Association fibers connecting the Broca center and the lateral superior frontal gyrus: a microsurgical and tractographic anatomy.

OBJECT Recently, intraoperative mapping has disclosed that, in addition to the classic language centers (that is, the Broca and Wernicke centers), other cortical regions may also play an important role in language organization. In the prefrontal cortex, although the lateral superior frontal gyrus (LSFG) could have language-related functions, there are no detailed reports that demonstrate the anatomical connection between the LSFG and other well-known language cortices, such as the Broca center. To show the existence of the structural connection, white matter association fibers between the inferior frontal gyrus (IFG) and the LSFG were examined using fiber dissection (FD) and diffusion tensor (DT) imaging-based tractography. METHODS Eight cadaveric cerebral hemispheres were dissected to reveal the association fibers between the IFG and LSFG. The DT imaging-based tractography studies targeting the prefrontal cortex were obtained in 53 right-handed patients who had no organic cerebral lesions. RESULTS The association fiber tract between Brodmann area 44/45 (the Broca center in the dominant hemisphere) and LSFG were detected in all specimens by FD. In the DT imaging-based tractography studies, the tract was identified in all patients bilaterally, except for the 4 in whom the tract was detected only in the left hemisphere. This tract was spread significantly wider in the left than in the right hemisphere, and left lateralization was evident in male patients. CONCLUSIONS Based on its character, this tract was named the Broca-LSFG pathway. These findings suggest a close relationship between this pathway and language organization. The structural anatomy of the Broca-LSFG pathway may explain speech disturbances induced by LSFG stimulation that are sometimes observed during intraoperative language mapping.

[1]  B. Dubois,et al.  Functions of the left superior frontal gyrus in humans: a lesion study. , 2006, Brain : a journal of neurology.

[2]  Jean-Luc Velay,et al.  Visual presentation of single letters activates a premotor area involved in writing , 2003, NeuroImage.

[3]  Giuseppe Scotti,et al.  Motor and language DTI Fiber Tracking combined with intraoperative subcortical mapping for surgical removal of gliomas , 2008, NeuroImage.

[4]  H. Shinohara [The lateral approach]. , 2005, No shinkei geka. Neurological surgery.

[5]  J. A. Frost,et al.  Language dominance in neurologically normal and epilepsy subjects , 1999 .

[6]  E Wyllie,et al.  Functional anatomy of the human supplementary sensorimotor area: results of extraoperative electrical stimulation. , 1994, Electroencephalography and clinical neurophysiology.

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

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

[9]  John S. Duncan,et al.  Hemispheric asymmetries in language-related pathways: A combined functional MRI and tractography study , 2006, NeuroImage.

[10]  B. Larsen,et al.  Activation of the supplementary motor area during voluntary movement in man suggests it works as a supramotor area. , 1979, Science.

[11]  Pratik Mukherjee,et al.  Subcortical pathways serving cortical language sites: initial experience with diffusion tensor imaging fiber tracking combined with intraoperative language mapping , 2004, NeuroImage.

[12]  Keith D. White,et al.  Structural connectivity of Broca's area and medial frontal cortex , 2010, NeuroImage.

[13]  G. McCarthy,et al.  Functional organization of human supplementary motor cortex studied by electrical stimulation , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[15]  Leslie G. Ungerleider,et al.  An area specialized for spatial working memory in human frontal cortex. , 1998, Science.

[16]  Derek K. Jones,et al.  Symmetries in human brain language pathways correlate with verbal recall , 2007, Proceedings of the National Academy of Sciences.

[17]  Hidenao Fukuyama,et al.  Discrimination of Exner's area and the frontal eye field in humans – functional magnetic resonance imaging during language and saccade tasks , 2003, Neuroscience Letters.

[18]  W PENFIELD,et al.  The supplementary motor area of the cerebral cortex; a clinical and experimental study. , 1951, A.M.A. archives of neurology and psychiatry.

[19]  H. Duffau,et al.  The functional architecture of the left posterior and lateral prefrontal cortex in humans. , 2008, Cerebral Cortex.

[20]  Byron Bernal,et al.  The connectivity of the superior longitudinal fasciculus: a tractography DTI study. , 2010, Magnetic resonance imaging.

[21]  Peggy Gatignol,et al.  The role of dominant premotor cortex in language: a study using intraoperative functional mapping in awake patients , 2003, NeuroImage.

[22]  Wilhelm Eisner,et al.  Surgical Resection of Grade II Astrocytomas in the Superior Frontal Gyrus , 2002, Neurosurgery.

[23]  Thomas R. Barrick,et al.  Atlas-based segmentation of white matter tracts of the human brain using diffusion tensor tractography and comparison with classical dissection , 2008, NeuroImage.

[24]  Nitin Tandon,et al.  Relationships between essential cortical language sites and subcortical pathways. , 2009, Journal of neurosurgery.

[25]  P. V. van Zijl,et al.  Three‐dimensional tracking of axonal projections in the brain by magnetic resonance imaging , 1999, Annals of neurology.

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

[27]  Wilder Penfield,et al.  The supplementary motor area in the cerebral cortex of man , 2004, Archiv für Psychiatrie und Nervenkrankheiten.

[28]  G A Ojemann,et al.  Postoperative deficits and functional recovery following removal of tumors involving the dominant hemisphere supplementary motor area. , 1991, Journal of neurosurgery.

[29]  Mitchel S Berger,et al.  Functional outcome after language mapping for glioma resection. , 2008, The New England journal of medicine.

[30]  A. Friedman,et al.  Fiber dissection technique: lateral aspect of the brain. , 2000, Neurosurgery.

[31]  Laurent Capelle,et al.  Somatotopy of the Supplementary Motor Area: Evidence from Correlation of the Extent of Surgical Resection with the Clinical Patterns of Deficit , 2002, Neurosurgery.

[32]  G. Ojemann,et al.  Cortical language localization in left, dominant hemisphere. An electrical stimulation mapping investigation in 117 patients. 1989. , 2008, Journal of neurosurgery.

[33]  J. Tanji,et al.  Concept-based behavioral planning and the lateral prefrontal cortex , 2007, Trends in Cognitive Sciences.

[34]  M. Berger,et al.  Preoperative correlation of intraoperative cortical mapping with magnetic resonance imaging landmarks to predict localization of the Broca area. , 2003, Journal of neurosurgery.

[35]  H. Duffau,et al.  A discrete area within the left dorsolateral prefrontal cortex involved in visual-verbal incongruence judgment. , 2008, Cerebral cortex.

[36]  G. Goldberg Supplementary motor area structure and function: Review and hypotheses , 1985, Behavioral and Brain Sciences.

[37]  Takashi Hanakawa,et al.  Functional Coupling of Human Prefrontal and Premotor Areas during Cognitive Manipulation , 2007, The Journal of Neuroscience.

[38]  C. Papagno,et al.  INTRAOPERATIVE LANGUAGE LOCALIZATIONIN MULTILINGUAL PATIENTS WITH GLIOMAS , 2006, Neurosurgery.

[39]  P. Bartolomeo,et al.  Left unilateral neglect as a disconnection syndrome. , 2007, Cerebral cortex.

[40]  J. Desmond,et al.  Left superior parietal cortex involvement in writing: integrating fMRI with lesion evidence. , 2001, Brain research. Cognitive brain research.

[41]  L. Fasotti,et al.  The internal representation of arithmetical word problem sentences: Frontal and posterior-injured patients compared , 1992, Brain and Cognition.

[42]  J. Pujol,et al.  Cerebral lateralization of language in normal left-handed people studied by functional MRI , 1999, Neurology.

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