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      Preoperative language lateralization in temporal lobe epilepsy (TLE) predicts peri-ictal, pre- and post-operative language performance: An fMRI study ☆☆

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          Abstract

          In patients with temporal lobe epilepsy (TLE), assessment of language lateralization is important as anterior temporal lobectomy may lead to language impairments. Despite the widespread use of fMRI, evidence of its usefulness in predicting postsurgical language performance is scant.

          We investigated whether preoperative functional lateralization is related to the preoperative language performance, peri-ictal aphasia, and can predict language outcome one year post-surgery.

          We studied a total of 72 TLE patients (42 left, 30 right), by using three fMRI tasks: Naming, Verb Generation and Fluency. Functional lateralization indices were analyzed with neuropsychological scores and presence of peri-ictal aphasia.

          The key findings are:

          • 1)

            Both left and right TLE patients show decreased left lateralization compared to controls.

          • 2)

            Lateralization correlates with language performance before surgery. In left TLE, decreased left lateralization correlates with better fluency performance. In right TLE, increased left lateralization during the Naming task correlates with better naming.

          • 3)

            Left lateralization correlates with peri-ictal aphasia in left TLE patients.

          • 4)

            Lateralization correlates with language performance after surgery. In a subgroup of left TLE who underwent surgery (17 left), decreased left lateralization is predictive of better naming performance at 6 and 12 months after surgery.

          The present study highlights the clinical relevance of fMRI language lateralization in TLE, especially to predict language outcome one year post-surgery. We also underline the importance of using fMRI tasks eliciting frontal and anterior temporal activations, when studying left and right TLE patients.

          Highlights

          • We used preoperative fMRI to predict language performance in 72 TLE patients.

          • Language lateralization is clinically important for left and right TLE patients.

          • Lateralization correlates with language performance before surgery.

          • Left lateralization correlates with peri-ictal aphasia in left TLE.

          • Left lateralization predicts language performance 1 year after surgery in left TLE.

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          Most cited references52

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          The ventral and inferolateral aspects of the anterior temporal lobe are crucial in semantic memory: evidence from a novel direct comparison of distortion-corrected fMRI, rTMS, and semantic dementia.

          Although there is an emerging consensus that the anterior temporal lobes (ATLs) are involved in semantic memory, it is currently unclear which specific parts of this region are implicated in semantic representation. Answers to this question are difficult to glean from the existing literature for 3 reasons: 1) lesions of relevant patient groups tend to encompass the whole ATL region; 2) while local effects of repetitive transcranial magnetic stimulation (rTMS) are spatially more specific, only the lateral aspects of the ATL are available to stimulation; and 3) until recently, functional magnetic resonance imaging (fMRI) studies were hindered by technical limitations such as signal distortion and dropout due to magnetic inhomogeneities and also, in some cases, by methodological factors, including a restricted field of view and the choice of baseline contrast for subtraction analysis. By utilizing the same semantic task across semantic dementia, rTMS, and distortion-corrected fMRI in normal participants, we directly compared the results across the 3 methods for the first time. The findings were highly convergent and indicated that crucial regions within the ATL for semantic representation include the anterior inferior temporal gyrus, anterior fusiform gyrus, and the anterior superior temporal sulcus.
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            Mapping anterior temporal lobe language areas with fMRI: a multicenter normative study.

