The claustrum and its projection system in the human brain: a microsurgical and tractographic anatomical study.

OBJECT The goal in this study was to examine the microsurgical and tractographic anatomy of the claustrum and its projection fibers, and to analyze the functional and surgical implications of the findings. METHODS Fifteen formalin-fixed human brain hemispheres were dissected using the Klingler fiber dissection technique, with the aid of an operating microscope at x 6-40 magnification. Magnetic resonance imaging studies of 5 normal brains were analyzed using diffusion tensor (DT) imaging-based tractography software. RESULTS Both the claustrum and external capsule have 2 parts: dorsal and ventral. The dorsal part of the external capsule is mainly composed of the claustrocortical fibers that converge into the gray matter of the dorsal claustrum. Results of the tractography studies coincided with the fiber dissection findings and showed that the claustrocortical fibers connect the claustrum with the superior frontal, precentral, postcentral, and posterior parietal cortices, and are topographically organized. The ventral part of the external capsule is formed by the uncinate and inferior occipitofrontal fascicles, which traverse the ventral part of the claustrum, connecting the orbitofrontal and prefrontal cortex with the amygdaloid, temporal, and occipital cortices. The relationship between the insular surface and the underlying fiber tracts, and between the medial lower surface of the claustrum and the lateral lenticulostriate arteries is described. CONCLUSIONS The combination of the fiber dissection technique and DT imaging-based tractography supports the presence of the claustrocortical system as an integrative network in humans and offers the potential to aid in understanding the diffusion of gliomas in the insula and other areas of the brain.

[1]  Albert L. Rhoton,et al.  The Supratentorial Cranial Space: Microsurgical Anatomy and Surgical Approaches , 2002 .

[2]  C. Nimsky,et al.  Implementation of Fiber Tract Navigation , 2006, Neurosurgery.

[3]  Functional compensation of the claustrum: lessons from low-grade glioma surgery , 2007, Journal of Neuro-Oncology.

[4]  S. Brand.  A serial section Golgi analysis of the primate claustrum , 2004, Anatomy and Embryology.

[5]  Derek K. Jones,et al.  Occipito-temporal connections in the human brain. , 2003, Brain : a journal of neurology.

[6]  F. Lang,et al.  Surgical Resection of Intrinsic Insular Tumors , 2005, Neurosurgery.

[7]  C. Stevens.  Consciousness: Crick and the claustrum , 2005, Nature.

[8]  Christopher Nimsky,et al.  Preoperative and Intraoperative Diffusion Tensor Imaging-based Fiber Tracking in Glioma Surgery , 2005, Neurosurgery.

[9]  J. Schramm,et al.  Intrinsic tumors of the insula: a prospective surgical study of 30 patients. , 1996, Journal of neurosurgery.

[10]  Ugur Türe,et al.  Impact of temporal lobe surgery. , 2004, Journal of neurosurgery.

[11]  Derek K. Jones,et al.  Virtual in Vivo Interactive Dissection of White Matter Fasciculi in the Human Brain , 2002, NeuroImage.

[12]  Christopher Nimsky,et al.  Implementation of fiber tract navigation. , 2006, Neurosurgery.

[13]  T. Powell,et al.  The cortico-striate projection in the monkey. , 1970, Brain : a journal of neurology.

[14]  A. Rae.  The connections of the claustrum. , 1954, Confinia neurologica.

[15]  A. Rae.  The form and structure of the human claustrum , 1954, The Journal of comparative neurology.

[16]  Manuel Lopes,et al.  The Insular Lobe: Physiopathological and Surgical Considerations , 2000, Neurosurgery.

[17]  J. Dziewia̧tkowski,et al.  Comparative Anatomy of the Claustrum in Selected Species: A Morphometric Analysis , 1998, Brain, Behavior and Evolution.

[18]  Pratik Mukherjee,et al.  Diffusion-tensor imaging-guided tracking of fibers of the pyramidal tract combined with intraoperative cortical stimulation mapping in patients with gliomas. , 2004, Journal of neurosurgery.

[19]  P E Roland,et al.  Cross-Modal Transfer of Information between the Tactile and the Visual Representations in the Human Brain: A Positron Emission Tomographic Study , 1998, The Journal of Neuroscience.

[20]  H. Krude,et al.  Severe transitory encephalopathy with reversible lesions of the claustrum , 1996, Pediatric Radiology.

[21]  O. Narkiewicz,et al.  Degenerations in the claustrum after regional neocortical ablations in the cat , 1964, The Journal of comparative neurology.

[22]  Saleem I Abdulrauf,et al.  White matter fiber dissection of the optic radiations of the temporal lobe and implications for surgical approaches to the temporal horn. , 2004, Journal of neurosurgery.

[23]  C. Poupon,et al.  Regularization of Diffusion-Based Direction Maps for the Tracking of Brain White Matter Fascicles , 2000, NeuroImage.

[24]  Alexandra J. Golby,et al.  Functional identification of the primary motor area by corticospinal tractography. , 2005 .

[25]  J. Dejerine.  Anatomie des centres nerveux , 1895 .

[26]  Nathalie Tzourio-Mazoyer,et al.  New insights into the anatomo-functional connectivity of the semantic system: a study using cortico-subcortical electrostimulations. , 2005, Brain : a journal of neurology.

