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Microsurgical anatomy of the isthmic cingulum: a new white matter crossroad and neurosurgical implications in the posteromedial interhemispheric approaches and the glioma invasion patterns

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The dichotomy of the cingulum bundle into the dorsal supracallosal and ventral parahippocampal parts is widely accepted; however, the retrosplenial component with its multiple alternative connections has not been revealed. The aim of this study was to delineate the microsurgical anatomy of a connectionally transition zone, the isthmic cingulum, in relation to the posteromedial interhemispheric access to the atrium and discuss the relevant patterns of glioma invasion on the basis of its fiber connections. White matter (WM) fibers were dissected layer by layer in a medial-to-lateral, lateral-to-medial, and posterior-to-anterior fashion. All related tracts and their connections were generated using deterministic tractography. The magnetic resonance imaging (MRI) tractography findings were correlated with those of fiber dissection. A medial parieto-occipital approach to reach the atrium was performed with special emphasis on the cingulate isthmus and underlying WM connections. The isthmic cingulum, introduced as a retrosplenial connectional crossroad for the first time, displayed multiple connections to the splenium and the superior thalamic radiations. Another new finding was the demonstration of lateral hemispheric extension of the isthmic cingulum fibers through the base of the posterior part of the precuneus at the base of the parieto-occipital sulcus. The laterally crossing cingulum fibers were interconnected with three distinct association tracts: the middle longitudinal (MdLF), the inferior frontooccipital fasciculi (IFOF), and the claustro-cortical fibers (CCF). In the process of entry to the atrium during posterior interhemispheric approaches, the splenial and thalamic connections, as well as the laterally crossing fibers of the isthmic cingulum, were all in jeopardy. The connectional anatomy of the retrosplenial area is much more complicated than previously known. The isthmic cingulum connections may explain the concept of interhemispheric and medial to lateral cerebral hemisphere invasion patterns in medial parieto-occipital and posteromesial temporal gliomas. The isthmic cingulum is of key importance in posteromedial interhemispheric approaches to both: the atrium and the posterior mesial temporal lobe.

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References

  1. Aggleton JP (2008) Understanding anterograde amnesia: disconnections and hidden lesions. Q J Exp Psychol 61(10):1441–1471. https://doi.org/10.1080/17470210802215335

    Article  Google Scholar 

  2. 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 252-4. https://doi.org/10.1227/NEU.0b013e318214ab79

    Article  PubMed  Google Scholar 

  3. Balestrini S, Francione S, Mai R, Castana L, Casaceli G, Marino D, Provinciali L, Cardinale F, Tassi L (2015) Multimodal responses induced by cortical stimulation of the parietal lobe: a stereo-electroencephalography study. Brain 138(Pt 9):2596–2607. https://doi.org/10.1093/brain/awv187

    Article  PubMed  Google Scholar 

  4. 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

    Article  PubMed  Google Scholar 

  5. Bonnelle V, Ham TE, Leech R, Kinnunen KM, Mehta MA, Greenwood RJ, Sharp DJ (2012) Salience network integrity predicts default mode network function after traumatic brain injury. Proc Natl Acad Sci USA 109(12):4690–4695. https://doi.org/10.1073/pnas.111345510

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Bonnelle V, Leech R, Kinnunen KM, Ham TE, Beckmann CF, De Boissezon X, Greenwood RJ, Sharp DJ (2011) Default mode network connectivity predicts sustained attention deficits after traumatic brain injury. J Neurosci 31(38):13442–13451. https://doi.org/10.1523/JNEUROSCI.1163-11.2011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Buckner RL, Andrews-Hanna JR, Schacter DL (2008) The brain's default network: anatomy, function, and relevance to disease. Ann NY Acad Sci 1124:1–38. https://doi.org/10.1196/annals.1440.011

    Article  PubMed  Google Scholar 

  8. Catani M, Dell'acqua F, Thiebaut de Schotten M (2013) A revised limbic system model for memory, emotion and behaviour. Neurosci Biobehav Rev 37(8):1724–1737. https://doi.org/10.1016/j.neubiorev.2013.07.001

    Article  PubMed  Google Scholar 

  9. Catani M, Thiebaut de Schotten M (2012) Surface neuroanatomy. In: Catani M, Thiebaut de Schotten M (eds) Atlas of Human Brain Connections. Oxford University Press, New York, pp 7–20

    Chapter  Google Scholar 

  10. Catani M, Zilles K (2021) Cerebral hemispheres. In: Standring S (ed) Gray's anatomy, the anatomical basis of clinical practice, 42th edn. Elsevier Limited, pp 512–539

