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THE HUMAN BRAIN EVOLVING: Paleoneurological Studies in Honor of Ralph L

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THE HUMAN BRAIN EVOLVING: Paleoneurological Studies in Honor of Ralph L STONE AGE INSTITUTE PUBLICATION SERIES NUMBER 4 Series Editors Kathy Schick and Nicholas Toth THE HUMAN BRAIN EVOLVING: Paleoneurological Studies in Honor of Ralph L. Holloway Editors Douglas Broadfield Florida Atlantic University Michael Yuan Columbia University Kathy Schick Stone Age Institute & Indiana University Nicholas Toth Stone Age Institute & Indiana University Stone Age Institute Press · www.stoneageinstitute.org 1392 W. Dittemore Road · Gosport, IN 47433 FRONT COVER CAPTIONS Center: Portrait of Ralph L. Holloway. Upper left: A modern human brain. Upper right: Ralph measuring landmarks on an endocast ca. 1976. Lower right: Homo habilis cranium KNM-ER-1813 from Koobi Fora, Kenya (photo by Holloway). Lower left: Ralph with an endocast of the Flores “hobbit” cranium. Published by the Stone Age Institute. ISBN-10: 0-9792276-3-1 ISBN-13: 978-0-9792276-3-9 Copyright © 2010, Stone Age Institute Press. All right reserved under International and Pan-American Copyright Conventions. No part of this book may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, without permission in writing from the publisher. CHAPTER 11 STRUCTURAL AND DIFFUSION MRI OF A GORILLA BRAIN PERFORMED EX VIVO at 9.4 TESLA JASON A. KAUFMAN, J. MICHAEL TYSZKA, FRANCINE “PENNY” PattersON, JOSEPH M. ERWIN, PatrICK R. HOF, JOHN M. ALLMAN ABSTRACT they are intended…all the diversity of our sensation and our movements depends upon this.” Data on brain connectivity in great apes are difficult to obtain because of the lack of reliable ex vivo chemi- -Nicolaus Steno (1671) cal tracers and the preclusion of terminal experimenta- The heterogeneity of the brain’s white matter was tion using in vivo tracers. A new method for obtaining apparent even to 17th century anatomists whose dissec- connectivity data, called diffusion-weighted MRI, is tions of large-scale fiber bundles were painstakingly de- a variant of conventional MRI that allows researchers scribed and illustrated [for a comprehensive review see to measure the coherence and orientation of fiber tracts (Schmahmann and Pandya, 2006)]. But the functional within an entire brain. From these imaging data, tract- significance of these pathways remained largely mys- tracing algorithms have been developed to conduct non- terious until the development of methods for localizing invasive tractography. Here we apply high-field diffu- particular functions to particular regions of the brain. sion-weighted MRI and probabilistic tractography on an White matter connectivity between functional regions isolated, fixed gorilla brain. To test the reliability of this was inferred first from lesion/degeneration studies (e.g., method, we attempt to reconstruct two well-known fiber Damasio and Damasio, 1989; Goldman et al., 1971; pathways: the visual (retino-geniculo-striate) pathway, Pribram and Mishkin, 1955) and later from chemical and the corticospinal pathway. The results produced neuronal tracers (e.g., Barbas and Pandya, 1987; Van Es- excellent reproductions of these pathways, but also in- sen et al., 1986). However, the terminal nature of these cluded “false-positive” pathways caused by “tract-jump- experiments restricts their application to laboratory ani- ing” among adjacent fiber pathways. We conclude that mals and precludes their use in humans or apes. For this diffusion-weighted MRI constitutes an important new reason there has been an absence of comparative data tool for studying brain connectivity in humans and great on structural brain connectivity for humans and our ape apes, but researchers must be vigilant for false-positive relatives–data that could contain important phylogenetic pathways. signals on the evolution of the brain’s wiring scheme. Diffusion-weighted magnetic resonance imaging INTRODUCTION (DW-MRI) provides a new means for obtaining quan- titative data on white matter connectivity. DW-MRI is “To say that the white matter is but a uniform sensitive to the magnitude and spatial orientation of substance like wax in which there is no hidden con- Brownian water diffusion in tissue, which occurs more trivance, would be too low an opinion of nature’s readily along axon tracts than across them (Basser et al., finest masterpiece. We are assured that wherever 1994; LeBihan et al., 2001). The method is non-inva- in the body there are fibers, they everywhere adopt sive, and has been used successfully to trace known fiber a certain arrangement among themselves, created pathways in laboratory animals and in humans (Basser et more or less according to the functions for which al., 2000; Conturo et al,. 