The frontal longitudinal system as revealed through the fiber microdissection technique: structural evidence underpinning the direct connectivity of the prefrontal-premotor circuitry

View More View Less
  • 1 Athens Microneurosurgery Laboratory, National and Kapodistrian University of Athens School of Medicine, Athens
  • 2 Department of Neurosurgery, National and Kapodistrian University of Athens
  • 3 Department of Anatomy, National and Kapodistrian University of Athens School of Medicine, Athens, Greece
  • 4 Department of Clinical Neurosciences, Western General Hospital, Edinburgh
  • 5 Department of Clinical Neurosciences, Edinburgh Microneurosurgery Education Laboratory, Edinburgh, UK; and
  • 6 Hellenic Center for Neurosurgical Research, “Petros Kokkalis,” Athens, Greece
Restricted access

Purchase Now

USD  $45.00

JNS + Pediatrics - 1 year subscription bundle (Individuals Only)

USD  $505.00

JNS + Pediatrics + Spine - 1 year subscription bundle (Individuals Only)

USD  $600.00
Print or Print + Online

OBJECTIVE

The purpose of this study was to investigate the morphology, connectivity, and correlative anatomy of the longitudinal group of fibers residing in the frontal area, which resemble the anterior extension of the superior longitudinal fasciculus (SLF) and were previously described as the frontal longitudinal system (FLS).

METHODS

Fifteen normal adult formalin-fixed cerebral hemispheres collected from cadavers were studied using the Klingler microdissection technique. Lateral to medial dissections were performed in a stepwise fashion starting from the frontal area and extending to the temporoparietal regions.

RESULTS

The FLS was consistently identified as a fiber pathway residing just under the superficial U-fibers of the middle frontal gyrus or middle frontal sulcus (when present) and extending as far as the frontal pole. The authors were able to record two different configurations: one consisting of two distinct, parallel, longitudinal fiber chains (13% of cases), and the other consisting of a single stem of fibers (87% of cases). The fiber chains’ cortical terminations in the frontal and prefrontal area were also traced. More specifically, the FLS was always recorded to terminate in Brodmann areas 6, 46, 45, and 10 (premotor cortex, dorsolateral prefrontal cortex, pars triangularis, and frontal pole, respectively), whereas terminations in Brodmann areas 4 (primary motor cortex), 47 (pars orbitalis), and 9 were also encountered in some specimens. In relation to the SLF system, the FLS represented its anterior continuation in the majority of the hemispheres, whereas in a few cases it was recorded as a completely distinct tract. Interestingly, the FLS comprised shorter fibers that were recorded to interconnect exclusively frontal areas, thus exhibiting different fiber architecture when compared to the long fibers forming the SLF.

CONCLUSIONS

The current study provides consistent, focused, and robust evidence on the morphology, architecture, and correlative anatomy of the FLS. This fiber system participates in the axonal connectivity of the prefrontal-premotor cortices and allegedly subserves cognitive-motor functions. Based in the SLF hypersegmentation concept that has been advocated by previous authors, the FLS should be approached as a distinct frontal segment within the superior longitudinal system.

ABBREVIATIONS BA = Brodmann area; DLPFC = dorsolateral prefrontal cortex; DTI = diffusion tensor imaging; FAT = frontal aslant tract; FLS = frontal longitudinal system; SLF = superior Longitudinal fasciculus.

JNS + Pediatrics - 1 year subscription bundle (Individuals Only)

USD  $505.00

JNS + Pediatrics + Spine - 1 year subscription bundle (Individuals Only)

USD  $600.00

Contributor Notes

Correspondence Christos Koutsarnakis: Evangelismos Hospital, University of Athens, Athens, Greece. ckouts@hotmail.co.uk.

INCLUDE WHEN CITING Published online October 4, 2019; DOI: 10.3171/2019.6.JNS191224.

S.K. and A.V.K. contributed equally to this study.

