Ismail Kaya, Ceren Kizmazoglu, Inan Uzunoglu, Gokhan Gurkan, Ilker Deniz Cingoz, Murat Atar, Nurullah Yuceer, Gulden Sozer, Ahmet Ozdilmac

A understanding of the three dimensional microsurgical anatomical architecture of the temporal lobe with its functions

Aim: This study aimed to evaluate the human brain temporal lobe white matter pathways with respect to microsurgical anatomy, reveal the relationship between these white matter pathways, evaluate their functions, which are already known in the literature, and contribute to the literature to establish safe temporal region surgical interventions. Material and Methods: 10 specimens of postmortem human brain hemispheres were fixed in accordance with Klingler’s method. Subsequently, dissection of the temporal lobe white matter pathways was performed under a surgical microscope. Each stage of dissection was achieved using the technique of merging multiple focus images in high-quality three-dimensional images. Results: The data obtained in lateral-to-medial and medial-to-lateral dissections were compatible with the literature. Moreover, microsurgical three-dimensional architectural structure of temporal lobe white matter pathways has been clearly revealed. The horizontal and vertical segments of superior longitudinal fasciculus were detected. The limbic system, connection of central cores with the temporal lobe, temporal stems region, and relationship with other fiber systems have been shown in this study. The importance of the temporal stem and Meyer’s loop for safe interventions on temporal lobe has been noted. Conclusion: Temporal region white matter pathways should be handled in a multimodal system, and anatomical knowledge of these white matter pathways should be mastered before performing temporal surgical interventions. Furthermore, the surgical strategy and preoperative planning should be discussed considering the relationship between the lesion and white matter pathways, thereby reducing neurosurgical morbidity and mortality

