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

Clinical article

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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.

Abbreviations used in this paper: DT = diffusion tensor; DW = diffusion-weighted; FD = fiber dissection; IFG = inferior frontal gyrus; LI = lateralization index; LSFG = lateral superior frontal gyrus; ROI = region of interest; SLF = superior longitudinal fascicle; SMA = supplementary motor area.

Article Information

Address correspondence to: Yutaka Hayashi, M.D., Department of Neurosurgery, Kanazawa University, 13-1 Takaramachi, Kanazawa 920-8641, Japan. email: yuh@ns.m.kanazawa-u.ac.jp.

Please include this information when citing this paper: published online November 11, 2011; DOI: 10.3171/2011.10.JNS11434.

© AANS, except where prohibited by US copyright law.

Headings

Figures

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    Magnetic resonance images and tractography studies reconstructed from DW images. The green lines in panels A–D outline the ROIs. A: Axial fractional anisotropy map at the level of the IFG. B: A T2-weighted image, in which ROIs are configured in the bilateral IFG. C: Axial fractional anisotropy map at the level of the LSFG. D: A T2-weighted image, in which ROIs are configured in the bilateral LSFG. E: Tractography study showing the fiber tracts connecting the IFG and SFG in an anterior view on a coronal T2-weighted image. Left fiber tract (F) and right fiber tract (G) in lateral views on a sagittal T2-weighted image.

  • View in gallery

    Photographs showing FD performed via a lateral approach (left hemisphere). Asterisks designate the opercular region in IFG. A: A lateral view showing the fiber tract ascending from the opercular region of the IFG to the LSFG (arrows show the posterior edge of the tract). B: A magnified image showing the SLF (triangles) that converges with the fiber tract between the IFG and LSFG. C: An upper view of the fiber tract that terminates in the lateral portion of the LSFG. CS = central sulcus.

  • View in gallery

    Tractography studies showing the targeted fiber tract between the IFG and LSFG in relation with other close fibers on a fractional anisotropy map. A: A targeted fiber tract running in proximity to the internal capsule (IC) or external capsule (EC) in an anterolateral view. B: An anterior view. C: A coronal image of the targeted fiber tract running outside both the internal and external capsule fibers. The label IFG-LSFG denotes the fiber tract between the IFG and LSFG.

  • View in gallery

    Bar graph showing average width of the tract on DT imaging–based tractography studies; the average width of the fiber tract terminations in the IFG and SFG is given.

  • View in gallery

    Point graphs of the LI in the SFG (A) and IFG (B). The midline of the diamond denotes the average index; the upper and lower portions denote the 95% confidence interval.

  • View in gallery

    A: Illustrative anterior view of fibers in the 3 lateralization groups, based on the results of cluster analysis. The fiber tract images are as marked on the individual panels. B and C: Box plot graphs of the 3 lateralization groups of the tract of the SFG (B) and IFG (C). Boxes represent the 25th and 75th percentiles, with the medians indicated by the middle lines in the boxes. Vertical bars (whiskers) indicate the range of data, except for the outliers. The percentage of each group is also given in the figures.

References

1

Abe MHanakawa TTakayama YKuroki COgawa SFukuyama H: Functional coupling of human prefrontal and premotor areas during cognitive manipulation. J Neurosci 27:342934382007

2

Aldenderfer MSBlashfield RK: Cluster Analysis Newbury Park, CASage Publications1984

3

Bartolomeo PThiebaut de Schotten MDoricchi F: Left unilateral neglect as a disconnection syndrome. Cereb Cortex 17:247924902007

4

Bello LAcerbi FGiussani CBaratta PTaccone PSonga V: Intraoperative language localization in multilingual patients with gliomas. Neurosurgery 59:1151252006

5

Bello LGambini ACastellano ACarrabba GAcerbi FFava E: Motor and language DTI Fiber Tracking combined with intraoperative subcortical mapping for surgical removal of gliomas. Neuroimage 39:3693822008

6

Bernal BAltman N: The connectivity of the superior longitudinal fasciculus: a tractography DTI study. Magn Reson Imaging 28:2172252010

7

Catani MAllin MPHusain MPugliese LMesulam MMMurray RM: Symmetries in human brain language pathways correlate with verbal recall. Proc Natl Acad Sci U S A 104:17163171682007

8

Courtney SMPetit LMaisog JMUngerleider LGHaxby JV: An area specialized for spatial working memory in human frontal cortex. Science 279:134713511998

9

du Boisgueheneuc FLevy RVolle ESeassau MDuffau HKinkingnehun S: Functions of the left superior frontal gyrus in humans: a lesion study. Brain 129:331533282006

10

Duffau HCapelle LDenvil DGatignol PSichez NLopes M: The role of dominant premotor cortex in language: a study using intraoperative functional mapping in awake patients. Neuroimage 20:190319142003

11

Ellmore TMBeauchamp MSO'Neill TJDreyer STandon N: Relationships between essential cortical language sites and subcortical pathways. Clinical article. J Neurosurg 111:7557662009

12

Fasotti LEling PABremer JJ: The internal representation of arithmetical word problem sentences: frontal and posterior-injured patients compared. Brain Cogn 20:2452631992

13

Fontaine DCapelle LDuffau H: Somatotopy of the supplementary motor area: evidence from correlation of the extent of surgical resection with the clinical patterns of deficit. Neurosurgery 50:2973052002

14

Ford AMcGregor KMCase KCrosson BWhite KD: Structural connectivity of Broca's area and medial frontal cortex. Neuroimage 52:123012372010

