetition in Poststroke Aphasics , 1996 .

[21]  R. Katzman.,et al.  Education and the prevalence of dementia and Alzheimer's disease , 1993, Neurology.

[22]  B. Balinsky.  An analysis of the mental factors of various age groups from nine to sixty. , 1941 .

[23]  K. Berman,et al.  Context-dependent, neural system-specific neurophysiological concomitants of ageing: mapping PET correlates during cognitive activation. , 1999, Brain : a journal of neurology.

[24]  E E Smith,et al.  The neural substrate and temporal dynamics of interference effects in working memory as revealed by event-related functional MRI. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[25]  D. Benson,et al.  Aphasia and the Lateralization of Language , 1986, Cortex.

[26]  Y Yonekura,et al.  An fMRI study of the functional neuroanatomy of picture encoding in younger and older adults. , 2001, Brain research. Cognitive brain research.

[27]  M. Ohyama,et al.  Role of the nondominant hemisphere and undamaged area during word repetition in poststroke aphasics. A PET activation study. , 1996, Stroke.

[28]  Edward E. Smith,et al.  Working Memory: A View from Neuroimaging , 1997, Cognitive Psychology.

[29]  Fergus I. M. Craik,et al.  Aging and cognitive deficits : The role of attentional resources , 1982 .

[30]  Fergus I. M. Craik,et al.  Aging and Cognitive Deficits , 1982 .

[31]  M. Weller,et al.  Increasing right hand dominance with age on a motor skill task , 1985, Psychological Medicine.

[32]  Pamela K. Smith,et al.  Models of visuospatial and verbal memory across the adult life span. , 2002, Psychology and aging.

[33]  R W Cox,et al.  Language processing is strongly left lateralized in both sexes. Evidence from functional MRI. , 1999, Brain : a journal of neurology.

[34]  R S Frackowiak,et al.  Motor recovery after acute ischaemic stroke: a metabolic study. , 1992, Journal of neurology, neurosurgery, and psychiatry.

[35]  R. Dixon,et al.  Age-related cognitive deficits mediated by changes in the striatal dopamine system. , 2000, The American journal of psychiatry.

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

[37]  F H Previc,et al.  A general theory concerning the prenatal origins of cerebral lateralization in humans. , 1991, Psychological review.

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

[39]  G Bernardi,et al.  Bilateral hemispheric activation in the early recovery of motor function after stroke. , 1998, Stroke.

[40]  M. Mitrushina,et al.  Analysis of longitudinal covariance structures in assessment of stability of cognitive functions in elderly , 1991 .

[41]  F Kehren,et al.  Left-right asymmetry of striatal dopamine D2 receptors. , 1998, Nuclear medicine communications.

[42]  R. Cabeza,et al.  Handbook of functional neuroimaging of cognition , 2001 .

[43]  V. Hömberg,et al.  Reorganization of motor output in the non-affected hemisphere after stroke. , 1997, Brain : a journal of neurology.

[44]  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.

[45]  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.

[46]  A. Jon Stoessl,et al.  Nigrostriatal dopamine system and motor lateralization , 2000, Behavioural Brain Research.

[47]  T. Elmo.  Hemispheric asymmetry of auditory evoked potentials to comparisons within and across phonetic categories. , 1987, Scandinavian journal of psychology.

[48]  M. Just,et al.  Plasticity of language-related brain function during recovery from stroke. , 1999, Stroke.

[49]  H. E. Garrett,et al.  A developmental theory of intelligence. , 2011, The American psychologist.

[50]  Siu Cheung Li,et al.  Cross-level unification: A computational exploration of the link between deterioration of neurotrans , 1999 .

[51]  R. Cabeza,et al.  Imaging Cognition II: An Empirical Review of 275 PET and fMRI Studies , 2000, Journal of Cognitive Neuroscience.

[52]  E. Bizzi,et al.  The Cognitive Neurosciences , 1996 .

[53]  E. Strauss,et al.  The neurobiological basis of lateralized cerebral function. A review. , 1983, Human neurobiology.

[54]  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.

[55]  M. Banich.  The Missing Link: The Role of Interhemispheric Interaction in Attentional Processing , 1998, Brain and Cognition.

[56]  M Corbetta,et al.  Preserved speech abilities and compensation following prefrontal damage. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[57]  E. Tulving,et al.  PET studies of encoding and retrieval: The HERA model , 1996, Psychonomic bulletin & review.

[58]  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.

[59]  L. Katz,et al.  Sex differences in the functional organization of the brain for language , 1995, Nature.

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

[61]  T. Salthouse,et al.  Interrelations of age, visual acuity, and cognitive functioning. , 1996, The journals of gerontology. Series B, Psychological sciences and social sciences.

