Circuitry underlying temporally extended spatial working memory

Extended maintenance delays decrease the accuracy of information stored in spatial working memory. In order to elucidate the network underlying sustained spatial working memory, 16 subjects were scanned using fast event-related fMRI as they performed an oculomotor delayed response task containing trials with "short" (2.5 s) or "long" (10 s) delay periods. Multiple cortical and subcortical regions were common to both delay trial types indicating core task regions. Three patterns of activity were found in a subset of core regions that reflect underlying processes: maintenance-related (e.g., left FEF, right supramarginal gyrus (SMG)), response planning-related (e.g., right FEF, SEF), and motor response-related (e.g., lateral cerebellum (declive)) activation. Several regions were more active during long than short delay trials, including multiple sites in DLPFC (BA 9, 46), indicating a circuitry dynamically recruited to support sustained working memory. Our results suggest that specialized brain processes support extended periods of working memory.

[1]  Jeffrey D. Schall,et al.  Relationship of presaccadic activity in frontal eye field and supplementary eye field to saccade initiation in macaque: Poisson spike train analysis , 2004, Experimental Brain Research.

[2]  T. Klingberg.  Development of a superior frontal–intraparietal network for visuo-spatial working memory , 2006, Neuropsychologia.

[3]  Clayton E Curtis,et al.  Selection and maintenance of saccade goals in the human frontal eye fields. , 2006, Journal of neurophysiology.

[4]  C R Olson,et al.  Object-centered direction selectivity in the macaque supplementary eye field , 1995, Science.

[5]  P. Goldman-Rakic,et al.  Synaptic mechanisms and network dynamics underlying spatial working memory in a cortical network model. , 2000, Cerebral cortex.

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

[7]  M. D’Esposito.  Working memory. , 2008, Handbook of clinical neurology.

[8]  R. Cabeza,et al.  Imaging Cognition II: An Empirical Review of 275 PET and fMRI Studies , 2000, Journal of Cognitive Neuroscience.

[9]  C. Ranganath.  Working memory for visual objects: Complementary roles of inferior temporal, medial temporal, and prefrontal cortex , 2006, Neuroscience.

[10]  B. Gaymard,et al.  The frontal eye field is involved in spatial short-term memory but not in reflexive saccade inhibition , 1999, Experimental Brain Research.

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

[12]  N. Lazar,et al.  Maturation of cognitive processes from late childhood to adulthood. , 2004, Child development.

[13]  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.

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

[15]  R. Leigh,et al.  The neurology of eye movements , 2006 .

[16]  O. Hikosaka,et al.  Functional properties of monkey caudate neurons. III. Activities related to expectation of target and reward. , 1989, Journal of neurophysiology.

[17]  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.

[18]  R. Andersen,et al.  Memory related motor planning activity in posterior parietal cortex of macaque , 1988, Experimental Brain Research.

[19]  J. Schall,et al.  Neuronal activity related to visually guided saccadic eye movements in the supplementary motor area of rhesus monkeys. , 1991, Journal of neurophysiology.

[20]  R. Wurtz,et al.  Saccade-related activity in monkey superior colliculus. I. Characteristics of burst and buildup cells. , 1995, Journal of neurophysiology.

[21]  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.

[22]  P. H. Schiller,et al.  Conditional task-related responses in monkey dorsomedial frontal cortex , 2004, Experimental Brain Research.

[23]  S. Dornič,et al.  Attention and performance V , 1976 .

[24]  B. Postle,et al.  Activity in Human Frontal Cortex Associated with Spatial Working Memory and Saccadic Behavior , 2000, Journal of Cognitive Neuroscience.

[25]  P. Goldman-Rakic,et al.  Neuronal activity related to saccadic eye movements in the monkey's dorsolateral prefrontal cortex. , 1991, Journal of neurophysiology.

