Abstract
The sledge runner fasciculus (SRF) has been recently identified as a discrete fiber tract of the occipital lobe and has been allegedly implicated in the axonal connectivity of cortical areas conveying spatial navigation and visuospatial imagery. However, detailed knowledge regarding its anatomic and tractographic morphology is lacking. We thus opted to investigate the anatomy and connectivity of the SRF through cadaveric dissections and DTI studies. Twenty normal, adult, cerebral, cadaveric hemispheres treated with the Klingler’s method were dissected through the fiber microdissection technique and 35 healthy participants from the MGH-USC Adult Diffusion Dataset (Human Connectome available dataset) underwent a tailored DTI protocol aiming to investigate the structural architecture of the SRF. SR was identified as a discrete fiber pathway, just under the U fibers of the medial occipital lobe, exhibiting a dorsomedial–ventrolateral trajectory and connecting the cortical areas of the anterior cuneus, anterior lingula, isthmus of the cingulum and posterior parahippocampal gyrus. The topography of the SR in relation to adjacent fiber pathways such as the cingulum, major forceps and stratum calcarinum is clearly delineated. Dissection and tractographic findings showed a good correspondence regarding SR topography, morphology and axonal connectivity. Our results support the hypothesis that the SRF is involved in the structural axonal connectivity of cerebral areas that strongly activate during spatial navigation and visuospatial imagery. Furthermore detailed anatomo-imaging evidence is provided on the microanatomic architecture of this newly discovered fiber tract.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Aguirre GK, D’Esposito M (1999) Topographical disorientation: a synthesis and taxonomy. Brain J Neurol 122(Pt 9):1613–1628
Alves RV, Ribas GC, Parraga RG, de Oliveira E (2012) The occipital lobe convexity sulci and gyri. J Neurosurg 116(5):1014–1023. https://doi.org/10.3171/2012.1.JNS11978
Arnts H, Kleinnijenhuis M, Kooloos JG, Schepens-Franke AN, van Cappellen van Walsum AM (2014) Combining fiber dissection, plastination, and tractography for neuroanatomical education: revealing the cerebellar nuclei and their white matter connections. Anat Sci Educ 7(1):47–55
Barrash J, Damasio H, Adolphs R, Tranel D (2000) The neuroanatomical correlates of route learning impairment. Neuropsychologia 38(6):820–836
Baydin S, Gungor A, Tanriover N, Baran O, Middlebrooks EH, Rhoton AL Jr (2017) Fiber tracts of the medial and inferior surfaces of the cerebrum. World Neurosurg 98:34–49. https://doi.org/10.1016/j.wneu.2016.05.016
Beyh A, Laguna Luque P, De Santiago Requejo F, Dell’Acqua F, Ffytche D, Catani M (2017) The medial occipital longitudinal tract: a white matter system for spatial navigation. In: Paper presented at the OHBM2017, Vancouver
Bisdas S, Bohning DE, Besenski N, Nicholas JS, Rumboldt Z (2008) Reproducibility, interrater agreement, and age-related changes of fractional anisotropy measures at 3T in healthy subjects: effect of the applied b-value. AJNR Am J Neuroradiol 29:1128–1133
Bottini G, Cappa S, Geminiani G, Sterzi R (1990) Topographic disorientation—a case report. Neuropsychologia 28(3):309–312
Bridge H, Harrold S, Holmes EA, Stokes M, Kennard C (2012) Vivid visual mental imagery in the absence of the primary visual cortex. J Neurol 259(6):1062–1070. https://doi.org/10.1007/s00415-011-6299-z
