II. Temporal patterns of longitudinal change in aging brain function

Time-dependent changes in brain activity were assessed in a group of older adults who maintained good physical and cognitive health at years 1, 3, 5, 7, and 9 of the Baltimore Longitudinal Study of Aging neuroimaging study. Each year, these participants underwent PET scans during rest and delayed verbal and figural recognition memory conditions. While memory performance remained stable over the 8 years, both generalized and modality-specific patterns of time-dependent changes in regional cerebral blood flow (rCBF) were found. Many brain regions showed steady, progressive changes in rCBF over the 8 years while others maintained rCBF for a number of years before showing incremental declines or increases in activity. These temporal patterns of change were observed in many regions of the brain, particularly in the frontal and temporal lobes, suggesting that there are distinctive patterns of age-related functional decline and compensatory activity over time. The precise patterns of regional involvement and the temporal dynamics of rCBF change within specific regions vary based on cognitive processing demands.

[1]  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.

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

[3]  Brenda Milner,et al.  Memory for different aspects of complex visual scenes after unilateral temporal- or frontal-lobe resection , 1993, Neuropsychologia.

[4]  Nancy Kanwisher,et al.  A cortical representation of the local visual environment , 1998, Nature.

[5]  J. Price.  The relationship between tangle and plaque formation during healthy aging and mild dementia , 1993, Neurobiology of Aging.

[6]  Yaakov Stern,et al.  Imaging hippocampal function across the human life span: Is memory decline normal or not? , 2002, Annals of neurology.

[7]  S. Resnick,et al.  Brain activation during encoding and recognition of verbal and figural information in older adults , 2005, Neurobiology of Aging.

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

[9]  T A Polk,et al.  The neural development and organization of letter recognition: evidence from functional neuroimaging, computational modeling, and behavioral studies. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[10]  R. Clark,et al.  The medial temporal lobe. , 2004, Annual review of neuroscience.

[11]  R Brookmeyer,et al.  Age-specific incidence rates of Alzheimer’s disease , 2000, Neurology.

[12]  A. Scheibel.  Structural and functional changes in the aging brain , 1996 .

[13]  P. Hof,et al.  The neuropathological changes associated with normal brain aging. , 1996, Histology and histopathology.

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

[15]  D. Tomasi,et al.  Practice-induced changes of brain function during visual attention: a parametric fMRI study at 4 Tesla , 2004, NeuroImage.

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

[17]  Lars-Göran Nilsson,et al.  New frontiers in cognitive aging , 2004 .

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

[19]  Joseph B. Sala,et al.  Increased neural efficiency with repeated performance of a working memory task is information-type dependent. , 2006, Cerebral cortex.

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

[21]  T. Allison,et al.  Differential Sensitivity of Human Visual Cortex to Faces, Letterstrings, and Textures: A Functional Magnetic Resonance Imaging Study , 1996, The Journal of Neuroscience.

[22]  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.

[23]  J. Haxby,et al.  Attribute-based neural substrates in temporal cortex for perceiving and knowing about objects , 1999, Nature Neuroscience.

[24]  R. Cabeza.  Cognitive neuroscience of aging: contributions of functional neuroimaging. , 2001, Scandinavian journal of psychology.

[25]  G. V. Van Hoesen,et al.  The topographical and neuroanatomical distribution of neurofibrillary tangles and neuritic plaques in the cerebral cortex of patients with Alzheimer's disease. , 1991, Cerebral cortex.

[26]  S. Resnick,et al.  One-year age changes in MRI brain volumes in older adults. , 2000, Cerebral cortex.

[27]  J. Morris.  The Challenge of Characterizing Normal Brain Aging in Relation to Alzheimer’s Disease , 1997, Neurobiology of Aging.

[28]  A. R. Damasio,et al.  Memory‐related neural systems in Alzheimer's disease , 1990, Neurology.

[29]  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.

[30]  M. Torrens.  Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

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

[32]  S. Resnick,et al.  Effects of Estrogen Replacement Therapy on PET Cerebral Blood Flow and Neuropsychological Performance , 1998, Hormones and Behavior.

[33]  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.

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

[35]  Tom Dening,et al.  Textbook of Geriatric Neuropsychiatry , 1996 .

[36]  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.

[37]  Alex Martin,et al.  Modulation of neural activity during object naming: effects of time and practice. , 2003, Cerebral cortex.

[38]  H. Braak,et al.  Frequency of Stages of Alzheimer-Related Lesions in Different Age Categories , 1997, Neurobiology of Aging.

[39]  S. M. Resnick,et al.  I. Longitudinal changes in aging brain function , 2008, Neurobiology of Aging.

[40]  John E. Desmond,et al.  Load- and practice-dependent increases in cerebro-cerebellar activation in verbal working memory: an fMRI study , 2005, NeuroImage.

[41]  D. Amaral,et al.  Three Cases of Enduring Memory Impairment after Bilateral Damage Limited to the Hippocampal Formation , 1996, The Journal of Neuroscience.

[42]  J. Price,et al.  The distribution of tangles, plaques and related immunohistochemical markers in healthy aging and Alzheimer's disease , 1991, Neurobiology of Aging.

[43]  J. Morrison,et al.  Regional distribution of neurofibrillary tangles and senile plaques in the cerebral cortex of elderly patients: a quantitative evaluation of a one-year autopsy population from a geriatric hospital. , 1994, Cerebral cortex.

[44]  S S Schochet,et al.  Neuropathology of aging. , 1998, Neurologic clinics.

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

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

[47]  Lars Nyberg,et al.  Cognitive aging : a view from brain imaging , 2004 .

[48]  W. Scoville,et al.  LOSS OF RECENT MEMORY AFTER BILATERAL HIPPOCAMPAL LESIONS , 1957, Journal of neurology, neurosurgery, and psychiatry.

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

[50]  David Arenberg,et al.  Normal Human Aging: The Baltimore Longitudinal Study on Aging , 1984 .

[51]  Richard S. J. Frackowiak,et al.  Cerebral blood flow, blood volume and oxygen utilization. Normal values and effect of age. , 1990, Brain : a journal of neurology.

[52]  D Comar,et al.  Regional Cerebral Blood Flow and Oxygen Consumption in Human Aging , 1984, Stroke.

[53]  P. Baltes,et al.  The strong connection between sensory and cognitive performance in old age: not due to sensory acuity reductions operating during cognitive assessment. , 2001 .

[54]  D J Madden,et al.  Adult age differences in visual search accuracy: attentional guidance and target detectability. , 1999, Psychology and aging.

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

[56]  Mark D'Esposito,et al.  A functional MRI study of the influence of practice on component processes of working memory , 2004, NeuroImage.

[57]  J. Raaijmakers,et al.  Neuroanatomical correlates of episodic encoding and retrieval in young and elderly subjects. , 2003, Brain : a journal of neurology.

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

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

[60]  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.