[26]  Edward E. Smith,et al.  Neuroimaging studies of working memory: , 2003, Cognitive, affective & behavioral neuroscience.

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

[28]  R. Wurtz,et al.  Visual and oculomotor functions of monkey substantia nigra pars reticulata. III. Memory-contingent visual and saccade responses. , 1983, Journal of neurophysiology.

[29]  O. Hikosaka,et al.  Functional properties of monkey caudate neurons. I. Activities related to saccadic eye movements. , 1989, Journal of neurophysiology.

[30]  P. Pietrini,et al.  Neural correlates of spatial working memory in humans: A functional magnetic resonance imaging study comparing visual and tactile processes , 2006, Neuroscience.

[31]  P. Goldman-Rakic,et al.  Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. , 1989, Journal of neurophysiology.

[32]  Stephen Grossberg,et al.  How laminar frontal cortex and basal ganglia circuits interact to control planned and reactive saccades , 2004, Neural Networks.

[33]  E. Ziegel,et al.  Proceedings in Computational Statistics , 1998 .

[34]  Carol L. Colby,et al.  Spatial working memory in human extrastriate cortex , 2002, Physiology & Behavior.

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

[36]  S. Bunge.  How we use rules to select actions: A review of evidence from cognitive neuroscience , 2004, Cognitive, affective & behavioral neuroscience.

[37]  M. Goldberg,et al.  Visual, presaccadic, and cognitive activation of single neurons in monkey lateral intraparietal area. , 1996, Journal of neurophysiology.

[38]  A. Baddeley,et al.  The selective disruption of spatial working memory by eye movements , 2006, Quarterly journal of experimental psychology.

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

[40]  Jonathan D. Cohen,et al.  Conflict monitoring versus selection-for-action in anterior cingulate cortex , 1999, Nature.

[41]  R. Turner,et al.  Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[42]  Kisou Kubota,et al.  Delay-related activity in the primate prefrontal cortex during sequential reaching tasks with delay , 1993, Neuroscience Research.

[43]  E. J. Tehovnik,et al.  Eye fields in the frontal lobes of primates , 2000, Brain Research Reviews.

[44]  Clayton E. Curtis,et al.  Coherence between fMRI time-series distinguishes two spatial working memory networks , 2005, NeuroImage.

[45]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[46]  P. Goldman-Rakic,et al.  Activation of human prefrontal cortex during spatial and nonspatial working memory tasks measured by functional MRI. , 1996, Cerebral cortex.

[47]  M. Schlag-Rey,et al.  Evidence for a supplementary eye field. , 1987, Journal of neurophysiology.

[48]  R. Passingham,et al.  Active maintenance in prefrontal area 46 creates distractor-resistant memory , 2002, Nature Neuroscience.

[49]  M. Botvinick,et al.  The Contribution of the Anterior Cingulate Cortex to Executive Processes in Cognition , 1999, Reviews in the neurosciences.

[50]  D. Gitelman,et al.  Neuroanatomic Overlap of Working Memory and Spatial Attention Networks: A Functional MRI Comparison within Subjects , 1999, NeuroImage.

[51]  C. Genovese,et al.  Functional Imaging Analysis Software — Computational Olio , 1996 .

[52]  S. Wise,et al.  Neuronal activity in the supplementary eye field during acquisition of conditional oculomotor associations. , 1995, Journal of neurophysiology.

[53]  Sharlene D. Newman,et al.  Frontal and parietal participation in problem solving in the Tower of London: fMRI and computational modeling of planning and high-level perception , 2003, Neuropsychologia.

[54]  Bradley R. Postle,et al.  Distraction-spanning sustained activity during delayed recognition of locations , 2006, NeuroImage.

[55]  Clayton E. Curtis,et al.  Maintenance of Spatial and Motor Codes during Oculomotor Delayed Response Tasks , 2004, The Journal of Neuroscience.