Buffalo EA, Bellgowan PS, Martin A (2006) Distinct roles for medial temporal lobe structures in memory for objects and their locations. Learn Mem 13(5):638–643. https://doi.org/10.1101/lm.251906
Catani M, de Schotten MT (2012) Introduction to diffusion imaging tractography. In: Catani M, de Schotten MT (eds) Atlas of human brain connections. Oxford University Press, New York
Catani M, Thiebaut de Schotten M (2008) A diffusion tensor imaging tractography atlas for virtual in vivo dissections. Cortex 44(8):1105–1132. https://doi.org/10.1016/j.cortex.2008.05.004
Catani M, Howard RJ, Pajevic S, Jones DK (2002) Virtual in vivo interactive dissection of white matter fasciculi in the human brain. Neuroimage 17(1):77–94
Catani M, Jones DK, Donato R, Ffytche DH (2003) Occipito-temporal connections in the human brain. Brain 126 (Pt 9):2093–2107. https://doi.org/10.1093/brain/awg203
Catani M, Jones DK, ffytche DH (2005) Perisylvian language networks of the human brain. Ann Neurol 57(1):8–16. https://doi.org/10.1002/ana.20319
Christidi F, Karavasilis E, Samiotis K, Bisdas S, Papanikolaou N (2016) Fiber tracking: a qualitative and quantitative comparison between four different software tools on the reconstruction of major white matter tracts. Eur J Radiol Open 3:153–161. https://doi.org/10.1016/j.ejro.2016.06.002
Christidi F, Karavasilis E, Zalonis I, Ferentinos P, Giavri Z, Wilde EA, Xirou S, Rentzos M, Zouvelou V, Velonakis G, Toulas P, Efstathopoulos E, Poulou L, Argyropoulos G, Athanasakos A, Zambelis T, Levin HS, Karandreas N, Kelekis N, Evdokimidis I (2017) Memory-related white matter tract integrity in amyotrophic lateral sclerosis: an advanced neuroimaging and neuropsychological study. Neurobiol Aging 49:69–78
Dammers J, Axer M, Gräßel D, Palm C, Zilles K, Amunts K, Pietrzyk U (2010) Signal enhancement in polarized light imaging by means of independent component analysis. Neuroimage 49:1241–1248
Danielian LE, Iwata NK, Thomasson DM, Floeter MK (2010) Reliability of fiber tracking measurements in diffusion tensor imaging for longitudinal study. Neuroimage 49:1572–1580
De Benedictis A, Duffau H (2011) Brain hodotopy: from esoteric concept to practical surgical applications. Neurosurgery 68(6):1709–1723. https://doi.org/10.1227/NEU.0b013e3182124690 (discussion 1723)
Descoteaux M, Poupon C (2012) Diffusion-weighted MRI. Compr Biomed Phys 3(6):81–97
Duffau H (2006) New concepts in surgery of WHO grade II gliomas: functional brain mapping, connectionism and plasticity—a review. J Neurooncol 79(1):77–115. https://doi.org/10.1007/s11060-005-9109-6
Duffau H (2011) Brain hodotopy: new insights provided by intrasurgical mapping. In: Duffau H (ed) Brain mapping. Springer, Wien, pp 335–347
Duffau H (2015) Stimulation mapping of white matter tracts to study brain functional connectivity. Nat Rev Neurol 11(5):255–265. https://doi.org/10.1038/nrneurol.2015.51
Duffau H (2017) Hodotopy, neuroplasticity and diffuse gliomas. Neurochirurgie 63(3):259–265. https://doi.org/10.1016/j.neuchi.2016.12.001
Duffau H, Capelle L, Sichez N, Denvil D, Lopes M, Sichez JP, Bitar A, Fohanno D (2002) Intraoperative mapping of the subcortical language pathways using direct stimulations. An anatomo-functional study. Brain 125(Pt 1):199–214
