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      Lost for emotion words: What motor and limbic brain activity reveals about autism and semantic theory

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          Abstract

          Autism spectrum conditions (ASC) are characterised by deficits in understanding and expressing emotions and are frequently accompanied by alexithymia, a difficulty in understanding and expressing emotion words. Words are differentially represented in the brain according to their semantic category and these difficulties in ASC predict reduced activation to emotion-related words in limbic structures crucial for affective processing. Semantic theories view ‘emotion actions’ as critical for learning the semantic relationship between a word and the emotion it describes, such that emotion words typically activate the cortical motor systems involved in expressing emotion actions such as facial expressions. As ASC are also characterised by motor deficits and atypical brain structure and function in these regions, motor structures would also be expected to show reduced activation during emotion-semantic processing. Here we used event-related fMRI to compare passive processing of emotion words in comparison to abstract verbs and animal names in typically-developing controls and individuals with ASC. Relatively reduced brain activation in ASC for emotion words, but not matched control words, was found in motor areas and cingulate cortex specifically. The degree of activation evoked by emotion words in the motor system was also associated with the extent of autistic traits as revealed by the Autism Spectrum Quotient. We suggest that hypoactivation of motor and limbic regions for emotion word processing may underlie difficulties in processing emotional language in ASC. The role that sensorimotor systems and their connections might play in the affective and social-communication difficulties in ASC is discussed.

          Highlights

          • Motor and limbic cortices are typically activated by emotion words.

          • In ASC, activity in these key regions is reduced for this word type specifically.

          • Hypoactivity does not appear in brain regions unrelated to emotion word processing.

          • ASC motor systems' hypoactivity to emotion words correlates with symptomatology.

          • Motor deficits may help explain emotion processing problems and other ASC symptoms.

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          Most cited references 110

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          Grounded cognition.

          Grounded cognition rejects traditional views that cognition is computation on amodal symbols in a modular system, independent of the brain's modal systems for perception, action, and introspection. Instead, grounded cognition proposes that modal simulations, bodily states, and situated action underlie cognition. Accumulating behavioral and neural evidence supporting this view is reviewed from research on perception, memory, knowledge, language, thought, social cognition, and development. Theories of grounded cognition are also reviewed, as are origins of the area and common misperceptions of it. Theoretical, empirical, and methodological issues are raised whose future treatment is likely to affect the growth and impact of grounded cognition.
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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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              The functional role of the parieto-frontal mirror circuit: interpretations and misinterpretations.

              The parieto-frontal cortical circuit that is active during action observation is the circuit with mirror properties that has been most extensively studied. Yet, there remains controversy on its role in social cognition and its contribution to understanding the actions and intentions of other individuals. Recent studies in monkeys and humans have shed light on what the parieto-frontal cortical circuit encodes and its possible functional relevance for cognition. We conclude that, although there are several mechanisms through which one can understand the behaviour of other individuals, the parieto-frontal mechanism is the only one that allows an individual to understand the action of others 'from the inside' and gives the observer a first-person grasp of the motor goals and intentions of other individuals.
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                Author and article information

                Contributors
                Journal
                Neuroimage
                Neuroimage
                Neuroimage
                Academic Press
                1053-8119
                1095-9572
                01 January 2015
                01 January 2015
                : 104
                : 413-422
                Affiliations
                [a ]MRC Cognition and Brain Sciences Unit, Cambridge, UK
                [b ]Autism Research Centre, Department of Psychiatry, University of Cambridge, UK
                [c ]Centre for Functionally Integrative Neuroscience, Aarhus University, Denmark
                [d ]Centre for Cognition & Decision Making, Faculty of Psychology, Higher School of Economics, Moscow, Russia
                [e ]Charité Universitätsmedizin, Department of Psychiatry and Psychotherapy, Campus Benjamin Franklin, Berlin, Germany
                [f ]Department of Psychology, University of Cyprus, Cyprus
                [g ]Cambridgeshire and Peterborough NHS Foundation Trust, CLASS Clinic, UK
                [h ]Brain Language Laboratory, Department of Philosophy and Humanities, Freie Universität Berlin, Germany
                [i ]Center for Applied Neuroscience, University of Cyprus, Cyprus
                Author notes
                [* ]Corresponding author at: Autism Research Centre, Department of Psychiatry, University of Cambridge, Douglas House, 18b Trumpington Road, Cambridge CB2 8AH, UK. rachel.moseley@ 123456cantab.net
                Article
                S1053-8119(14)00788-5
                10.1016/j.neuroimage.2014.09.046
                4265725
                25278250
                © 2014 The Authors
                Categories
                Article

                Neurosciences

                semantics, emotion, embodied cognition, autism

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