Working Memory for Location and Time: Activity in Prefrontal Area 46 Relates to Selection Rather than Maintenance in Memory

The role of the dorsal prefrontal cortex in working memory remains controversial. Influential proposals include a role in the maintenance of domain-specific information, and the processes of executive functions on remembered information. We used event-related functional magnetic resonance imaging to demonstrate a functional dissociation within prefrontal cortex in terms of the components of complex working memory tasks. The maintenance in working memory of spatial locations and their temporal order was associated with activation of area 8 and intraparietal cortex. In contrast, the selection of one location, according to its order, was associated with a distinct frontoparietal network, including dorsolateral prefrontal area 46, ventrolateral prefrontal cortex and anterior cingulate cortex and medial parietal cortex. The different contributions of these areas to selection are considered in the light of recent electrophysiological and lesion studies. We suggest a general role of the dorsolateral prefrontal area 46 in attentional selection, including selection from within working memory.

[1]  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.

[2]  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.

[3]  R. Knight,et al.  Prefrontal–cingulate interactions in action monitoring , 2000, Nature Neuroscience.

[4]  P. Goldman-Rakic The prefrontal landscape: implications of functional architecture for understanding human mentation and the central executive. , 1996, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[5]  Karl J. Friston,et al.  How Many Subjects Constitute a Study? , 1999, NeuroImage.

[6]  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.

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

[8]  J. Cohen,et al.  Dissociating the role of the dorsolateral prefrontal and anterior cingulate cortex in cognitive control. , 2000, Science.

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

[10]  Edward E. Smith,et al.  Spatial working memory in humans as revealed by PET , 1993, Nature.

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

[12]  D. Pandya,et al.  Dorsolateral prefrontal cortex: comparative cytoarchitectonic analysis in the human and the macaque brain and corticocortical connection patterns , 1999, The European journal of neuroscience.

[13]  B. Postle,et al.  Prefrontal cortical contributions to working memory: evidence from event-related fMRI studies , 2000, Experimental Brain Research.

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

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

[16]  H. Niki Differential activity of prefrontal units during right and left delayed response trials. , 1974, Brain research.

[17]  L. Goldstein The frontal lobes and voluntary action , 1996 .

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

[19]  N Butters,et al.  Behavioral deficits in monkeys after selective lesions within the middle third of sulcus principalis. , 1971, Journal of comparative and physiological psychology.

[20]  Y. Miyashita,et al.  Top-down signal from prefrontal cortex in executive control of memory retrieval , 1999, Nature.

[21]  Goldman-Rakic Ps,et al.  Motor control function of the prefrontal cortex. , 1987 .

[22]  Edward E. Smith,et al.  A parametric study of prefrontal cortex involvement in human working memory , 1996, NeuroImage.

[23]  E. DeYoe,et al.  A physiological correlate of the 'spotlight' of visual attention , 1999, Nature Neuroscience.

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

[25]  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.

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

[27]  M. Petrides Comparative architectonic analysis of the human and the macaque frontal cortex , 1994 .

[28]  Karl J. Friston,et al.  Detecting Activations in PET and fMRI: Levels of Inference and Power , 1996, NeuroImage.

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

[30]  T. Sawaguchi,et al.  Properties of delay-period neuronal activity in the monkey dorsolateral prefrontal cortex during a spatial delayed matching-to-sample task. , 1999, Journal of neurophysiology.

[31]  D. Gitelman,et al.  Covert Visual Spatial Orienting and Saccades: Overlapping Neural Systems , 2000, NeuroImage.

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

[33]  Shozo Kojima,et al.  Functional analysis of spatially discriminative neurons in prefrontal cortex of rhesus monkey , 1984, Brain Research.

[34]  Jordan Grafman,et al.  Handbook of Neuropsychology , 1991 .

[35]  M. Farah,et al.  A functional MRI study of mental image generation , 1997, Neuropsychologia.

[36]  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..

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

[38]  R. Desimone,et al.  Neural mechanisms of selective visual attention. , 1995, Annual review of neuroscience.

[39]  P. Goldman-Rakic,et al.  Prefrontal neuronal activity in rhesus monkeys performing a delayed anti-saccade task , 1993, Nature.

[40]  Jonathan D. Cohen,et al.  Anterior cingulate and prefrontal cortex: who's in control? , 2000, Nature Neuroscience.

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

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

[43]  R. Dolan,et al.  Neural systems engaged by planning: a PET study of the Tower of London task , 1996, Neuropsychologia.

[44]  M. Mintun,et al.  Positron emission tomography study of voluntary saccadic eye movements and spatial working memory. , 1996, Journal of neurophysiology.

[45]  G. E. Alexander,et al.  Neuron Activity Related to Short-Term Memory , 1971, Science.

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

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

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

[49]  M. D’Esposito,et al.  Isolating the neural mechanisms of age-related changes in human working memory , 2000, Nature Neuroscience.

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

[51]  Richard S. J. Frackowiak,et al.  The Mind's Eye—Precuneus Activation in Memory-Related Imagery , 1995, NeuroImage.

[52]  J. Cohen,et al.  Context, cortex, and dopamine: a connectionist approach to behavior and biology in schizophrenia. , 1992, Psychological review.

[53]  B R Postle,et al.  "What"-Then-Where" in visual working memory: an event-related fMRI study. , 1999, Journal of cognitive neuroscience.

[54]  Irene P. Kan,et al.  Verb generation in patients with focal frontal lesions: a neuropsychological test of neuroimaging findings. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[55]  M. Farah,et al.  Role of left inferior prefrontal cortex in retrieval of semantic knowledge: a reevaluation. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[56]  Karl J. Friston,et al.  The physiological basis of attentional modulation in extrastriate visual areas , 1999, Nature Neuroscience.

[57]  J V Haxby,et al.  Dissociation of saccade-related and pursuit-related activation in human frontal eye fields as revealed by fMRI. , 1997, Journal of neurophysiology.

[58]  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.

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

[60]  E. Miller,et al.  The Prefrontal Cortex Complex Neural Properties for Complex Behavior , 1999, Neuron.

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

[62]  Karl J. Friston,et al.  Subtractions, conjunctions, and interactions in experimental design of activation studies , 1997, Human brain mapping.

[63]  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.

[64]  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.

[65]  K Friston,et al.  Signal-, set- and movement-related activity in the human brain: an event-related fMRI study. , 1999, Cerebral cortex.

[66]  Bradley R Postle,et al.  The dependence of span and delayed-response performance on prefrontal cortex , 1999, Neuropsychologia.

[67]  R. Desimone Visual attention mediated by biased competition in extrastriate visual cortex. , 1998, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

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

[69]  T. Robbins,et al.  The prefrontal cortex: Executive and cognitive functions. , 1998 .

[70]  Richard S. J. Frackowiak,et al.  Two Modulatory Effects of Attention That Mediate Object Categorization in Human Cortex , 1997, Science.

[71]  P. Goldman-Rakic,et al.  Matching patterns of activity in primate prefrontal area 8a and parietal area 7ip neurons during a spatial working memory task. , 1998, Journal of neurophysiology.

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

[73]  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 .

[74]  B. J. McCurtain,et al.  Dorsal cortical regions subserving visually guided saccades in humans: an fMRI study. , 1998, Cerebral cortex.