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      Lexical-Semantic Search Under Different Covert Verbal Fluency Tasks: An fMRI Study

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          Abstract

          Background: Verbal fluency is a measure of cognitive flexibility and word search strategies that is widely used to characterize impaired cognitive function. Despite the wealth of research on identifying and characterizing distinct aspects of verbal fluency, the anatomic and functional substrates of retrieval-related search and post-retrieval control processes still have not been fully elucidated.

          Methods: Twenty-one native English-speaking, healthy, right-handed, adult volunteers (mean age = 31 years; range = 21–45 years; 9 F) took part in a block-design functional Magnetic Resonance Imaging (fMRI) study of free recall, covert word generation tasks when guided by phonemic (P), semantic-category (C), and context-based fill-in–the-blank sentence completion (S) cues. General linear model (GLM), Independent Component Analysis (ICA), and psychophysiological interaction (PPI) were used to further characterize the neural substrate of verbal fluency as a function of retrieval cue type.

          Results: Common localized activations across P, C, and S tasks occurred in the bilateral superior and left inferior frontal gyrus, left anterior cingulate cortex, bilateral supplementary motor area (SMA), and left insula. Differential task activations were centered in the occipital, temporal and parietal regions as well as the thalamus and cerebellum. The context-based fluency task, i.e., the S task, elicited higher differential brain activity in a lateralized frontal-temporal network typically engaged in complex language processing. P and C tasks elicited activation in limited pathways mainly within the left frontal regions. ICA and PPI results of the S task suggested that brain regions distributed across both hemispheres, extending beyond classical language areas, are recruited for lexical-semantic access and retrieval during sentence completion.

          Conclusion: Study results support the hypothesis of overlapping, as well as distinct, neural networks for covert word generation when guided by different linguistic cues. The increased demand on word retrieval is met by the concurrent recruitment of classical as well as non-classical language-related brain regions forming a large cognitive neural network. The retrieval-related search and post-retrieval control processes that subserve verbal fluency, therefore, reverberates across distinct functional networks as determined by respective task demands.

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          Most cited references99

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          Meta-analyzing left hemisphere language areas: phonology, semantics, and sentence processing.

          The advent of functional neuroimaging has allowed tremendous advances in our understanding of brain-language relationships, in addition to generating substantial empirical data on this subject in the form of thousands of activation peak coordinates reported in a decade of language studies. We performed a large-scale meta-analysis of this literature, aimed at defining the composition of the phonological, semantic, and sentence processing networks in the frontal, temporal, and inferior parietal regions of the left cerebral hemisphere. For each of these language components, activation peaks issued from relevant component-specific contrasts were submitted to a spatial clustering algorithm, which gathered activation peaks on the basis of their relative distance in the MNI space. From a sample of 730 activation peaks extracted from 129 scientific reports selected among 260, we isolated 30 activation clusters, defining the functional fields constituting three distributed networks of frontal and temporal areas and revealing the functional organization of the left hemisphere for language. The functional role of each activation cluster is discussed based on the nature of the tasks in which it was involved. This meta-analysis sheds light on several contemporary issues, notably on the fine-scale functional architecture of the inferior frontal gyrus for phonological and semantic processing, the evidence for an elementary audio-motor loop involved in both comprehension and production of syllables including the primary auditory areas and the motor mouth area, evidence of areas of overlap between phonological and semantic processing, in particular at the location of the selective human voice area that was the seat of partial overlap of the three language components, the evidence of a cortical area in the pars opercularis of the inferior frontal gyrus dedicated to syntactic processing and in the posterior part of the superior temporal gyrus a region selectively activated by sentence and text processing, and the hypothesis that different working memory perception-actions loops are identifiable for the different language components. These results argue for large-scale architecture networks rather than modular organization of language in the left hemisphere.
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            Constructing inferences during narrative text comprehension.

            The authors describe a constructionist theory that accounts for the knowledge-based inferences that are constructed when readers comprehend narrative text. Readers potentially generate a rich variety of inferences when they construct a referential situation model of what the text is about. The proposed constructionist theory specifies that some, but not all, of this information is constructed under most conditions of comprehension. The distinctive assumptions of the constructionist theory embrace a principle of search (or effort) after meaning. According to this principle, readers attempt to construct a meaning representation that addresses the reader's goals, that is coherent at both local and global levels, and that explains why actions, events, and states are mentioned in the text. This study reviews empirical evidence that addresses this theory and contrasts it with alternative theoretical frameworks.
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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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                Author and article information

                Contributors
                Journal
                Front Behav Neurosci
                Front Behav Neurosci
                Front. Behav. Neurosci.
                Frontiers in Behavioral Neuroscience
                Frontiers Media S.A.
                1662-5153
                08 August 2017
                2017
                : 11
                : 131
                Affiliations
                [1] 1Department of Radiology, Pennsylvania State University College of Medicine Hershey, PA, United States
                [2] 2Department of Psychology and Center for Brain, Behavior, and Cognition, Pennsylvania State University University Park, PA, United States
                [3] 3Department of Neurosurgery, Pennsylvania State University College of Medicine Hershey, PA, United States
                [4] 4Department of Neurology, Pennsylvania State University College of Medicine Hershey, PA, United States
                [5] 5Department of Neural and Behavioral Sciences, Pennsylvania State University College of Medicine Hershey, PA, United States
                Author notes

                Edited by: Pietro Pietrini, IMT School for Advanced Studies Lucca, Italy

                Reviewed by: Valentina Bambini, Istituto Universitario di Studi Superiori di Pavia (IUSS), Italy; Wenhai Zhang, Chengdu University, China

                *Correspondence: Prasanna Karunanayaka pkarunanayaka@ 123456pennstatehealth.psu.edu
                Article
                10.3389/fnbeh.2017.00131
                5550713
                28848407
                92943d2e-3e55-4198-b97f-5915976021ca
                Copyright © 2017 Li, Li, Yang, Eslinger, Sica and Karunanayaka.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 04 February 2017
                : 30 June 2017
                Page count
                Figures: 6, Tables: 3, Equations: 0, References: 119, Pages: 15, Words: 10875
                Categories
                Neuroscience
                Original Research

                Neurosciences
                fmri,neuropsychology,language,verbal fluency,semantics,phonemic,sentence completion
                Neurosciences
                fmri, neuropsychology, language, verbal fluency, semantics, phonemic, sentence completion

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