[27]  Laurent Capelle,et al.  Extension of paralimbic low grade gliomas: toward an anatomical classification based on white matter invasion patterns , 2006, Journal of Neuro-Oncology.

[28]  M. Yașargil,et al.  Topographic anatomy of the insular region. , 1999, Journal of neurosurgery.

[29]  Pratik Mukherjee,et al.  Subcortical pathways serving cortical language sites: initial experience with diffusion tensor imaging fiber tracking combined with intraoperative language mapping , 2004, NeuroImage.

[30]  T. P. S. Powell,et al.  The organization of the connections between the cortex and the claustrum in the monkey , 1982, Brain Research.

[31]  Z. Gokaslan,et al.  Surgical resection of intrinsic insular tumors: complication avoidance. , 2001, Journal of neurosurgery.

[32]  Jan Goffin,et al.  Anatomy of the Anterior Temporal Lobe and the Frontotemporal Region Demonstrated by Fiber Dissection , 2004, Neurosurgery.

[33]  S. Lehéricy,et al.  3-D diffusion tensor axonal tracking shows distinct SMA and pre-SMA projections to the human striatum. , 2004, Cerebral cortex.

[34]  A. Alexander,et al.  White matter tractography using diffusion tensor deflection , 2003, Human brain mapping.

[35]  Alexandre Yasuda,et al.  Microsurgical anatomy of the insula and the sylvian fissure. , 2004, Journal of neurosurgery.

[36]  E. Bullmore,et al.  Response amplification in sensory-specific cortices during crossmodal binding. , 1999, Neuroreport.

[37]  Christopher Nimsky,et al.  Intraoperative diffusion-tensor MR imaging: shifting of white matter tracts during neurosurgical procedures--initial experience. , 2005, Radiology.

[38]  Kensuke Kawai,et al.  Functional Monitoring for Visual Pathway Using Real-time Visual Evoked Potentials and Optic-radiation Tractography , 2005, Neurosurgery.

[39]  A. Friedman,et al.  Fiber dissection technique: lateral aspect of the brain. , 2000, Neurosurgery.

[40]  H. Wiśniewski,et al.  Neuronal loss in the human claustrum following ulegyria , 1993, Brain Research.

[41]  M. Catani,et al.  The rises and falls of disconnection syndromes. , 2005, Brain : a journal of neurology.

[42]  L. Edelstein,et al.  The claustrum: a historical review of its anatomy, physiology, cytochemistry and functional significance. , 2004, Cellular and molecular biology.

[43]  D. Pandya,et al.  Fiber Pathways of the Brain , 2006 .

[44]  H. Osaka,et al.  Symmetrical External Capsule Lesions in a Patient with Herpes Simplex Encephalitis , 1994, Neuropediatrics.

[45]  D. Pandya,et al.  Segmentation of subcomponents within the superior longitudinal fascicle in humans: a quantitative, in vivo, DT-MRI study. , 2005, Cerebral cortex.

[46]  T. Dóczi,et al.  Tumours of the limbic and paralimbic systems , 2005, Acta Neurochirurgica.

[47]  Denis Le Bihan,et al.  Looking into the functional architecture of the brain with diffusion MRI , 2003, Nature Reviews Neuroscience.

[48]  C. Geula,et al.  Nucleus basalis (Ch4) and cortical cholinergic innervation in the human brain: Observations based on the distribution of acetylcholinesterase and choline acetyltransferase , 1988, The Journal of comparative neurology.

[49]  Xiaoguang Tong,et al.  Three-dimensional Relationships of The Optic Radiation , 2005, Neurosurgery.

[50]  S. Piantadosi,et al.  Spinal Cord Stimulation versus Repeated Lumbosacral Spine Surgery for Chronic Pain: A Randomized, Controlled Trial , 2005, Neurosurgery.

[51]  Kenji Ino,et al.  Combined use of tractography-integrated functional neuronavigation and direct fiber stimulation. , 2005, Journal of neurosurgery.

[52]  C. Koch,et al.  What is the function of the claustrum? , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[53]  Xiaoguang Tong,et al.  Three-dimensional relationships of the optic radiation. Commentary , 2005 .

[54]  Carl-Fredrik Westin,et al.  High-resolution line scan diffusion tensor MR imaging of white matter fiber tract anatomy. , 2002, AJNR. American journal of neuroradiology.

[55]  W. Cowan,et al.  The cortical projection upon the claustrum1 , 1964, Journal of neurology, neurosurgery, and psychiatry.

[56]  P. V. van Zijl,et al.  Three‐dimensional tracking of axonal projections in the brain by magnetic resonance imaging , 1999, Annals of neurology.

[57]  S. Wakana,et al.  Fiber tract-based atlas of human white matter anatomy. , 2004, Radiology.

[58]  G. Ettlinger,et al.  Cross-modal performance: behavioural processes, phylogenetic considerations and neural mechanisms , 1990, Behavioural Brain Research.

[59]  N. Swindale,et al.  Diffusion tensor fiber tracking shows distinct corticostriatal circuits in humans , 2004, Annals of neurology.

[60]  M. E. Corcoran,et al.  Susceptibility to Kindling and Neuronal Connections of the Anterior Claustrum , 2001, The Journal of Neuroscience.