            Removal of the anterior temporal lobe (ATL) is an effective surgical treatment for intractable temporal lobe epilepsy but carries a risk of language and verbal memory deficits. Preoperative localization of functional zones in the ATL might help reduce these risks, yet fMRI protocols in current widespread use produce very little activation in this region. Based on recent evidence suggesting a role for the ATL in semantic integration, we designed an fMRI protocol comparing comprehension of brief narratives (Story task) with a semantically shallow control task involving serial arithmetic (Math task). The Story > Math contrast elicited strong activation throughout the ATL, lateral temporal lobe, and medial temporal lobe bilaterally in an initial cohort of 18 healthy participants. The task protocol was then implemented at 6 other imaging centers using identical methods. Data from a second cohort of participants scanned at these centers closely replicated the results from the initial cohort. The Story-Math protocol provides a reliable method for activation of surgical regions of interest in the ATL. The bilateral activation supports previous claims that conceptual processing involves both temporal lobes. Used in combination with language lateralization measures, reliable ATL activation maps may be useful for predicting cognitive outcome in ATL surgery, though the validity of this approach needs to be established in a prospective surgical series. Copyright © 2010 Elsevier Inc. All rights reserved.
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              Language dominance in neurologically normal and epilepsy subjects: a functional MRI study.

              Language dominance and factors that influence language lateralization were investigated in right-handed, neurologically normal subjects (n = 100) and right-handed epilepsy patients (n = 50) using functional MRI. Increases in blood oxygenation-dependent signal during a semantic language activation task relative to a non-linguistic, auditory discrimination task provided an index of language system lateralization. As expected, the majority of both groups showed left hemisphere dominance, although a continuum of activation asymmetry was evident, with nearly all subjects showing some degree of right hemisphere activation. Using a categorical dominance classification, 94% of the normal subjects were considered left hemisphere dominant and 6% had bilateral, roughly symmetric language representation. None of the normal subjects had rightward dominance. There was greater variability of language dominance in the epilepsy group, with 78% showing left hemisphere dominance, 16% showing a symmetric pattern and 6% showing right hemisphere dominance. Atypical language dominance in the epilepsy group was associated with an earlier age of brain injury and with weaker right hand dominance. Language lateralization in the normal group was weakly related to age, but was not significantly related to sex, education, task performance or familial left-handedness.
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                Author and article information

                Contributors
                Journal
                Neuroimage (Amst)
                Neuroimage (Amst)
                NeuroImage : Clinical
                Elsevier
                2213-1582
                11 July 2013
                11 July 2013
                2013
                : 3
                : 73-83
                Affiliations
                [a ]Neuroradiology Dept., Fondazione IRCCS Istituto Neurologico “Carlo Besta”, Milano, Italy
                [b ]Scientific Dept., Fondazione IRCCS Istituto Neurologico “Carlo Besta”, Milano, Italy
                [c ]Health Dept., Fondazione IRCCS Istituto Neurologico “Carlo Besta”, Milano, Italy
                [d ]Brain MRI 3T Mondino Research Center, Istituto Neurologico “C. Mondino”, Pavia, Italy
                [e ]Neuropsychology Laboratory, Dept. of Clinical Neurosciences, Fondazione IRCCS Istituto Neurologico “Carlo Besta”, Milano, Italy
                [f ]Division of Clinical Epileptology and Experimental Neurophysiology, Fondazione IRCCS Istituto Neurologico “Carlo Besta”, Milano, Italy
                [g ]Neurosurgery Dept., Fondazione IRCCS Istituto Neurologico “Carlo Besta”, Milano, Italy
                [h ]Dept. of Neuroscience Bambino Gesù Children Hospital, Rome, Italy
                Author notes
                [* ]Corresponding author at: Scientific Department and Neuroradiology Dept., Fondazione IRCCS Istituto Neurologico “Carlo Besta”, Via Celoria 11, 20133 Milano, Italy. cristina.rosazza@ 123456istituto-besta.it
                [1]

                These authors gave equal contributions to the study.

                Article
                S2213-1582(13)00086-7
                10.1016/j.nicl.2013.07.001
                3807502
                24179851
                e2ae5cde-39ff-4afb-8084-56819fce4bbf
                © 2013 The Authors

                This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial-No Derivative Works License, which permits non-commercial use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 3 April 2013
                : 31 May 2013
                : 1 July 2013
                Categories
                Article

                temporal lobe epilepsy,language lateralization,functional mri,temporal lobectomy

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