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      Lesion mapping in acute stroke aphasia and its implications for recovery

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          Abstract

          Patients with stroke offer a unique window into understanding human brain function. Mapping stroke lesions poses several challenges due to the complexity of the lesion anatomy and the mechanisms causing local and remote disruption on brain networks. In this prospective longitudinal study, we compare standard and advanced approaches to white matter lesion mapping applied to acute stroke patients with aphasia. Eighteen patients with acute left hemisphere stroke were recruited and scanned within two weeks from symptom onset. Aphasia assessment was performed at baseline and six-month follow-up. Structural and diffusion MRI contrasts indicated an area of maximum overlap in the anterior external/extreme capsule with diffusion images showing a larger overlap extending into posterior perisylvian regions. Anatomical predictors of recovery included damage to ipsilesional tracts (as shown by both structural and diffusion images) and contralesional tracts (as shown by diffusion images only). These findings indicate converging results from structural and diffusion lesion mapping methods but also clear differences between the two approaches in their ability to identify predictors of recovery outside the lesioned regions.

          Highlights

          • Lesion mapping methods determine different lesion extents and associated outcomes.

          • Voxel-based methods are sensitive to lesions associated with aphasia recovery.

          • Diffusion data can reveal anatomical predictors of recovery beyond the lesion.

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          Most cited references49

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          Perisylvian language networks of the human brain.

          Early anatomically based models of language consisted of an arcuate tract connecting Broca's speech and Wernicke's comprehension centers; a lesion of the tract resulted in conduction aphasia. However, the heterogeneous clinical presentations of conduction aphasia suggest a greater complexity of perisylvian anatomical connections than allowed for in the classical anatomical model. This article re-explores perisylvian language connectivity using in vivo diffusion tensor magnetic resonance imaging tractography. Diffusion tensor magnetic resonance imaging data from 11 right-handed healthy male subjects were averaged, and the arcuate fasciculus of the left hemisphere reconstructed from this data using an interactive dissection technique. Beyond the classical arcuate pathway connecting Broca's and Wernicke's areas directly, we show a previously undescribed, indirect pathway passing through inferior parietal cortex. The indirect pathway runs parallel and lateral to the classical arcuate fasciculus and is composed of an anterior segment connecting Broca's territory with the inferior parietal lobe and a posterior segment connecting the inferior parietal lobe to Wernicke's territory. This model of two parallel pathways helps explain the diverse clinical presentations of conduction aphasia. The anatomical findings are also relevant to the evolution of language, provide a framework for Lichtheim's symptom-based neurological model of aphasia, and constrain, anatomically, contemporary connectionist accounts of language.
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            Assignment of functional activations to probabilistic cytoarchitectonic areas revisited.

            Probabilistic cytoarchitectonic maps in standard reference space provide a powerful tool for the analysis of structure-function relationships in the human brain. While these microstructurally defined maps have already been successfully used in the analysis of somatosensory, motor or language functions, several conceptual issues in the analysis of structure-function relationships still demand further clarification. In this paper, we demonstrate the principle approaches for anatomical localisation of functional activations based on probabilistic cytoarchitectonic maps by exemplary analysis of an anterior parietal activation evoked by visual presentation of hand gestures. After consideration of the conceptual basis and implementation of volume or local maxima labelling, we comment on some potential interpretational difficulties, limitations and caveats that could be encountered. Extending and supplementing these methods, we then propose a supplementary approach for quantification of structure-function correspondences based on distribution analysis. This approach relates the cytoarchitectonic probabilities observed at a particular functionally defined location to the areal specific null distribution of probabilities across the whole brain (i.e., the full probability map). Importantly, this method avoids the need for a unique classification of voxels to a single cortical area and may increase the comparability between results obtained for different areas. Moreover, as distribution-based labelling quantifies the "central tendency" of an activation with respect to anatomical areas, it will, in combination with the established methods, allow an advanced characterisation of the anatomical substrates of functional activations. Finally, the advantages and disadvantages of the various methods are discussed, focussing on the question of which approach is most appropriate for a particular situation.
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              The Neural Architecture of the Language Comprehension Network: Converging Evidence from Lesion and Connectivity Analyses

              While traditional models of language comprehension have focused on the left posterior temporal cortex as the neurological basis for language comprehension, lesion and functional imaging studies indicate the involvement of an extensive network of cortical regions. However, the full extent of this network and the white matter pathways that contribute to it remain to be characterized. In an earlier voxel-based lesion-symptom mapping analysis of data from aphasic patients (Dronkers et al., 2004), several brain regions in the left hemisphere were found to be critical for language comprehension: the left posterior middle temporal gyrus, the anterior part of Brodmann's area 22 in the superior temporal gyrus (anterior STG/BA22), the posterior superior temporal sulcus (STS) extending into Brodmann's area 39 (STS/BA39), the orbital part of the inferior frontal gyrus (BA47), and the middle frontal gyrus (BA46). Here, we investigated the white matter pathways associated with these regions using diffusion tensor imaging from healthy subjects. We also used resting-state functional magnetic resonance imaging data to assess the functional connectivity profiles of these regions. Fiber tractography and functional connectivity analyses indicated that the left MTG, anterior STG/BA22, STS/BA39, and BA47 are part of a richly interconnected network that extends to additional frontal, parietal, and temporal regions in the two hemispheres. The inferior occipito-frontal fasciculus, the arcuate fasciculus, and the middle and inferior longitudinal fasciculi, as well as transcallosal projections via the tapetum were found to be the most prominent white matter pathways bridging the regions important for language comprehension. The left MTG showed a particularly extensive structural and functional connectivity pattern which is consistent with the severity of the impairments associated with MTG lesions and which suggests a central role for this region in language comprehension.
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                Author and article information

                Contributors
                Journal
                Neuropsychologia
                Neuropsychologia
                Neuropsychologia
                Pergamon Press
                0028-3932
                1873-3514
                01 July 2018
                01 July 2018
                : 115
                : 88-100
                Affiliations
                [a ]Natbrainlab, King's College London, Department of Neuroimaging, Institute of Psychiatry, Psychology, and Neuroscience (IoPPN), De Crespigny Park, London SE5 8AF, United Kingdom
                [b ]Natbrainlab, Department of Forensic and Neurodevelopmental Sciences and Sackler Institute of Translational Neurodevelopment, Institute of Psychiatry, Psychology, and Neuroscience (IoPPN), King's College London De Crespigny Park, London SE5 8AF, United Kingdom
                Author notes
                [* ]Corresponding author at: Natbrainlab, King's College London, Department of Neuroimaging, Institute of Psychiatry, Psychology, and Neuroscience (IoPPN), De Crespigny Park, London SE5 8AF, United Kingdom. Stephanie.forkel@ 123456kcl.ac.uk
                Article
                S0028-3932(18)30129-5
                10.1016/j.neuropsychologia.2018.03.036
                6018610
                29605593
                b96cb4ef-84f5-47ae-a2fc-ed2de55ff834
                © 2018 The Author(s)

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

                History
                : 21 August 2017
                : 21 March 2018
                : 27 March 2018
                Categories
                Article

                Neurology
                lesion mapping,vlsm,white matter atlas,tractography,acute stroke,aphasia recovery
                Neurology
                lesion mapping, vlsm, white matter atlas, tractography, acute stroke, aphasia recovery

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