Damage to the Fronto-Polar Cortex Is Associated with Impaired Multitasking

Background A major question in understanding the functional organization of the brain is to delineate the functional divisions of the prefrontal cortex. Of particular importance to the cognitive capacities that are uniquely human is the fronto-polar cortex (Brodmann's area 10), which is disproportionally larger in humans relative to the rest of the brain than it is in the ape's brain. The specific function of this brain region remains poorly understood, but recent neuroimaging studies have proposed that it may hold goals in mind while exploring and processing secondary goals. Principal Findings Here we show that the extent of damage to the fronto-polar cortex predicts impairment in the management of multiple goals. This result reveals that the integrity of the fronto-polar cortex is necessary to perform tasks that require subjects to maintain a primary goal in mind while processing secondary goals, an ability which is crucial for complex human cognitive abilities. Conclusion/Significance These results provide important new insights concerning the cerebral basis of complex human cognition such as planning and multitasking.

[1]  J. Desmond,et al.  Neural Substrates of Fluid Reasoning: An fMRI Study of Neocortical Activation during Performance of the Raven's Progressive Matrices Test , 1997, Cognitive Psychology.

[2]  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.

[3]  D. Yves von Cramon,et al.  The functional neuroanatomy of human working memory revisited Evidence from 3-T fMRI studies using classical domain-specific interference tasks , 2003, NeuroImage.

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

[5]  C. Curtis,et al.  Success and Failure Suppressing Reflexive Behavior , 2003, Journal of Cognitive Neuroscience.

[6]  D. Pandya,et al.  Efferent Association Pathways from the Rostral Prefrontal Cortex in the Macaque Monkey , 2007, The Journal of Neuroscience.

[7]  M. Petrides Lateral prefrontal cortex: architectonic and functional organization , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[8]  Joseph B. Sala,et al.  Binding of What and Where During Working Memory Maintenance , 2007, Cortex.

[9]  E. Koechlin,et al.  The Architecture of Cognitive Control in the Human Prefrontal Cortex , 2003, Science.

[10]  R. Poldrack,et al.  Recovering Meaning Left Prefrontal Cortex Guides Controlled Semantic Retrieval , 2001, Neuron.

[11]  R. Cabeza,et al.  Handbook of functional neuroimaging of cognition , 2001 .

[12]  J J Pekar,et al.  Dissociation of the neural systems for working memory maintenance of verbal and nonspatial visual information , 2001, Cognitive, affective & behavioral neuroscience.

[13]  C. Summerfield,et al.  An information theoretical approach to prefrontal executive function , 2007, Trends in Cognitive Sciences.

[14]  Jonathan D. Cohen,et al.  Anterior Cingulate Conflict Monitoring and Adjustments in Control , 2004, Science.

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

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

[17]  M. Walton,et al.  Action sets and decisions in the medial frontal cortex , 2004, Trends in Cognitive Sciences.

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

[19]  S. Scott,et al.  The role of the rostral frontal cortex (area 10) in prospective memory: a lateral versus medial dissociation , 2003, Neuropsychologia.

[20]  Vinod Menon,et al.  Temporal dynamics of basal ganglia response and connectivity during verbal working memory , 2007, NeuroImage.

[21]  J. Gabrieli,et al.  The frontopolar cortex and human cognition: Evidence for a rostrocaudal hierarchical organization within the human prefrontal cortex , 2000, Psychobiology.

[22]  P. Dayan,et al.  Cortical substrates for exploratory decisions in humans , 2006, Nature.

[23]  A. Owen,et al.  Anterior prefrontal cortex: insights into function from anatomy and neuroimaging , 2004, Nature Reviews Neuroscience.

[24]  K. Amunts,et al.  Neural correlates of dual task interference can be dissociated from those of divided attention: an fMRI study. , 2001, Cerebral cortex.

