Dissecting the default mode network: direct structural evidence on the morphology and axonal connectivity of the fifth component of the cingulum bundle

View More View Less
  • 1 Athens Microneurosurgery Laboratory, Evangelismos Hospital, Athens;
  • 2 Department of Neurosurgery, National and Kapodistrian University of Athens;
  • 3 Department of Anatomy, Medical School, National and Kapodistrian University of Athens;
  • 4 Hellenic Center for Neurosurgical Research, “Petros Kokkalis,” Athens, Greece;
  • 5 Department of Neurosurgery, Toronto Western Hospital, University Health Network, Toronto, Ontario, Canada;
  • 6 Department of Neurosurgery, NYU School of Medicine, New York, New York;
  • 7 Departments of Radiology and
  • 8 Neurosurgery, School of Medicine, University of Thessaly, Larisa, Greece;
  • 9 Department of Neurosurgery, Mount Sinai Union Square, New York; and
  • 10 Department of Neurosurgery, Icahn School of Medicine at Mount Sinai, New York, New York
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

Although a growing body of data support the functional connectivity between the precuneus and the medial temporal lobe during states of resting consciousness as well as during a diverse array of higher-order functions, direct structural evidence on this subcortical circuitry is scarce. Here, the authors investigate the very existence, anatomical consistency, morphology, and spatial relationships of the cingulum bundle V (CB-V), a fiber tract that has been reported to reside close to the inferior arm of the cingulum (CingI).

METHODS

Fifteen normal, formalin-fixed cerebral hemispheres from adults were treated with Klingler’s method and subsequently investigated through the fiber microdissection technique in a medial to lateral direction.

RESULTS

A distinct group of fibers is invariably identified in the subcortical territory of the posteromedial cortex, connecting the precuneus and the medial temporal lobe. This tract follows the trajectory of the parietooccipital sulcus in a close spatial relationship with the CingI and the sledge runner fasciculus. It extends inferiorly to the parahippocampal place area and retrosplenial complex area, followed by a lateral curve to terminate toward the fusiform face area (Brodmann area [BA] 37) and lateral piriform area (BA35). Taking into account the aforementioned subcortical architecture, the CB-V allegedly participates as a major subcortical stream within the default mode network, possibly subserving the transfer of multimodal cues relevant to visuospatial, facial, and mnemonic information to the precuneal hub. Although robust clinical evidence on the functional role of this stream is lacking, the modern neurosurgeon should be aware of this tract when manipulating cerebral areas en route to lesions residing in or around the ventricular trigone.

CONCLUSIONS

Through the fiber microdissection technique, the authors were able to provide original, direct structural evidence on the existence, morphology, axonal connectivity, and correlative anatomy of what proved to be a discrete white matter pathway, previously described as the CB-V, connecting the precuneus and medial temporal lobe.

ABBREVIATIONS BA = Brodmann area; CB-V = cingulum bundle V; CingI = inferior arm of the cingulum; CTTP = contralateral interhemispheric transfalcine transprecuneus approach; DMN = default mode network; FFA = fusiform face area; FrM = forceps major; ILF = inferior longitudinal fasciculus; POS = parietooccipital sulcus; PPA = parahippocampal place area; RSC = retrosplenial cortex; Slg = sledge runner fasciculus; STTS = supracerebellar transtentorial transcollateral sulcus.

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, National and Kapodistrian University of Athens, Greece. ckouts@hotmail.co.uk.

INCLUDE WHEN CITING Published online April 24, 2020; DOI: 10.3171/2020.2.JNS193177.

Disclosures Dr. Hadjipanayis is a consultant for Synaptive and receives royalties from NX Development Corp.

  • 1

    Hebscher M , Levine B , Gilboa A . The precuneus and hippocampus contribute to individual differences in the unfolding of spatial representations during episodic autobiographical memory . Neuropsychologia . 2018 ;110 :123 133 .

    • Search Google Scholar
    • Export Citation
  • 2

    Mancini M , Mastropasqua C , Bonnì S , Theta burst stimulation of the precuneus modulates resting state connectivity in the left temporal pole . Brain Topogr . 2017 ;30 (3 ):312 319 .