    Google Scholar 

  11. Choi C, Rubino PA, Fernandez-Miranda JC, Abe H, Rhoton AL Jr (2006) Meyer's loop and the optic radiations in the transsylvian approach to the mediobasal temporal lobe. Neurosurgery 59(4 Suppl 2):ONS228-35; discussion ONS235-6. https://doi.org/10.1227/01.NEU.0000223374.69144.81

    Article  PubMed  Google Scholar 

  12. Dejerine JJ, Dejerine-Klumpke A (1895) Substance blanche des hémisphères cérébraux. In: Dejerine JJ, Dejerine-Klumpke A (eds) Anatomie des centres nerveux, vol I. Rueff, Paris, pp 742–810

    Google Scholar 

  13. Domesick VB (1970) The fasciculus cinguli in the rat. Brain Res 20(1):19–32. https://doi.org/10.1016/0006-8993(70)90150-2

    Article  CAS  PubMed  Google Scholar 

  14. Fernandez-Miranda JC, Xu Y, Hendricks BK, Cohen-Gadol A (2020) Contralateral interhemispheric transfalcine transprecuneus approach: advancing operative angles to deep-seated lesions. World Neurosurg. 144:341–350

    Article  PubMed  Google Scholar 

  15. Goga C, Türe U (2015) The anatomy of Meyer's loop revisited: changing the anatomical paradigm of the temporal loop based on evidence from fiber microdissection. J Neurosurg 122(6):1253–1262. https://doi.org/10.3171/2014.12.JNS14281

    Article  PubMed  Google Scholar 

  16. Gusnard DA, Raichle ME, Raichle ME (2001) Searching for a baseline: functional imaging and the resting human brain. Nat Rev Neurosci 2(10):685–694. https://doi.org/10.1038/35094500

    Article  CAS  PubMed  Google Scholar 

  17. Güngör 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

    Article  PubMed  Google Scholar 

  18. Hahn B, Ross TJ, Stein EA (2007) Cingulate activation increases dynamically with response speed under stimulus unpredictability. Cereb Cortex 17(7):1664–1671. https://doi.org/10.1093/cercor/bhl075

    Article  PubMed  Google Scholar 

  19. Hampson M, Driesen NR, Skudlarski P, Gore JC, Constable RT (2006) Brain connectivity related to working memory performance. J Neurosci 26(51):13338–13343. https://doi.org/10.1523/JNEUROSCI.3408-06.2006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Harrison BJ, Pujol J, López-Solà M, Hernández-Ribas R, Deus J, Ortiz H, Soriano-Mas C, Yücel M, Pantelis C, Cardoner N (2008) Consistency and functional specialization in the default mode brain network. Proc Natl Acad Sci U S A 105(28):9781–9786. https://doi.org/10.1073/pnas.071179110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Hung Y, Uchida M, Gaillard SL, Woodworth H, Kelberman C, Capella J et al (2020) Cingulum-Callosal white-matter microstructure associated with emotional dysregulation in children: A diffusion tensor imaging study. Neuroimage Clin 27:102266. https://doi.org/10.1016/j.nicl.2020.102266

    Article  PubMed  PubMed Central  Google Scholar 

  22. Klingler J (1935) Erleichterung der makroskopischen Praeparation des Gehirns durch den Gefrierprozess. Schweiz Arch Neurol Psychiatr 36:247–256

    Google Scholar 

  23. Koutsarnakis C, Kalyvas AV, Skandalakis GP, Karavasilis E, Christidi F, Komaitis S et al (2019) Sledge runner fasciculus: anatomic architecture and tractographic morphology. Brain Struct Funct 224(3):1051–1066. https://doi.org/10.1007/s00429-018-01822-4

    Article  PubMed  Google Scholar 

  24. Küçükyürük B, Uzan M, Avyasov R, Tahmazoğlu B, İşler C, Sanus GZ, Tanrıöver N (2020) Evaluation of ideal extent of corpus callosotomy based on the location of intracallosal motor fibers. World Neurosurg 144:e568–e575. https://doi.org/10.1016/j.wneu.2020.09.006