[25]  E Tulving,et al.  Neuroanatomical correlates of retrieval in episodic memory: auditory sentence recognition. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[26]  V Menon,et al.  Modality effects in verbal working memory: differential prefrontal and parietal responses to auditory and visual stimuli , 2004, NeuroImage.

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

[28]  H. Damasio,et al.  Humans and great apes share a large frontal cortex , 2002, Nature Neuroscience.

[29]  T. Shallice,et al.  The cognitive and neuroanatomical correlates of multitasking , 2000, Neuropsychologia.

[30]  J. Desmond,et al.  Functional Specialization for Semantic and Phonological Processing in the Left Inferior Prefrontal Cortex , 1999, NeuroImage.

[31]  Edward E. Smith,et al.  PET Evidence for an Amodal Verbal Working Memory System , 1996, NeuroImage.

[32]  Noah A. Shamosh,et al.  Frontopolar cortex mediates abstract integration in analogy , 2006, Brain Research.

[33]  John J. Foxe,et al.  Jumping the gun: is effective preparation contingent upon anticipatory activation in task-relevant neural circuitry? , 2006, Cerebral cortex.

[34]  Jordan Grafman,et al.  The Roles of Timing and Task Order during Task Switching , 2002, NeuroImage.

[35]  S. Courtney,et al.  Attention and cognitive control as emergent properties of information representation in working memory , 2004, Cognitive, affective & behavioral neuroscience.

[36]  Leslie G. Ungerleider,et al.  Object and spatial visual working memory activate separate neural systems in human cortex. , 1996, Cerebral cortex.

[37]  D. V. von Cramon,et al.  Localization of Executive Functions in Dual-Task Performance with fMRI , 2002, Journal of Cognitive Neuroscience.

[38]  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.

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

[40]  Adrian Danek,et al.  Quantification of brain lesions using interactive automated software , 2002, Behavior research methods, instruments, & computers : a journal of the Psychonomic Society, Inc.

[41]  G. V. Van Hoesen,et al.  Prefrontal cortex in humans and apes: a comparative study of area 10. , 2001, American journal of physical anthropology.

[42]  J. Fiez,et al.  Functional Magnetic Resonance Imaging (fmri) Was Used to Investigate the Neural Substrates of Component Processes in Verbal Working Memory. Based on Behavioral Research Using , 2022 .

[43]  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.

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

[45]  Alan C. Evans,et al.  Functional activation of the human frontal cortex during the performance of verbal working memory tasks. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[46]  R. Passingham,et al.  Prefrontal interactions reflect future task operations , 2003, Nature Neuroscience.

[47]  E Zarahn,et al.  Replication and further studies of neural mechanisms of spatial mnemonic processing in humans. , 2000, Brain research. Cognitive brain research.

[48]  Russell A. Poldrack,et al.  What Can Neuroimaging Tell Us About the Mind? , 2004 .

[49]  Tom Schoenemann From Monkey Brain to Human Brain: A Fyssen Foundation Symposium , 2006 .

[50]  R. Poldrack,et al.  Dissociable Controlled Retrieval and Generalized Selection Mechanisms in Ventrolateral Prefrontal Cortex , 2005, Neuron.

[51]  John D E Gabrieli,et al.  Evaluating self-generated information: anterior prefrontal contributions to human cognition. , 2003, Behavioral neuroscience.

[52]  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.

[53]  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..

[54]  J. Grafman,et al.  Human prefrontal cortex: processing and representational perspectives , 2003, Nature Reviews Neuroscience.

[55]  Joseph B. Sala,et al.  Dissociable functional cortical topographies for working memory maintenance of voice identity and location. , 2004, Cerebral cortex.

[56]  Andreas Bartels,et al.  fMRI and its interpretations: an illustration on directional selectivity in area V5/MT , 2008, Trends in Neurosciences.

[57]  James K. Kroger,et al.  Rostrolateral Prefrontal Cortex Involvement in Relational Integration during Reasoning , 2001, NeuroImage.

