Maintenance versus manipulation in verbal working memory revisited: an fMRI study

Working memory (WM) is the ability to keep a limited amount of information "on line" for immediate use during short intervals. Verbal WM has been hypothesized to consist of neuroanatomically segregated components, i.e., maintenance (storage, rehearsal, and matching) and manipulation (reordering or updating), corresponding to ventrolateral and dorsolateral prefrontal cortex. Previous imaging studies of maintenance vs manipulation processes in WM have produced inconsistent results, which may have been due to methodological issues such as low statistical power and the use of insertion (subtraction) designs. In the present functional magnetic resonance imaging study we used parametric versions of both a prototypical maintenance task (Sternberg) and a prototypical manipulation task (n-letter back task) in 21 healthy subjects. Increased signal correlated with load common for both tasks was found in bilateral dorsolateral and anterior prefrontal, left ventrolateral prefrontal, and bilateral parietal regions. Workload x task interactions were found in bilateral dorsolateral prefrontal cortex for manipulation vs maintenance, but also for responding vs encoding (storage) in the maintenance task. Therefore, our data support a functional rather than a neuroanatomical distinction between maintenance and manipulation, given our finding that these tasks differentially activate virtually identical systems.

[1]  M. Petrides,et al.  Functional organization of spatial and nonspatial working memory processing within the human lateral frontal cortex. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

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

[3]  Jonathan D. Cohen,et al.  Working Memory for Letters, Shapes, and Locations: fMRI Evidence against Stimulus-Based Regional Organization in Human Prefrontal Cortex , 2000, NeuroImage.

[4]  B. Postle,et al.  Maintenance versus Manipulation of Information Held in Working Memory: An Event-Related fMRI Study , 1999, Brain and Cognition.

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

[6]  D. Schacter,et al.  Prefrontal Contributions to Executive Control: fMRI Evidence for Functional Distinctions within Lateral Prefrontal Cortex , 2001, NeuroImage.

[8]  R. Coppola,et al.  Specific versus Nonspecific Brain Activity in a Parametric N-Back Task , 2000, NeuroImage.

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

[10]  B. Postle,et al.  An fMRI Investigation of Cortical Contributions to Spatial and Nonspatial Visual Working Memory , 2000, NeuroImage.

[11]  C. Stern,et al.  Medial temporal and prefrontal contributions to working memory tasks with novel and familiar stimuli , 2001, Hippocampus.

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

[13]  T. Braver,et al.  The Role of Frontopolar Cortex in Subgoal Processing during Working Memory , 2002, NeuroImage.

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

[15]  S. C. Strother,et al.  Are brain functions really additive? , 1996, NeuroImage.

[16]  A Baddeley,et al.  The fractionation of working memory. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[17]  Edward T. Bullmore,et al.  Prolonged Reaction Time to a Verbal Working Memory Task Predicts Increased Power of Posterior Parietal Cortical Activation , 2000, NeuroImage.

[18]  R. Passingham,et al.  The prefrontal cortex: response selection or maintenance within working memory? , 2000, 5th IEEE EMBS International Summer School on Biomedical Imaging, 2002..

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

[20]  P. Goldman-Rakic,et al.  Segregation of working memory functions within the dorsolateral prefrontal cortex , 2000, Experimental Brain Research.

[21]  Jerwen Jou The magic number four: Can it explain Sternberg's serial memory scan data? , 2001, Behavioral and Brain Sciences.

[22]  P. Goldman-Rakic,et al.  Localization of Function All Over Again , 2000, NeuroImage.

[23]  R. Henson,et al.  Frontal lobes and human memory: insights from functional neuroimaging. , 2001, Brain : a journal of neurology.

[24]  N. Cowan The magical number 4 in short-term memory: A reconsideration of mental storage capacity , 2001, Behavioral and Brain Sciences.

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

[26]  M. Petrides,et al.  Specialized systems for the processing of mnemonic information within the primate frontal cortex. , 1996, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[27]  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.

[28]  Earl K. Miller,et al.  The Prefrontal Cortex: No Simple Matter , 2000, NeuroImage.

[29]  Karl J. Friston,et al.  The Trouble with Cognitive Subtraction , 1996, NeuroImage.

[30]  Leslie G. Ungerleider,et al.  Distinguishing the Functional Roles of Multiple Regions in Distributed Neural Systems for Visual Working Memory , 2000, NeuroImage.

[31]  M. Inase,et al.  Neuroanatomical discrimination between manipulating and maintaining processes involved in verbal working memory; a functional MRI study. , 2001, Brain research. Cognitive brain research.

[32]  C. Degueldre,et al.  Regional brain activity during tasks devoted to the central executive of working memory. , 1999, Brain research. Cognitive brain research.

[33]  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 .

[34]  Bruce R. Rosen,et al.  Activity in Ventrolateral and Mid-Dorsolateral Prefrontal Cortex during Nonspatial Visual Working Memory Processing: Evidence from Functional Magnetic Resonance Imaging , 2000, NeuroImage.

[35]  B. Postle,et al.  Functional neuroanatomical double dissociation of mnemonic and executive control processes contributing to working memory performance. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[36]  J. Fuster Prefrontal Cortex , 2018 .