Functional Specialization within Rostral Prefrontal Cortex (Area 10): A Meta-analysis

One of the least well understood regions of the human brain is rostral prefrontal cortex, approximating Brodmann's area 10. Here, we investigate the possibility that there are functional subdivisions within this region by conducting a meta-analysis of 104 functional neuroimaging studies (using positron emission tomography/functional magnetic resonance imaging). Studies involving working memory and episodic memory retrieval were disproportionately associated with lateral activations, whereas studies involving mentalizing (i.e., attending to one's own emotions and mental states or those of other agents) were disproportionately associated with medial activations. Functional variation was also observed along a rostral-caudal axis, with studies involving mentalizing yielding relatively caudal activations and studies involving multiple-task coordination yielding relatively rostral activations. A classification algorithm was trained to predict the task, given the coordinates of each activation peak. Performance was well above chance levels (74% for the three most common tasks; 45% across all eight tasks investigated) and generalized to data not included in the training set. These results point to considerable functional segregation within rostral prefrontal cortex.

[1]  M. E. Raichle,et al.  Right Anterior Prefrontal Cortex Activation during Semantic Monitoring and Working Memory , 1998, NeuroImage.

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

[3]  G. Shulman,et al.  Medial prefrontal cortex and self-referential mental activity: Relation to a default mode of brain function , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[4]  Jesper Andersson,et al.  Valid conjunction inference with the minimum statistic , 2005, NeuroImage.

[5]  Tor D Wager,et al.  Neuroimaging studies of shifting attention: a meta-analysis , 2004, NeuroImage.

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

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

[8]  Karl J. Friston,et al.  Conjunction revisited , 2005, NeuroImage.

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

[10]  P. Goldman-Rakic,et al.  Direct and indirect pathways from the amygdala to the frontal lobe in rhesus monkeys , 1981, The Journal of comparative neurology.

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

[12]  G. Fink In search of one's own past: the neural bases of autobiographical memories. , 2003, Brain : a journal of neurology.

[13]  Paul L. Harris,et al.  From Simulation to Folk Psychology: The Case for Development , 1992 .

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

[15]  Marcia K. Johnson,et al.  The role of prefrontal cortex during tests of episodic memory , 1998, Trends in Cognitive Sciences.

[16]  J. Csernansky,et al.  A proposal for MRI-based parcellation of the frontal pole , 2007, Brain Structure and Function.

[17]  B. Kopp,et al.  Kognitive Hirnleistungen des präfrontalen Kortex , 2007, Der Nervenarzt.

[18]  C. Frith,et al.  Functional imaging of ‘theory of mind’ , 2003, Trends in Cognitive Sciences.

[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]  C. N. Macrae,et al.  Finding the Self? An Event-Related fMRI Study , 2002, Journal of Cognitive Neuroscience.

[21]  Adrian M Owen,et al.  Distinct roles for lateral and medial anterior prefrontal cortex in contextual recollection. , 2005, Journal of neurophysiology.

[22]  C. Frith,et al.  Development and neurophysiology of mentalizing. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[23]  J. Price,et al.  Architectonic subdivision of the human orbital and medial prefrontal cortex , 2003, The Journal of comparative neurology.

[24]  Masatoshi Itoh,et al.  Thinking of the future and past: the roles of the frontal pole and the medial temporal lobes , 2003, NeuroImage.

[25]  Marc Leman,et al.  The Cortical Topography of Tonal Structures Underlying Western Music , 2002, Science.

[26]  Justin L. Vincent,et al.  Distinct brain networks for adaptive and stable task control in humans , 2007, Proceedings of the National Academy of Sciences.

[27]  E. Phelps,et al.  Social learning of fear , 2007, Nature Neuroscience.

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

[29]  P. McLeod,et al.  Measuring the mind speed, control, and age , 2005 .

[30]  Jordan Grafman,et al.  Event frequency modulates the processing of daily life activities in human medial prefrontal cortex. , 2007, Cerebral cortex.

[31]  J. Duncan An adaptive coding model of neural function in prefrontal cortex , 2001 .

[32]  E. Rolls,et al.  The functional neuroanatomy of the human orbitofrontal cortex: evidence from neuroimaging and neuropsychology , 2004, Progress in Neurobiology.

[33]  Iroise Dumontheil,et al.  The gateway hypothesis of rostral prefrontal cortex (area 10) function , 2007, Trends in Cognitive Sciences.

[34]  J. D Steele,et al.  Segregation of cognitive and emotional function in the prefrontal cortex: a stereotactic meta-analysis , 2004, NeuroImage.

[35]  G. Winocur,et al.  In Search of the Self: A Positron Emission Tomography Study , 1999 .

[36]  G. Fink,et al.  Neural activation during selective attention to subjective emotional responses , 1997, Neuroreport.

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

[38]  C. Frith,et al.  Performance-related activity in medial rostral prefrontal cortex (area 10) during low-demand tasks. , 2006, Journal of experimental psychology. Human perception and performance.

[40]  W. Prinz,et al.  Disorders of volition , 2006 .