Duffau H, Gatignol P, Mandonnet E, Peruzzi P, Tzourio-Mazoyer N, Capelle L (2005) New insights into the anatomo-functional connectivity of the semantic system: a study using cortico–subcortical electrostimulations. Brain 128(Pt 4):797–810. https://doi.org/10.1093/brain/awh423
Duffau H, Moritz-Gasser S, Mandonnet E (2014) A re-examination of neural basis of language processing: proposal of a dynamic hodotopical model from data provided by brain stimulation mapping during picture naming. Brain Lang 131:1–10. https://doi.org/10.1016/j.bandl.2013.05.011
Epstein RA (2008) Parahippocampal and retrosplenial contributions to human spatial navigation. Trends Cogn Sci 12(10):388–396. https://doi.org/10.1016/j.tics.2008.07.004
Epstein R, Kanwisher N (1998) A cortical representation of the local visual environment. Nature 392(6676):598–601. https://doi.org/10.1038/33402
Epstein R, Deyoe EA, Press DZ, Rosen AC, Kanwisher N (2001) Neuropsychological evidence for a topographical learning mechanism in parahippocampal cortex. Cogn Neuropsychol 18(6):481–508. https://doi.org/10.1080/02643290125929
Epstein RA, Higgins JS, Jablonski K, Feiler AM (2007a) Visual scene processing in familiar and unfamiliar environments. J Neurophysiol 97(5):3670–3683. https://doi.org/10.1152/jn.00003.2007
Epstein RA, Parker WE, Feiler AM (2007b) Where am I now? Distinct roles for parahippocampal and retrosplenial cortices in place recognition. J Neurosci 27(23):6141–6149. https://doi.org/10.1523/JNEUROSCI.0799-07.2007
Epstein RA, Patai EZ, Julian JB, Spiers HJ (2017) The cognitive map in humans: spatial navigation and beyond. Nat Neurosci 20(11):1504–1513. https://doi.org/10.1038/nn.4656
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. https://doi.org/10.1227/01.neu.0000333767.05328.49 (discussion 1026–1028)
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. https://doi.org/10.3171/JNS/2008/108/4/0764
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. https://doi.org/10.1227/NEU.0b013e3182592faa
Forkel SJ, Thiebaut de Schotten M, Kawadler JM, Dell’Acqua F, Danek A, Catani M (2014) The anatomy of fronto-occipital connections from early blunt dissections to contemporary tractography. Cortex 56:73–84. https://doi.org/10.1016/j.cortex.2012.09.005
Froeling M, Pullens P, Leemans A (2016) DTI analysis methods: region of interest analysis. In: Van Hecke W et al (eds) Diffusion tensor imaging. Springer Science + Business Media, New York
Goergen CJ, Radhakrishnan H, Sakadžić S, Mandeville ET, Lo EH, Sosnovik DE, Srinivasan VJ (2012) Optical coherence tractography using intrinsic contrast. Opt Lett 37:3882–3884
Goh JO, Siong SC, Park D, Gutchess A, Hebrank A, Chee MW (2004) Cortical areas involved in object, background, and object-background processing revealed with functional magnetic resonance adaptation. J Neurosci 24(45):10223–10228. https://doi.org/10.1523/JNEUROSCI.3373-04.2004
Gong G, He Y, Concha L, Lebel C, Gross DW, Evans AC, Beaulieu C (2009) Mapping anatomical connectivity patterns of human cerebral cortex using in vivo diffusion tensor imaging tractography. Cereb Cortex 19(3):524–536. https://doi.org/10.1093/cercor/bhn102
Gungor A, Baydin S, Middlebrooks EH, Tanriover N, Isler C, Rhoton AL Jr (2017) The white matter tracts of the cerebrum in ventricular surgery and hydrocephalus. J Neurosurg 126(3):945–971. https://doi.org/10.3171/2016.1.JNS152082