    • Search Google Scholar
    • Export Citation
  • 3

    Burles F , Slone E , Iaria G . Dorso-medial and ventro-lateral functional specialization of the human retrosplenial complex in spatial updating and orienting . Brain Struct Funct . 2017 ;222 (3 ):1481 1493 .

    • Search Google Scholar
    • Export Citation
  • 4

    Epstein RA , Patai EZ , Julian JB , Spiers HJ . The cognitive map in humans: spatial navigation and beyond . Nat Neurosci . 2017 ;20 (11 ):1504 1513 .

    • Search Google Scholar
    • Export Citation
  • 5

    Marchette SA , Vass LK , Ryan J , Epstein RA . Anchoring the neural compass: coding of local spatial reference frames in human medial parietal lobe . Nat Neurosci . 2014 ;17 (11 ):1598 1606 .

    • Search Google Scholar
    • Export Citation
  • 6

    Raichle ME . The brain’s default mode network . Annu Rev Neurosci . 2015 ;38 :433 447 .

  • 7

    Sheldon S , Farb N , Palombo DJ , Levine B . Intrinsic medial temporal lobe connectivity relates to individual differences in episodic autobiographical remembering . Cortex . 2016 ;74 :206 216 .

    • Search Google Scholar
    • Export Citation
  • 8

    Sun J , Liu Z , Rolls ET , Verbal creativity correlates with the temporal variability of brain networks during the resting state . Cereb Cortex . 2019 ;29 (3 ):1047 1058 .

    • Search Google Scholar
    • Export Citation
  • 9

    Tosoni A , Pitzalis S , Committeri G , Resting-state connectivity and functional specialization in human medial parieto-occipital cortex . Brain Struct Funct . 2015 ;220 (6 ):3307 3321 .

    • Search Google Scholar
    • Export Citation
  • 10

    Utevsky AV , Smith DV , Huettel SA . Precuneus is a functional core of the default-mode network . J Neurosci . 2014 ;34 (3 ):932 940 .

    • Search Google Scholar
    • Export Citation
  • 11

    Zhang J , Andreano JM , Dickerson BC , Stronger functional connectivity in the default mode and salience networks is associated with youthful memory in superaging . Cereb Cortex . 2020 ;30 (1 ):72 84 .

    • Search Google Scholar
    • Export Citation
  • 12

    Liu Z , Zhang J , Zhang K , Distinguishable brain networks relate disease susceptibility to symptom expression in schizophrenia . Hum Brain Mapp . 2018 ;39 (9 ):3503 3515 .

    • Search Google Scholar
    • Export Citation
  • 13

    Wang Z , Williams VJ , Stephens KA , The effect of white matter signal abnormalities on default mode network connectivity in mild cognitive impairment . Hum Brain Mapp . 2020 ;41 (5 ):1237 1248 .

    • Search Google Scholar
    • Export Citation
  • 14

    Zhu Y , Tang Y , Zhang T , Reduced functional connectivity between bilateral precuneus and contralateral parahippocampus in schizotypal personality disorder . BMC Psychiatry . 2017 ;17 (1 ):48 .

    • Search Google Scholar
    • Export Citation
  • 15

    Wu Y , Sun D , Wang Y , Segmentation of the cingulum bundle in the human brain: a new perspective based on DSI tractography and fiber dissection study . Front Neuroanat . 2016 ;10 :84 .

    • Search Google Scholar
    • Export Citation
  • 16

    Komaitis S , Kalyvas AV , Skandalakis GP , The frontal longitudinal system as revealed through the fiber microdissection technique: structural evidence underpinning the direct connectivity of the prefrontal-premotor circuitry [published online October 4, 2019] . J Neurosurg . doi:10.3171/2019.6.JNS191224

    • Search Google Scholar
    • Export Citation
  • 17

    Koutsarnakis C , Kalyvas AV , Komaitis S , Defining the relationship of the optic radiation to the roof and floor of the ventricular atrium: a focused microanatomical study . J Neurosurg . 2019 ;130 (5 ):1728 1739 .

