Clinical utility of functional magnetic resonance imaging for brain mapping in epilepsy surgery
Introduction
fMRI, which measures the blood oxygen level-dependent (BOLD) response (Ogawa et al., 1990) is a noninvasive methodology that is commonly used to localize functional brain areas. In the clinical setting, fMRI is increasingly being used to lateralize language function and to localize motor and language function (Hirsch et al., 2000, Ruge et al., 1999, Binder et al., 1996, Binder et al., 1997, Carpentier et al., 2001, Desmond et al., 1995, Gaillard et al., 2004, Rosenberger et al., 2009). However, the utility of fMRI in guiding surgical decision-making remains unclear. The ability to validate fMRI signal analysis with a more direct invasive method may help resolve this issue. Staged epilepsy surgery, where invasive electrodes are implanted in order to define the ictal onset and functional zones, provides an opportunity to correlate the noninvasive BOLD signal to more invasively obtained methods such as electrical stimulation mapping (ESM) in the extraoperative setting (Carpentier et al., 2001).
A good correlation has been demonstrated between language lateralization assessed using fMRI and the intracarotid amytal (Wada) test (Gaillard et al., 2004, Thesen et al., 2007). Localization of the motor cortex using BOLD signal has been accurate in some studies (Ruge et al., 1999). However, factors such as brain shift may limit their utility in patients undergoing electrode implantation for staged epilepsy surgery (Hill et al., 2000). Prior studies have shown poor sensitivity, specificity and predictive values of the location of the BOLD signal to areas defined by language using intraoperative ESM (Roux et al., 2003). The present study aims to assess the clinical utility of fMRI in the circumstance of extraoperative ESM with additional image processing is performed to account for the brain shift caused by the electrodes. Use of extraoperative ESM allows for more accurate integration and coregistration of intracranial electrodes while accounting for brain shift. In addition, time is permitted to perform reliability testing and to integrate ESM and fMRI data prior to the operative intervention that involves the possibility of resection.
Some studies have examined the effect of varying the threshold for activation for language localization in efforts to reduce Type 1 and Type 2 error, but no standard criteria exist (Loring et al., 2002). This type of analysis is critical for determining the clinical utility of fMRI and may be explored by examining the relationship between ESM and fMRI across a range of statistical values. A further analysis beyond the traditional post hoc analysis would be focused upon determining which ESM-positive sites do not show fMRI activation in order to determine whether certain areas should always be tested via ESM, regardless of fMRI activation. The present study investigates these issues in order to determine the clinical utility of fMRI language mapping in predicting the effects of extraoperative ESM.
Section snippets
Subjects
Four patients were used as subjects for this study. Demographics are shown in Table 1. All patients, after undergoing video electroencephalographic testing, MRI and neuropsychological assessment, were deemed candidates for epilepsy surgery based upon medication-resistant partial complex epilepsy. All subjects had normal MRI with no lesions, dysplasia or masses, and therefore, electrodes were implanted primarily in order to assess seizure localization. When electrodes were near regions of
Motor cortex
67 sites were tested with ESM for motor function of the hand in 2 subjects. ESM at 8 sites elicited motor response of the contralateral hand. For these sites, using a threshold of a T score of 2.5 (p < .01 corrected FDR), sensitivity for hand motor cortex was 1.0 and specificity was .96 for the two subjects where electrode contacts lay over the hand area of motor cortex (Fig. 1). PPV and NPV were 0.8 and 1.0, respectively. In the two remaining subjects an additional 10 sites were found on ESM
Sensitivity and specificity
Comparing the results of fMRI and ESM is complicated by the fact that fMRI involves the observation of normal function while ESM involves interference with function. Therefore, it may be hypothesized that fMRI could show participation of brain areas that are involved in, but not critical to, language function and that these areas overlap with critical sites identified by ESM. If this were the case, then the sensitivity would be high and the specificity would be low. Thus, the BOLD response may
Acknowledgements
Funding support is from the Page and Otto Marx Foundation. Additional support provided by the Feinstein Institute for Medical Research NSLIJ General Clinical Research Center, Grant #M01 RR018535 from the National Center for Research Resources (NCRR).
References (21)
- et al.
Improved optimization for the robust and accurate linear registration and motion correction of brain images
Neuroimage
(2002) - et al.