Hagmann P, Kurant M, Gigandet X, Thiran P, Wedeen VJ, Meuli R, Thiran JP (2007) Mapping human whole-brain structural networks with diffusion MRI. PLoS One 2(7):e597. https://doi.org/10.1371/journal.pone.0000597
Hecaen H, Tzortzis C, Rondot P (1980) Loss of topographic memory with learning deficits. Cortex 16(4):525–542
Heiervang E, Behrens TEJ, Mackay CE, Robson MD, Johansen-Berg H (2006) Between session reproducibility and between subject variability of diffusion MR and tractography measures. Neuroimage 33:867–877
Henderson JM, Larson CL, Zhu DC (2008) Full scenes produce more activation than close-up scenes and scene-diagnostic objects in parahippocampal and retrosplenial cortex: an fMRI study. Brain Cogn 66(1):40–49. https://doi.org/10.1016/j.bandc.2007.05.001
Honey CJ, Kotter R, Breakspear M, Sporns O (2007) Network structure of cerebral cortex shapes functional connectivity on multiple time scales. Proc Natl Acad Sci USA 104(24):10240–10245. https://doi.org/10.1073/pnas.0701519104
Ino T, Inoue Y, Kage M, Hirose S, Kimura T, Fukuyama H (2002) Mental navigation in humans is processed in the anterior bank of the parieto-occipital sulcus. Neurosci Lett 322(3):182–186
Ino T, Doi T, Hirose S, Kimura T, Ito J, Fukuyama H (2007) Directional disorientation following left retrosplenial hemorrhage: a case report with fMRI studies. Cortex 43(2):248–254
Ito K, Sasaki M, Takahashi J, Uwano I, Yamashita F, Higuchi S, Goodwin J, Harada T, Kudo K, Terayama Y (2015) Detection of early changes in the parahippocampal and posterior cingulum bundles during mild cognitive impairment by using high-resolution multi-parametric diffusion tensor imaging. Psychiatry Res Neuroimaging 231(3):346–352
Janzen G, van Turennout M (2004) Selective neural representation of objects relevant for navigation. Nature Neurosci 7(6):673–677. https://doi.org/10.1038/nn1257
Johansen-Berg H, Behrens TE (2006) Just pretty pictures? What diffusion tractography can add in clinical neuroscience. Curr Opin Neurol 19(4):379–385. https://doi.org/10.1097/01.wco.0000236618.82086.01
Johansen-Berg H, Rushworth MF (2009) Using diffusion imaging to study human connectional anatomy. Annu Rev Neurosci 32:75–94. https://doi.org/10.1146/annurev.neuro.051508.135735
Jones DK, Cercignani M (2010) Twenty-five pitfalls in the analysis of diffusion MRI data. NMR Biomed 23:803–820
Jones DK, Christiansen KF, Chapman RJ, Aggleton JP (2013a) Distinct subdivisions of the cingulum bundle revealed by diffusion MRI fibre tracking: implications for neuropsychological investigations. Neuropsychologia 51(1):67–78
Jones DK, Knösche TR, Turner R (2013b) White matter integrity, fiber count, and other fallacies: the do’s and don’ts of diffusion MRI. Neuroimage 73:239–254
Karavasilis E, Christidi F, Velonakis G, Giavri Z, Kelekis NL, Efstathopoulos EP, Evdokimidis I, Dellatolas G (2018) Ipsilateral and contralateral cerebro cerebellar white matter connections: a diffusion tensor imaging study in healthy adults. J Neuroradiol. https://doi.org/10.1016/j.neurad.2018.07.004
Katayama K, Takahashi N, Ogawara K, Hattori T (1999) Pure topographical disorientation due to right posterior cingulate lesion. Cortex 35(2):279–282
Keil B, Blau JN, Biber S, Hoecht P, Tountcheva V, Setsompop K, Triantafyllou C, Wald LL (2013) A 64-channel 3T array coil for accelerated brain. MRI Magn Reson Med 70:248–258
Kier EL, Staib LH, Davis LM, Bronen RA (2004a) MR imaging of the temporal stem: anatomic dissection tractography of the uncinate fasciculus, inferior occipitofrontal fasciculus, and Meyer’s loop of the optic radiation. AJNR Am J Neuroradiol 25(5):677–691