[41]  C. Frith,et al.  Involvement of rostral prefrontal cortex in selection between stimulus‐oriented and stimulus‐independent thought , 2005, The European journal of neuroscience.

[42]  T. Shallice,et al.  The functional roles of prefrontal cortex in episodic memory. I. Encoding. , 1998, Brain : a journal of neurology.

[43]  Stefan Pollmann,et al.  Anterior prefrontal cortex contributions to attention control. , 2004, Experimental psychology.

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

[45]  A. Friederici Towards a neural basis of auditory sentence processing , 2002, Trends in Cognitive Sciences.

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

[47]  Jiro Okuda,et al.  Rostral prefrontal brain regions (area 10): A gateway between inner thought and the external world? , 2005 .

[48]  Beate Sodian,et al.  Neural correlates of true and false belief reasoning , 2007, NeuroImage.

[49]  J. Price,et al.  Architectonic subdivision of the orbital and medial prefrontal cortex in the macaque monkey , 1994, The Journal of comparative neurology.

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

[51]  J. Lancaster,et al.  Using the talairach atlas with the MNI template , 2001, NeuroImage.

[52]  C. Frith,et al.  Interacting minds--a biological basis. , 1999, Science.

[53]  C. Frith,et al.  Comment on "Wandering Minds: The Default Network and Stimulus-Independent Thought" , 2007, Science.

[54]  C. Frith,et al.  Differential involvement of regions of rostral prefrontal cortex (Brodmann area 10) in time- and event-based prospective memory. , 2007, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[55]  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 .

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

[57]  A. Damasio,et al.  Subcortical and cortical brain activity during the feeling of self-generated emotions , 2000, Nature Neuroscience.

[58]  Todd B. Parrish,et al.  The posterior cingulate and medial prefrontal cortex mediate the anticipatory allocation of spatial attention , 2003, NeuroImage.

[59]  M. Posner,et al.  Cognitive and emotional influences in anterior cingulate cortex , 2000, Trends in Cognitive Sciences.

[60]  C. Rorden,et al.  Stereotaxic display of brain lesions. , 2000, Behavioural neurology.

[61]  G. Glover,et al.  Reflecting upon Feelings: An fMRI Study of Neural Systems Supporting the Attribution of Emotion to Self and Other , 2004, Journal of Cognitive Neuroscience.

[62]  Kalina Christoff,et al.  Localizing the rostrolateral prefrontal cortex at the individual level , 2007, NeuroImage.

[63]  K. Luan Phan,et al.  Functional Neuroanatomy of Emotion: A Meta-Analysis of Emotion Activation Studies in PET and fMRI , 2002, NeuroImage.

[64]  P W Burgess,et al.  Strategy application disorder: the role of the frontal lobes in human multitasking , 2000, Psychological research.

[65]  Iroise Dumontheil,et al.  Function and localization within rostral prefrontal cortex (area 10) , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[66]  Andy C. H. Lee,et al.  “Pray or Prey?” Dissociation of Semantic Memory Retrieval from Episodic Memory Processes Using Positron Emission Tomography and a Novel Homophone Task , 2002, NeuroImage.

[67]  E. Koechlin,et al.  Anterior Prefrontal Function and the Limits of Human Decision-Making , 2007, Science.

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

[69]  Paul C. Fletcher,et al.  Anterior prefrontal cortex and the recollection of contextual information , 2005, Neuropsychologia.

[70]  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.

[71]  Stephanie Spengler,et al.  Differential functions of lateral and medial rostral prefrontal cortex (area 10) revealed by brain-behavior associations. , 2005, Cerebral cortex.

[72]  Sterling C. Johnson,et al.  Neural correlates of self-reflection. , 2002, Brain : a journal of neurology.

[73]  Jeremy R. Reynolds,et al.  Neural Mechanisms of Transient and Sustained Cognitive Control during Task Switching , 2003, Neuron.

[74]  M. Davies,et al.  Folk Psychology: The Theory of Mind Debate , 1995 .

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

[76]  D. Perrett,et al.  Cortical and subcortical mechanisms at the core of imitation , 2007, Social neuroscience.

[77]  C. Frith The social brain? , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[78]  Cyrus R. Mehta,et al.  SPSS Exact Tests 7.0 for Windows , 2004 .

[79]  Peter K. Smith,et al.  Theories of theories of mind: References , 1996 .

[80]  Wolfgang Prinz,et al.  Is it really my turn? An event-related fMRI study of task sharing , 2007, Social neuroscience.

[81]  K. Ochsner,et al.  The role of social cognition in emotion , 2008, Trends in Cognitive Sciences.

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

[83]  Russell A. Poldrack,et al.  On the fundamental role of anatomy in functional imaging: Reply to commentaries on “In praise of tedious anatomy” , 2007, NeuroImage.

[84]  D. Collins,et al.  Automatic 3D Intersubject Registration of MR Volumetric Data in Standardized Talairach Space , 1994, Journal of computer assisted tomography.

[85]  Anna-Lisa Cohen,et al.  Modulation of the Prospective and Retrospective Components of Memory for Intentions in Younger and Older Adults , 2001 .