[56]  S. Funahashi,et al.  Delay-period activity in the primate prefrontal cortex encoding multiple spatial positions and their order of presentation , 1997, Behavioural Brain Research.

[57]  A M Dale,et al.  Optimal experimental design for event‐related fMRI , 1999, Human brain mapping.

[58]  B. Douglas Ward,et al.  Deconvolution Analysis of FMRI Time Series Data , 2006 .

[59]  Terrence R Stanford,et al.  Contextual modulation of central thalamic delay-period activity: representation of visual and saccadic goals. , 2004, Journal of neurophysiology.

[60]  A. Hartley,et al.  Locating and fractionating working memory using functional neuroimaging: Storage, maintenance, and executive functions , 2000, Microscopy research and technique.

[61]  P. Strick,et al.  Cerebellar Projections to the Prefrontal Cortex of the Primate , 2001, The Journal of Neuroscience.

[62]  M. Corbetta,et al.  Neural Systems for Visual Orienting and Their Relationships to Spatial Working Memory , 2002, Journal of Cognitive Neuroscience.

[63]  B. Mazoyer,et al.  PET study of the human foveal fixation system , 1999, Human brain mapping.

[64]  Ravi S. Menon,et al.  Comparison of memory- and visually guided saccades using event-related fMRI. , 2004, Journal of neurophysiology.

[65]  P. Strick,et al.  Anatomical evidence for cerebellar and basal ganglia involvement in higher cognitive function. , 1994, Science.

[66]  Katsuyuki Sakai,et al.  The prefrontal cortex and working memory: physiology and brain imaging , 2004, Current Opinion in Neurobiology.

[67]  Ravi S. Menon,et al.  Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

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

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

[70]  M. A. Basso,et al.  Modulation of Neuronal Activity in Superior Colliculus by Changes in Target Probability , 1998, The Journal of Neuroscience.

[71]  G. McCarthy,et al.  The Influence of Memory Load Upon Delay-Interval Activity in a Working-Memory Task: An Event-Related Functional MRI Study , 2000, Journal of Cognitive Neuroscience.

[72]  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..

[73]  D. Heeger,et al.  Topographic organization for delayed saccades in human posterior parietal cortex. , 2005, Journal of neurophysiology.

[74]  Darren R Gitelman,et al.  ILAB: A program for postexperimental eye movement analysis , 2002, Behavior research methods, instruments, & computers : a journal of the Psychonomic Society, Inc.

[75]  Hoi-Chung Leung,et al.  The effect of memory load on cortical activity in the spatial working memory circuit , 2004, Cognitive, affective & behavioral neuroscience.

[76]  Nick Fogt,et al.  The Neurology of Eye Movements, 3rd ed. , 2000 .

[77]  Beatriz Luna,et al.  Brain Basis of Developmental Change in Visuospatial Working Memory , 2006, Journal of Cognitive Neuroscience.

[78]  D. Heeger,et al.  Sustained Activity in Topographic Areas of Human Posterior Parietal Cortex during Memory-Guided Saccades , 2006, The Journal of Neuroscience.

[79]  C. Curtis.  Prefrontal and parietal contributions to spatial working memory , 2006, Neuroscience.

[80]  John A. Sweeney,et al.  Functional magnetic resonance imaging studies of eye movements in first episode schizophrenia: Smooth pursuit, visually guided saccades and the oculomotor delayed response task , 2006, Psychiatry Research: Neuroimaging.

[81]  R. Leigh,et al.  The neurology of eye movements , 1984 .

[82]  J. Fuster.  Prefrontal Cortex , 2018 .

[83]  Leslie G. Ungerleider,et al.  A neural system for human visual working memory. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[84]  S. Zeki,et al.  The neurology of saccades and covert shifts in spatial attention: an event-related fMRI study. , 2000, Brain : a journal of neurology.

[85]  A. Dale,et al.  Selective averaging of rapidly presented individual trials using fMRI , 1997, Human brain mapping.