PDF

___

1. Ludwig E, Klingler J. Atlas Cerebri Humani. Der inere Bau des Gehirns dargestellt auf Grund mackroskopischer Praparate. Boston: Brown; 1956
2. Wanibuchi M, Friedmann AH, Fukushima T. Photo atlasof skull base dissection: techniques and operative approaches. Ann R Coll Surg Engl 2010; 92:717-9.
3. Duffau H, Capelle L, Denvil D, Sichez N, et al. Usefulness of intraoperative electrical subcortical mapping during surgery for low-grade gliomas located within eloquent brain regions: functional results in a consecutive series of 103 patients. J Neurosurg 2003; 98:764-78.
4. Fernandez-Miranda JC, Rhoton AL Jr, Kakizawa Y, et al. The claustrum and its projection system in the human brain: a microsurgical and tractographic anatomical study. J Neurosurg 2008;108:764-74.
5. Catani M, Howard RJ, Pajevic S, Jones DK. Virtual in vivo interactive dissection of white matter fasciculi in the human brain. Neuroimage 2002;17:77-94.
6. Catani M, Jones DK, Ffytche DH. Perisylvian language networks of the human brain. Ann Neurol 2005;57:8- 16.
7. Catani M, Mesulam M. The arcuate fasciculus and the disconnection theme in language and aphasia: History and current state. Cortex 2008;44:953-61.
8. Fernandez-Miranda JC, Rhoton AL, Jr., AlvarezLinera J, et al. Three-dimensional microsurgical and tractographic anatomy of the white matter of the human brain. Neurosurgery 2008;62: 989-1026; discussion 1026-8.
9. Martino J, De Witt Hamer PC, Berger MS, et al. Analysis of the subcomponents and cortical terminations of the perisylvian superior longitudinal fasciculus: A fiber dissection and DTI tractography study. Brain Struct Funct 2013;218:105-21.
10. Thiebaut de Schotten M, Dell0Acqua F, Forkel SJ, et al. A lateralized brain network for visuospatial attention. Nat Neurosci 2011;14:1245-6.
11. Kaplan E, Naeser MA, Martin PI, , et al. Horizontal portion of arcuate fasciculus fibers track to pars opercularis, not pars triangularis, in right and left hemispheres: A DTI study. Neuroimage 2010;52:436- 44.
12. Ingham RJ, Fox PT, Ingham JC, et al. Brain correlates of stuttering and syllable production: Gender comparison and replication. J Speech Lang Hear Res 2004;47:321-41.
13. Duffau H, Gatignol P, Denvil D, et al. The articulatory loop: Study of the subcortical connectivity by electro stimulation. Neuroreport 2003;14:2005-8.
14. Parker GJ, Luzzi S, Alexander DC, et al. Lateralization of ventral and dorsal auditory-language pathways in the human brain. Neuroimage 2005;24:656-66.
15. Bernal B, Altman N. The connectivity of the superior longitudinal fasciculus: A tractography DTI study. Magn Reson Imaging 2010;28:217-25.
16. Glasser MF, Rilling JK. DTI tractography of the human brains language pathways. Cereb Cortex 2008;18:2471-82.
17. Duffau H, Capelle L, Sichez N, Denvil D, Lopes M, et al. Intraoperative mapping of the subcortical language pathways using direct stimulations. An anatomofunctional study. Brain 2002;125:199-214.
18. Saur D, Kreher BW, Schnell S, et al. Ventral and dorsal pathways for language. Proc Natl Acad Sci USA 2008;105:18035-40.
19. Naeser MA, Alexander MP, Helm-Estabrooks N, et al. Aphasia with predominantly subcortical lesion sites: Description of three capsular/putaminal aphasia syndromes. Arch Neurol 1982;39:2-14.
20. Hickok G, Poeppel D. Dorsal and ventral streams: A framework for understanding aspects of the functional anatomy of language. Cognition 2004;92:67-99.
21. Schmahmann JD, Pandya DN, Wang R, et al. Association fibre pathways of the brain: Parallel observations from diffusion spectrum imaging and autoradiography. Brain 2007;130:630-53.
22. Makris N, Kennedy DN, McInerney S, et al. Segmentation of subcomponents within the superior longitudinal fascicle in humans: A quantitative, in vivo, DT-MRI study. Cereb Cortex 2005;15:854-69
23. Cabeza R, Ciaramelli E, Olson IR, Moscovitch M. The parietal cortex and episodic memory: An attentional account. Nat Rev Neurosci 2008;9:613-25.
24. Makris N, Papadimitriou GM, Kaiser JR, et al. Delineation of the middle longitudinal fascicle in humans: A quantitative, in vivo, DT-MRI study. Cereb Cortex 2009;19:777-85.
25. De Witt Hamer PC, Moritz-Gasser S, Gatignol P, Duffau H. Is the human left middle longitudinal fascicle essential for language? A brain electrostimulation study. Hum Brain Mapp 2011;32:962-73.
26. Catani M, Jones DK, Donato R, Ffytche DH. Occipitotemporal connections in the human brain. Brain 2003;126: 2093-107.
27. Epelbaum S, Pinel P, Gaillard R, et al. Pure alexia as a disconnection syndrome: New diffusion imaging evidence for an old concept. Cortex 2008;44:962-74.
28. Martino J, De Witt Hamer PC, Vergani F, et al. Cortexsparing fiber dissection: An improved method for the study of white matter anatomy in the human brain. J Anat 2011;219:531-41.
29. Mandonnet E, Nouet A, Gatignol P, et al. Does the left inferior longitudinal fasciculus play a role in language? A brain stimulation study. Brain 2007;130:623-9.
30. Agosta F, Henry RG, Migliaccio R, et al.Language networks in semantic dementia. Brain 2010;133:286- 99.
31. Vigneau M, Beaucousin V, Herve PY, et al. Meta – analyzing left hemi-sphere language areas: Phonology, semantics, and sentence processing. Neuroimage 2006;30:1414-32.
32. Duffau H, Gatignol P, Moritz-Gasser S, Mandonnet E. Is the left uncinate fasciculus essential for language? A cerebral stimu-lation study. J Neurol 2009;256:382- 9.
33. Damasio H, Tranel D, Grabowski T, et al. Neural systems behind word and concept retrieval. Cognition 2004;92:179-29.
34. Wang YX, Zhu XL, Deng M, et al. The use of diffusion tensor tractography to measure the distance between the anterior tip of the Meyer loop and the temporal pole in a cohort from Southern China. J Neurosurg. 2010;113:1144-51.
35. Taoka T, Sakamoto M, Nakagawa H, et al. Diffusion tensor tractography of the Meyer loop in cases of temporal lobe resection for temporal lobe epilepsy: correlation between postsurgical visual field defect and anterior limit of Meyer loop on tractography. AJNR Am J Neuroradiol 2008;29:1329-34.
36. Peltier J, Travers N, Destrieux C, Velut S. Optic radiations: a microsurgical anatomical study. J Neurosurg 2006;105:294-300.
37. Fabri M, Pierpaoli C, Barbaresi P, Polonara G. Functional topography of the corpus callosum investigated by DTI and fMRI.World JRadiol 2014;6: 895-906.
38. Thompson PM, Narr KL, Blanton RE, Toga AW. Mapping structural alterations of the corpus callosum during brain developmentand degeneration. In: Zaidel, E., Iacoboni, M. (Eds.), The Parallel Brain: The Cognitive Neuroscience of the Corpus Callosum, 2003;93-130.
39. Yasargil MG, Ture U, Yasargil DC. Impact of temporal lobe surgery. J Neurosurg 2004;101:725-38.
40. Peuskens D, van Loon J, van Calenbergh F, et al: Anatomy of the anterior temporal lobe and the frontotemporal region demonstrated by fiber dissection. Implications for surgical approaches to the mesial temporal lobe. Neurosurgery 2004;55:1174-84.