Disclosures The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

  • 1

    Abe M, Hanakawa T, Takayama Y, Kuroki C, Ogawa S, Fukuyama H: Functional coupling of human prefrontal and premotor areas during cognitive manipulation. J Neurosci 27:34293438, 2007

    • Search Google Scholar
    • Export Citation
  • 2

    Baker CM, Burks JD, Briggs RG, Conner AK, Glenn CA, Morgan JP, : A connectomic atlas of the human cerebrum—Chapter 2: The lateral frontal lobe. Oper Neurosurg (Hagerstown) 15 (Suppl 1):S10S74, 2018

    • Search Google Scholar
    • Export Citation
  • 3

    Bernal B, Altman N: The connectivity of the superior longitudinal fasciculus: a tractography DTI study. Magn Reson Imaging 28:217225, 2010

    • Search Google Scholar
    • Export Citation
  • 4

    Bozkurt B, Yagmurlu K, Middlebrooks EH, Cayci Z, Cevik OM, Karadag A, : Fiber connections of the supplementary motor area revisited: methodology of fiber dissection, DTI, and three dimensional documentation. J Vis Exp (123):55681, 2017

    • Search Google Scholar
    • Export Citation
  • 5

    Catani M, Dell’acqua F, Vergani F, Malik F, Hodge H, Roy P, : Short frontal lobe connections of the human brain. Cortex 48:273291, 2012

    • Search Google Scholar
    • Export Citation
  • 6

    Chouinard PA, Paus T: The primary motor and premotor areas of the human cerebral cortex. Neuroscientist 12:143152, 2006

  • 7

    Conner AK, Briggs RG, Rahimi M, Sali G, Baker CM, Burks JD, : A connectomic atlas of the human cerebrum—Chapter 10: Tractographic description of the superior longitudinal fasciculus. Oper Neurosurg (Hagerstown) 15 (Suppl 1):S407S422, 2018

    • Search Google Scholar
    • Export Citation
  • 8

    Dammers J, Axer M, Grässel D, Palm C, Zilles K, Amunts K, : Signal enhancement in polarized light imaging by means of independent component analysis. Neuroimage 49:12411248, 2010

    • Search Google Scholar
    • Export Citation
  • 9

    Desrochers TM, Chatham CH, Badre D: The necessity of rostrolateral prefrontal cortex for higher-level sequential behavior. Neuron 87:13571368, 2015

    • Search Google Scholar
    • Export Citation
  • 10

    Duque J, Labruna L, Verset S, Olivier E, Ivry RB: Dissociating the role of prefrontal and premotor cortices in controlling inhibitory mechanisms during motor preparation. J Neurosci 32:806816, 2012

    • Search Google Scholar
    • Export Citation
  • 11

    Goergen CJ, Radhakrishnan H, Sakadžić S, Mandeville ET, Lo EH, Sosnovik DE, : Optical coherence tractography using intrinsic contrast. Opt Lett 37:38823884, 2012

    • Search Google Scholar
    • Export Citation
  • 12

    Hanakawa T: Rostral premotor cortex as a gateway between motor and cognitive networks. Neurosci Res 70:144154, 2011

  • 13

    Hardwick RM, Rottschy C, Miall RC, Eickhoff SB: A quantitative meta-analysis and review of motor learning in the human brain. Neuroimage 67:283297, 2013

    • Search Google Scholar
    • Export Citation
  • 14

    Hoshi E: Functional specialization within the dorsolateral prefrontal cortex: a review of anatomical and physiological studies of non-human primates. Neurosci Res 54:7384, 2006

    • Search Google Scholar
    • Export Citation
  • 15

    Kamali A, Flanders AE, Brody J, Hunter JV, Hasan KM: Tracing superior longitudinal fasciculus connectivity in the human brain using high resolution diffusion tensor tractography. Brain Struct Funct 219:269281, 2014

    • Search Google Scholar
    • Export Citation
  • 16

    Klingler J: Erleichterung der makrokopischen Präparation des Gehirns durch den Gefrierprozess. Schweiz Arch Neurol Psych 36:247256, 1935

