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      Sentential Context Modulates the Involvement of the Motor Cortex in Action Language Processing: An fMRI Study

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          Abstract

          Theories of embodied cognition propose that language comprehension is based on perceptual and motor processes. More specifically, it is hypothesized that neurons processing verbs describing bodily actions, and those that process the corresponding physical actions, fire simultaneously during action verb learning. Thus the concept and motor activation become strongly linked. According to this view, the language-induced activation of the neural substrates for action is automatic. By contrast, a weak view of embodied cognition proposes that activation of these motor regions is modulated by context. In recent studies it was found that action verbs in literal sentences activate the motor system, while mixed results were observed for action verbs in non-literal sentences. Thus, whether the recruitment of motor regions is automatic or context dependent remains a question. We investigated functional magnetic resonance imaging activation in response to non-literal and literal sentences including arm and leg related actions. The sentence structure was such that the action verb was the last word in the subordinate clause. Thus, the constraining context was presented well before the verb. Region of interest analyses showed that action verbs in literal context engage the motor regions to a greater extent than non-literal action verbs. There was no evidence for a semantic somatotopic organization of the motor cortex. Taken together, these results indicate that during comprehension, the degree to which motor regions are recruited is context dependent, supporting the weak view of embodied cognition.

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          Most cited references28

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          Perceptual symbol systems.

          Prior to the twentieth century, theories of knowledge were inherently perceptual. Since then, developments in logic, statistics, and programming languages have inspired amodal theories that rest on principles fundamentally different from those underlying perception. In addition, perceptual approaches have become widely viewed as untenable because they are assumed to implement recording systems, not conceptual systems. A perceptual theory of knowledge is developed here in the context of current cognitive science and neuroscience. During perceptual experience, association areas in the brain capture bottom-up patterns of activation in sensory-motor areas. Later, in a top-down manner, association areas partially reactivate sensory-motor areas to implement perceptual symbols. The storage and reactivation of perceptual symbols operates at the level of perceptual components--not at the level of holistic perceptual experiences. Through the use of selective attention, schematic representations of perceptual components are extracted from experience and stored in memory (e.g., individual memories of green, purr, hot). As memories of the same component become organized around a common frame, they implement a simulator that produces limitless simulations of the component (e.g., simulations of purr). Not only do such simulators develop for aspects of sensory experience, they also develop for aspects of proprioception (e.g., lift, run) and introspection (e.g., compare, memory, happy, hungry). Once established, these simulators implement a basic conceptual system that represents types, supports categorization, and produces categorical inferences. These simulators further support productivity, propositions, and abstract concepts, thereby implementing a fully functional conceptual system. Productivity results from integrating simulators combinatorially and recursively to produce complex simulations. Propositions result from binding simulators to perceived individuals to represent type-token relations. Abstract concepts are grounded in complex simulations of combined physical and introspective events. Thus, a perceptual theory of knowledge can implement a fully functional conceptual system while avoiding problems associated with amodal symbol systems. Implications for cognition, neuroscience, evolution, development, and artificial intelligence are explored.
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            Imaging the premotor areas.

            Recent imaging studies of motor function provide new insights into the organization of the premotor areas of the frontal lobe. The pre-supplementary motor area and the rostral portion of the dorsal premotor cortex, the 'pre-PMd', are, in many respects, more like prefrontal areas than motor areas. Recent data also suggest the existence of separate functional divisions in the rostral cingulate zone.
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              Listening to action-related sentences activates fronto-parietal motor circuits.

              Observing actions made by others activates the cortical circuits responsible for the planning and execution of those same actions. This observation-execution matching system (mirror-neuron system) is thought to play an important role in the understanding of actions made by others. In an fMRI experiment, we tested whether this system also becomes active during the processing of action-related sentences. Participants listened to sentences describing actions performed with the mouth, the hand, or the leg. Abstract sentences of comparable syntactic structure were used as control stimuli. The results showed that listening to action-related sentences activates a left fronto-parieto-temporal network that includes the pars opercularis of the inferior frontal gyrus (Broca's area), those sectors of the premotor cortex where the actions described are motorically coded, as well as the inferior parietal lobule, the intraparietal sulcus, and the posterior middle temporal gyrus. These data provide the first direct evidence that listening to sentences that describe actions engages the visuomotor circuits which subserve action execution and observation.
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                Author and article information

                Journal
                Front Hum Neurosci
                Front Hum Neurosci
                Front. Hum. Neurosci.
                Frontiers in Human Neuroscience
                Frontiers Media S.A.
                1662-5161
                08 April 2013
                2013
                : 7
                : 100
                Affiliations
                [1] 1Erasmus University Rotterdam Rotterdam, Netherlands
                [2] 2Department of Radiology, Erasmus MC – University Medical Center Rotterdam Rotterdam, Netherlands
                Author notes

                Edited by: Barbara Tomasino, IRCCS E. Medea, Italy

                Reviewed by: Roel M. Willems, Donders Institute for Brain, Cognition and Behaviour, Netherlands; Frank Garcea, University of Rochester, USA

                *Correspondence: Karen D. I. Schuil, Institute of Psychology, Erasmus University Rotterdam, T 13-09 Burgemeester Oudlaan 50, Post Box 1738, 3000 DR Rotterdam, Netherlands. e-mail: schuil@ 123456fsw.eur.nl
                Article
                10.3389/fnhum.2013.00100
                3619111
                23580364
                89e38a0b-b5c6-4b20-af0b-67f5ecba08a4
                Copyright © 2013 Schuil, Smits and Zwaan.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in other forums, provided the original authors and source are credited and subject to any copyright notices concerning any third-party graphics etc.

                History
                : 28 November 2012
                : 09 March 2013
                Page count
                Figures: 9, Tables: 6, Equations: 0, References: 38, Pages: 13, Words: 9602
                Categories
                Neuroscience
                Original Research

                Neurosciences
                action simulation,embodied cognition,fmri,language comprehension,semantic somatotopy
                Neurosciences
                action simulation, embodied cognition, fmri, language comprehension, semantic somatotopy

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