1999; Mori et al., 1999; Xue et 172 3 The Human Brain Evolving: Papers in Honor of Ralph L. Holloway Kaufman et al. 4 173 al., 1999), and to quantify the coherence of white matter Two series of scans were performed. The first was fiber tracts in healthy and diseased individuals (Barnea- a high-resolution 3D FLASH sequence, lasting approxi- Goraly et al., 2004; Michael, 2002; Moseley et al., 2002; mately 16 hours, with an anatomical resolution of 250 Neil et al., 2002; Nguyen et al., 2005; Ramnani et al., microns isotropic. The second series were high-angular- 2004; Sundgren et al., 2004). Technical advances in DW- resolution diffusion scans (PGHE) weighted isotropi- MRI have significantly improved the angular resolution cally along 72 directions. A series of 6 diffusion scans, of diffusion scanning (Jones et al., 1999), and an analyti- lasting approximately 36 hours in total, were averaged cal method has been developed to characterize the uncer- together in order to boost the signal-to-noise ratio, with a tainty associated with DW-MRI tract-tracing (Behrens et final resolution of 1mm isotropic. al., 2003b). This process, called probabilistic tractogra- All post-processing of the images were performed phy, has also recently been expanded to model crossing- using Amira (Mercury, San Diego) and the FSL suite fibers within voxels (Behrens et al., 2007). of MRI applications (Smith et al., 2004). For the diffu- Our purpose here is to demonstrate the feasibility of sion imaging, post-processing steps included corrections conducting DW-MRI tractography on an isolated, fixed for eddy-current distortions, followed by a computation brain using a high-field experimental imaging system. termed Bayesian Estimation of Diffusion Parameters Fixed tissue is entirely compatible with DW-MRI, and Obtained using Sampling Techniques (known as a BED- there are distinct advantages for imaging ex vivo as op- POST operation). This computation involves a Markov posed to in vivo: fixed tissue allows for extended scanning Chain Monte Carlo resampling technique to construct periods which substantially boosts the signal-to-noise ra- probability distributions for diffusion parameters within tio; and fixed tissue can be processed histologically fol- each voxel (Behrens et al., 2003b). The BEDPOST op- lowing scanning. (Obviously, functional imaging (fMRI) eration requires complex computations for every voxel is not possible ex vivo.) In this chapter, we present results within the brain, and the computing time can be substan- from an ex vivo structural–(i.e., grey-white contrast) and tial: in this case it took approximately two weeks of com- diffusion–MRI experiment on a gorilla brain conducted puting time on a high-end Linux workstation to complete on a 9.4 Tesla MRI system. To test the reliability of the the BEDPOST operation. For each tractography trial, probabilistic tractography method, we attempt to recon- 10,000 samples were drawn from the global probability struct two well-understood white matter pathways: the density function for each voxel in the seed mask. visual (retino-geniculo-striate) pathway and the motor Probabilistic tractography of the retino-geniculo- (corticospinal) pathway. striate pathway was performed using the method of Behrens et al. (Behrens et al., 2003a). Specifically, seeds METHODS were placed at the grey-white border surrounding the lateral geniculate nucleus (LGN). This single-mask ap- The brain is that of an adult male gorilla, named proach should identify projections both in the anterior Michael, who at the age of 27 succumbed to a myocar- direction (afferent fibers from the retina) and posterior dial disease characterized by deterioration of the heart’s direction (efferent fibers to the striate cortex). electrical conduction pathway. It is particularly impor- Tractography of the corticospinal tract was per- tant to note that careful prior preparations were made for formed using the method of Ciccarelli et al. (Ciccarelli quick and precise extraction of the brain with a minimal et al., 2006). First, the neocortex is segmented and the post-mortem interval. This type of preparation yields boundaries of primary motor cortex are defined both especially good tissue preservation, and should serve as morphologically (the posterior bank of the precentral a model for the compassionate use of tissue from great gyrus) and histologically by the presence of Betz cells apes who have died from natural causes. in Nissl-stained coronal sections. The M1 region-of- Within four hours post-mortem the brain was im- interest is then mapped into MRI space using an affine mersion fixed in 4% paraformaldehyde (freshly de- registration algorithm (Jenkinson and Smith, 2001). polymerized) and subsequently stored in phosphate- Next, a connectivity-based seed classification is per- buffered-saline with 0.01% sodium azide added as a formed on an axial mask through the internal capsule. preservative. This step identifies voxels within the posterior limb of An acrylic canister was constructed so that the brain the internal capsule mask that are most-likely to connect could be submerged in a high-viscosity perfluoropoly- with primary motor cortex. Probabilistic tractography is ether (Galden, Solvay Solexis) that has a zero MR sig- then performed from the motor cortex seed mask, with nal. The zero MR signal yields images of the brain in the condition that only projections passing through the “black” or “empty” space, thereby aiding in subsequent internal capsule mask are retained. In other words, the tissue segmentation.
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