    • Search Google Scholar
    • Export Citation
  • 18

    Koutsarnakis C , Kalyvas AV , Skandalakis GP , Sledge runner fasciculus: anatomic architecture and tractographic morphology . Brain Struct Funct . 2019 ;224 (3 ):1051 1066 .

    • Search Google Scholar
    • Export Citation
  • 19

    Koutsarnakis C , Liakos F , Kalyvas AV , Approaching the atrium through the intraparietal sulcus: mapping the sulcal morphology and correlating the surgical corridor to underlying fiber tracts . Oper Neurosurg (Hagerstown) . 2017 ;13 (4 ):503 516 .

    • Search Google Scholar
    • Export Citation
  • 20

    Panesar SS , Belo JTA , Yeh FC , Fernandez-Miranda JC . Structure, asymmetry, and connectivity of the human temporo-parietal aslant and vertical occipital fasciculi . Brain Struct Funct . 2019 ;224 (2 ):907 923 .

    • Search Google Scholar
    • Export Citation
  • 21

    Panesar SS , Yeh FC , Jacquesson T , A quantitative tractography study into the connectivity, segmentation and laterality of the human inferior longitudinal fasciculus . Front Neuroanat . 2018 ;12 :47 .

    • Search Google Scholar
    • Export Citation
  • 22

    Jones DK , Christiansen KF , Chapman RJ , Aggleton JP . Distinct subdivisions of the cingulum bundle revealed by diffusion MRI fibre tracking: implications for neuropsychological investigations . Neuropsychologia . 2013 ;51 (1 ):67 78 .

    • Search Google Scholar
    • Export Citation
  • 23

    Fransson P , Marrelec G . The precuneus/posterior cingulate cortex plays a pivotal role in the default mode network: Evidence from a partial correlation network analysis . Neuroimage . 2008 ;42 (3 ):1178 1184 .

    • Search Google Scholar
    • Export Citation
  • 24

    Cavanna AE , Trimble MR . The precuneus: a review of its functional anatomy and behavioural correlates . Brain . 2006 ;129 (Pt 3 ):564 583 .

    • Search Google Scholar
    • Export Citation
  • 25

    Greicius MD , Krasnow B , Reiss AL , Menon V . Functional connectivity in the resting brain: a network analysis of the default mode hypothesis . Proc Natl Acad Sci U S A . 2003 ;100 (1 ):253 258 .

    • Search Google Scholar
    • Export Citation
  • 26

    Raichle ME , MacLeod AM , Snyder AZ , A default mode of brain function . Proc Natl Acad Sci U S A . 2001 ;98 (2 ):676 682 .

  • 27

    Vatansever D , Menon DK , Manktelow AE , Default mode network connectivity during task execution . Neuroimage . 2015 ;122 :96 104 .

    • Search Google Scholar
    • Export Citation
  • 28

    Paladini RE , Müri RM , Meichtry J , The influence of alertness on the spatial deployment of visual attention is mediated by the excitability of the posterior parietal cortices . Cereb Cortex . 2017 ;27 (1 ):233 243 .

    • Search Google Scholar
    • Export Citation
  • 29

    Rosen ML , Stern CE , Devaney KJ , Somers DC . Cortical and subcortical contributions to long-term memory-guided visuospatial attention . Cereb Cortex . 2018 ;28 (8 ):2935 2947 .

    • Search Google Scholar
    • Export Citation
  • 30

    Müller NG , Riemer M , Brandt L , Wolbers T . Repetitive transcranial magnetic stimulation reveals a causal role of the human precuneus in spatial updating . Sci Rep . 2018 ;8 (1 ):10171 .

    • Search Google Scholar
    • Export Citation
  • 31

    Baumann O , Mattingley JB . Functional organization of the parahippocampal cortex: dissociable roles for context representations and the perception of visual scenes . J Neurosci . 2016 ;36 (8 ):2536 2542 .

    • Search Google Scholar
    • Export Citation
  • 32

    Harvey DY , Burgund ED . Neural adaptation across viewpoint and exemplar in fusiform cortex . Brain Cogn . 2012 ;80 (1 ):33 44 .

