Distinct functional connectivity associated with lateral versus medial rostral prefrontal cortex: A meta-analysis

Recent studies have shown that functional connectivity in the human brain may be detected by analyzing the likelihood with which different brain regions are simultaneously activated, or "co-activated", across multiple neuroimaging experiments. We applied this technique to investigate whether distinct subregions within rostral prefrontal cortex (RoPFC) tend to co-activate with distinct sets of brain regions outside RoPFC, in a meta-analysis of 200 activation peaks within RoPFC (approximating Brodmann Area 10) and 1712 co-activations outside this region, drawn from 162 studies. There was little evidence for distinct connectivity between hemispheres or along rostral/caudal or superior/inferior axes. However, there was a clear difference between lateral and medial RoPFC: activation in lateral RoPFC was particularly associated with co-activation in dorsal anterior cingulate, dorsolateral PFC, anterior insula and lateral parietal cortex; medial RoPFC activation was particularly associated with co-activation in posterior cingulate, posterior superior temporal sulcus and temporal pole. These findings are consistent with anatomical studies of connectivity in non-human primates, despite strong cross-species differences in RoPFC. Furthermore, associations between brain regions inside and outside RoPFC were in some cases strongly influenced by the type of task being performed. For example, dorsolateral PFC, anterior cingulate and lateral parietal cortex tended to co-activate with lateral RoPFC in most tasks but with medial RoPFC in tasks involving mentalizing. These results suggest the importance of changes in effective connectivity in the performance of cognitive tasks.

[1]  A. Dagher,et al.  Basal ganglia functional connectivity based on a meta-analysis of 126 positron emission tomography and functional magnetic resonance imaging publications. , 2006, Cerebral cortex.

[2]  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.

[3]  J. Fodor The Modularity of mind. An essay on faculty psychology , 1986 .

[4]  M. Lindquist,et al.  Meta-analysis of functional neuroimaging data: current and future directions. , 2007, Social cognitive and affective neuroscience.

[5]  Paul C. Fletcher,et al.  Separable Forms of Reality Monitoring Supported by Anterior Prefrontal Cortex , 2008, Journal of Cognitive Neuroscience.

[6]  R. Henson What can Functional Neuroimaging Tell the Experimental Psychologist? , 2005, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[7]  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.

[9]  Lisa Feldman Barrett,et al.  Functional grouping and cortical–subcortical interactions in emotion: A meta-analysis of neuroimaging studies , 2008, NeuroImage.

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

[11]  K. Christoff,et al.  Experience sampling during fMRI reveals default network and executive system contributions to mind wandering , 2009, Proceedings of the National Academy of Sciences.

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

[13]  Angela M. Uecker,et al.  ALE meta‐analysis: Controlling the false discovery rate and performing statistical contrasts , 2005, Human brain mapping.

[14]  Richard N A Henson,et al.  The Scale of Functional Specialization within Human Prefrontal Cortex , 2010, The Journal of Neuroscience.

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

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

[17]  Lisa Koski,et al.  Erratum to: Functional connectivity of the anterior cingulate cortex within the human frontal lobe: a brain-mapping meta-analysis , 2000, Experimental Brain Research.

[18]  Maurizio Corbetta,et al.  The human brain is intrinsically organized into dynamic, anticorrelated functional networks. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[19]  G L Shulman,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:A default mode of brain function , 2001 .

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

[21]  Heidi Johansen-Berg,et al.  Using diffusion imaging to study human connectional anatomy. , 2009, Annual review of neuroscience.

[22]  Scott T. Grafton,et al.  Wandering Minds: The Default Network and Stimulus-Independent Thought , 2007, Science.

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

[24]  F. Overwalle Social cognition and the brain: a meta-analysis. , 2009 .

[25]  H. Barbas,et al.  Medial Prefrontal Cortices Are Unified by Common Connections With Superior Temporal Cortices and Distinguished by Input From Memory‐Related Areas in the Rhesus Monkey , 1999, The Journal of comparative neurology.

[26]  Karl J. Friston,et al.  Functional topography: multidimensional scaling and functional connectivity in the brain. , 1996, Cerebral cortex.

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

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

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

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

[31]  C. Frith,et al.  Distinct regions of medial rostral prefrontal cortex supporting social and nonsocial functions. , 2007, Social cognitive and affective neuroscience.

[32]  J. Duncan Prefrontal cortex and Spearman's g , 2012 .

[33]  T. Paus,et al.  Functional coactivation map of the human brain. , 2008, Cerebral cortex.

[34]  Jason P. Mitchell,et al.  Dissociable Medial Prefrontal Contributions to Judgments of Similar and Dissimilar Others , 2006, Neuron.

[35]  K. Christoff,et al.  Prefrontal organization of cognitive control according to levels of abstraction , 2009, Brain Research.

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

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

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

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

[40]  Stephen Lawrie,et al.  Functional Specialization within Rostral Prefrontal Cortex (Area 10): A Meta-analysis , 2006, Journal of Cognitive Neuroscience.

[41]  Guinevere F. Eden,et al.  Meta-Analysis of the Functional Neuroanatomy of Single-Word Reading: Method and Validation , 2002, NeuroImage.