The reliability of neuroanatomy as a predictor of eloquence: A review

Department of Neurosurgery, David Geffen School of Medicine at UCLA, Los Angeles, California 90095-7049, USA.
Neurosurgical FOCUS (Impact Factor: 2.11). 02/2010; 28(2):E3. DOI: 10.3171/2009.11.FOCUS09239
Source: PubMed


The adjacency of intracranial pathology to canonical regions of eloquence has long been considered a significant source of potential morbidity in the neurosurgical care of patients. Yet, several reports exist of patients who undergo resection of gliomas or other intracranial pathology in eloquent regions without adverse effects. This raises the question of whether anatomical and intracranial location can or should be used as a means of estimating eloquence. In this review, the authors systematically evaluate the factors that are known to affect anatomical-functional relationships, including anatomical, functional, pathology-related, and modality-specific sources of variability. This review highlights the unpredictability of functional eloquence based on anatomical features alone and the fact that patients should not be considered ineligible for surgical intervention based on anatomical considerations alone. Rather, neurosurgeons need to take advantage of modern technology and mapping techniques to create individualized maps and management plans. An individualized approach allows one to expand the number of patients who are considered for and who potentially may benefit from surgical intervention. Perhaps most importantly, an individualized approach to mapping patients with brain tumors ensures that the risk of iatrogenic functional injury is minimized while maximizing the extent of resection.