    • Search Google Scholar
    • Export Citation
  • 33

    Tokunaga K , Tamiya T , Date I . Transient memory disturbance after removal of an intraventricular trigonal meningioma by a parieto-occipital interhemispheric precuneus approach: case report . Surg Neurol . 2006 ;65 (2 ):167 169 .

    • Search Google Scholar
    • Export Citation
  • 34

    Bohnstedt BN , Kulwin CG , Shah MV , Cohen-Gadol AA . Posterior interhemispheric transfalcine transprecuneus approach for microsurgical resection of periatrial lesions: indications, technique, and outcomes . J Neurosurg . 2015 ;123 (4 ):1045 1054 .

    • Search Google Scholar
    • Export Citation
  • 35

    Xie T , Sun C , Zhang X , The contralateral transfalcine transprecuneus approach to the atrium of the lateral ventricle: operative technique and surgical results . Neurosurgery . 2015 ;11 (suppl 2 ):110 118 .

    • Search Google Scholar
    • Export Citation
  • 36

    Zhao X , Borba Moreira L , Cavallo C , Quantitative endoscopic comparison of contralateral interhemispheric transprecuneus and supracerebellar transtentorial transcollateral sulcus approaches to the atrium . World Neurosurg . 2019 ;122 :e215 e225 .

    • Search Google Scholar
    • Export Citation
  • 37

    Maier-Hein KH , Neher PF , Houde JC , The challenge of mapping the human connectome based on diffusion tractography . Nat Commun . 2017 ;8 (1 ):1349 .

    • Search Google Scholar
    • Export Citation
  • 38

    Reveley C , Seth AK , Pierpaoli C , Superficial white matter fiber systems impede detection of long-range cortical connections in diffusion MR tractography . Proc Natl Acad Sci U S A . 2015 ;112 (21 ):E2820 E2828 .

    • Search Google Scholar
    • Export Citation
  • 39

    Schilling K , Gao Y , Janve V , Confirmation of a gyral bias in diffusion MRI fiber tractography . Hum Brain Mapp . 2018 ;39 (3 ):1449 1466 .

    • Search Google Scholar
    • Export Citation
  • 40

    Sinke MRT , Otte WM , Christiaens D , Diffusion MRI-based cortical connectome reconstruction: dependency on tractography procedures and neuroanatomical characteristics . Brain Struct Funct . 2018 ;223 (5 ):2269 2285 .

    • Search Google Scholar
    • Export Citation
  • 41

    Thomas C , Ye FQ , Irfanoglu MO , Anatomical accuracy of brain connections derived from diffusion MRI tractography is inherently limited . Proc Natl Acad Sci U S A . 2014 ;111 (46 ):16574 16579 .

    • Search Google Scholar
    • Export Citation
  • 42

    Zemmoura I , Blanchard E , Raynal PI , How Klingler’s dissection permits exploration of brain structural connectivity? An electron microscopy study of human white matter . Brain Struct Funct . 2016 ;221 (5 ):2477 2486 .

    • Search Google Scholar
    • Export Citation
  • 43

    Martino J , De Witt Hamer PC , Vergani F , Cortex-sparing fiber dissection: an improved method for the study of white matter anatomy in the human brain . J Anat . 2011 ;219 (4 ):531 541 .

    • Search Google Scholar
    • Export Citation
  • 44

    Liakos F , Koutsarnakis C . The role of white matter dissection technique in modern neuroimaging: can neuroradiologists benefit from its use? Surg Radiol Anat . 2016 ;38 (2 ):275 276 .

    • Search Google Scholar
    • Export Citation
  • 45

    Wang H , Black AJ , Zhu J , Reconstructing micrometer-scale fiber pathways in the brain: multi-contrast optical coherence tomography based tractography . Neuroimage . 2011 ;58 (4 ):984 992 .

    • Search Google Scholar
    • Export Citation

Metrics

All Time Past Year Past 30 Days
Abstract Views 32 32 32
Full Text Views 25 25 25
PDF Downloads 23 23 23
EPUB Downloads 0 0 0