Elsevier

NeuroImage

Volume 21, Issue 2, February 2004, Pages 616-622
NeuroImage

Subcortical pathways serving cortical language sites: initial experience with diffusion tensor imaging fiber tracking combined with intraoperative language mapping

https://doi.org/10.1016/j.neuroimage.2003.09.047Get rights and content

Abstract

The combination of mapping functional cortical neurons by intraoperative cortical stimulation and axonal architecture by diffusion tensor MRI fiber tracking can be used to delineate the pathways between functional regions. In this study the authors investigated the feasibility of combining these techniques to yield connectivity associated with motor speech and naming. Diffusion tensor MRI fiber tracking provides maps of axonal bundles and was combined with intraoperative mapping of eloquent cortex for a patient undergoing brain tumor surgery. Tracks from eight stimulated sites in the inferior frontal cortex including mouth motor, speech arrest, and anomia were generated from the diffusion tensor MRI data. The regions connected by the fiber tracking were compared to foci from previous functional imaging reports on language tasks. Connections were found between speech arrest, mouth motor, and anomia sites and the SMA proper and cerebral peduncle. The speech arrest and a mouth motor site were also seen to connect to the putamen via the external capsule. This is the first demonstration of delineation of subcortical pathways using diffusion tensor MRI fiber tracking with intraoperative cortical stimulation. The combined techniques may provide improved preservation of eloquent regions during neurological surgery, and may provide access to direct connectivity information between functional regions of the brain.

Introduction

Diffusion tensor magnetic resonance imaging (DT-MRI) fiber tracking provides us with the first technique that can noninvasively identify specific white matter tracts in the brain in vivo, and can delineate the subcortical path of these tracts Basser et al., 2000, Conturo et al., 1999, Jones et al., 1999, Mori et al., 1999. The DT-MRI fiber tracking technique can provide new information about white matter architecture and structural connectivity in normal and pathological conditions. While tracks can be generated, the relation of these tracks to specific functions is unknown. Functional mapping techniques complement the DT-MRI fiber tracking technique by providing seed regions of known functionality from which to initiate tracks.

In each voxel the dominant direction of the white matter tracts can be represented by the direction associated with the fastest diffusion or the maximum eigenvector (Basser et al., 2000). In the case where there are many fibers crossing each other within a voxel, the fiber direction will not be well defined. Therefore fiber tracking algorithms estimate the voxels that contribute to a contiguous tract by linking neighboring pixels that are colinear within a defined angular deviation Basser et al., 2000, Conturo et al., 1999, Jones et al., 1999, Mori et al., 1999. Intraoperative stimulation Berger, 1995, Berger and Ojemann, 1992, Berger and Ojemann, 1994, Ojemann et al., 1989, Penfield and Rasmussen, 1950, Skirboll et al., 1996 is the gold standard for identifying functional cortical areas but is somewhat limited in its ability to localize subcortical extensions of these neurons. Therefore the subcortical extensions of these functional areas are largely unknown and are often distorted from their normal arrangement by a mass lesion. DT-MRI fiber tracking can localize subcortical tracts. Although much is known about the functional arrangement of the brain in terms of specific cortical locations, within these areas there is much variation between individuals as to the exact location of the neurons associated with specific functions.

The overall aim of this work is to be able to associate functional information with the structural data from DT-MRI fiber tracking. In this manuscript are the results of DT-MRI fiber tracking in a patient undergoing intraoperative mapping during surgery to remove a brain tumor. The data from this patient illustrate the possibility of determination of previously unknown brain connections associated with speech and naming using these combined techniques. New models of motor speech have been formulated based on data from functional studies that suggest a widespread involvement of cortical and subcortical areas for speech. The results herein provide the first in vivo delineation of speech and naming pathways and are consistent with new models of motor speech that indicate the involvement of supplementary motor area, putamen, and corticospinal tracts.

Section snippets

Materials and methods

The patient is a 40-year-old, right-handed male who presented with a grand malseizure that included postictal speech arrest. The magnetic resonance imaging study demonstrated a large noncontrast enhancing intraaxial mass in the left frontotemporal region, consistent with a low-grade glial neoplasm. The patient's seizures were controlled with antiepileptic drugs, and he was referred to the Neurosurgery Service at our institution for a definitive surgical resection. This clinical research

Results

The intraoperative mapping on this patient identified eight regions corresponding to stimulation of jaw/mouth, mouth (two regions), speech arrest, and four regions (one in pars opercularis and three in precentral gyrus) resulting in anomia (inhibited object naming with intact speech). The MNI coordinates and estimated macroanatmical labels are shown (Table 1). DT-MRI fiber tracking resulted in tracks from all eight regions with connectivity to two to four regions for each site. The regions used

Discussion

This study represents the first human in vivo subcortical delineation of pathways involved in speech and naming using DT-MRI fiber tracking initiated from intraoperative cortical stimulation sites. The results indicate the involvement of the supplementary motor cortex, putamen, and cerebral peduncle in motor speech and illustrate the similar but distinct white matter connectivity associated with speech arrest, anomia, and mouth motor function. The identified pathways include cortico-spinal,

Acknowledgements

The support for Roland G. Henry by NIH/NCI K01 CA76998 is acknowledged. Thanks to Maria Luisa Gorno-Tempini and Howard Rosen for discussions on fMRI with language paradigms and to William P. Dillon for helpful critique and discussions.

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