Kier EL, Staib LH, Davis LM, Bronen RA (2004b) Anatomic dissection tractography: a new method for precise MR localization of white matter tracts. Am J Neuroradiol 25(5):670–676
King JA, Burgess N, Hartley T, Vargha-Khadem F, O’Keefe J (2002) Human hippocampus and viewpoint dependence in spatial memory. Hippocampus 12(6):811–820. https://doi.org/10.1002/hipo.10070
Klingler J (1935) Erleichterung der makrokopischen Präparation des Gehirns durch den Gefrierprozess. Orell Füssli, Zurich
Klingler J, Ludwig E (1956) Atlas Cerebri Humani. Karger, Basel
Knauff M, Kassubek J, Mulack T, Greenlee MW (2000) Cortical activation evoked by visual mental imagery as measured by fMRI. Neuroreport 11(18):3957–3962
Koutsarnakis C, Liakos F, Kalyvas AV, Sakas DE, Stranjalis G (2015) A laboratory manual for stepwise cerebral white matter fiber dissection. World Neurosurg 84(2):483–493. https://doi.org/10.1016/j.wneu.2015.04.018
Koutsarnakis C, Liakos F, Liouta E, Themistoklis K, Sakas D, Stranjalis G (2016) The cerebral isthmus: fiber tract anatomy, functional significance, and surgical considerations. J Neurosurg 124(2):450–462. https://doi.org/10.3171/2015.3.JNS142680
Koutsarnakis C, Liakos F, Kalyvas AV, Komaitis S, Stranjalis G (2017a) Letter to the Editor: White matter fiber tract architecture and ventricular surgery. J Neurosurg 126(4):1368–1371. https://doi.org/10.3171/2016.9.JNS162239
Koutsarnakis C, Liakos F, Kalyvas AV, Skandalakis GP, Komaitis S, Christidi F, Karavasilis E, Liouta E, Stranjalis G (2017b) The superior frontal transsulcal approach to the anterior ventricular system: exploring the sulcal and subcortical anatomy using anatomic dissections and diffusion tensor imaging tractography. World Neurosurg 106:339–354
Koutsarnakis C, Kalyvas AV, Komaitis S, Liakos F, Skandalakis GP, Anagnostopoulos C, Stranjalis G (2018) Defining the relationship of the optic radiation to the roof and floor of the ventricular atrium: a focused microanatomical study J Neurosurg:1–12 https://doi.org/10.3171/2017.10.JNS171836
Kravitz DJ, Saleem KS, Baker CI, Mishkin M (2011) A new neural framework for visuospatial processing. Nat Rev Neurosci 12(4):217–230. https://doi.org/10.1038/nrn3008
Le Bihan D, Poupon C, Amadon A, Lethimonnier F (2006) Artifacts and pitfalls in diffusion MRI. J Magn Reson Imaging JMRI 24(3):478–488. https://doi.org/10.1002/jmri.20683
Lee AC, Buckley MJ, Pegman SJ, Spiers H, Scahill VL, Gaffan D, Bussey TJ, Davies RR, Kapur N, Hodges JR, Graham KS (2005) Specialization in the medial temporal lobe for processing of objects and scenes. Hippocampus 15(6):782–797. https://doi.org/10.1002/hipo.20101
Magnain C et al (2014) Blockface histology with optical coherence tomography: a comparison with Nissl staining. Neuroimage 84:524–533. https://doi.org/10.1016/j.neuroimage.2013.08.072
Maguire EA, Frackowiak RS, Frith CD (1997) Recalling routes around london: activation of the right hippocampus in taxi drivers. J Neurosci 17(18):7103–7110
Malykhin N, Concha L, Seres P, Beaulieu C, Coupland NJ (2008) Diffusion tensor imaging tractography and reliability analysis for limbic and paralimbic white matter tracts. Psychiatry Res 164(2):132–142. https://doi.org/10.1016/j.pscychresns.2007.11.007
