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      Computational analysis in epilepsy neuroimaging: A survey of features and methods

      review-article
      a , * , b , 1 , a , c , 1
      NeuroImage : Clinical
      Elsevier
      Multimodal neuroimaging, Epilepsy, Drug resistant epilepsy, Focal cortical dysplasia, Malformations of cortical development, Machine learning, FCD, focal cortical dysplasia, GM, gray matter, WM, white matter, T1W, T1-weighted MRI, T2W, T2-weighted MRI, DRE, drug resistant epilepsy, FLAIR, fluid-attenuated inversion recovery, VBM, voxel-based morphometry, SBM, surface-based morphometry, DWI, diffusion weighted imaging, DTI, diffusion tensor imaging, PET, positron emission tomography, GW, gray-white junction, HARDI, high angular resolution diffusion imaging, MEG, magnetoencephalography, MRS, magnetic resonance spectroscopy imaging, PNH, periventricular nodular heterotopia

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          Abstract

          Epilepsy affects 65 million people worldwide, a third of whom have seizures that are resistant to anti-epileptic medications. Some of these patients may be amenable to surgical therapy or treatment with implantable devices, but this usually requires delineation of discrete structural or functional lesion(s), which is challenging in a large percentage of these patients.

          Advances in neuroimaging and machine learning allow semi-automated detection of malformations of cortical development (MCDs), a common cause of drug resistant epilepsy. A frequently asked question in the field is what techniques currently exist to assist radiologists in identifying these lesions, especially subtle forms of MCDs such as focal cortical dysplasia (FCD) Type I and low grade glial tumors. Below we introduce some of the common lesions encountered in patients with epilepsy and the common imaging findings that radiologists look for in these patients. We then review and discuss the computational techniques introduced over the past 10 years for quantifying and automatically detecting these imaging findings. Due to large variations in the accuracy and implementation of these studies, specific techniques are traditionally used at individual centers, often guided by local expertise, as well as selection bias introduced by the varying prevalence of specific patient populations in different epilepsy centers. We discuss the need for a multi-institutional study that combines features from different imaging modalities as well as computational techniques to definitively assess the utility of specific automated approaches to epilepsy imaging. We conclude that sharing and comparing these different computational techniques through a common data platform provides an opportunity to rigorously test and compare the accuracy of these tools across different patient populations and geographical locations. We propose that these kinds of tools, quantitative imaging analysis methods and open data platforms for aggregating and sharing data and algorithms, can play a vital role in reducing the cost of care, the risks of invasive treatments, and improve overall outcomes for patients with epilepsy.

          Highlights

          • We introduce common epileptogenic lesions encountered in patients with drug resistant epilepsy.

          • We discuss state of the art computational techniques used to detect lesions.

          • There is a need for multi-institutional studies that combine these techniques.

          • Clinically validated pipelines alongside the advances in imaging and electrophysiology will improve outcomes.

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          Most cited references132

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          A developmental and genetic classification for malformations of cortical development: update 2012

          Malformations of cerebral cortical development include a wide range of developmental disorders that are common causes of neurodevelopmental delay and epilepsy. In addition, study of these disorders contributes greatly to the understanding of normal brain development and its perturbations. The rapid recent evolution of molecular biology, genetics and imaging has resulted in an explosive increase in our knowledge of cerebral cortex development and in the number and types of malformations of cortical development that have been reported. These advances continue to modify our perception of these malformations. This review addresses recent changes in our perception of these disorders and proposes a modified classification based upon updates in our knowledge of cerebral cortical development.
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            Automated 3-D extraction and evaluation of the inner and outer cortical surfaces using a Laplacian map and partial volume effect classification.