    Article  PubMed  Google Scholar 

  25. Leech R, Kamourieh S, Beckmann CF, Sharp DJ (2011) Fractionating the default mode network: distinct contributions of the ventral and dorsal posterior cingulate cortex to cognitive control. J Neurosci 31(9):3217–3224. https://doi.org/10.1523/JNEUROSCI.5626-10.2011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Maclean PD (1952) Some psychiatric implications of physiological studies on frontotemporal portion of limbic system (visceral brain). Electroencephalogr Clin Neurophysiol 4(4):407–418. https://doi.org/10.1016/0013-4694(52)90073-4

    Article  CAS  PubMed  Google Scholar 

  27. Mahaney KB, Abdulrauf SI (2008) Anatomic relationship of the optic radiations to the atrium of the lateral ventricle: description of a novel entry point to the trigone. Neurosurgery 63(4 Suppl 2):195–202; discussion 202-3. https://doi.org/10.1227/01.NEU.0000313121.58694.4A

    Article  PubMed  Google Scholar 

  28. Margulies DS, Vincent JL, Kelly C, Lohmann G, Uddin LQ, Biswal BB, Villringer A, Castellanos FX, Milham MP, Petrides M (2009) Precuneus shares intrinsic functional architecture in humans and monkeys. Proc Natl Acad Sci USA 106 (47):20069–20074. https://doi.org/10.1073/pnas.0905314106

  29. Mufson EJ, Pandya DN (1984) Some observations on the course and composition of the cingulum bundle in the rhesus monkey. J Comp Neurol 225(1):31–43. https://doi.org/10.1002/cne.902250105

    Article  CAS  PubMed  Google Scholar 

  30. Nieuwenhuys R, Voogd J, van Huijzen C (2008) Telencephalon: hippocampus and related structures. In: Nieuwenhuys R, Voogd J, van Huijzen C (eds) The human central nervous system, 4th edn. springer, Berlin, pp 361–400

    Chapter  Google Scholar 

  31. Panteli A, Güngör A, Fırat Z, Sarıtepe F, Türe H, Türe U (2022) The posterior interhemispheric transparieto-occipital fissure approach to the atrium of the lateral ventricle: a fiber microdissection study with case series. Neurosurg Rev 45(2):1663–1674. https://doi.org/10.1007/s10143-021-01693-0

    Article  PubMed  Google Scholar 

  32. Papez JW (1995) A proposed mechanism of emotion. 1937. J Neuropsychiatry Clin Neurosci 7(1):103–112. https://doi.org/10.1176/jnp.7.1.103

    Article  CAS  PubMed  Google Scholar 

  33. Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, Shulman GL (2001) A default mode of brain function. Proc Natl Acad Sci USA 98(2):676–682. https://doi.org/10.1073/pnas.98.2.676

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Rhoton AL Jr (2007) The cerebrum. Anatomy. Neurosurgery 61(1 Suppl):37–118; discussion 118-9. https://doi.org/10.1227/01.NEU.0000255490.88321.CE

    Article  PubMed  Google Scholar 

  35. Rhoton AL Jr (2002) The lateral and third ventricles. Neurosurgery 51(4 Suppl):S207–S271. https://doi.org/10.1097/00006123-200210001-00006

    Article  PubMed  Google Scholar 

  36. Ribas GC, Yasuda A, Ribas EC, Nishikuni K, Rodrigues AJ Jr (2006) Surgical anatomy of microneurosurgical sulcal key points. Neurosurgery 59(4 Suppl 2):ONS177-210; discussion ONS210-1. https://doi.org/10.1227/01.NEU.0000240682.28616.b2

    Article  PubMed  Google Scholar 

  37. Rubino PA, Rhoton AL Jr, Tong X, Oliveira Ed (2005) Three-dimensional relationships of the optic radiation. Neurosurgery 57(4 Suppl):219-227; discussion 219-27. https://doi.org/10.1227/01.neu.0000176415.83417.16

  38. Schmahmann JD, Pandya DN (2006) Principles of organization. In: Schmahmann JD, Pandya DN (eds) Fiber pathways of the brain. Oxford University Press, New York, pp 81–87

    Chapter  Google Scholar 

  39. Schmahmann JD, Pandya DN (2006) Cingulum Bundle. In: Schmahmann JD, Pandya DN (eds) Fiber pathways of the brain. Oxford University Press, New York, pp 427–440

    Chapter  Google Scholar 

  40. Shibahara I, Saito R, Kanamori M, Sonoda Y, Sato S, Hide T, Tominaga T, Kumabe T (2021) Role of the parietooccipital fissure and its implications in the pathophysiology of posterior medial temporal gliomas. J Neurosurg 14:1–10. https://doi.org/10.3171/2021.7.JNS21990