    • Search Google Scholar
    • Export Citation
  • 17

    Komaitis S, Skandalakis GP, Kalyvas AV, Drosos E, Lani E, Emelifeonwu J, : Dorsal component of the superior longitudinal fasciculus revisited: novel insights from a focused fiber dissection study. J Neurosurg [epub ahead of print March 1, 2019; DOI: 10.3171/2018.11.JNS182908]

    • Search Google Scholar
    • Export Citation
  • 18

    Koutsarnakis C, Kalyvas AV, Komaitis S, Liakos F, Skandalakis GP, Anagnostopoulos C, : Defining the relationship of the optic radiation to the roof and floor of the ventricular atrium: a focused microanatomical study. J Neurosurg 130:17281739, 2019

    • Search Google Scholar
    • Export Citation
  • 19

    Koutsarnakis C, Kalyvas AV, Skandalakis GP, Karavasilis E, Christidi F, Komaitis S, : Sledge runner fasciculus: anatomic architecture and tractographic morphology. Brain Struct Funct 224:10511066, 2019

    • Search Google Scholar
    • Export Citation
  • 20

    Koutsarnakis C, Liakos F, Kalyvas AV, Sakas DE, Stranjalis G: A laboratory manual for stepwise cerebral white matter fiber dissection. World Neurosurg 84:483493, 2015

    • Search Google Scholar
    • Export Citation
  • 21

    Koutsarnakis C, Liakos F, Liouta E, Themistoklis K, Sakas D, Stranjalis G: The cerebral isthmus: fiber tract anatomy, functional significance, and surgical considerations. J Neurosurg 124:450462, 2016

    • Search Google Scholar
    • Export Citation
  • 22

    Le Bihan D, Poupon C, Amadon A, Lethimonnier F: Artifacts and pitfalls in diffusion MRI. J Magn Reson Imaging 24:478488, 2006

  • 23

    Lee JH, van Donkelaar P: The human dorsal premotor cortex generates on-line error corrections during sensorimotor adaptation. J Neurosci 26:33303334, 2006

    • Search Google Scholar
    • Export Citation
  • 24

    Levy BJ, Wagner AD: Cognitive control and right ventrolateral prefrontal cortex: reflexive reorienting, motor inhibition, and action updating. Ann N Y Acad Sci 1224:4062, 2011

    • Search Google Scholar
    • Export Citation
  • 25

    Lu MT, Preston JB, Strick PL: Interconnections between the prefrontal cortex and the premotor areas in the frontal lobe. J Comp Neurol 341:375392, 1994

    • Search Google Scholar
    • Export Citation
  • 26

    Magnain C, Augustinack JC, Reuter M, Wachinger C, Frosch MP, Ragan T, : Blockface histology with optical coherence tomography: a comparison with Nissl staining. Neuroimage 84:524533, 2014

    • Search Google Scholar
    • Export Citation
  • 27

    Makris N, Kennedy DN, McInerney S, Sorensen AG, Wang R, Caviness VS Jr, : Segmentation of subcomponents within the superior longitudinal fascicle in humans: a quantitative, in vivo, DT-MRI study. Cereb Cortex 15:854869, 2005

    • Search Google Scholar
    • Export Citation
  • 28

    Martino J, De Lucas EM: Subcortical anatomy of the lateral association fascicles of the brain: a review. Clin Anat 27:563569, 2014

  • 29

    Martino J, De Witt Hamer PC, Berger MS, Lawton MT, Arnold CM, de Lucas EM, : Analysis of the subcomponents and cortical terminations of the perisylvian superior longitudinal fasciculus: a fiber dissection and DTI tractography study. Brain Struct Funct 218:105121, 2013

    • Search Google Scholar
    • Export Citation
  • 30

    Mayka MA, Corcos DM, Leurgans SE, Vaillancourt DE: Three-dimensional locations and boundaries of motor and premotor cortices as defined by functional brain imaging: a meta-analysis. Neuroimage 31:14531474, 2006

    • Search Google Scholar
    • Export Citation
  • 31

    Palm C, Axer M, Gräßel D, Dammers J, Lindemeyer J, Zilles K, : 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, 2010

