Cargando…
Functional Connectivity between the Cerebellum and Somatosensory Areas Implements the Attenuation of Self-Generated Touch
Since the early 1970s, numerous behavioral studies have shown that self-generated touch feels less intense and less ticklish than the same touch applied externally. Computational motor control theories have suggested that cerebellar internal models predict the somatosensory consequences of our movem...
Autores principales: | , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Society for Neuroscience
2020
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6975290/ https://www.ncbi.nlm.nih.gov/pubmed/31811029 http://dx.doi.org/10.1523/JNEUROSCI.1732-19.2019 |
_version_ | 1783490260487897088 |
---|---|
author | Kilteni, Konstantina Ehrsson, H. Henrik |
author_facet | Kilteni, Konstantina Ehrsson, H. Henrik |
author_sort | Kilteni, Konstantina |
collection | PubMed |
description | Since the early 1970s, numerous behavioral studies have shown that self-generated touch feels less intense and less ticklish than the same touch applied externally. Computational motor control theories have suggested that cerebellar internal models predict the somatosensory consequences of our movements and that these predictions attenuate the perception of the actual touch. Despite this influential theoretical framework, little is known about the neural basis of this predictive attenuation. This is due to the limited number of neuroimaging studies, the presence of conflicting results about the role and the location of cerebellar activity, and the lack of behavioral measures accompanying the neural findings. Here, we combined psychophysics with fMRI to detect the neural processes underlying somatosensory attenuation in male and female healthy human participants. Activity in bilateral secondary somatosensory areas was attenuated when the touch was presented during a self-generated movement (self-generated touch) than in the absence of movement (external touch). An additional attenuation effect was observed in the cerebellum that is ipsilateral to the passive limb receiving the touch. Importantly, we further found that the degree of functional connectivity between the ipsilateral cerebellum and the contralateral primary and bilateral secondary somatosensory areas was linearly and positively related to the degree of behaviorally assessed attenuation; that is, the more participants perceptually attenuated their self-generated touches, the stronger this corticocerebellar coupling. Collectively, these results suggest that the ipsilateral cerebellum is fundamental in predicting self-generated touch and that this structure implements somatosensory attenuation via its functional connectivity with somatosensory areas. SIGNIFICANCE STATEMENT When we touch our hand with the other, the resulting sensation feels less intense than when another person or a machine touches our hand with the same intensity. Early computational motor control theories have proposed that the cerebellum predicts and cancels the sensory consequences of our movements; however, the neural correlates of this cancelation remain unknown. By means of fMRI, we show that the more participants attenuate the perception of their self-generated touch, the stronger the functional connectivity between the cerebellum and the somatosensory cortical areas. This provides conclusive evidence about the role of the cerebellum in predicting the sensory feedback of our movements and in attenuating the associated percepts via its connections to early somatosensory areas. |
format | Online Article Text |
id | pubmed-6975290 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2020 |
publisher | Society for Neuroscience |
record_format | MEDLINE/PubMed |
spelling | pubmed-69752902020-01-23 Functional Connectivity between the Cerebellum and Somatosensory Areas Implements the Attenuation of Self-Generated Touch Kilteni, Konstantina Ehrsson, H. Henrik J Neurosci Research Articles Since the early 1970s, numerous behavioral studies have shown that self-generated touch feels less intense and less ticklish than the same touch applied externally. Computational motor control theories have suggested that cerebellar internal models predict the somatosensory consequences of our movements and that these predictions attenuate the perception of the actual touch. Despite this influential theoretical framework, little is known about the neural basis of this predictive attenuation. This is due to the limited number of neuroimaging studies, the presence of conflicting results about the role and the location of cerebellar activity, and the lack of behavioral measures accompanying the neural findings. Here, we combined psychophysics with fMRI to detect the neural processes underlying somatosensory attenuation in male and female healthy human participants. Activity in bilateral secondary somatosensory areas was attenuated when the touch was presented during a self-generated movement (self-generated touch) than in the absence of movement (external touch). An additional attenuation effect was observed in the cerebellum that is ipsilateral to the passive limb receiving the touch. Importantly, we further found that the degree of functional connectivity between the ipsilateral cerebellum and the contralateral primary and bilateral secondary somatosensory areas was linearly and positively related to the degree of behaviorally assessed attenuation; that is, the more participants perceptually attenuated their self-generated touches, the stronger this corticocerebellar coupling. Collectively, these results suggest that the ipsilateral cerebellum is fundamental in predicting self-generated touch and that this structure implements somatosensory attenuation via its functional connectivity with somatosensory areas. SIGNIFICANCE STATEMENT When we touch our hand with the other, the resulting sensation feels less intense than when another person or a machine touches our hand with the same intensity. Early computational motor control theories have proposed that the cerebellum predicts and cancels the sensory consequences of our movements; however, the neural correlates of this cancelation remain unknown. By means of fMRI, we show that the more participants attenuate the perception of their self-generated touch, the stronger the functional connectivity between the cerebellum and the somatosensory cortical areas. This provides conclusive evidence about the role of the cerebellum in predicting the sensory feedback of our movements and in attenuating the associated percepts via its connections to early somatosensory areas. Society for Neuroscience 2020-01-22 /pmc/articles/PMC6975290/ /pubmed/31811029 http://dx.doi.org/10.1523/JNEUROSCI.1732-19.2019 Text en Copyright © 2020 Kilteni and Ehrsson https://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License Creative Commons Attribution 4.0 International (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed. |
spellingShingle | Research Articles Kilteni, Konstantina Ehrsson, H. Henrik Functional Connectivity between the Cerebellum and Somatosensory Areas Implements the Attenuation of Self-Generated Touch |
title | Functional Connectivity between the Cerebellum and Somatosensory Areas Implements the Attenuation of Self-Generated Touch |
title_full | Functional Connectivity between the Cerebellum and Somatosensory Areas Implements the Attenuation of Self-Generated Touch |
title_fullStr | Functional Connectivity between the Cerebellum and Somatosensory Areas Implements the Attenuation of Self-Generated Touch |
title_full_unstemmed | Functional Connectivity between the Cerebellum and Somatosensory Areas Implements the Attenuation of Self-Generated Touch |
title_short | Functional Connectivity between the Cerebellum and Somatosensory Areas Implements the Attenuation of Self-Generated Touch |
title_sort | functional connectivity between the cerebellum and somatosensory areas implements the attenuation of self-generated touch |
topic | Research Articles |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6975290/ https://www.ncbi.nlm.nih.gov/pubmed/31811029 http://dx.doi.org/10.1523/JNEUROSCI.1732-19.2019 |
work_keys_str_mv | AT kiltenikonstantina functionalconnectivitybetweenthecerebellumandsomatosensoryareasimplementstheattenuationofselfgeneratedtouch AT ehrssonhhenrik functionalconnectivitybetweenthecerebellumandsomatosensoryareasimplementstheattenuationofselfgeneratedtouch |