    Article  Google Scholar 

  41. Shimizu S, Tanaka R, Rhoton AL Jr, Fukushima Y, Osawa S, Kawashima M, Oka H, Fujii K (2006) Anatomic dissection and classic three-dimensional documentation: a unit of education for neurosurgical anatomy revisited. Neurosurgery 58(5):E1000; discussion E1000. https://doi.org/10.1227/01.NEU.0000210247.37628.43

  42. Singh KD, Fawcett IP (2008) Transient and linearly graded deactivation of the human default-mode network by a visual detection task. Neuroimage 41(1):100–112. https://doi.org/10.1016/j.neuroimage.2008.01.051

    Article  CAS  PubMed  Google Scholar 

  43. Vann S, Aggleton J, Maguire E (2009) What does the retrosplenial cortex do? Nat Rev Neurosci 10:792–802. https://doi.org/10.1038/nrn2733

    Article  CAS  PubMed  Google Scholar 

  44. Vincent JL, Snyder AZ, Fox MD, Shannon BJ, Andrews JR, Raichle ME, Buckner RL (2006) Coherent spontaneous activity identifies a hippocampal-parietal memory network. J Neurophysiol 96(6):3517–3531. https://doi.org/10.1152/jn.00048.2006

    Article  PubMed  Google Scholar 

  45. Witelson SF (1989) Hand and sex differences in the isthmus and genu of the human corpus callosum. A postmortem morphological study. Brain 112(Pt 3):799–835. https://doi.org/10.1093/brain/112.3.799

    Article  PubMed  Google Scholar 

  46. 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 7(10):84. https://doi.org/10.3389/fnana.2016.00084

    Article  Google Scholar 

  47. Yasargil MG, Abernathey CD (1996) Microneurosurgery of CNS Tumors. In: Yasargil MG (ed) Microneurosurgery, vol IVB. Georg Thieme, Stuttgart, pp 313–338

    Google Scholar 

  48. Yeh FC, Panesar S, Fernandes D, Meola A, Yoshino M, Fernandez-Miranda JC, Vettel JM, Verstynen T (2018) Population-averaged atlas of the macroscale human structural connectome and its network topology. Neuroimage 178:57–68. https://doi.org/10.1016/j.neuroimage.2018.05.027

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Microsurgical Neuroanatomy Laboratory, Department of Neurosurgery, Cerrahpasa Medical Faculty, Istanbul University – Cerrahpasa, Istanbul, Turkey

    Tahsin Saygi, Rashid Avyasov, Ozan Barut, Zeynep Daglar, Oguz Baran & Necmettin Tanriover

  2. Department of Neurosurgery, Haseki Training and Research Hospital, University of Health Sciences, Istanbul, Turkey

    Tahsin Saygi

  3. Department of Neurosurgery, Basaksehir Cam Sakura Training and Research Hospital, University of Health Sciences, Istanbul, Turkey

    Ozan Barut & Ozan Hasimoglu

  4. Department of Neurosurgery, Koç University Hospital, Istanbul, Turkey

    Oguz Baran

  5. Department of Neurology, Basaksehir Cam Sakura Training and Research Hospital, University of Health Sciences, Istanbul, Turkey

    Ayca Altinkaya

  6. Department of Neurosurgery, Cerrahpasa Medical Faculty, Istanbul University – Cerrahpasa, Cerrahpasa Street, No: 53, Fatih, Istanbul, Turkey

    Necmettin Tanriover

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Contributions

TS: cadaver dissections, conducted the study method, literature search, collected the data, writing the manuscript, revised the manuscript, and final approval; RA: cadaver dissections, revised the manuscript, and final approval; OzB: cadaver dissections, revised the manuscript, and final approval; ZD: cadaver dissections, revised the manuscript, and final approval; OgB: collected the data, revised the manuscript, and final approval; OH: diffusion tensor imaging and 3D radiologic figures, revised the manuscript, and final approval; AA: diffusion tensor imaging and 3D radiologic figures, revised the manuscript, and final approval; NT: conceived the idea, study supervision, collected data, revised the manuscript, and final approval.

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Correspondence to Necmettin Tanriover.

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Saygi, T., Avyasov, R., Barut, O. et al. Microsurgical anatomy of the isthmic cingulum: a new white matter crossroad and neurosurgical implications in the posteromedial interhemispheric approaches and the glioma invasion patterns. Neurosurg Rev 46, 82 (2023). https://doi.org/10.1007/s10143-023-01982-w

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