Structural connectivity of Broca's area and medial frontal cortex

Despite over 140 years of research on Broca's area, the connections of this region to medial frontal cortex remain unclear. The current study investigates this structural connectivity using diffusion-weighted MRI tractography in living humans. Our results show connections between Broca's area and Brodmann's areas (BA) 9, 8, and 6 (both supplementary motor area (SMA) in caudal BA 6, and Pre-SMA in rostral BA 6). Trajectories follow an anterior-to-posterior gradient, wherein the most anterior portions of Broca's area connect to BA 9 and 8 while posterior Broca's area connects to Pre-SMA and SMA. This anterior-posterior connectivity gradient is also present when connectivity-based parcellation of Broca's area is performed. Previous studies of language organization suggest involvement of anterior Broca's area in semantics and posterior Broca's area in syntax/phonology. Given corresponding patterns of functional and structural organization of Broca's area, it seems well warranted to investigate carefully how anterior vs. posterior medial frontal cortex differentially affect semantics, syntax and phonology.

[1]  C. Wernicke.  Der aphasische Symptomenkomplex , 1974 .

[2]  Stephen M. Smith,et al.  A global optimisation method for robust affine registration of brain images , 2001, Medical Image Anal..

[3]  A. Dale,et al.  Life-span changes of the human brain white matter: diffusion tensor imaging (DTI) and volumetry. , 2010, Cerebral cortex.

[4]  Timothy Edward John Behrens,et al.  Characterization and propagation of uncertainty in diffusion‐weighted MR imaging , 2003, Magnetic resonance in medicine.

[5]  A. Braun,et al.  Activation of Broca’s area during the production of spoken and signed language: a combined cytoarchitectonic mapping and PET analysis , 2003, Neuropsychologia.

[6]  G. Rizzolatti,et al.  The mirror-neuron system. , 2004, Annual review of neuroscience.

[7]  Timothy E. J. Behrens,et al.  Functional organization of the medial frontal cortex , 2007, Current Opinion in Neurobiology.

[8]  Richard W Briggs,et al.  Left and right basal ganglia and frontal activity during language generation: Contributions to lexical, semantic, and phonological processes , 2003, Journal of the International Neuropsychological Society.

[9]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[10]  A. Schleicher,et al.  Broca's region revisited: Cytoarchitecture and intersubject variability , 1999, The Journal of comparative neurology.

[11]  Matthew F Glasser,et al.  DTI tractography of the human brain's language pathways. , 2008, Cerebral cortex.

[12]  Timothy Edward John Behrens,et al.  Between session reproducibility and between subject variability of diffusion MR and tractography measures , 2006, NeuroImage.

[13]  A. Anwander,et al.  Connectivity-Based Parcellation of Broca's Area. , 2006, Cerebral cortex.

[14]  P. Strick,et al.  Motor areas of the medial wall: a review of their location and functional activation. , 1996, Cerebral cortex.

[15]  A. Pfefferbaum,et al.  Quantitative fiber tracking of lateral and interhemispheric white matter systems in normal aging: Relations to timed performance , 2010, Neurobiology of Aging.

[16]  E. Koechlin,et al.  Motivation and cognitive control in the human prefrontal cortex , 2009, Nature Neuroscience.

[17]  James Theiler,et al.  Testing for nonlinearity in time series: the method of surrogate data , 1992 .

[18]  R W BARRIS,et al.  Bilateral Anterior Cingulate Gyrus Lesions , 1953, Neurology.

[19]  B. Horwitz,et al.  Functional connectivity of the angular gyrus in normal reading and dyslexia. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[20]  C. C. Tijssen,et al.  Aphasia with a left frontal interhemispheric hematoma , 1984, Neurology.

[21]  Scott Barbay,et al.  Interhemispheric connections of the ventral premotor cortex in a new world primate , 2007, The Journal of comparative neurology.

[22]  S Jonas,et al.  The supplementary motor region and speech emission. , 1981, Journal of communication disorders.

[23]  Jung-Lung Hsu,et al.  Gender differences and age-related white matter changes of the human brain: A diffusion tensor imaging study , 2008, NeuroImage.

[24]  K. Amunts,et al.  Advances in cytoarchitectonic mapping of the human cerebral cortex. , 2001, Neuroimaging clinics of North America.

[25]  J M NIELSEN,et al.  Bilateral lesions of the anterior cingulate gyri; report of case. , 1951, Bulletin of the Los Angeles Neurological Society.

[26]  Jennifer S. W. Campbell,et al.  Dissociating the Human Language Pathways with High Angular Resolution Diffusion Fiber Tractography , 2008, The Journal of Neuroscience.

