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Insula as the Interface Between Body Awareness and Movement: A Neurofeedback-Guided Kinesthetic Motor Imagery Study in Parkinson’s Disease

Intentional movement is an internally driven process that requires the integration of motivational and sensory cues with motor preparedness. In addition to the motor cortical-basal ganglia circuits, the limbic circuits are also involved in the integration of these cues. Individuals with Parkinson’s...

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Autores principales: Tinaz, Sule, Para, Kiran, Vives-Rodriguez, Ana, Martinez-Kaigi, Valeria, Nalamada, Keerthana, Sezgin, Mine, Scheinost, Dustin, Hampson, Michelle, Louis, Elan D., Constable, R. Todd
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6292989/
https://www.ncbi.nlm.nih.gov/pubmed/30581383
http://dx.doi.org/10.3389/fnhum.2018.00496
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author Tinaz, Sule
Para, Kiran
Vives-Rodriguez, Ana
Martinez-Kaigi, Valeria
Nalamada, Keerthana
Sezgin, Mine
Scheinost, Dustin
Hampson, Michelle
Louis, Elan D.
Constable, R. Todd
author_facet Tinaz, Sule
Para, Kiran
Vives-Rodriguez, Ana
Martinez-Kaigi, Valeria
Nalamada, Keerthana
Sezgin, Mine
Scheinost, Dustin
Hampson, Michelle
Louis, Elan D.
Constable, R. Todd
author_sort Tinaz, Sule
collection PubMed
description Intentional movement is an internally driven process that requires the integration of motivational and sensory cues with motor preparedness. In addition to the motor cortical-basal ganglia circuits, the limbic circuits are also involved in the integration of these cues. Individuals with Parkinson’s disease (PD) have a particular difficulty with internally generating intentional movements and maintaining the speed, size, and vigor of movements. This difficulty improves when they are provided with external cues suggesting that there is a problem with the internal motivation of movement in PD. The prevailing view attributes this difficulty in PD to the dysfunction of motor cortical-basal ganglia circuits. First, we argue that the standard cortical-basal ganglia circuit model of motor dysfunction in PD needs to be expanded to include the insula which is a major hub within the limbic circuits. We propose a neural circuit model highlighting the interaction between the insula and dorsomedial frontal cortex which is involved in generating intentional movements. The insula processes a wide range of sensory signals arising from the body and integrates them with the emotional and motivational context. In doing so, it provides the impetus to the dorsomedial frontal cortex to initiate and sustain movement. Second, we present the results of our proof-of-concept experiment demonstrating that the functional connectivity of the insula-dorsomedial frontal cortex circuit can be enhanced with neurofeedback-guided kinesthetic motor imagery using functional magnetic resonance imaging in subjects with PD. Specifically, we found that the intensity and quality of body sensations evoked during motor imagery and the emotional and motivational context of motor imagery determined the direction (i.e., negative or positive) of the insula-dorsomedial frontal cortex functional connectivity. After 10–12 neurofeedback sessions and “off-line” practice of the successful motor imagery strategies all subjects showed a significant increase in the insula-dorsomedial frontal cortex functional connectivity. Finally, we discuss the implications of these results regarding motor function in patients with PD and propose suggestions for future studies.
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spelling pubmed-62929892018-12-21 Insula as the Interface Between Body Awareness and Movement: A Neurofeedback-Guided Kinesthetic Motor Imagery Study in Parkinson’s Disease Tinaz, Sule Para, Kiran Vives-Rodriguez, Ana Martinez-Kaigi, Valeria Nalamada, Keerthana Sezgin, Mine Scheinost, Dustin Hampson, Michelle Louis, Elan D. Constable, R. Todd Front Hum Neurosci Neuroscience Intentional movement is an internally driven process that requires the integration of motivational and sensory cues with motor preparedness. In addition to the motor cortical-basal ganglia circuits, the limbic circuits are also involved in the integration of these cues. Individuals with Parkinson’s disease (PD) have a particular difficulty with internally generating intentional movements and maintaining the speed, size, and vigor of movements. This difficulty improves when they are provided with external cues suggesting that there is a problem with the internal motivation of movement in PD. The prevailing view attributes this difficulty in PD to the dysfunction of motor cortical-basal ganglia circuits. First, we argue that the standard cortical-basal ganglia circuit model of motor dysfunction in PD needs to be expanded to include the insula which is a major hub within the limbic circuits. We propose a neural circuit model highlighting the interaction between the insula and dorsomedial frontal cortex which is involved in generating intentional movements. The insula processes a wide range of sensory signals arising from the body and integrates them with the emotional and motivational context. In doing so, it provides the impetus to the dorsomedial frontal cortex to initiate and sustain movement. Second, we present the results of our proof-of-concept experiment demonstrating that the functional connectivity of the insula-dorsomedial frontal cortex circuit can be enhanced with neurofeedback-guided kinesthetic motor imagery using functional magnetic resonance imaging in subjects with PD. Specifically, we found that the intensity and quality of body sensations evoked during motor imagery and the emotional and motivational context of motor imagery determined the direction (i.e., negative or positive) of the insula-dorsomedial frontal cortex functional connectivity. After 10–12 neurofeedback sessions and “off-line” practice of the successful motor imagery strategies all subjects showed a significant increase in the insula-dorsomedial frontal cortex functional connectivity. Finally, we discuss the implications of these results regarding motor function in patients with PD and propose suggestions for future studies. Frontiers Media S.A. 2018-12-07 /pmc/articles/PMC6292989/ /pubmed/30581383 http://dx.doi.org/10.3389/fnhum.2018.00496 Text en Copyright © 2018 Tinaz, Para, Vives-Rodriguez, Martinez-Kaigi, Nalamada, Sezgin, Scheinost, Hampson, Louis and Constable. http://creativecommons.org/licenses/by/4.0/ 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.
spellingShingle Neuroscience
Tinaz, Sule
Para, Kiran
Vives-Rodriguez, Ana
Martinez-Kaigi, Valeria
Nalamada, Keerthana
Sezgin, Mine
Scheinost, Dustin
Hampson, Michelle
Louis, Elan D.
Constable, R. Todd
Insula as the Interface Between Body Awareness and Movement: A Neurofeedback-Guided Kinesthetic Motor Imagery Study in Parkinson’s Disease
title Insula as the Interface Between Body Awareness and Movement: A Neurofeedback-Guided Kinesthetic Motor Imagery Study in Parkinson’s Disease
title_full Insula as the Interface Between Body Awareness and Movement: A Neurofeedback-Guided Kinesthetic Motor Imagery Study in Parkinson’s Disease
title_fullStr Insula as the Interface Between Body Awareness and Movement: A Neurofeedback-Guided Kinesthetic Motor Imagery Study in Parkinson’s Disease
title_full_unstemmed Insula as the Interface Between Body Awareness and Movement: A Neurofeedback-Guided Kinesthetic Motor Imagery Study in Parkinson’s Disease
title_short Insula as the Interface Between Body Awareness and Movement: A Neurofeedback-Guided Kinesthetic Motor Imagery Study in Parkinson’s Disease
title_sort insula as the interface between body awareness and movement: a neurofeedback-guided kinesthetic motor imagery study in parkinson’s disease
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6292989/
https://www.ncbi.nlm.nih.gov/pubmed/30581383
http://dx.doi.org/10.3389/fnhum.2018.00496
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