Disintegration of Multisensory Signals from the Real Hand Reduces Default Limb Self-Attribution: An fMRI Study
Identifieur interne : 002875 ( Ncbi/Merge ); précédent : 002874; suivant : 002876Disintegration of Multisensory Signals from the Real Hand Reduces Default Limb Self-Attribution: An fMRI Study
Auteurs : Giovanni Gentile [Suède] ; Arvid Guterstam [Suède] ; Claudio Brozzoli [Suède] ; H. Henrik Ehrsson [Suède]Source :
- The Journal of Neuroscience [ 0270-6474 ] ; 2013.
Abstract
The perception of our limbs in space is built upon the integration of visual, tactile, and proprioceptive signals. Accumulating evidence suggests that these signals are combined in areas of premotor, parietal, and cerebellar cortices. However, it remains to be determined whether neuronal populations in these areas integrate hand signals according to basic temporal and spatial congruence principles of multisensory integration. Here, we developed a setup based on advanced 3D video technology that allowed us to manipulate the spatiotemporal relationships of visuotactile (
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DOI: 10.1523/JNEUROSCI.1363-13.2013
PubMed: 23946393
PubMed Central: 3742923
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<front><div type="abstract" xml:lang="en"><p>The perception of our limbs in space is built upon the integration of visual, tactile, and proprioceptive signals. Accumulating evidence suggests that these signals are combined in areas of premotor, parietal, and cerebellar cortices. However, it remains to be determined whether neuronal populations in these areas integrate hand signals according to basic temporal and spatial congruence principles of multisensory integration. Here, we developed a setup based on advanced 3D video technology that allowed us to manipulate the spatiotemporal relationships of visuotactile (<italic>VT</italic>
) stimuli delivered on a healthy human participant's real hand during fMRI and investigate the ensuing neural and perceptual correlates. Our experiments revealed two novel findings. First, we found responses in premotor, parietal, and cerebellar regions that were dependent upon the spatial and temporal congruence of <italic>VT</italic>
stimuli. This multisensory integration effect required a simultaneous match between the seen and felt postures of the hand, which suggests that congruent visuoproprioceptive signals from the upper limb are essential for successful <italic>VT</italic>
integration. Second, we observed that multisensory conflicts significantly disrupted the default feeling of ownership of the seen real limb, as indexed by complementary subjective, psychophysiological, and BOLD measures. The degree to which self-attribution was impaired could be predicted from the attenuation of neural responses in key multisensory areas. These results elucidate the neural bases of the integration of multisensory hand signals according to basic spatiotemporal principles and demonstrate that the <italic>dis</italic>
integration of these signals leads to “disownership” of the seen real hand.</p>
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<front><journal-meta><journal-id journal-id-type="nlm-ta">J Neurosci</journal-id>
<journal-id journal-id-type="iso-abbrev">J. Neurosci</journal-id>
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<title-group><article-title>Disintegration of Multisensory Signals from the Real Hand Reduces Default Limb Self-Attribution: An fMRI Study</article-title>
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<author-notes><corresp>Correspondence should be addressed to Giovanni Gentile,
<addr-line>Department of Neuroscience, Karolinska Institutet, Retzius väg 8, 17177 Stockholm, Sweden.</addr-line>
<email>Giovanni.Gentile@ki.se</email>
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<fn fn-type="con"><p>Author contributions: G.G., A.G., C.B., and H.H.E. designed research; G.G. and A.G. performed research; G.G. analyzed data; G.G., A.G., C.B., and H.H.E. wrote the paper.</p>
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<abstract><p>The perception of our limbs in space is built upon the integration of visual, tactile, and proprioceptive signals. Accumulating evidence suggests that these signals are combined in areas of premotor, parietal, and cerebellar cortices. However, it remains to be determined whether neuronal populations in these areas integrate hand signals according to basic temporal and spatial congruence principles of multisensory integration. Here, we developed a setup based on advanced 3D video technology that allowed us to manipulate the spatiotemporal relationships of visuotactile (<italic>VT</italic>
) stimuli delivered on a healthy human participant's real hand during fMRI and investigate the ensuing neural and perceptual correlates. Our experiments revealed two novel findings. First, we found responses in premotor, parietal, and cerebellar regions that were dependent upon the spatial and temporal congruence of <italic>VT</italic>
stimuli. This multisensory integration effect required a simultaneous match between the seen and felt postures of the hand, which suggests that congruent visuoproprioceptive signals from the upper limb are essential for successful <italic>VT</italic>
integration. Second, we observed that multisensory conflicts significantly disrupted the default feeling of ownership of the seen real limb, as indexed by complementary subjective, psychophysiological, and BOLD measures. The degree to which self-attribution was impaired could be predicted from the attenuation of neural responses in key multisensory areas. These results elucidate the neural bases of the integration of multisensory hand signals according to basic spatiotemporal principles and demonstrate that the <italic>dis</italic>
integration of these signals leads to “disownership” of the seen real hand.</p>
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