[62]  Robert A. Koeppe,et al.  Age Differences in Behavior and PET Activation Reveal Differences in Interference Resolution in Verbal Working Memory , 2000, Journal of Cognitive Neuroscience.

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

[64]  Mark S. Seidenberg,et al.  Changes in cerebral functioning associated with normal aging. , 1989, Journal of clinical and experimental neuropsychology.

[65]  Anthony R. McIntosh,et al.  Age-Related Changes in Regional Cerebral Blood Flow during Working Memory for Faces , 1998, NeuroImage.

[66]  Lars Nyberg,et al.  Asymmetric frontal activation during episodic memory: what kind of specificity? , 1998, Trends in Cognitive Sciences.

[67]  Klaus F. Riegel,et al.  Age differences in response speed as a function of controlled variations of stimulus conditions: evidence of a general speed factor. , 1962, Gerontologia.

[68]  P M Rossini,et al.  Post-stroke reorganization of brain motor output to the hand: a 2-4 month follow-up with focal magnetic transcranial stimulation. , 1997, Electroencephalography and clinical neurophysiology.

[69]  Lars Bäckman,et al.  Psychological compensation: a theoretical framework. , 1992, Psychological bulletin.

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

[71]  Louise Stanczak,et al.  Neural Recruitment and Cognitive Aging: Two Hemispheres Are Better Than One, Especially as You Age , 1999 .

[72]  R. Nebes,et al.  The effect of age on hemispheric asymmetry in visual and auditory identification. , 1983, Experimental aging research.

[73]  HighWire Press.  Philosophical Transactions of the Royal Society of London , 1781, The London Medical Journal.

[74]  S. Houle,et al.  Activation of medial temporal structures during episodic memory retrieval , 1996, Nature.

[75]  D. Kahneman.  Attention and Effort , 1973 .

[76]  H. Markowitsch.  Cognitive neuroscience of memory , 1998 .

[77]  James M Provenzale,et al.  Aging and attentional guidance during visual search: functional neuroanatomy by positron emission tomography. , 2002, Psychology and aging.

[78]  M. Rastatter,et al.  Some effects of advanced aging on the visual-language processing capacity of the left and right hemispheres: evidence from unilateral tachistoscopic viewing. , 1990, Journal of speech and hearing research.

[79]  N. Raz.  Aging of the brain and its impact on cognitive performance: Integration of structural and functional findings. , 2000 .

[80]  R. Woods,et al.  Recovery from wernicke's aphasia: A positron emission tomographic study , 1995, Annals of neurology.

[81]  E. Glisky,et al.  Double dissociation between item and source memory. , 1995 .

[82]  David J. Madden,et al.  Adult Age Differences in Regional Cerebral Blood Flow during Visual Word Identification: Evidence from H2 15O PET , 1996, NeuroImage.

[83]  A. Damasio,et al.  Normative observations on neuropsychological test performances in old age. , 1981, Journal of clinical neuropsychology.

[84]  M. D’Esposito,et al.  Isolating the neural mechanisms of age-related changes in human working memory , 2000, Nature Neuroscience.

[85]  N. Volkow,et al.  Association between decline in brain dopamine activity with age and cognitive and motor impairment in healthy individuals. , 1998, The American journal of psychiatry.

[86]  Svetlana Levitan,et al.  Interhemispheric effects on map organization following simulated cortical lesions , 1999, Artif. Intell. Medicine.

[87]  Barry Horwitz,et al.  Age differences in intercorrelations between regional cerebral metabolic rates for glucose , 1986, Annals of neurology.

[88]  A. Parkin,et al.  Human memory , 1999, Current Biology.

[89]  N. Raz,et al.  Pathoclysis in aging human cerebral cortex: Evidence from in vivo MRI morphometry , 1993, Psychobiology.

[90]  N. Tzourio,et al.  Functional Anatomy of Dominance for Speech Comprehension in Left Handers vs Right Handers , 1998, NeuroImage.

[91]  C M Epstein,et al.  Transcranial magnetic stimulation: language function. , 1998, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[92]  E. Tulving,et al.  Age‐related differences in effective neural connectivity during encoding and recall , 1997, Neuroreport.

[93]  J. Brion,et al.  Evidence of cortical reorganization in hemiparetic patients. , 1989, Stroke.

[94]  J D Cohen,et al.  A network model of catecholamine effects: gain, signal-to-noise ratio, and behavior. , 1990, Science.

[95]  Hidenao Fukuyama,et al.  Movement-related cortical potentials and regional cerebral blood flow change in patients with stroke after motor recovery , 1997, Journal of the Neurological Sciences.

[96]  G. Demeurisse,et al.  Brain Activation During a Linguistic Task in Conduction Aphasia , 1991, Cortex.

[97]  C Caltagirone,et al.  Correlations of flow velocity changes during mental activity and recovery from aphasia in ischemic stroke , 1998, Neurology.

