Age Differences in the Frontal Lateralization of Verbal and Spatial Working Memory Revealed by PET

Age-related decline in working memory figures prominently in theories of cognitive aging. However, the effects of aging on the neural substrate of working memory are largely unknown. Positron emission tomography (PET) was used to investigate verbal and spatial short-term storage (3 sec) in older and younger adults. Previous investigations with younger subjects performing these same tasks have revealed asymmetries in the lateral organization of verbal and spatial working memory. Using volume of interest (VOI) analyses that specifically compared activation at sites identified with working memory to their homologous twin in the opposite hemisphere, we show pronounced age differences in this organization, particularly in the frontal lobes: In younger adults, activation is predominantly left lateralized for verbal working memory, and right lateralized for spatial working memory, whereas older adults show a global pattern of anterior bilateral activation for both types of memory. Analyses of frontal subregions indicate that several underlying patterns contribute to global bilaterality in older adults: most notably, bilateral activation in areas associated with rehearsal, and paradoxical laterality in dorsolateral prefrontal sites (DLPFC; greater left activation for spatial and greater right activation for verbal). We consider several mechanisms that could account for these age differences including the possibility that bilateral activation reflects recruitment to compensate for neural decline.

[1]  M. Lamb,et al.  The Two Sides of Perception , 1998, Trends in Cognitive Sciences.

[2]  J. Jonides,et al.  Neuroimaging analyses of human working memory. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[3]  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 .

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

[5]  上村 和夫,et al.  Quantification of brain function : tracer kinetics and image analysis in brain PET : proceedings of Brain PET '93 Akita : Quantification of Brain Function, Akita, Japan, 29-31 May, 1993 , 1993 .

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

[7]  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.

[8]  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.

[9]  Marcel Adam Just,et al.  The Role of Working Memory in Language Comprehension , 1988 .

[10]  M. Mintun,et al.  Automated detection of the intercommissural line for stereotactic localization of functional brain images. , 1993, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[11]  T. Goldberg,et al.  Isolating the Mnemonic Component in Spatial Delayed Response: A Controlled PET15O-Labeled Water Regional Cerebral Blood Flow Study in Normal Humans , 1996, NeuroImage.

[12]  Leslie G. Ungerleider,et al.  Object and spatial visual working memory activate separate neural systems in human cortex. , 1996, Cerebral cortex.

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

[14]  M. Kinsbourne The minor cerebral hemisphere as a source of aphasic speech. , 1971, Archives of neurology.

[15]  Edward E. Smith,et al.  Dissociation of Storage and Rehearsal in Verbal Working Memory: Evidence From Positron Emission Tomography , 1996 .

[16]  M. Kinsbourne The Minor Cerebral Hemisphere , 1971 .

[17]  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.

[18]  S E Petersen,et al.  A positron emission tomography study of the short-term maintenance of verbal information , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  Alan C. Evans,et al.  A Three-Dimensional Statistical Analysis for CBF Activation Studies in Human Brain , 1992, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[20]  M. D’Esposito,et al.  Functional MRI studies of spatial and nonspatial working memory. , 1998, Brain research. Cognitive brain research.

[21]  Alan C. Evans,et al.  Functional activation of the human frontal cortex during the performance of verbal working memory tasks. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[22]  S Minoshima,et al.  An automated method for rotational correction and centering of three-dimensional functional brain images. , 1992, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[23]  Peter Herscovitch,et al.  Dissociation of Object and Spatial Vision in Human Extrastriate Cortex: Age-Related Changes in Activation of Regional Cerebral Blood Flow Measured with [15 O]Water and Positron Emission Tomography , 1992, Journal of Cognitive Neuroscience.

[24]  J C Froment,et al.  Positron Emission Tomography Metabolic Data Corrected for Cortical Atrophy Using Magnetic Resonance Imaging , 1996, Alzheimer disease and associated disorders.

[25]  Edward E. Smith,et al.  Spatial versus Object Working Memory: PET Investigations , 1995, Journal of Cognitive Neuroscience.

[26]  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.

[27]  Alan C. Evans,et al.  Evidence for a two-stage model of spatial working memory processing within the lateral frontal cortex: a positron emission tomography study. , 1996, Cerebral cortex.

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

[29]  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.

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

[31]  J. Jonides,et al.  Dissociating verbal and spatial working memory using PET. , 1996, Cerebral cortex.

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

[33]  Karl J. Friston,et al.  Functional mapping of brain areas implicated in auditory--verbal memory function. , 1993, Brain : a journal of neurology.

[34]  Edward E. Smith,et al.  The Role of Parietal Cortex in Verbal Working Memory , 1998, The Journal of Neuroscience.

[35]  Edward Awh,et al.  Verbal and Spatial Working Memory in Humans , 1996 .

[36]  Edward E. Smith,et al.  Verbal Working Memory Load Affects Regional Brain Activation as Measured by PET , 1997, Journal of Cognitive Neuroscience.

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

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

[39]  M Moscovitch,et al.  Frontal Lobes, Memory, and Aging , 1995, Annals of the New York Academy of Sciences.

[40]  Robert H. Logie,et al.  Working Memory and Thinking: Current Issues In Thinking And Reasoning , 1998 .

[41]  Edward E. Smith,et al.  PET Evidence for an Amodal Verbal Working Memory System , 1996, NeuroImage.

[42]  P. Goldman-Rakic Working memory and the mind. , 1992, Scientific American.

[43]  Edward E. Smith,et al.  Spatial working memory in humans as revealed by PET , 1993, Nature.

[44]  C. Degueldre,et al.  Regional brain activity during working memory tasks. , 1996, Brain : a journal of neurology.

[45]  J. Desmond,et al.  Load-Dependent Roles of Frontal Brain Regions in the Maintenance of Working Memory , 1999, NeuroImage.

[46]  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.

[47]  T. Salthouse Mechanisms of Age Cognition Relations in Adulthood , 1992 .

[48]  R. Koeppe,et al.  Anatomic standardization: linear scaling and nonlinear warping of functional brain images. , 1994, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

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

[50]  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.

[51]  Edward E. Smith,et al.  An Invitation to cognitive science , 1997 .

[52]  Richard S. J. Frackowiak,et al.  The neural correlates of the verbal component of working memory , 1993, Nature.

[53]  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.

[54]  Leslie G. Ungerleider,et al.  An area specialized for spatial working memory in human frontal cortex. , 1998, Science.

[55]  Tim Shallice,et al.  Neuropsychological impairments of short-term memory , 1992 .

[56]  R. Knight,et al.  Prefrontal deficits in attention and inhibitory control with aging. , 1997, Cerebral cortex.