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    • "Several proposals for ‘surgical eloquence’ have been published, [38]–[40] but these are based on surface anatomy with presumed functionality, and not on functional outcome. This may not be the most reliable source for surgical planning [41]. Furthermore, localization information is often limited to lobe involvement or categorization by eloquence in reports of surgical outcome [5], [6], [42]. "
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    ABSTRACT: Intraoperative brain stimulation mapping reduces permanent postoperative deficits and extends tumor removal in resective surgery for glioma patients. Successful functional mapping is assumed to depend on the surgical team's expertise. In this study, glioma resection results are quantified and compared using a novel approach, so-called resection probability maps (RPM), exemplified by a surgical team comparison, here with long and short experience in mapping. Adult patients with glioma were included by two centers with two and fifteen years of mapping experience. Resective surgery was targeted at non-enhanced MRI extension and was limited by functional boundaries. Neurological outcome was compared. To compare resection results, we applied RPMs to quantify and compare the resection probability throughout the brain at 1 mm resolution. Considerations for spatial dependence and multiple comparisons were taken into account. The senior surgical team contributed 56, and the junior team 52 patients. The patient cohorts were comparable in age, preoperative tumor volume, lateralization, and lobe localization. Neurological outcome was similar between teams. The resection probability on the RPMs was very similar, with none (0%) of 703,967 voxels in left-sided tumors being differentially resected, and 124 (0.02%) of 644,153 voxels in right-sided tumors. RPMs provide a quantitative volumetric method to compare resection results, which we present as standard for quality assessment of resective glioma surgery because brain location bias is avoided. Stimulation mapping is a robust surgical technique, because the neurological outcome and functional-based resection results using stimulation mapping are independent of surgical experience, supporting wider implementation.
    PLoS ONE 09/2013; 8(9):e73353. DOI:10.1371/journal.pone.0073353 · 3.23 Impact Factor
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    • "High test–retest reliability is mandatory for achieving valid results. This is particularly true when brain mapping techniques are used in clinical applications with strong impact on neurological functions like, e.g., preoperative mapping of motor cortex representations to achieve total tumor resection (Gorlia et al., 2008; Lacroix et al., 2001) while preserving neurological functions (Duffau et al., 2005; Pouratian and Bookheimer, 2010). However, both fMRI and TMS are only indirect measures of neuronal representations. "
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    ABSTRACT: Introduction: Functional magnetic resonance imaging (fMRI) is a frequently used non-invasive mapping technique for investigating the human motor system. Recently, neuronavigated transcranial magnetic stimulation (nTMS) has been established as an alternative approach. We here compared the test-retest reliability of both mapping techniques with regard to the cortical representations of the hand, leg, face and tongue areas. Methods: Ten healthy subjects were examined three times (intervals: 3-5days/21-35days) with fMRI and nTMS. Motor-evoked potentials were recorded from the abductor pollicis brevis, plantaris, mentalis and the tongue muscles. The same muscles were activated in an fMRI motor task. Euclidean distances (ED) between hotspots and centers of gravity (CoG) were computed for the respective somatotopic representations. Furthermore, spatial reliability was tested by intersession overlap volumes (OV) and voxel-wise intraclass correlations (ICC). Results: Feasibility of fMRI was 100% for all body parts and sessions. In contrast, nTMS was feasible in all sessions and subjects only for the hand area, while mappings of the foot (90%), face (70%) and tongue representations (40%) remained incomplete in several subjects due to technical constraints and co-stimulation artifacts. On average, the mean ED of the hotspots was better for fMRI (6.2±1.1mm) compared to nTMS (10.8±1.9mm) while stability of CoG was similar for both methods. Peak voxel reliability (ICC) was high for both methods (>0.8), and there was no influence of inter-session intervals. In contrast, the reliability of mapping the spatial extent of the hand, foot, lips and tongue representations was poor to moderate for both fMRI and nTMS (OVs and ICC<50%). Especially nTMS mappings of the face and tongue areas yielded poor reliability estimates. Conclusion: Both methods are highly reliable when mapping the core region of a given target muscle, especially for the hand representation area. In contrast, mapping the spatial extent of a cortical representation area was only little reliable for both nTMS and fMRI. In summary, fMRI was better suited when mapping motor representations of the head, while nTMS showed equal reliability for mapping the hand and foot representation areas. Hence, both methods may well complement each other.
    NeuroImage 10/2012; 66. DOI:10.1016/j.neuroimage.2012.10.046 · 6.36 Impact Factor
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    • "So a future project might include the creation of pediatric masks. However, while anatomical localizers have been used in the past and have the merit to be easily and reproducibly applicable to larger groups and across studies, there is an inherent danger to over-interpret the structure–function correspondence (Pouratian and Bookheimer, 2010) even in adults, which is evident with more and more cytoarchitectonic reference data becoming available (Eickhoff et al., 2007). For children, with the brain undergoing substantial maturation both on the structural (Giedd et al., 1999; Wilke et al., 2002, 2003) as well as the functional (Johnson, 2001) level, we believe it is preferable to use functional localizers whenever feasible on theoretical grounds alone, and we suggest our results support this conclusion. "
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    ABSTRACT: In this study, we analyzed the structural connectivity of cortico-cortical and cortico-subcortical language networks in healthy children, using probabilistic tractography based on high angular resolution diffusion imaging. In addition to anatomically defining seed and target regions for tractography, we used fMRI to target inferior frontal and superior temporal cortical language areas on an individual basis. Further, connectivity between these cortical and subcortical (thalamus, caudate nucleus) language regions was assessed. Overall, data from 15 children (8f) aged 8-17years (mean age 12.1±3years) could be included. A slight but non-significant trend towards leftward lateralization was found in the arcuate fasciculus/superior longitudinal fasciculus (AF/SLF) using anatomically defined masks (p>.05, Wilcoxon rank test), while the functionally-guided tractography showed a significant lateralization to the left (p<.01). Connectivity of the thalamus with language regions was strong but not lateralized. Connectivity of the caudate nucleus with inferior-frontal language regions was also symmetrical, while connectivity with superior-temporal language regions was strongly lateralized to the left (p<.01). To conclude, we could show that tracking the arcuate fasciculus/superior longitudinal fasciculus is possible using both anatomically and functionally-defined seed and target regions. With the latter approach, we could confirm the presence of structurally-lateralized cortico-cortical language networks already in children, and finally, we could demonstrate a strongly asymmetrical connectivity of the caudate nucleus with superior temporal language regions. Further research is necessary in order to assess the usability of such an approach to assess language dominance in children unable to participate in an active fMRI study.
    NeuroImage 08/2012; 63(3):1561-70. DOI:10.1016/j.neuroimage.2012.07.060 · 6.36 Impact Factor
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