[98]  C. Nelson,et al.  The lateralization of language comprehension using event-related potentials , 1990, Brain and Cognition.

[99]  Functional neuroimaging of neuropsychologically impaired patients , 2001 .

[100]  Reaction times of aging subjects to monaural verbal stimuli: some evidence for a reduction in right-hemisphere linguistic processing capacity. , 1987, Journal of speech and hearing research.

[101]  G. Ojemann.  Cortical organization of language , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[102]  P. Satz.  Brain reserve capacity on symptom onset after brain injury: A formulation and review of evidence for threshold theory. , 1993 .

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

[104]  David J. Madden,et al.  Aging and Recognition Memory: Changes in Regional Cerebral Blood Flow Associated with Components of Reaction Time Distributions , 1999, Journal of Cognitive Neuroscience.

[105]  C. Hertzog,et al.  Metacognition in adulthood and old age. , 2000 .

[106]  Nina Kraus,et al.  Aging Affects Hemispheric Asymmetry in the Neural Representation of Speech Sounds , 2000, The Journal of Neuroscience.

[107]  Lynn Hasher,et al.  Working Memory, Comprehension, and Aging: A Review and a New View , 1988 .

[108]  E. Stein,et al.  Right hemispheric dominance of inhibitory control: an event-related functional MRI study. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[109]  D. Head,et al.  Selective aging of the human cerebral cortex observed in vivo: differential vulnerability of the prefrontal gray matter. , 1997, Cerebral cortex.

[110]  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.

[111]  Sandra E. Trehub,et al.  Aging and cognitive processes , 1982 .

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

[113]  J. Jonides,et al.  Inhibition in verbal working memory revealed by brain activation. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[114]  Leslie G. Ungerleider,et al.  Age-related reductions in human recognition memory due to impaired encoding. , 1995, Science.

[115]  L A Beckett,et al.  Education and other measures of socioeconomic status and risk of incident Alzheimer disease in a defined population of older persons. , 1997, Archives of neurology.

[116]  J E Desmond,et al.  Age differences in prefrontal cortical activity in working memory. , 2001, Psychology and aging.

[117]  F. Craik,et al.  Hemispheric encoding/retrieval asymmetry in episodic memory: positron emission tomography findings. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[118]  Francis Eustache,et al.  New questions on the hemispheric encoding/retrieval asymmetry (HERA) model assessed by divided visual-field tachistoscopy in normal subjects , 2001, Neuropsychologia.

[119]  R. Friedland,et al.  Epidemiology, education, and the ecology of Alzheimer's disease , 1993, Neurology.

[120]  A. Benton,et al.  Journal of Clinical Neuropsychology , 1981 .

[121]  C. Calautti,et al.  Effects of Age on Brain Activation During Auditory-Cued Thumb-to-Index Opposition: A Positron Emission Tomography Study , 2001, Stroke.

[122]  K. F. Berman,et al.  Age-related changes in rCBF activation during an N-back working memory paradigm occur prior to age 50 , 2000, NeuroImage.

[123]  A Engelien,et al.  The functional anatomy of recovery from auditory agnosia. A PET study of sound categorization in a neurological patient and normal controls. , 1995, Brain : a journal of neurology.

[124]  A. R. McIntosh,et al.  Recruitment of unique neural systems to support visual memory in normal aging , 1999, Current Biology.

[125]  A. Beaton,et al.  The Relation of Planum Temporale Asymmetry and Morphology of the Corpus Callosum to Handedness, Gender, and Dyslexia: A Review of the Evidence , 1997, Brain and Language.

[126]  Nicole D. Anderson,et al.  The attentional demands of encoding and retrieval in younger and older adults: 2. Evidence from secondary task reaction time distributions. , 1999, Psychology and aging.

[127]  Robert Sekuler,et al.  Corticolimbic Interactions Associated with Performance on a Short-Term Memory Task Are Modified by Age , 2000, The Journal of Neuroscience.

[128]  S. Langenecker,et al.  Differences in the functional neuroanatomy of inhibitory control across the adult life span. , 2002, Psychology and aging.

[129]  N. Geschwind,et al.  Right-left asymmetrics in the brain. , 1978, Science.

[130]  Hemisphericity in aphasic language recovery. , 1983, Journal of speech and hearing research.

[131]  Lateralization of peripherally and centrally masked words in young and elderly people. , 1984, Journal of gerontology.

[132]  E Altenmüller,et al.  Language processing in aphasia: changes in lateralization patterns during recovery reflect cerebral plasticity in adults. , 1997, Electroencephalography and clinical neurophysiology.

[133]  P. Meudell,et al.  Age Related Differences in Left and Right Hand Skill and In Visuo-Spatial Performance: Their Possible Relationships to the Hypothesis that the Right Hemisphere Ages More Rapidly than the Left , 1987, Cortex.