Hemispheric specialization of the lateral prefrontal cortex for strategic processing during spatial and shape working memory

OBJECTIVE We investigated whether spatial working memory (WM) is associated with functional specialization of the right prefrontal cortex (PFC) relative to WM for shapes. We designed spatial and shape WM tasks that are relatively easy to perform and that minimize both task-switching and manipulation demands. The tasks use identical stimuli and require the same motor response. METHODS We presented 12 subjects with target shapes that appeared in particular locations. Subjects maintained either the location or the shape of the targets in WM and responded to each probe by indicating whether it was a target. During a non-WM control task, subjects indicated whether the probe appeared on the right or left side of the screen. Subjects were scanned with a 3.0 T Siemens scanner and data were analyzed using SPM99. The WM tasks were compared to identify PFC activation that was different for spatial versus shape WM. Each WM task was also compared to the control task. RESULTS compared with shape WM, spatial WM performance was faster and more accurate and was associated with increased right ventrolateral and frontopolar PFC activation. In contrast, compared to spatial WM, shape WM was associated with increased left ventrolateral PFC activity. CONCLUSIONS These findings demonstrate hemispheric specialization for spatial versus shape WM in the ventrolateral PFC. The increased activity in the right PFC for spatial WM cannot be attributed to increased task difficulty, the stimuli used, or the response requirements. Rather, we propose that differences in performance and activation reflect the use of configural processing strategies for spatial WM.

[1]  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.

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

[3]  Z Kourtzi,et al.  Representation of Perceived Object Shape by the Human Lateral Occipital Complex , 2001, Science.

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

[5]  F ATTNEAVE,et al.  The quantitative study of shape and pattern perception. , 1956, Psychological bulletin.

[6]  G. Mandler,et al.  Subitizing: an analysis of its component processes. , 1982, Journal of experimental psychology. General.

[7]  A. Dove,et al.  Prefrontal cortex activation in task switching: an event-related fMRI study. , 2000, Brain research. Cognitive brain research.

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

[9]  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.

[10]  M. D’Esposito,et al.  The Influence of Working-Memory Demand and Subject Performance on Prefrontal Cortical Activity , 2002, Journal of Cognitive Neuroscience.

[11]  P. Goldman-Rakic,et al.  Sustained Mnemonic Response in the Human Middle Frontal Gyrus during On-Line Storage of Spatial Memoranda , 2002, Journal of Cognitive Neuroscience.

[12]  Douglas N Greve,et al.  Identifying regional activity associated with temporally separated components of working memory using event-related functional MRI , 2003, NeuroImage.

[13]  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.

[14]  John R. Anderson,et al.  The role of prefrontal cortex and posterior parietal cortex in task switching. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

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

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

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

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

[19]  J. Duncan,et al.  Encoding Strategies Dissociate Prefrontal Activity from Working Memory Demand , 2003, Neuron.

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

[21]  B. Postle,et al.  Using event-related fMRI to assess delay-period activity during performance of spatial and nonspatial working memory tasks. , 2000, Brain research. Brain research protocols.

[22]  S C Rao,et al.  Integration of what and where in the primate prefrontal cortex. , 1997, Science.

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

[24]  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.

[25]  M. Petrides Dissociable Roles of Mid-Dorsolateral Prefrontal and Anterior Inferotemporal Cortex in Visual Working Memory , 2000, The Journal of Neuroscience.

[27]  O. Spreen,et al.  Predicting premorbid IQ: A revision of the national adult reading test , 1989 .

[28]  M. D’Esposito,et al.  Modulation of task-related neural activity in task-switching: an fMRI study. , 2000, Brain research. Cognitive brain research.

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

[30]  E. Tulving,et al.  PET studies of encoding and retrieval: The HERA model , 1996, Psychonomic bulletin & review.

[31]  J. Duncan,et al.  Common regions of the human frontal lobe recruited by diverse cognitive demands , 2000, Trends in Neurosciences.

[32]  Z. Pylyshyn,et al.  What enumeration studies can show us about spatial attention: evidence for limited capacity preattentive processing. , 1993, Journal of experimental psychology. Human perception and performance.

[33]  Erik D. Reichle,et al.  From the Selectedworks of Marcel Adam Just Working Memory and Executive Function: Evidence from Neuroimaging Classic Issues Neuroimaging Results Working Memory and Executive Function: Evidence from Neuroimaging Reconstruals Suggested by the Neuroimaging Data Collaboration and Redundancy , 2022 .

[34]  David J. Freedman,et al.  Neural correlates of categories and concepts , 2003, Current Opinion in Neurobiology.

[35]  P S Goldman-Rakic,et al.  Association of Storage and Processing Functions in the Dorsolateral Prefrontal Cortex of the Nonhuman Primate , 1999, The Journal of Neuroscience.

[36]  S Monsell,et al.  Reconfiguration of task-set: Is it easier to switch to the weaker task? , 2000, Psychological research.

[37]  M. Petrides,et al.  Functional Organization of the Human Frontal Cortex for Mnemonic Processing. , 1995, Annals of the New York Academy of Sciences.

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

[39]  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..

[40]  J M VANDERPLAS,et al.  The association value of random shapes. , 1959, Journal of experimental psychology.

[41]  A. Owen The Functional Organization of Working Memory Processes Within Human Lateral Frontal Cortex: The Contribution of Functional Neuroimaging , 1997, The European journal of neuroscience.

[42]  R. Ashton,et al.  Handedness assessment inventory , 1976, Neuropsychologia.

[43]  James B. Rowe,et al.  Working Memory for Location and Time: Activity in Prefrontal Area 46 Relates to Selection Rather than Maintenance in Memory , 2001, NeuroImage.

[44]  Yungtai Lo,et al.  Spatial and object working memory impairments in schizophrenia patients: a Bayesian item-response theory analysis. , 2002, Journal of abnormal psychology.