Mamata H, Mamata Y, Westin CF, Shenton ME, Kikinis R, Jolesz FA, Maier SE (2002) High-resolution line scan diffusion tensor MR imaging of white matter fiber tract anatomy. AJNR Am J Neuroradiol 23(1):67–75
Mandonnet E, Capelle L, Duffau H (2006) Extension of paralimbic low grade gliomas: toward an anatomical classification based on white matter invasion patterns. J Neuro-Oncol 78(2):179–185. https://doi.org/10.1007/s11060-005-9084-y
Martino J, Vergani F, Robles SG, Duffau H (2010) New insights into the anatomic dissection of the temporal stem with special emphasis on the inferior fronto-occipital fasciculus: implications in surgical approach to left mesiotemporal and temporoinsular structures. Neurosurgery 66(3 Suppl Operative):4–12. https://doi.org/10.1227/01.NEU.0000348564.28415.FA
Martino J, De Witt Hamer PC, Berger MS et al (2013) Analysis of the subcomponents and cortical terminations of the perisylvian superior longitudinal fasciculus: a fiber dissection and DTI tractography study. Brain Struct Funct 218:105–121
Mori S, Zhang J (2006) Principles of diffusion tensor imaging and its applications to basic neuroscience research. Neuron 51(5):527–539
Mori S, Crain BJ, Chacko VP, van Zijl PC (1999) Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging. Ann Neurol 45(2):265–269
Mori S, Wakana S, Van Zijl PC, Nagae-Poetscher L (2005) MRI atlas of human white matter. Elsevier, Oxford
Nimsky C, Bauer M, Carl B (2016) Merits and limits of tractography techniques for the uninitiated. In: Schramm J (ed) Advances and technical standards in neurosurgery. Advances and technical standards in neurosurgery, vol 43. Springer, Cham
O’Craven KM, Kanwisher N (2000) Mental imagery of faces and places activates corresponding stiimulus-specific brain regions. J Cogn Neurosci 12(6):1013–1023
Oouchi H, Yamada K, Sakai K, Kizu O, Kubota T, Ito H, Nishimura T (2007) Diffusion anisotropy measurement of brain white matter is affected by voxel size: underestimation occurs in areas with crossing fibers. AJNR Am J Neuroradiol 28(6):1102–1106. https://doi.org/10.3174/ajnr.A0488
Osawa A, Maeshima S, Kunishio K (2008) Topographic disorientation and amnesia due to cerebral hemorrhage in the left retrosplenial region. Eur Neurol 59(1–2):79–82. https://doi.org/10.1159/000109572
Pallis CA (1955) Impaired identification of faces and places with agnosia for colours; report of a case due to cerebral embolism. J Neurol Neurosurg Psychiatry 18(3):218–224
Palm C et al (2010) Towards ultra-high resolution fibre tract mapping of the human brain-registration of polarised light images and reorientation of fibre vectors. Front Hum Neurosci 4:9
Pascalau R, Stănilă RP, Sfrângeu S, Szabo B (2018) Anatomy of the limbic white matter tracts as revealed by fiber dissection and tractography. World Neurosurg 113:e672–e689. https://doi.org/10.1016/j.wneu.2018.02.121
Peltier J, Verclytte S, Delmaire C, Deramond H, Pruvo JP, Le Gars D, Godefroy O (2010a) Microsurgical anatomy of the ventral callosal radiations: new destination, correlations with diffusion tensor imaging fiber-tracking, and clinical relevance. J Neurosurg 112(3):512–519. https://doi.org/10.3171/2009.6.JNS081712
Peltier J, Verclytte S, Delmaire C, Pruvo JP, Godefroy O, Le Gars D (2010b) Microsurgical anatomy of the temporal stem: clinical relevance and correlations with diffusion tensor imaging fiber tracking. J Neurosurg 112(5):1033–1038. https://doi.org/10.3171/2009.6.JNS08132