    • Search Google Scholar
    • Export Citation
  • 32

    Pilacinski A, Wallscheid M, Lindner A: Human posterior parietal and dorsal premotor cortex encode the visual properties of an upcoming action. PLoS One 13:e0198051, 2018

    • Search Google Scholar
    • Export Citation
  • 33

    Preuss TM, Stepniewska I, Kaas JH: Movement representation in the dorsal and ventral premotor areas of owl monkeys: a microstimulation study. J Comp Neurol 371:649676, 1996

    • Search Google Scholar
    • Export Citation
  • 34

    Rizzolatti G, Fogassi L, Gallese V: Motor and cognitive functions of the ventral premotor cortex. Curr Opin Neurobiol 12:149154, 2002

    • Search Google Scholar
    • Export Citation
  • 35

    Sarubbo S, De Benedictis A, Maldonado IL, Basso G, Duffau H: Frontal terminations for the inferior fronto-occipital fascicle: anatomical dissection, DTI study and functional considerations on a multi-component bundle. Brain Struct Funct 218:2137, 2013

    • Search Google Scholar
    • Export Citation
  • 36

    Schmahmann JD, Smith EE, Eichler FS, Filley CM: Cerebral white matter: neuroanatomy, clinical neurology, and neurobehavioral correlates. Ann N Y Acad Sci 1142:266309, 2008

    • Search Google Scholar
    • Export Citation
  • 37

    Schubotz RI, Anwander A, Knösche TR, von Cramon DY, Tittgemeyer M: Anatomical and functional parcellation of the human lateral premotor cortex. Neuroimage 50:396408, 2010

    • Search Google Scholar
    • Export Citation
  • 38

    Schubotz RI, von Cramon DY: Functional-anatomical concepts of human premotor cortex: evidence from fMRI and PET studies. Neuroimage 20 (Suppl 1):S120S131, 2003

    • Search Google Scholar
    • Export Citation
  • 39

    Simon SR, Meunier M, Piettre L, Berardi AM, Segebarth CM, Boussaoud D: Spatial attention and memory versus motor preparation: premotor cortex involvement as revealed by fMRI. J Neurophysiol 88:20472057, 2002

    • Search Google Scholar
    • Export Citation
  • 40

    Thomas C, Ye FQ, Irfanoglu MO, Modi P, Saleem KS, Leopold DA, : Anatomical accuracy of brain connections derived from diffusion MRI tractography is inherently limited. Proc Natl Acad Sci U S A 111:1657416579, 2014

    • Search Google Scholar
    • Export Citation
  • 41

    Vos SB, Jones DK, Viergever MA, Leemans A: Partial volume effect as a hidden covariate in DTI analyses. Neuroimage 55:15661576, 2011

  • 42

    Wang H, Black AJ, Zhu J, Stigen TW, Al-Qaisi MK, Netoff TI, : Reconstructing micrometer-scale fiber pathways in the brain: multi-contrast optical coherence tomography based tractography. Neuroimage 58:984992, 2011

    • Search Google Scholar
    • Export Citation
  • 43

    Wang X, Pathak S, Stefaneanu L, Yeh FC, Li S, Fernandez-Miranda JC: Subcomponents and connectivity of the superior longitudinal fasciculus in the human brain. Brain Struct Funct 221:20752092, 2016

    • Search Google Scholar
    • Export Citation
  • 44

    Yagmurlu K, Middlebrooks EH, Tanriover N, Rhoton AL Jr: Fiber tracts of the dorsal language stream in the human brain. J Neurosurg 124:13961405, 2016

    • Search Google Scholar
    • Export Citation
  • 45

    Zemmoura I, Blanchard E, Raynal PI, Rousselot-Denis C, Destrieux C, Velut S: How Klingler’s dissection permits exploration of brain structural connectivity? An electron microscopy study of human white matter. Brain Struct Funct 221:24772486, 2016

    • Search Google Scholar
    • Export Citation

Metrics

All Time Past Year Past 30 Days
Abstract Views 128 128 67
Full Text Views 5 5 3
PDF Downloads 4 4 2
EPUB Downloads 0 0 0