Skip to main content
Log in

Subcomponents and connectivity of the superior longitudinal fasciculus in the human brain

  • Original Article
  • Published:
Brain Structure and Function Aims and scope Submit manuscript

Abstract

The subcomponents of the human superior longitudinal fasciculus (SLF) are disputed. The objective of this study was to investigate the segments, connectivity and asymmetry of the SLF. We performed high angular diffusion spectrum imaging (DSI) analysis on ten healthy adults. We also conducted fiber tracking on a 30-subject DSI template (CMU-30) and 488-subject template from the Human Connectome Project (HCP-488). In addition, five normal brains obtained at autopsy were microdissected. Based on tractography and microdissection results, we show that the human SLF differs significantly from that of monkey. The fibers corresponding to SLF-I found in 6 out of 20 hemispheres proved to be part of the cingulum fiber system in all cases and confirmed on both DSI and HCP-488 template. The most common patterns of connectivity bilaterally were as follows: from angular gyrus to caudal middle frontal gyrus and dorsal precentral gyrus representing SLF-II (or dorsal SLF), and from supramarginal gyrus to ventral precentral gyrus and pars opercularis to form SLF-III (or ventral SLF). Some connectivity features were, however, clearly asymmetric. Thus, we identified a strong asymmetry of the dorsal SLF (SLF-II), where the connectivity between the supramarginal gyrus with the dorsal precentral gyrus and the caudal middle frontal gyrus was only present in the left hemisphere. Contrarily, the ventral SLF (SLF-III) showed fairly constant connectivity with pars triangularis only in the right hemisphere. The results provide a novel neuroanatomy of the SLF that may help to better understand its functional role in the human brain.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12

Similar content being viewed by others

Abbreviations

SLF:

Superior longitudinal fasciculus

AF:

Arcuate fasciculus

ROI:

Region of interest

ROA:

Region of avoidance

QA:

Quantitative anisotropy

DSI:

Diffusion spectrum imaging

References

  • Agrawal A, Kapfhammer JP, Kress A, Wichers H, Deep A, Feindel W, Sonntag VK, Spetzler RF, Preul MC (2011) Josef Klingler’s models of white matter tracts: influences on neuroanatomy, neurosurgery, and neuroimaging. Neurosurgery 69(2):238–252 (discussion 252–234). doi:10.1227/NEU.0b013e318214ab79

  • Basser PJ, Pajevic S, Pierpaoli C, Duda J, Aldroubi A (2000) In vivo fiber tractography using DT-MRI data. Magn Reson Med 44(4):625–632

    Article  CAS  PubMed  Google Scholar 

  • Brown EC, Jeong JW, Muzik O, Rothermel R, Matsuzaki N, Juhasz C, Sood S, Asano E (2013) Evaluating the arcuate fasciculus with combined diffusion-weighted MRI tractography and electrocorticography. Hum Brain Mapp. doi:10.1002/hbm.22331

    PubMed  PubMed Central  Google Scholar 

  • Catani M, de Schotten MT (2012) Atlas of human brain connections. OUP Oxford

  • Desikan RS, Segonne F, Fischl B, Quinn BT, Dickerson BC, Blacker D, Buckner RL, Dale AM, Maguire RP, Hyman BT, Albert MS, Killiany RJ (2006) An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage 31(3):968–980. doi:10.1016/j.neuroimage.2006.01.021

    Article  PubMed  Google Scholar 

  • Dick AS, Tremblay P (2012) Beyond the arcuate fasciculus: consensus and controversy in the connectional anatomy of language. Brain. doi:10.1093/brain/aws222

    PubMed Central  Google Scholar 

  • Fernandez-Miranda JC, Rhoton AL, Jr., Alvarez-Linera J, Kakizawa Y, Choi C, de Oliveira EP (2008a) Three-dimensional microsurgical and tractographic anatomy of the white matter of the human brain. Neurosurgery 62 (6 Suppl 3):989–1026 (discussion 1026–1028). doi:10.1227/01.neu.0000333767.05328.49

  • Fernandez-Miranda JC, Rhoton AL Jr, Kakizawa Y, Choi C, Alvarez-Linera J (2008b) The claustrum and its projection system in the human brain: a microsurgical and tractographic anatomical study. J Neurosurg 108(4):764–774. doi:10.3171/jns/2008/108/4/0764

