Organization of the Human Frontal Pole Revealed by Large-Scale DTI-Based Connectivity: Implications for Control of Behavior

The goal of the current study was to examine the pattern of anatomical connectivity of the human frontal pole so as to inform theories of function of the frontal pole, perhaps one of the least understood region of the human brain. Rather than simply parcellating the frontal pole into subregions, we focused on examining the brain regions to which the frontal pole is anatomically and functionally connected. While the current findings provided support for previous work suggesting the frontal pole is connected to higher-order sensory association cortex, we found novel evidence suggesting that the frontal pole in humans is connected to posterior visual cortex. Furthermore, we propose a functional framework that incorporates these anatomical connections with existing cognitive theories of the functional organization of the frontal pole. In addition to a previously discussed medial-lateral distinction, we propose a dorsal-ventral gradient based on the information the frontal pole uses to guide behavior. We propose that dorsal regions are connected to other prefrontal regions that process goals and action plans, medial regions are connected to other brain regions that monitor action outcomes and motivate behaviors, and ventral regions connect to regions that process information about stimuli, values, and emotion. By incorporating information across these different levels of information, the frontal pole can effectively guide goal-directed behavior.

[1]  John H. R. Maunsell,et al.  Hierarchical organization and functional streams in the visual cortex , 1983, Trends in Neurosciences.

[2]  K. Davis,et al.  Connectivity-based parcellation of the human frontal polar cortex , 2014, Brain Structure and Function.

[3]  M. Brass,et al.  Unconscious determinants of free decisions in the human brain , 2008, Nature Neuroscience.

[4]  M. Berger,et al.  Q-Ball of Inferior Fronto-Occipital Fasciculus and Beyond , 2013, PloS one.

[5]  Manuel Graña,et al.  Model‐based analysis of multishell diffusion MR data for tractography: How to get over fitting problems , 2012, Magnetic resonance in medicine.

[6]  D. V. van Essen,et al.  Cell structure and function in the visual cortex of the cat , 1974, The Journal of physiology.

[7]  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.

[8]  Mark Jenkinson,et al.  The minimal preprocessing pipelines for the Human Connectome Project , 2013, NeuroImage.

[9]  Michael L. Anderson,et al.  Describing functional diversity of brain regions and brain networks , 2013, NeuroImage.

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

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

[12]  Hugues Duffau,et al.  Anatomic dissection of the inferior fronto-occipital fasciculus revisited in the lights of brain stimulation data , 2010, Cortex.

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

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

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

[16]  Desmond J. Higham,et al.  Connectivity-based parcellation of human cortex using diffusion MRI: Establishing reproducibility, validity and observer independence in BA 44/45 and SMA/pre-SMA , 2007, NeuroImage.

[17]  Mark W. Woolrich,et al.  Probabilistic diffusion tractography with multiple fibre orientations: What can we gain? , 2007, NeuroImage.

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

[19]  Chunshui Yu,et al.  Connectivity-Based Parcellation of the Human Frontal Pole with Diffusion Tensor Imaging , 2013, The Journal of Neuroscience.

[20]  M. Petrides,et al.  Broca’s region: linking human brain functional connectivity data and non‐human primate tracing anatomy studies , 2010, The European journal of neuroscience.

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

[22]  M. Catani,et al.  A lateralized brain network for visuospatial attention , 2011, Nature Neuroscience.

[23]  H. Duffau,et al.  Frontal terminations for the inferior fronto-occipital fascicle: anatomical dissection, DTI study and functional considerations on a multi-component bundle , 2011, Brain Structure and Function.

[24]  R. Luján.  Fiber Pathways of the Brain, J.D. Schmahmann, D.N. Pandya (Eds.). Oxford University Press (2006), ISBN: 0-19-510423-4 , 2008 .

[25]  D. V. van Essen,et al.  Visual areas of the mammalian cerebral cortex. , 1979, Annual review of neuroscience.

[26]  Peter Dechent,et al.  A gateway system in rostral PFC? Evidence from biasing attention to perceptual information and internal representations , 2011, NeuroImage.

[27]  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.

[28]  Russell A. Poldrack,et al.  Large-scale automated synthesis of human functional neuroimaging data , 2011, Nature Methods.

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

[30]  D. Pandya,et al.  The Complex History of the Fronto-Occipital Fasciculus , 2007, Journal of the history of the neurosciences.

[31]  D. C. Essen,et al.  Visual areas of the mammalian cerebral cortex. , 1979 .

[32]  Luke J. Chang,et al.  Connectivity-Based Parcellation of the Human Orbitofrontal Cortex , 2012, The Journal of Neuroscience.

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

[34]  Steen Moeller,et al.  Advances in diffusion MRI acquisition and processing in the Human Connectome Project , 2013, NeuroImage.

[35]  D. V. van Essen,et al.  Mapping Human Cortical Areas In Vivo Based on Myelin Content as Revealed by T1- and T2-Weighted MRI , 2011, The Journal of Neuroscience.

[36]  Remco J. Renken,et al.  Group analyses of connectivity-based cortical parcellation using repeated k-means clustering , 2009, NeuroImage.

[37]  Paul W. Burgess,et al.  Distinct functional connectivity associated with lateral versus medial rostral prefrontal cortex: A meta-analysis , 2010, NeuroImage.

[38]  Steen Moeller,et al.  Pushing spatial and temporal resolution for functional and diffusion MRI in the Human Connectome Project , 2013, NeuroImage.

[39]  Angela R. Laird,et al.  Cytoarchitecture, probability maps and functions of the human frontal pole , 2014, NeuroImage.

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

[41]  Gaël Varoquaux,et al.  Scikit-learn: Machine Learning in Python , 2011, J. Mach. Learn. Res..

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

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

[44]  Luke J. Chang,et al.  Decoding the role of the insula in human cognition: functional parcellation and large-scale reverse inference. , 2013, Cerebral cortex.

[45]  Marcel Brass,et al.  Biasing free choices: The role of the rostral cingulate zone in intentional control , 2013, NeuroImage.

[46]  A. Nobre,et al.  Heterogeneity of Cingulate Contributions to Spatial Attention , 2001, NeuroImage.

[47]  M. Meilă.  Comparing clusterings---an information based distance , 2007 .

[48]  R. O’Reilly.  The What and How of prefrontal cortical organization , 2010, Trends in Neurosciences.

[49]  T. Egner,et al.  Emotional processing in anterior cingulate and medial prefrontal cortex , 2011, Trends in Cognitive Sciences.

[50]  N. Volkow,et al.  Dysfunction of the prefrontal cortex in addiction: neuroimaging findings and clinical implications , 2011, Nature Reviews Neuroscience.

[51]  Marie T. Banich,et al.  The neural mechanisms underlying internally and externally guided task selection , 2014, NeuroImage.

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

[53]  Jelliffe.  Vergleichende Lokalisationslehre der Grosshirnrinde , 1910 .

[54]  Hsin-Hao Yu,et al.  Cortical input to the frontal pole of the marmoset monkey. , 2011, Cerebral Cortex.