Neuroanatomic Overlap of Working Memory and Spatial Attention Networks: A Functional MRI Comparison within Subjects

Frontal and posterior parietal activations have been reported in numerous studies of working memory and visuospatial attention. To directly compare the brain regions engaged by these two cognitive functions, the same set of subjects consecutively participated in tasks of working memory and spatial attention while undergoing functional MRI (fMRI). The working memory task required the subject to maintain an on-line representation of foveally displayed letters against a background of distracters. The spatial attention task required the subject to shift visual attention covertly in response to a centrally presented directional cue. The spatial attention task had no working memory requirement, and the working memory task had no covert spatial attention requirement. Subjects' ability to maintain central fixation was confirmed outside the MRI scanner using infrared oculography. According to cognitive conjunction analysis, the set of activations common to both tasks included the intraparietal sulcus, ventral precentral sulcus, supplementary motor area, frontal eye fields, thalamus, cerebellum, left temporal neocortex, and right insula. Double-subtraction analyses yielded additional activations attributable to verbal working memory in premotor cortex, left inferior prefrontal cortex, right inferior parietal lobule, precuneus, and right cerebellum. Additional activations attributable to covert spatial attention included the occipitotemporal junction and extrastriate cortex. The use of two different tasks in the same set of subjects allowed us to provide an unequivocal demonstration that the neural networks subserving spatial attention and working memory intersect at several frontoparietal sites. These findings support the view that major cognitive domains are represented by partially overlapping large-scale neural networks. The presence of this overlap also suggests that spatial attention and working memory share common cognitive features related to the dynamic shifting of attentional resources.

[1]  S. Sternberg High-Speed Scanning in Human Memory , 1966, Science.

[2]  M. Posner,et al.  Orienting of Attention* , 1980, The Quarterly journal of experimental psychology.

[3]  M. Mesulam A cortical network for directed attention and unilateral neglect , 1981, Annals of neurology.

[4]  G. Carpenter,et al.  Which behavior does the lamprey central motor program mediate? , 1983, Science.

[5]  René Müri,et al.  Cortical control of saccades , 1995, Annals of neurology.

[6]  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 .

[7]  M M Mesulam,et al.  Large‐scale neurocognitive networks and distributed processing for attention, language, and memory , 1990, Annals of neurology.

[8]  C Pierrot-Deseilligny,et al.  Cortical control of saccades in man. , 1991, Acta neurologica Belgica.

[9]  M. Corbetta,et al.  A PET study of visuospatial attention , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  A. Gevins,et al.  Spatiotemporal dynamics of component processes in human working memory. , 1993, Electroencephalography and clinical neurophysiology.

[11]  Richard S. J. Frackowiak,et al.  Cortical control of saccades and fixation in man. A PET study. , 1994, Brain : a journal of neurology.

[12]  B J Ransil,et al.  Test-Retest Reliability of the Edinburgh Handedness Inventory and Global Handedness Preference Measurements, and Their Correlation , 1994, Perceptual and motor skills.

[13]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[14]  Karl J. Friston,et al.  Analysis of fMRI Time-Series Revisited , 1995, NeuroImage.

[15]  Karl J. Friston,et al.  Spatial registration and normalization of images , 1995 .

[16]  Gregory McCarthy,et al.  Review : Functional Neuroimaging of Memory , 1995 .

[17]  Lynn C. Robertson,et al.  The neurology of visual attention. , 1995 .

[18]  Karl J. Friston,et al.  Analysis of fMRI Time-Series Revisited—Again , 1995, NeuroImage.

[19]  R. J. Zatorre,et al.  PET Studies of Phonological Processing: A Critical Reply to Poeppel , 1996, Brain and Language.

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

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

[22]  C. Butter,et al.  Ipsilesional Displacement of Egocentric Midline in Neglect Patients with, but Not in Those Without, Extensive Right Parietal Damage , 1997 .

[23]  R. Cabeza,et al.  Imaging Cognition: An Empirical Review of PET Studies with Normal Subjects , 1997, Journal of Cognitive Neuroscience.

[24]  Todd B. Parrish,et al.  The large-scale neural network for spatial attention displays multi-functional overlap , 1997 .

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

[26]  Karl J. Friston,et al.  Cognitive Conjunction: A New Approach to Brain Activation Experiments , 1997, NeuroImage.

[27]  V. Mountcastle The columnar organization of the neocortex. , 1997, Brain : a journal of neurology.

[28]  Leslie G. Ungerleider,et al.  Transient and sustained activity in a distributed neural system for human working memory , 1997, Nature.

[29]  Edward E. Smith,et al.  Temporal dynamics of brain activation during a working memory task , 1997, Nature.

[30]  Leslie G. Ungerleider,et al.  Mechanisms of directed attention in the human extrastriate cortex as revealed by functional MRI. , 1998, Science.

[31]  A. Nobre,et al.  Where and When to Pay Attention: The Neural Systems for Directing Attention to Spatial Locations and to Time Intervals as Revealed by Both PET and fMRI , 1998, The Journal of Neuroscience.

[32]  M. Mesulam,et al.  From sensation to cognition. , 1998, Brain : a journal of neurology.

[33]  Activation of Overlapping but not Identical Frontal and Parietal Regions by Saccadic Eye Movement and Overt Spatial Attention Tasks , 1998, NeuroImage.

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

[35]  M Corbetta,et al.  Frontoparietal cortical networks for directing attention and the eye to visual locations: identical, independent, or overlapping neural systems? , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[36]  S. Carlson,et al.  Distribution of cortical activation during visuospatial n-back tasks as revealed by functional magnetic resonance imaging. , 1998, Cerebral cortex.

[37]  D. Gitelman,et al.  Clinical fMRI: Is patient motion really an issue? , 1998, NeuroImage.

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

[39]  D. Gitelman,et al.  The Overlap of Brain Regions that Control Saccades and Covert Visual Spatial Attention Revealed by fMRI. , 1998, NeuroImage.

[40]  G. Rees,et al.  Neural correlates of perceptual rivalry in the human brain. , 1998, Science.

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

[42]  Joel R. Meyer,et al.  A large-scale distributed network for covert spatial attention: further anatomical delineation based on stringent behavioural and cognitive controls. , 1999, Brain : a journal of neurology.

[43]  A. Nobre,et al.  The Large-Scale Neural Network for Spatial Attention Displays Multifunctional Overlap But Differential Asymmetry , 1999, NeuroImage.

[44]  M. Manosevitz High-Speed Scanning in Human Memory , .