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      Comparison of Activation Patterns in Mirror Neurons and the Swallowing Network During Action Observation and Execution: A Task-Based fMRI Study

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          Abstract

          Background

          Observation of a goal-directed motor action can excite the respective mirror neurons, and this is the theoretical basis for action observation (AO) as a novel tool for functional recovery during stroke rehabilitation. To explore the therapeutic potential of AO for dysphagia, we conducted a task-based functional magnetic resonance imaging (fMRI) study to identify the brain areas activated during observation and execution of swallowing in healthy participants.

          Methods

          Twenty-nine healthy volunteers viewed the following stimuli during fMRI scanning: an action-video of swallowing (condition 1, defined as AO), a neutral image with a Chinese word for “watching” (condition 2), and a neutral image with a Chinese word for “swallowing” (condition 3). Action execution (AE) was defined as condition 3 minus condition 2. One-sample t-tests were performed to define the brain regions activated during AO and AE.

          Results

          Many brain regions were activated during AO, including the middle temporal gyrus, inferior frontal gyrus, pre- and postcentral gyrus, supplementary motor area, hippocampus, brainstem, and pons. AE resulted in activation of motor areas as well as other brain areas, including the inferior parietal lobule, vermis, middle frontal gyrus, and middle temporal gyrus. Two brain areas, BA6 and BA21, were activated with both AO and AE.

          Conclusion

          The left supplementary motor area (BA6) and left middle temporal gyrus (BA21), which contains mirror neurons, were activated in both AO and AE of swallowing. In this study, AO activated mirror neurons and the swallowing network in healthy participants, supporting its potential value in the treatment of dysphagia.

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          Most cited references45

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          Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging.

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            A multimodal cortical network for the detection of changes in the sensory environment.

            Sensory stimuli undergoing sudden changes draw attention and preferentially enter our awareness. We used event-related functional magnetic-resonance imaging (fMRI) to identify brain regions responsive to changes in visual, auditory and tactile stimuli. Unimodally responsive areas included visual, auditory and somatosensory association cortex. Multimodally responsive areas comprised a right-lateralized network including the temporoparietal junction, inferior frontal gyrus, insula and left cingulate and supplementary motor areas. These results reveal a distributed, multimodal network for involuntary attention to events in the sensory environment. This network contains areas thought to underlie the P300 event-related potential and closely corresponds to the set of cortical regions damaged in patients with hemineglect syndromes.
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              Mirror neurons: from origin to function.

              This article argues that mirror neurons originate in sensorimotor associative learning and therefore a new approach is needed to investigate their functions. Mirror neurons were discovered about 20 years ago in the monkey brain, and there is now evidence that they are also present in the human brain. The intriguing feature of many mirror neurons is that they fire not only when the animal is performing an action, such as grasping an object using a power grip, but also when the animal passively observes a similar action performed by another agent. It is widely believed that mirror neurons are a genetic adaptation for action understanding; that they were designed by evolution to fulfill a specific socio-cognitive function. In contrast, we argue that mirror neurons are forged by domain-general processes of associative learning in the course of individual development, and, although they may have psychological functions, they do not necessarily have a specific evolutionary purpose or adaptive function. The evidence supporting this view shows that (1) mirror neurons do not consistently encode action "goals"; (2) the contingency- and context-sensitive nature of associative learning explains the full range of mirror neuron properties; (3) human infants receive enough sensorimotor experience to support associative learning of mirror neurons ("wealth of the stimulus"); and (4) mirror neurons can be changed in radical ways by sensorimotor training. The associative account implies that reliable information about the function of mirror neurons can be obtained only by research based on developmental history, system-level theory, and careful experimentation.
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                Author and article information

                Contributors
                Journal
                Front Neurosci
                Front Neurosci
                Front. Neurosci.
                Frontiers in Neuroscience
                Frontiers Media S.A.
                1662-4548
                1662-453X
                21 August 2020
                2020
                : 14
                : 867
                Affiliations
                [1] 1Department of Rehabilitation Medicine, Guangzhou First People’s Hospital, School of Medicine, South China University of Technology , Guangzhou, China
                [2] 2Department of Rehabilitation Medicine, Guangzhou First People’s Hospital, Guangzhou Medical University , Guangzhou, China
                [3] 3Department of Rehabilitation Medicine, Beijing Tian Tan Hospital, Capital Medical University , Beijing, China
                [4] 4China National Clinical Research Center for Neurological Diseases , Beijing, China
                Author notes

                Edited by: Szilvia Anett Nagy, University of Pécs, Hungary

                Reviewed by: Jiu Chen, Nanjing Medical University, China; Lihua Qiu, The Second People’s Hospital of Yibin, China

                *Correspondence: Guang-qing Xu, guangchingx@ 123456163.com

                These authors have contributed equally to this work

                This article was submitted to Brain Imaging Methods, a section of the journal Frontiers in Neuroscience

                Article
                10.3389/fnins.2020.00867
                7472888
                32973431
                61abe8f2-df22-45eb-9b6c-f96470816e61
                Copyright © 2020 Jing, Lin, Li, Wu, Li, Ding, Wu, Xu and Lan.

                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) and the copyright owner(s) 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 June 2020
                : 27 July 2020
                Page count
                Figures: 4, Tables: 2, Equations: 0, References: 52, Pages: 10, Words: 0
                Funding
                Funded by: National Natural Science Foundation of China 10.13039/501100001809
                Award ID: 81772438
                Award ID: 81802227
                Award ID: 81974357
                Funded by: Science and Technology Planning Project of Guangdong Province 10.13039/501100012245
                Award ID: 2016A020213003
                Categories
                Neuroscience
                Original Research

                Neurosciences
                mirror neurons,swallowing network,action observation,action execution,functional magnetic resonance imaging

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