Noninvasive identification of human central sulcus: a comparison of gyral morphology, functional MRI, dipole localization, and direct cortical mapping

Abstract

The locations of the human primary hand cortical somatosensory and motor areas were estimated using structural and functional MRI, scalp-recorded somatosensory-evoked potential dipole localization, expert judgments based on cortical anatomy, and direct cortical stimulation and recording studies. The within-subject reliability of localization (across 3 separate days) was studied for eight normal subjects. Intraoperative validation was obtained from five neurosurgical patients. The mean discrepancy between the different noninvasive functional imaging methods ranged from 6 to 26 mm. Quantitative comparison of the noninvasive methods with direct intraoperative stimulation and recording studies did not reveal a significant mean difference in accuracy. However, the expert judgments of the location of the sensory hand areas were significantly more variable (maximum error, 39 mm) than the dipole or functional MRI techniques. It is concluded that because expert judgments are less reliable for identifying the cortical hand area, consideration of the findings of noninvasive functional MRI and dipole localization studies is desirable for preoperative surgical planning.

Introduction

The development of accurate noninvasive techniques for determining the location of the human primary motor and sensory cortex is of interest to researchers in a variety of areas, particularly those interested in functional localization Geyer et al 2000, Van Essen et al 2000, cortical plasticity Pons et al 1991, Mogilner et al 1993, Wunderlich et al 1998, Chu et al 2000, and stroke Jenkins and Merzenich 1987, Chollet et al 1991, Cao et al 1998. Such information is of practical value as an aid in planning neurosurgical procedures involving the Rolandic area but, with few exceptions Stapleton et al 1997, Mine et al 1998, Pujol et al 1998, is still obtained through surgical procedures (King and Schell, 1987; Burchiel et al., 1989; Berger et al 1989, Suzuki and Yasui 1992, Hirsch et al 2000. Because of the known relationship of primary sensory and motor cortex to the central sulcus, several noninvasive strategies have been proposed to identify this sulcus on the basis of gyral morphology as seen on CT or MRI Kido et al 1980, Iwasaki et al 1991, Naidich et al 1995, Yousry et al 1997. Unfortunately, such morphologically based judgements have only rarely been verified by alternate means (Berger et al., 1990; White et al., 1997) and have been found to be unreliable across observers Sobel et al 1993, Kennedy et al 1998. In such a situation, converging evidence from independent techniques would increase the confidence that the central sulcus has been correctly identified. Potential confirmation can be sought through noninvasive functional imaging techniques such as positron emission tomography (PET) Fox et al 1987, Nyberg et al 1996, Bittar et al 1999, functional magnetic resonance imaging (fMRI) Hammeke et al 1994, Rao et al 1995, Lin et al 1996, Sakai et al 1995, transcranial magnetic stimulation (Krings et al., 1999), and dipole source localization using magnetoencephalography (MEG) Hari et al 1984, Gallen et al 1993, Yang et al 1993 Kristeva-Feige et al., 1994) or electroencephalographic (EEG) recordings Henderson et al 1975, Suk et al 1991, Buchner et al 1994, Buchner et al 1995, Nakamura et al 1998.

Direct cortical stimulation is widely accepted as a the best means for identifying the motor and sensory cortex in awake humans Penfield and Boldrey 1937, Berger and Rostomily 1997. Somatosensory evoked potentials (SEPs) recorded directly from the surface of the brain have also been used to identify primary sensory cortex during surgery as a means to reduce postoperative morbidity Woolsey et al 1979, Wood et al 1988, Allison 1982; Allison et al 1989, Allison et al 1989. In this study we compare (1) expert judgments based on gyral morphology, (2) sensory and motor functional MRI activations of the hand, and (3) noninvasive scalp dipole localization studies of the hand sensory area to (4) direct mapping studies of the sensory and motor cortices to determine which of these noninvasive procedures most accurately reflects intraoperative findings. Their location and reliability are described for normal subjects, and their accuracy and validity are assessed through quantitative comparisons with direct surgical mapping studies.