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Illusory limb movements activate different brain networks than imposed limb movements: an ALE meta-analysis

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Abstract

Proprioceptive information allows us to perform smooth coordinated movements by constantly updating us with knowledge of the position of our limbs in space. How this information is combined and processed to form conscious perceptions of limb position is still relatively unknown. Several functional neuroimaging studies have attempted to tease out the brain areas responsible for proprioceptive processing in the human brain. Yet there still exists some disagreement in the specific brain regions involved. In order to consolidate the current knowledge in the field, we performed a systematic review of the literature and an activation likelihood estimation (ALE) meta-analysis of functional neuroimaging studies of proprioception. We identified 12 studies that used a proprioceptive stimulus of the upper extremity for ALE analysis (n = 141 participants). Two types of stimuli (illusion of movement induced through muscle tendon vibration and passive/imposed movements) were found to be most commonly used to probe proprioceptive networks in the brain. ALE analysis of these two stimulus types revealed that both were associated with activation in the left precentral, postcentral, and anterior cingulate gyri. Interestingly, different patterns of activation were also observed between illusions of movement and imposed movement. In the left hemisphere, imposed movements resulted in activations that were more inferior in the post-central gyrus. In the right hemisphere, imposed movements resulted in two clusters of activation in the inferior aspect of the precentral gyrus and the hand area of the post-central gyrus, while illusions of movement resulted in a single cluster of activation in the inferior parietal lobule. These results suggest that illusions of movement without limb displacement may activate different brain areas compared with actual limb displacement. Careful consideration should be made in future studies when selecting a proprioceptive stimulus to probe these brain networks.

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Acknowledgements

This work was supported by the RHISE HBI-Melbourne Trainee Exchange Program (awarded to JMK and supervised by LMC; the program is co-supported by Rebecca Hotchkiss International Scholar Exchange and Hotchkiss Brain Institute, Calgary, and the University of Melbourne and Florey Institute of Neuroscience and Mental Health, Melbourne). JMK was supported by an Alberta-Innovates Health-Solutions MD/PhD studentship. The work was also supported by NHMRC project grant (APP1022684 to LMC); James S. McDonnell Foundation Collaborative Award (#220020413 to LMC); NHMRC Centre of Research Excellence in Stroke Rehabilitation and Brain Injury (#1077898 to LMC); Victorian Government’s Operational Infrastructure Support Program; an Australian Research Council Future Fellowship awarded to LMC [#FT0992299].

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Correspondence to Jeffrey M. Kenzie.

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This work was supported by a RHISE HBI-Melbourne Trainee Exchange Program (awarded to JMK and supervised by LMC; the program is co-supported by Rebecca Hotchkiss International Scholar Exchange and Hotchkiss Brain Institute, Calgary, and the University of Melbourne and Florey Institute of Neuroscience and Mental Health, Melbourne). JMK was supported by an Alberta-Innovates Health-Solutions MD/PhD studentship. The work was also supported by NHMRC project grant (APP1022684 to LMC); James S. McDonnell Foundation Collaborative Award (#220020413 to LMC); NHMRC Centre of Research Excellence in Stroke Rehabilitation and Brain Injury (#1077898 to LMC); Victorian Government’s Operational Infrastructure Support Program; an Australian Research Council Future Fellowship awarded to LMC [#FT0992299].

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Kenzie, J.M., Ben-Shabat, E., Lamp, G. et al. Illusory limb movements activate different brain networks than imposed limb movements: an ALE meta-analysis. Brain Imaging and Behavior 12, 919–930 (2018). https://doi.org/10.1007/s11682-017-9756-1

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