Petrides M (2012) The human cerebral cortex: an MRI atlas of the sulci and gyri in MNI stereotaxic space. Elsevier/Academic Press, New York
Ploner CJ, Gaymard BM, Rivaud-Pechoux S, Baulac M, Clemenceau S, Samson S, Pierrot-Deseilligny C (2000) Lesions affecting the parahippocampal cortex yield spatial memory deficits in humans. Cereb Cortex 10(12):1211–1216
Powell HW, Guye M, Parker GJ, Symms MR, Boulby P, Koepp MJ, Barker GJ, Duncan JS (2004) Noninvasive in vivo demonstration of the connections of the human parahippocampal gyrus. Neuroimage 22(2):740–747. https://doi.org/10.1016/j.neuroimage.2004.01.011
Rosenbaum RS, Ziegler M, Winocur G, Grady CL, Moscovitch M (2004) “I have often walked down this street before”: fMRI studies on the hippocampus and other structures during mental navigation of an old environment. Hippocampus 14(7):826–835. https://doi.org/10.1002/hipo.10218
Sachs H (1892) Das Hemisphärenmark des menschlichen Grosshirns: Der Hinterhauptlappen/von Heinrich Sachs. Thieme, Leipzig
Sarubbo S, Benedictis A, Maldonado IL et al (2013) Frontal terminations for the inferior fronto-occipital fascicle: anatomical dissection, DTI study and functional considerations on a multicomponent bundle. Brain Struct Funct 218:21–37
Schmahmann J, Pandya D (2009) Fiber pathways of the brain. OUP, Oxford
Setsompop K, Kimmlingen R, Eberlein E, Witzel T, Cohen-Adad J, McNab JA, Keil B, Tisdall MD, Hoecht P, Dietz P, Cauley SF, Tountcheva V, Matschl V, Lenz VH, Heberlein K, Potthast A, Thein H, Van Horn J, Toga A, Schmitt F, Lehne D, Rosen BR, Wedeen V, Wald LL (2013) Pushing the limits of in vivo diffusion MRI for the Human Connectome Project. Neuroimage 80:220–233
Seunarine KK, Alexander DC (2014) Multiple fibers: beyond the diffusion tensor. In: Johansen-Berg H, Behrens TE (eds) Diffusion MRI, 2nd edn. Elsevier, New York, USA, pp 105–123
Shrout PE, Fleiss JL (1979) Intraclass correlations: uses in assessing rater reliability. Psychol Bull 86(2):420–428
Silva SM, Andrade JP (2016) Neuroanatomy: the added value of the Klingler method. Ann Anat 208:187–193
Spiers HJ, Maguire EA (2006) Thoughts, behaviour, and brain dynamics during navigation in the real world. Neuroimage 31(4):1826–1840. https://doi.org/10.1016/j.neuroimage.2006.01.037
Spiers HJ, Maguire EA (2007) The neuroscience of remote spatial memory: a tale of two cities. Neuroscience 149(1):7–27. https://doi.org/10.1016/j.neuroscience.2007.06.056
Sugiura M, Shah NJ, Zilles K, Fink GR (2005) Cortical representations of personally familiar objects and places: functional organization of the human posterior cingulate cortex. J Cogn Neurosci 17(2):183–198. https://doi.org/10.1162/0898929053124956
Takahashi N, Kawamura M, Shiota J, Kasahata N, Hirayama K (1997) Pure topographic disorientation due to right retrosplenial lesion. Neurology 49(2):464–469
Takao H, Hayashi N, Kabasawa H, Ohtomo K (2012) Effect of scanner in longitudinal diffusion tensor imaging studies. Hum Brain Mapp 33:466–477
Thiebaut de Schotten M, Urbanski M, Valabregue R, Bayle DJ, Volle E (2014) Subdivision of the occipital lobes: an anatomical and functional MRI connectivity study. Cortex 56:121–137. https://doi.org/10.1016/j.cortex.2012.12.007
Thomas C, Ye FQ, Irfanoglu MO et al (2014) Anatomical accuracy of brain connections derived from diffusion MRI tractography is inherently limited. Proc Natl Acad Sci 111:16574–16579