[27]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

[28]  M. Arbib,et al.  Language within our grasp , 1998, Trends in Neurosciences.

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

[30]  Keith D. White,et al.  Functional MRI of Language in Aphasia: A Review of the Literature and the Methodological Challenges , 2007, Neuropsychology Review.

[31]  Timothy Edward John Behrens,et al.  Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging , 2003, Nature Neuroscience.

[32]  Simon B. Eickhoff,et al.  Analysis of neural mechanisms underlying verbal fluency in cytoarchitectonically defined stereotaxic space—The roles of Brodmann areas 44 and 45 , 2004, NeuroImage.

[33]  E. Auerbach,et al.  Relative Shift in Activity from Medial to Lateral Frontal Cortex During Internally Versus Externally Guided Word Generation , 2001, Journal of Cognitive Neuroscience.

[34]  S Grootoonk,et al.  Regional cerebral blood flow during volitional expiration in man: a comparison with volitional inspiration. , 1993, The Journal of physiology.

[35]  S. Ghosh,et al.  A comparison of the ipsilateral cortical projections to the dorsal and ventral subdivisions of the macaque premotor cortex. , 1995, Somatosensory & motor research.

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

[37]  K. Amunts,et al.  The human parietal operculum. II. Stereotaxic maps and correlation with functional imaging results. , 2006, Cerebral cortex.

[38]  D. Pandya,et al.  Comparative cytoarchitectonic analysis of the human and the macaque ventrolateral prefrontal cortex and corticocortical connection patterns in the monkey , 2002, The European journal of neuroscience.

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

[40]  Derek K. Jones,et al.  Perisylvian language networks of the human brain , 2005, Annals of neurology.

[41]  A. Dale,et al.  Age‐Related Changes in Prefrontal White Matter Measured by Diffusion Tensor Imaging , 2005, Annals of the New York Academy of Sciences.

[42]  T. Okada,et al.  Ideographic characters call for extra processing to correspond with phonemes , 2001, Neuroreport.

[43]  Angela D. Friederici,et al.  Pathways to language: fiber tracts in the human brain , 2009, Trends in Cognitive Sciences.

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

[45]  Nielsen Jm,et al.  Bilateral lesions of the anterior cingulate gyri; report of case. , 1951 .

[46]  A. R. Lurii︠a︡.  Human brain and psychological processes , 1966 .

[47]  K. Amunts,et al.  Broca's region , 2006 .

[48]  Alan C. Evans,et al.  The neural substrates underlying word generation: a bilingual functional-imaging study. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[49]  P. Broca.  Remarques sur le siège de la faculté du langage articulé, suivies d'une observation d'aphémie (perte de la parole) , 1861 .

[50]  W J BANGS,et al.  Bilateral lesions of the anterior cingulate gyri; report of case. , 1956, Bulletin of the Los Angeles Neurological Society.

[51]  Bruce Crosson,et al.  Subcortical Mechanisms in Language: Lexical–Semantic Mechanisms and the Thalamus , 1999, Brain and Cognition.

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

[53]  K. Amunts,et al.  Broca's region subserves imagery of motion: A combined cytoarchitectonic and fMRI study , 2000, Human brain mapping.

[54]  P. Strick,et al.  Imaging the premotor areas , 2001, Current Opinion in Neurobiology.

[55]  Stephen M. Rao,et al.  Human Brain Language Areas Identified by Functional Magnetic Resonance Imaging , 1997, The Journal of Neuroscience.

[56]  Timothy Edward John Behrens,et al.  Probabilistic diffusion tractography: a potential tool to assess the rate of disease progression in amyotrophic lateral sclerosis. , 2006, Brain : a journal of neurology.

[57]  P. Basser,et al.  MR diffusion tensor spectroscopy and imaging. , 1994, Biophysical journal.

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

[59]  Peter Hagoort.  On Broca, Brain and Binding , 2004 .

[60]  K. R. Ridderinkhof,et al.  The Role of the Medial Frontal Cortex in Cognitive Control , 2004, Science.

[61]  A. Benton,et al.  On Aphasia , 1874, British medical journal.

[62]  P. Broca,et al.  Remarques sur le siege de la faculte du langage articule suivies d'une observation d'aphemie , 1861 .

[63]  L. Katz,et al.  Sex differences in the functional organization of the brain for language , 1995, Nature.

[64]  Derek K. Jones,et al.  Virtual in Vivo Interactive Dissection of White Matter Fasciculi in the Human Brain , 2002, NeuroImage.

[65]  J. Townsend,et al.  Normal brain development and aging: quantitative analysis at in vivo MR imaging in healthy volunteers. , 2000, Radiology.