    Article  PubMed  Google Scholar 

  • Fernandez-Miranda JC, Pathak S, Engh J, Jarbo K, Verstynen T, Yeh FC, Wang Y, Mintz A, Boada F, Schneider W, Friedlander R (2012) High-definition fiber tractography of the human brain: neuroanatomical validation and neurosurgical applications. Neurosurgery 71(2):430–453. doi:10.1227/NEU.0b013e3182592faa

    Article  PubMed  Google Scholar 

  • Fernandez-Miranda JC, Wang Y, Pathak S, Stefaneanu L, Verstynen T, Yeh FY (2014) Asymmetry, connectivity, and segmentation of the arcuate fascicle in the human brain. Brain Struct Funct 11(4):341–352. doi:10.1007/s00429-014-0751-7

    Google Scholar 

  • Fonov V, Evans AC, Botteron K, Almli CR, McKinstry RC, Collins DL (2011) Unbiased average age-appropriate atlases for pediatric studies. Neuroimage 54(1):313–327. doi:10.1016/j.neuroimage.2010.07.033

    Article  PubMed  PubMed Central  Google Scholar 

  • Hartwigsen G, Bestmann S, Ward NS, Woerbel S, Mastroeni C, Granert O, Siebner HR (2012) Left dorsal premotor cortex and supramarginal gyrus complement each other during rapid action reprogramming. J Neurosci 32(46):16162–16171a. doi:10.1523/jneurosci.1010-12.2012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jang SH, Hong JH (2012) The anatomical characteristics of superior longitudinal fasciculus I in human brain: diffusion tensor tractography study. Neurosci Lett 506(1):146–148. doi:10.1016/j.neulet.2011.10.069

    Article  CAS  PubMed  Google Scholar 

  • Kawamura K, Naito J (1984) Corticocortical projections to the prefrontal cortex in the rhesus monkey investigated with horseradish peroxidase techniques. Neurosci Res 1(2):89–103

    Article  CAS  PubMed  Google Scholar 

  • Krestel H, Annoni JM, Jagella C (2013) White matter in aphasia: a historical review of the Dejerines’ studies. Brain Lang 127(3):526–532. doi:10.1016/j.bandl.2013.05.019

    Article  PubMed  Google Scholar 

  • Makris N, Kennedy DN, McInerney S, Sorensen AG, Wang R, Caviness VS Jr, Pandya DN (2005) Segmentation of subcomponents within the superior longitudinal fascicle in humans: a quantitative, in vivo, DT-MRI study. Cereb Cortex 15(6):854–869. doi:10.1093/cercor/bhh186

    Article  PubMed  Google Scholar 

  • Maldonado IL, Moritz-Gasser S, Duffau H (2011) Does the left superior longitudinal fascicle subserve language semantics? A brain electrostimulation study. Brain Struct Funct 216(3):263–274. doi:10.1007/s00429-011-0309-x

    Article  PubMed  Google Scholar 

  • Margulies DS, Petrides M (2013) Distinct parietal and temporal connectivity profiles of ventrolateral frontal areas involved in language production. J Neurosci 33(42):16846–16852. doi:10.1523/jneurosci.2259-13.2013

    Article  CAS  PubMed  Google Scholar 

  • Martino J, De Witt Hamer PC, Berger MS, Lawton MT, Arnold CM, de Lucas EM, Duffau H (2012) Analysis of the subcomponents and cortical terminations of the perisylvian superior longitudinal fasciculus: a fiber dissection and DTI tractography study. Brain Struct Funct. doi:10.1007/s00429-012-0386-5

    PubMed  Google Scholar 

  • Muthusami P, James J, Thomas B, Kapilamoorthy TR, Kesavadas C (2013) Diffusion tensor imaging and tractography of the human language pathways: moving into the clinical realm. J Magn Reson Imaging. doi:10.1002/jmri.24528

    PubMed  Google Scholar 

  • Nowinski WL (2005) The cerefy brain atlases: continuous enhancement of the electronic talairach-tournoux brain atlas. Neuroinformatics 3(4):293–300. doi:10.1385/ni:3:4:293