[58]  K. Jellinger Principles of frontal lobe function , 2003 .

[59]  M. Brass,et al.  The role of the frontal cortex in task preparation. , 2002, Cerebral cortex.

[60]  M. Rushworth,et al.  Behavioral / Systems / Cognitive Connectivity-Based Parcellation of Human Cingulate Cortex and Its Relation to Functional Specialization , 2008 .

[61]  Joseph B. Sala,et al.  Functional topography of a distributed neural system for spatial and nonspatial information maintenance in working memory , 2003, Neuropsychologia.

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

[63]  Leslie G. Ungerleider,et al.  The role of prefrontal cortex in working memory: examining the contents of consciousness. , 1998, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[64]  C. Frith,et al.  Brain regions involved in prospective memory as determined by positron emission tomography , 2001, Neuropsychologia.

[65]  Timothy Edward John Behrens,et al.  Changes in connectivity profiles define functionally distinct regions in human medial frontal cortex. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[66]  J. D. E. Gabrieli,et al.  Integration of diverse information in working memory within the frontal lobe , 2000, Nature Neuroscience.

[67]  Randy L Buckner,et al.  Functional–Anatomic Correlates of Control Processes in Memory , 2003, The Journal of Neuroscience.

[68]  K. Hikosaka,et al.  Domain‐related differentiation of working memory in the Japanese macaque (Macaca fuscata) frontal cortex: a positron emission tomography study , 2007, The European journal of neuroscience.

[69]  M. D’Esposito,et al.  The neural effect of stimulus-response modality compatibility on dual-task performance: an fMRI study , 2006, Psychological research.

[70]  J. Fiez,et al.  Functional heterogeneity within Broca's area during verbal working memory , 2002, Physiology & Behavior.

[71]  W. Singer,et al.  Distributed cortical systems in visual short-term memory revealed by event-related functional magnetic resonance imaging. , 2002, Cerebral cortex.

[72]  J B Poline,et al.  The neural system that bridges reward and cognition in humans: An fMRI study , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[73]  Timothy Edward John Behrens,et al.  Triangulating a Cognitive Control Network Using Diffusion-Weighted Magnetic Resonance Imaging (MRI) and Functional MRI , 2007, The Journal of Neuroscience.

[74]  A. Wagner,et al.  Domain-general and domain-sensitive prefrontal mechanisms for recollecting events and detecting novelty. , 2005, Cerebral cortex.

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

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

[77]  R L Buckner,et al.  Functional neuroimaging studies of encoding, priming, and explicit memory retrieval. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[78]  J. Grafman,et al.  Dissociating the roles of the rostral anterior cingulate and the lateral prefrontal cortices in performing two tasks simultaneously or successively. , 2003, Cerebral cortex.

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

[80]  E. Koechlin,et al.  The role of the anterior prefrontal cortex in human cognition , 1999, Nature.

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

[82]  E. Tulving,et al.  Task-related and item-related brain processes of memory retrieval. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[83]  E. Koechlin,et al.  Medial Prefrontal and Subcortical Mechanisms Underlying the Acquisition of Motor and Cognitive Action Sequences in Humans , 2002, Neuron.

[84]  K. Berman,et al.  Fractionating the neural substrate of cognitive control processes , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[85]  Emmanuel Dupoux,et al.  Expe: An expandable programming language for on-line psychological experiments , 1997 .

[86]  S E Petersen,et al.  A positron emission tomography study of the short-term maintenance of verbal information , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[87]  David Badre,et al.  Functional Magnetic Resonance Imaging Evidence for a Hierarchical Organization of the Prefrontal Cortex , 2007, Journal of Cognitive Neuroscience.

[88]  J. Desmond,et al.  Lobular Patterns of Cerebellar Activation in Verbal Working-Memory and Finger-Tapping Tasks as Revealed by Functional MRI , 1997, The Journal of Neuroscience.