            Accurate reconstruction of the inner and outer cortical surfaces of the human cerebrum is a critical objective for a wide variety of neuroimaging analysis purposes, including visualization, morphometry, and brain mapping. The Anatomic Segmentation using Proximity (ASP) algorithm, previously developed by our group, provides a topology-preserving cortical surface deformation method that has been extensively used for the aforementioned purposes. However, constraints in the algorithm to ensure topology preservation occasionally produce incorrect thickness measurements due to a restriction in the range of allowable distances between the gray and white matter surfaces. This problem is particularly prominent in pediatric brain images with tightly folded gyri. This paper presents a novel method for improving the conventional ASP algorithm by making use of partial volume information through probabilistic classification in order to allow for topology preservation across a less restricted range of cortical thickness values. The new algorithm also corrects the classification of the insular cortex by masking out subcortical tissues. For 70 pediatric brains, validation experiments for the modified algorithm, Constrained Laplacian ASP (CLASP), were performed by three methods: (i) volume matching between surface-masked gray matter (GM) and conventional tissue-classified GM, (ii) surface matching between simulated and CLASP-extracted surfaces, and (iii) repeatability of the surface reconstruction among 16 MRI scans of the same subject. In the volume-based evaluation, the volume enclosed by the CLASP WM and GM surfaces matched the classified GM volume 13% more accurately than using conventional ASP. In the surface-based evaluation, using synthesized thick cortex, the average difference between simulated and extracted surfaces was 4.6 +/- 1.4 mm for conventional ASP and 0.5 +/- 0.4 mm for CLASP. In a repeatability study, CLASP produced a 30% lower RMS error for the GM surface and a 8% lower RMS error for the WM surface compared with ASP.
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              Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation.

              Neuronal activity causes local changes in cerebral blood flow, blood volume, and blood oxygenation. Magnetic resonance imaging (MRI) techniques sensitive to changes in cerebral blood flow and blood oxygenation were developed by high-speed echo planar imaging. These techniques were used to obtain completely noninvasive tomographic maps of human brain activity, by using visual and motor stimulus paradigms. Changes in blood oxygenation were detected by using a gradient echo (GE) imaging sequence sensitive to the paramagnetic state of deoxygenated hemoglobin. Blood flow changes were evaluated by a spin-echo inversion recovery (IR), tissue relaxation parameter T1-sensitive pulse sequence. A series of images were acquired continuously with the same imaging pulse sequence (either GE or IR) during task activation. Cine display of subtraction images (activated minus baseline) directly demonstrates activity-induced changes in brain MR signal observed at a temporal resolution of seconds. During 8-Hz patterned-flash photic stimulation, a significant increase in signal intensity (paired t test; P less than 0.001) of 1.8% +/- 0.8% (GE) and 1.8% +/- 0.9% (IR) was observed in the primary visual cortex (V1) of seven normal volunteers. The mean rise-time constant of the signal change was 4.4 +/- 2.2 s for the GE images and 8.9 +/- 2.8 s for the IR images. The stimulation frequency dependence of visual activation agrees with previous positron emission tomography observations, with the largest MR signal response occurring at 8 Hz. Similar signal changes were observed within the human primary motor cortex (M1) during a hand squeezing task and in animal models of increased blood flow by hypercapnia. By using intrinsic blood-tissue contrast, functional MRI opens a spatial-temporal window onto individual brain physiology.
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                Author and article information

                Contributors
                Journal
                Neuroimage Clin
                Neuroimage Clin
                NeuroImage : Clinical
                Elsevier
                2213-1582
                23 February 2016
                2016
                23 February 2016
                : 11
                : 515-529
                Affiliations
                [a ]Department of Bioengineering, University of Pennsylvania, 240 Skirkanich Hall, 210 South 33rd Street, Philadelphia, PA 19104-6321, USA
                [b ]Department of Radiology, Hospital of the University of Pennsylvania, Richards - 6th Floor, 3700 Hamilton Walk, Philadelphia, PA 19104-6116, USA
                [c ]Department of Neurology, Hospital of the University of Pennsylvania, 3400 Spruce Street, 3 West Gates Bldg., Philadelphia, PA 19104, USA
                Author notes
                [* ]Corresponding author. lkini@ 123456mail.med.upenn.edu
                [1]

                Co-senior authors.

                Article
                S2213-1582(16)30035-3
                10.1016/j.nicl.2016.02.013
                4833048
                27114900
                4cc66a25-2de3-4b37-9d5b-9538541e0d4a
                © 2016 The Authors

                This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

                History
                : 10 December 2015
                : 11 February 2016
                : 22 February 2016
                Categories
                Review Article

                multimodal neuroimaging,epilepsy,drug resistant epilepsy,focal cortical dysplasia,malformations of cortical development,machine learning,fcd, focal cortical dysplasia,gm, gray matter,wm, white matter,t1w, t1-weighted mri,t2w, t2-weighted mri,dre, drug resistant epilepsy,flair, fluid-attenuated inversion recovery,vbm, voxel-based morphometry,sbm, surface-based morphometry,dwi, diffusion weighted imaging,dti, diffusion tensor imaging,pet, positron emission tomography,gw, gray-white junction,hardi, high angular resolution diffusion imaging,meg, magnetoencephalography,mrs, magnetic resonance spectroscopy imaging,pnh, periventricular nodular heterotopia

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