Tournier J, Calamante F, Connelly A (2012) MRtrix: diffusion tractography in crossing fiber regions. Int J Imaging Syst Technol 22(1):53–66
Ture U, Yasargil MG, Friedman AH, Al-Mefty O (2000) Fiber dissection technique: lateral aspect of the brain. Neurosurgery 47(2):417–426 (discussion 417–426)
Vann SD, Aggleton JP, Maguire EA (2009) What does the retrosplenial cortex do? Nat Rev Neurosci 10(11):792–802. https://doi.org/10.1038/nrn2733
Veenith TV et al (2013) Inter subject variability and reproducibility of diffusion tensor imaging within and between different imaging sessions. PLoS One 8:e65941. https://doi.org/10.1371/journal.pone.0065941
Vergani F, Mahmood S, Morris CM, Mitchell P, Forkel SJ (2014) Intralobar fibres of the occipital lobe: a post mortem dissection study. Cortex 56:145–156. https://doi.org/10.1016/j.cortex.2014.03.002
Vos SB, Jones DK, Viergever MA, Leemans A (2011) Partial volume effect as a hidden covariate in DTI analyses. Neuroimage 55(4):1566–1576. https://doi.org/10.1016/j.neuroimage.2011.01.048
Wakana S, Caprihan A, Panzenboeck MM, Fallon JH, Perry M, Gollub RL, Hua K, Zhang J, Jiang H, Dubey P, Blitz A, van Zijl P, Mori S (2007) Reproducibility of quantitative tractography methods applied to cerebral white matter. Neuroimage 36(3):630–644. https://doi.org/10.1016/j.neuroimage.2007.02.049
Wang H et al (2011) Reconstructing micrometer-scale fiber pathways in the brain: multi-contrast optical coherence tomography based tractography. Neuroimage 58:984–992
Whittingstall K, Bernier M, Houde JC, Fortin D, Descoteaux M (2014) Structural network underlying visuospatial imagery in humans. Cortex 56:85–98. https://doi.org/10.1016/j.cortex.2013.02.004
Wolbers T, Buchel C (2005) Dissociable retrosplenial and hippocampal contributions to successful formation of survey representations. J Neurosci 25(13):3333–3340. https://doi.org/10.1523/JNEUROSCI.4705-04.2005
Wu Y, Sun D, Wang Y, Wang Y, Ou S (2016) Segmentation of the cingulum bundle in the human brain: a new perspective based on DSI tractography and fiber dissection study. Front Neuroanat 10:84
Zemmoura I, Blanchard E, Raynal PI, Rousselot-Denis C, Destrieux C, Velut S (2016) How Klingler’s dissection permits exploration of brain structural connectivity? An electron microscopy study of human white matter. Brain Struct Funct 221(5):2477–2486
Funding
No funding was received for this study.
Author information
Authors and Affiliations
Contributions
Conception and design: CK, AVK. Acquisition of data: AVK, CK, GPS, FC, EK, NK, GV. Analysis and interpretation of data: AVK, CK, FC, EK, NK, FL, JE, ZG. Drafting the article: CK, AVK, FC, EK. Critically revising the article: CK, AVK, SK, TK, FL, JE, GS. Reviewed submitted version of manuscript: All authors. Administrative technical, material support: GS. Study supervision: CK.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest regarding the materials or methods used in the current study or the findings specified in this paper.
Informed consent
Informed consent was obtained from all participants included in the study.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Koutsarnakis, C., Kalyvas, A.V., Skandalakis, G.P. et al. Sledge runner fasciculus: anatomic architecture and tractographic morphology. Brain Struct Funct 224, 1051–1066 (2019). https://doi.org/10.1007/s00429-018-01822-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00429-018-01822-4