A global optimisation method for robust affine registration of brain images
Med. Image Anal.
(2001) - et al.
Now you see it now you don’t: statistical and methodological considerations in fMRI
Epilepsy Behav.
(2002) - et al.
Temporal autocorrelation in univariate linear modeling of fMRI data
Neuroimage
(2001) An improved theortical P value for SPMs based on discrete local maxima
Neuroimage
(2005)- Arora, J., Pugh, K.R., Westerveld, M., Spencer, S., Spencer, D.D., Constable, R.T., in press. Language lateralization...
- et al.
Human brain language areas identified by functional magnetic resonance imaging
J. Neurosci.
(1997) - et al.
Determination of language dominance using functional MRI: a comparison with the Wada test
Neurology
(1996) - et al.
Functional MRI of language processing: dependence on input modality and temporal lobe epilepsy
Epilepsia
(2001) - et al.
Functional MRI measurement of language lateralization in WADA-tested patients
Brain
(1995)
Cited by (22)
A Novel Functional Magnetic Resonance Imaging Paradigm for the Preoperative Assessment of Auditory Perception in a Musician Undergoing Temporal Lobe Surgery
2018, World NeurosurgeryCitation Excerpt :Although multiple studies have used fMRI to map the auditory processing pathways,1,11,12 its accuracy compared with the gold standard of extraoperative ESM has never been investigated.13-15 Furthermore, prior studies assessing the accuracy of fMRI used inconsistent methodologies for comparison both between and within studies.16-22 Although fMRI has been demonstrated to have a high positive predictive value for locating motor and language areas compared with ESM, the negative predictive value for fMRI locating functional areas of the brain, which in this case is essential for determining areas safe to surgically excise, is much more variable.16-22
Combining task-evoked and spontaneous activity to improve pre-operative brain mapping with fMRI
2016, NeuroImageCitation Excerpt :Now that our technique is validated with motor mapping, there is good motivation to begin testing it for language and memory. Pre-operative fMRI mapping of these functions tends to be less robust than motor mapping and thus there is greater need for improvement (Hirsch et al., 2000; Kapsalakis et al., 2012; Mehta and Klein, 2010). Further, there is good reason to think that our algorithm will prove useful in these other domains.
Clinical applications of the functional connectome
2013, NeuroImageCitation Excerpt :Clearly, a noninvasive methodology to image cortical function without sampling bias that is sensitive to activity in deeper regions and that does not disrupt function would be desirable. While task-based fMRI has been used extensively to study normal brain function, the clinical utility of this method has yet to be firmly established (Hill et al., 2000; Mehta and Klein, 2010; Roux et al., 2003). A major factor that limits clinical utility involves poor task performance in patients with cognitive impairment and neurological deficits — the very patients who need neurosurgical intervention (Pujol et al., 1998).
Language dominance in children with epilepsy: Concordance of fMRI with intracarotid amytal testing and cortical stimulation
2013, Epilepsy and BehaviorCitation Excerpt :In particular, language localization by fMRI in patients 5, 14, and 15 was confirmed by ESM, which positively mapped language in left frontal and temporal lobe regions. In a recent study by Mehta and Klein comparing fMRI with ESM, the language fMRI t-score was significantly higher under electrode sites that were associated with a language deficit during ESM testing [34]. In our cohort, ESM failed to identify language in 13 children.
AveLI: A robust lateralization index in functional magnetic resonance imaging using unbiased threshold-free computation
2012, Journal of Neuroscience MethodsCitation Excerpt :If a specific LI computational method were able to better estimate the recovery rate from strokes (Naccarato et al., 2006; Calautti et al., 2007, 2010), then that LI method would be optimal for that purpose. If we consider the congruence of LIs to the Wada test as the standard, the LI that best replicates the results of the Wada test is the optimal method (Desmond et al., 1995; Deblaere et al., 2002; Powell and Duncan, 2005; Chlebus et al., 2007; Kamada et al., 2007; Binder et al., 2008; Suarez et al., 2009; Jones et al., 2010; Mehta and Klein, 2010; Binder, 2011). In addition, quick and practical evaluations are essential in clinical situations (Fernández et al., 2001; Deblaere et al., 2002; Jones et al., 2010).