Functional neuroanatomical double dissociation of mnemonic and executive control processes contributing to working memory performance.

We used event-related functional MRI to investigate the neural bases of two categories of mental processes believed to contribute to performance of an alphabetization working memory task: memory storage and memory manipulation. Our delayed-response tasks required memory for the identity and position-in-the-display of items in two- or five-letter memory sets (to identify load-sensitive regions) or memory for the identity and relative position-in-the-alphabet of items in five-letter memory sets (to identify manipulation-sensitive regions). Results revealed voxels in the left perisylvian cortex of five of five subjects showing load sensitivity (as contrasted with alphabetization-sensitive voxels in this region in only one subject) and voxels of dorsolateral prefrontal cortex in all subjects showing alphabetization sensitivity (as contrasted with load-sensitive voxels in this region in two subjects). This double dissociation was reliable at the group level. These data are consistent with the hypothesis that the nonmnemonic executive control processes that can contribute to working memory function are primarily prefrontal cortex-mediated whereas mnemonic processes necessary for working memory storage are primarily posteriorly mediated. More broadly, they support the view that working memory is a faculty that arises from the coordinated interaction of computationally and neuroanatomically dissociable processes.

[1]  M. Mesulam,et al.  Insula of the old world monkey. III: Efferent cortical output and comments on function , 1982, The Journal of comparative neurology.

[2]  B. Milner,et al.  Deficits on subject-ordered tasks after frontal- and temporal-lobe lesions in man , 1982, Neuropsychologia.

[3]  M. Scarpa,et al.  Language disturbances following vascular lesions restricted to the left basal ganglia, thalamus, and white matter. , 1989 .

[4]  Richard J. Brown.  Neuropsychology Mental Structure , 1989 .

[5]  Dylan M. Jones,et al.  Memory updating in working memory : the role of the central executive , 1990 .

[6]  Adèle,et al.  The Development and Neural Bases of Higher Cognitive Functions. A conference. May 20-24, 1989, Philadelphia, Pa. , 1990, Annals of the New York Academy of Sciences.

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

[8]  M Petrides,et al.  Monitoring of selections of visual stimuli and the primate frontal cortex , 1991, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[9]  Alan C. Evans,et al.  Dissociation of human mid-dorsolateral from posterior dorsolateral frontal cortex in memory processing. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

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

[11]  John G. Seamon,et al.  Double dissociation of spatial and object visual memory: Evidence from selective interference in intact human subjects , 1993, Neuropsychologia.

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

[13]  G. Engel,et al.  Neuropsychology , 1994, Schizophrenia Research.

[14]  R. Knight,et al.  Human prefrontal lesions increase distractibility to irrelevant sensory inputs , 1995, Neuroreport.

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

[16]  Leslie G. Ungerleider.  Functional Brain Imaging Studies of Cortical Mechanisms for Memory , 1995, Science.

[17]  A Ptito,et al.  Visual‐spatial localization by patients with frontallobe lesions invading or sparing area 46 , 1995, Neuroreport.

[18]  M. D’Esposito,et al.  The neural basis of the central executive system of working memory , 1995, Nature.

[19]  M Petrides,et al.  Impairments on nonspatial self-ordered and externally ordered working memory tasks after lesions of the mid-dorsal part of the lateral frontal cortex in the monkey , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[21]  C D Marsden,et al.  Motor reorganization in acquired hemidystonia , 1995, Annals of neurology.

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

[23]  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.

[24]  J. Cacioppo,et al.  Brain imaging and cognitive neuroscience. Toward strong inference in attributing function to structure. , 1996, The American psychologist.

[25]  D. Heeger,et al.  Linear Systems Analysis of Functional Magnetic Resonance Imaging in Human V1 , 1996, The Journal of Neuroscience.

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

[27]  Edward E. Smith,et al.  A Parametric Study of Prefrontal Cortex Involvement in Human Working Memory , 1996, NeuroImage.

[28]  M. D’Esposito,et al.  Empirical Analyses of BOLD fMRI Statistics , 1997, NeuroImage.

[29]  M. D’Esposito,et al.  A Trial-Based Experimental Design for fMRI , 1997, NeuroImage.

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

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

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

[33]  B. McElree,et al.  Attended and Non-Attended States in Working Memory: Accessing Categorized Structures , 1998 .

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

[35]  Hugh Garavan,et al.  Serial attention within working memory , 1998, Memory & cognition.

[36]  I. Kiss,et al.  Central executive function in working memory: event-related brain potential studies. , 1998, Brain research. Cognitive brain research.

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

[38]  M. D’Esposito,et al.  Human Prefrontal Cortex Is Not Specific for Working Memory: A Functional MRI Study , 1998, NeuroImage.

[39]  A. D. Friederici,et al.  Double dissociation of processing temporal and spatial information in working memory , 1998, Neuropsychologia.

[40]  M. D’Esposito,et al.  The Variability of Human, BOLD Hemodynamic Responses , 1998, NeuroImage.

[41]  E E Smith,et al.  Components of verbal working memory: evidence from neuroimaging. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[42]  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.

[43]  M D'Esposito,et al.  The roles of prefrontal brain regions in components of working memory: effects of memory load and individual differences. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[44]  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.

[45]  P. B. Cipolloni,et al.  Cortical connections of the frontoparietal opercular areas in the Rhesus monkey , 1999, The Journal of comparative neurology.

[46]  M. D’Esposito,et al.  Temporal isolation of the neural correlates of spatial mnemonic processing with fMRI. , 1999, Brain research. Cognitive brain research.

[47]  A. Miyake,et al.  Models of Working Memory: Mechanisms of Active Maintenance and Executive Control , 1999 .

[48]  N. J. Herrod,et al.  Redefining the functional organization of working memory processes within human lateral prefrontal cortex , 1999, The European journal of neuroscience.

[49]  J. Jonides,et al.  Storage and executive processes in the frontal lobes. , 1999, Science.

[50]  E Zarahn,et al.  Event-related functional MRI: implications for cognitive psychology. , 1999, Psychological bulletin.