15

Fried IKatz AMcCarthy GSass KJWilliamson PSpencer SS: Functional organization of human supplementary motor cortex studied by electrical stimulation. J Neurosci 11:365636661991

16

Friederici AD: Pathways to language: fiber tracts in the human brain. Trends Cogn Sci 13:1751812009

17

Goldberg G: Supplementary motor area structure and function: review and hypotheses. Behav Brain Sci 8:5676161985

18

Henry RGBerman JINagarajan SSMukherjee PBerger MS: Subcortical pathways serving cortical language sites: initial experience with diffusion tensor imaging fiber tracking combined with intraoperative language mapping. Neuroimage 21:6166222004

19

Jonas S: The supplementary motor region and speech emission. J Commun Disord 14:3493731981

20

Klingler J: Erleichterung der makroskopischen Praeparation des Gehirns durch den Gefrierprozess. Schweiz Arch Neurol Psychiatr 36:2472561935

21

Krieg WJS: Architectonics of Human Cerebral Fiber Systems Evanston, ILBrain Books1973

22

Lawes INBarrick TRMurugam VSpierings NEvans DRSong M: Atlas-based segmentation of white matter tracts of the human brain using diffusion tensor tractography and comparison with classical dissection. Neuroimage 39:62792008

23

Lim SHDinner DSPillay PKLüders HMorris HHKlem G: Functional anatomy of the human supplementary sensorimotor area: results of extraoperative electrical stimulation. Electroencephalogr Clin Neurophysiol 91:1791931994

24

Longcamp MAnton JLRoth MVelay JL: Visual presentation of single letters activates a premotor area involved in writing. Neuroimage 19:149215002003

25

Matsuo KKato CSumiyoshi CToma KDuy Thuy DHMoriya T: Discrimination of Exner's area and the frontal eye field in humans—functional magnetic resonance imaging during language and saccade tasks. Neurosci Lett 340:13162003

26

Menon VDesmond JE: Left superior parietal cortex involvement in writing: integrating fMRI with lesion evidence. Brain Res Cogn Brain Res 12:3373402001

27

Mori SCrain BJChacko VPvan Zijl PC: Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging. Ann Neurol 45:2652691999

28

Ojemann GOjemann JLettich EBerger M: Cortical language localization in left, dominant hemisphere. An electrical stimulation mapping investigation in 117 patients. J Neurosurg 71:3163261989

29

Orgogozo JMLarsen B: Activation of the supplementary motor area during voluntary movement in man suggests it works as a supramotor area. Science 206:8478501979

30

Penfield WWelch K: The supplementary motor area in the cerebral cortex of man. Trans Am Neurol Assoc 74:1791841949

31

Penfield WWelch K: The supplementary motor area of the cerebral cortex; a clinical and experimental study. AMA Arch Neurol Psychiatry 66:2893171951

32

Peraud AMeschede MEisner WIlmberger JReulen HJ: Surgical resection of grade II astrocytomas in the superior frontal gyrus. Neurosurgery 50:9669772002

33

Plaza MGatignol PCohen HBerger BDuffau H: A discrete area within the left dorsolateral prefrontal cortex involved in visual-verbal incongruence judgment. Cereb Cortex 18:125312592008

34

Powell HWParker GJAlexander DCSymms MRBoulby PAWheeler-Kingshott CA: Hemispheric asymmetries in language-related pathways: a combined functional MRI and tractography study. Neuroimage 32:3883992006

35

Pujol JDeus JLosilla JMCapdevila A: Cerebral lateralization of language in normal left-handed people studied by functional MRI. Neurology 52:103810431999

36

Quiñones-Hinojosa AOjemann SGSanai NDillon WPBerger MS: Preoperative correlation of intraoperative cortical mapping with magnetic resonance imaging landmarks to predict localization of the Broca area. J Neurosurg 99:3113182003

37

Ridderinkhof KRUllsperger MCrone EANieuwenhuis S: The role of the medial frontal cortex in cognitive control. Science 306:4434472004

38

Rostomily RCBerger MSOjemann GALettich E: Postoperative deficits and functional recovery following removal of tumors involving the dominant hemisphere supplementary motor area. J Neurosurg 75:62681991

39

Rushworth MFBuckley MJBehrens TEWalton MEBannerman DM: Functional organization of the medial frontal cortex. Curr Opin Neurobiol 17:2202272007

40

Rushworth MFWalton MEKennerley SWBannerman DM: Action sets and decisions in the medial frontal cortex. Trends Cogn Sci 8:4104172004

41

Sanai NMirzadeh ZBerger MS: Functional outcome after language mapping for glioma resection. N Engl J Med 358:18272008

42

Shinohara H: [The lateral approach.]. No Shinkei Geka 33:105710702005. (Jpn)

43

Springer JABinder JRHammeke TASwanson SJFrost JABellgowan PS: Language dominance in neurologically normal and epilepsy subjects: a functional MRI study. Brain 122:203320461999

44

Tanji JShima KMushiake H: Concept-based behavioral planning and the lateral prefrontal cortex. Trends Cogn Sci 11:5285342007

45

Türe UYaşargil MGFriedman AHAl-Mefty O: Fiber dissection technique: lateral aspect of the brain. Neurosurgery 47:4174272000

46

Volle EKinkingnéhun SPochon JBMondon KThiebaut de Schotten MSeassau M: The functional architecture of the left posterior and lateral prefrontal cortex in humans. Cereb Cortex 18:246024692008

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