    Article  PubMed  Google Scholar 

  • Pandya DN, Kuypers HG (1969) Cortico-cortical connections in the rhesus monkey. Brain Res 13(1):13–36

    Article  CAS  PubMed  Google Scholar 

  • Petrides M, Pandya DN (1984) Projections to the frontal cortex from the posterior parietal region in the rhesus monkey. J Comp Neurol 228(1):105–116. doi:10.1002/cne.902280110

    Article  CAS  PubMed  Google Scholar 

  • Ramayya AG, Glasser MF, Rilling JK (2010) A DTI investigation of neural substrates supporting tool use. Cereb Cortex 20(3):507–516. doi:10.1093/cercor/bhp141

    Article  PubMed  Google Scholar 

  • Ramnani N (2012) Frontal lobe and posterior parietal contributions to the cortico-cerebellar system. Cerebellum 11(2):366–383. doi:10.1007/s12311-011-0272-3

    Article  PubMed  Google Scholar 

  • Schmahmann JD, Pandya DN (2007) The complex history of the fronto-occipital fasciculus. J Hist Neurosci 16(4):362–377. doi:10.1080/09647040600620468

    Article  PubMed  Google Scholar 

  • Thiebaut de Schotten M, Dell’Acqua F, Forkel SJ, Simmons A, Vergani F, Murphy DG, Catani M (2011a) A lateralized brain network for visuospatial attention. Nat Neurosci 14(10):1245–1246. doi:10.1038/nn.2905

    Article  CAS  PubMed  Google Scholar 

  • Thiebaut de Schotten M, Ffytche DH, Bizzi A, Dell’Acqua F, Allin M, Walshe M, Murray R, Williams SC, Murphy DG, Catani M (2011b) Atlasing location, asymmetry and inter-subject variability of white matter tracts in the human brain with MR diffusion tractography. Neuroimage 54(1):49–59. doi:10.1016/j.neuroimage.2010.07.055

    Article  PubMed  Google Scholar 

  • Thiebaut de Schotten M, Dell’Acqua F, Valabregue R, Catani M (2012) Monkey to human comparative anatomy of the frontal lobe association tracts. Cortex 48(1):82–96. doi:10.1016/j.cortex.2011.10.001

    Article  PubMed  Google Scholar 

  • Ture U, Yasargil MG, Friedman AH, Al-Mefty O (2000) Fiber dissection technique: lateral aspect of the brain. Neurosurgery 47(2):417–426 (discussion 426–417)

  • Wang Y, Fernandez-Miranda JC, Verstynen T, Pathak S, Schneider W, Yeh FC (2012) Rethinking the role of the middle longitudinal fascicle in language and auditory pathways. Cereb Cortex. doi:10.1093/cercor/bhs225

    Google Scholar 

  • Wedeen VJ, Hagmann P, Tseng WY, Reese TG, Weisskoff RM (2005) Mapping complex tissue architecture with diffusion spectrum magnetic resonance imaging. Magn Reson Med 54(6):1377–1386

    Article  PubMed  Google Scholar 

  • Yeh FC, Tseng WY (2011) NTU-90: a high angular resolution brain atlas constructed by q-space diffeomorphic reconstruction. Neuroimage 58(1):91–99. doi:10.1016/j.neuroimage.2011.06.021

    Article  PubMed  Google Scholar 

  • Yeh FC, Wedeen VJ, Tseng WY (2010) Generalized q-sampling imaging. IEEE Trans Med Imaging 29(9):1626–1635. doi:10.1109/tmi.2010.2045126

    Article  PubMed  Google Scholar 

  • Yeterian EH, Pandya DN, Tomaiuolo F, Petrides M (2012) The cortical connectivity of the prefrontal cortex in the monkey brain. Cortex 48(1):58–81. doi:10.1016/j.cortex.2011.03.004

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Conflict of interest

None to declare.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Juan C. Fernandez-Miranda.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, X., Pathak, S., Stefaneanu, L. et al. Subcomponents and connectivity of the superior longitudinal fasciculus in the human brain. Brain Struct Funct 221, 2075–2092 (2016). https://doi.org/10.1007/s00429-015-1028-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00429-015-1028-5

Keywords

Navigation