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      Using a combination of fMRI and anterior temporal lobe rTMS to measure intrinsic and induced activation changes across the semantic cognition network

      research-article
      a , b , a , *
      Neuropsychologia
      Pergamon Press
      Semantic cognition, TMS, fMRI, Anterior temporal lobe

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          Abstract

          By developing and applying a method which combines fMRI and rTMS to explore semantic cognition, we identified both intrinsic (related to automatic changes in task/stimulus-related processing) and induced (i.e., associated with the effect of TMS) activation changes in the core, functionally-coupled network elements. Low-frequency rTMS applied to the human anterior temporal lobe (ATL) induced: (a) a local suppression at the site of stimulation; (b) remote suppression in three other ipsilateral semantic regions; and (c) a compensatory up-regulation in the contralateral ATL. Further examination of activity over time revealed that the compensatory changes appear to be a modulation of intrinsic variations that occur within the unperturbed network. As well as providing insights into the dynamic collaboration between core regions, the ability to observe intrinsic and induced changes in vivo may provide an important opportunity to understand the key mechanisms that underpin recovery of function in neurological patient groups.

          Highlights

          • First use of combined fMRI and rTMS to explore semantic cognition.

          • Intrinsic-automatic and TMS-induced activation changes were identified.

          • rTMS induced local suppression and up-regulation in the contralateral ATL.

          • Compensatory changes relate to intrinsic variations in the unperturbed network.

          • These key mechanisms may underpin recovery of function in neurological patients.

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          Most cited references51

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          Unified segmentation

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            Role of left inferior prefrontal cortex in retrieval of semantic knowledge: a reevaluation.

            A number of neuroimaging findings have been interpreted as evidence that the left inferior frontal gyrus (IFG) subserves retrieval of semantic knowledge. We provide a fundamentally different interpretation, that it is not retrieval of semantic knowledge per se that is associated with left IFG activity but rather selection of information among competing alternatives from semantic memory. Selection demands were varied across three semantic tasks in a single group of subjects. Functional magnetic resonance imaging signal in overlapping regions of left IFG was dependent on selection demands in all three tasks. In addition, the degree of semantic processing was varied independently of selection demands in one of the tasks. The absence of left IFG activity for this comparison counters the argument that the effects of selection can be attributed solely to variations in degree of semantic retrieval. Our findings suggest that it is selection, not retrieval, of semantic knowledge that drives activity in the left IFG.
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              Semantic processing in the anterior temporal lobes: a meta-analysis of the functional neuroimaging literature.

              The role of the anterior temporal lobes (ATLs) in semantic cognition is not clear from the current literature. Semantic dementia patients show a progressive and a specific semantic impairment, following bilateral atrophy of the ATLs. Neuroimaging studies of healthy participants, however, do not consistently show ATL activation during semantic tasks. Consequently, several influential theories of semantic memory do not ascribe a central role to the ATLs. We conducted a meta-analysis of 164 functional neuroimaging studies of semantic processing to investigate factors that might contribute to the inconsistency in previous results. Four factors influenced the likelihood of finding ATL activation: (1) the use of PET versus fMRI, reflecting the fact that fMRI but not PET is sensitive to distortion artifacts caused by large variations in magnetic susceptibility in the area of the ATL; (2) a field of view (FOV) of more than 15 cm, thereby ensuring whole-brain coverage; (3) the use of a high baseline task to prevent subtraction of otherwise uncontrolled semantic activation; (4) the inclusion of the ATL as an ROI. The type of stimuli or task did not influence the likelihood of ATL activation, consistent with the view that this region underpins an amodal semantic system. Spoken words, written words, and picture stimuli produced overlapping ATL peaks. On average, these were more inferior for picture-based tasks. We suggest that the specific pattern of ATL activation may be influenced by stimulus type due to variations across this region in the degree of connectivity with modality-specific areas in posterior temporal cortex.
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                Author and article information

                Contributors
                Journal
                Neuropsychologia
                Neuropsychologia
                Neuropsychologia
                Pergamon Press
                0028-3932
                1873-3514
                1 September 2015
                September 2015
                : 76
                : 170-181
                Affiliations
                [a ]Neuroscience and Aphasia Research Unit (NARU), School of Psychological Sciences, University of Manchester, UK
                [b ]Eleanor M. Saffran Center for Cognitive Neuroscience, Temple University, Philadelphia, PA, USA
                Author notes
                [* ]Correspondence to: Neuroscience and Aphasia Research Unit (NARU), Zochonis Building, School of Psychological Sciences, University of Manchester, Oxford Road, Manchester, M13 9PL, UK. Fax: +44 161 275 2873. matt.lambon-ralph@ 123456manchester.ac.uk
                Article
                S0028-3932(14)00421-7
                10.1016/j.neuropsychologia.2014.11.009
                4582802
                25448851
                38d62e5b-4746-41f4-84b0-dbd6c1467d54
                © 2014 The Authors

                This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/3.0/).

                History
                : 22 August 2014
                : 3 November 2014
                : 7 November 2014
                Categories
                Article

                Neurology
                semantic cognition,tms,fmri,anterior temporal lobe
                Neurology
                semantic cognition, tms, fmri, anterior temporal lobe

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