Amputees but Not Healthy Subjects Optimally Integrate Non-spatially Matched Visuo-tactile Stimuli

Overview

Journal iScience

Publisher Cell Press

Date 2025 Jan 31

PMID 39886468

Authors

Giuseppe Valerio Aurucci

Greta Preatoni

Gaia Risso

Stanisa Raspopovic

Affiliations

Soon will be listed here.

Abstract

Our brain combines sensory inputs to create a univocal perception, enhanced when stimuli originate from the same location. Following amputation, distorted body representations may disrupt visuo-tactile integration at the amputated leg. We aim to unveil the principles guiding optimal and cognitive-efficient visuo-tactile integration at both intact and amputated legs. Hence, we designed a VR electro-stimulating platform to assess the functional and cognitive correlates of visuo-tactile integration in two amputees and sixteen healthy subjects performing a 2-alternative forced choice (2AFC) task. We showed that amputees optimally integrate non-spatially matched stimuli at the amputated leg but not the intact leg (tactile cue at the stump/thigh and visual cue under the virtual foot), while healthy controls only integrated spatially matched visuo-tactile stimuli. Optimal integration also reduced 2AFC task reaction times and was confirmed by cognitive EEG-based mental workload reduction. These findings offer insights into multisensory integration processes, opening new perspectives on amputees' brain plasticity.

References

Petrini F, Bumbasirevic M, Valle G, Ilic V, Mijovic P, Cvancara P . Sensory feedback restoration in leg amputees improves walking speed, metabolic cost and phantom pain. Nat Med. 2019; 25(9):1356-1363. DOI: 10.1038/s41591-019-0567-3. View

Schone H, Baker C, Katz J, Nikolajsen L, Limakatso K, Flor H . Making sense of phantom limb pain. J Neurol Neurosurg Psychiatry. 2022; . PMC: 9304093. DOI: 10.1136/jnnp-2021-328428. View

Schott G . Revealing the invisible: the paradox of picturing a phantom limb. Brain. 2013; 137(Pt 3):960-9. DOI: 10.1093/brain/awt244. View

Chee L, Valle G, Marazzi M, Preatoni G, Haufe F, Xiloyannis M . Optimally-calibrated non-invasive feedback improves amputees' metabolic consumption, balance and walking confidence. J Neural Eng. 2022; 19(4). DOI: 10.1088/1741-2552/ac883b. View

Chancel M, Ehrsson H . Which hand is mine? Discriminating body ownership perception in a two-alternative forced-choice task. Atten Percept Psychophys. 2020; 82(8):4058-4083. PMC: 7593318. DOI: 10.3758/s13414-020-02107-x. View

Doehrmann O, Naumer M . Semantics and the multisensory brain: how meaning modulates processes of audio-visual integration. Brain Res. 2008; 1242:136-50. DOI: 10.1016/j.brainres.2008.03.071. View

Risso G, Bassolino M . Assess and rehabilitate body representations (neuro)robotics: An emergent perspective. Front Neurorobot. 2022; 16:964720. PMC: 9498221. DOI: 10.3389/fnbot.2022.964720. View

Chen Y, Spence C . When hearing the bark helps to identify the dog: semantically-congruent sounds modulate the identification of masked pictures. Cognition. 2009; 114(3):389-404. DOI: 10.1016/j.cognition.2009.10.012. View

Flor H, Elbert T, Knecht S, Wienbruch C, Pantev C, Birbaumer N . Phantom-limb pain as a perceptual correlate of cortical reorganization following arm amputation. Nature. 1995; 375(6531):482-4. DOI: 10.1038/375482a0. View

10.

Klimesch W . EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis. Brain Res Brain Res Rev. 1999; 29(2-3):169-95. DOI: 10.1016/s0165-0173(98)00056-3. View

11.

Risso G, Preatoni G, Valle G, Marazzi M, Bracher N, Raspopovic S . Multisensory stimulation decreases phantom limb distortions and is optimally integrated. iScience. 2022; 25(4):104129. PMC: 8980810. DOI: 10.1016/j.isci.2022.104129. View

12.

Spence C . Crossmodal correspondences: a tutorial review. Atten Percept Psychophys. 2011; 73(4):971-95. DOI: 10.3758/s13414-010-0073-7. View

13.

Tremmel C, Herff C, Sato T, Rechowicz K, Yamani Y, Krusienski D . Estimating Cognitive Workload in an Interactive Virtual Reality Environment Using EEG. Front Hum Neurosci. 2019; 13:401. PMC: 6868478. DOI: 10.3389/fnhum.2019.00401. View

14.

Bucciarelli V, Gozzi N, Katic N, Aiello G, Razzoli M, Valle G . Multiparametric non-linear TENS modulation to integrate intuitive sensory feedback. J Neural Eng. 2023; 20(3). DOI: 10.1088/1741-2552/acd4e8. View

15.

Welch R, Warren D . Immediate perceptual response to intersensory discrepancy. Psychol Bull. 1980; 88(3):638-67. View

16.

Petrini F, Valle G, Bumbasirevic M, Barberi F, Bortolotti D, Cvancara P . Enhancing functional abilities and cognitive integration of the lower limb prosthesis. Sci Transl Med. 2019; 11(512). DOI: 10.1126/scitranslmed.aav8939. View

17.

Muret D, Makin T . The homeostatic homunculus: rethinking deprivation-triggered reorganisation. Curr Opin Neurobiol. 2020; 67:115-122. DOI: 10.1016/j.conb.2020.08.008. View

18.

Helbig H, Ernst M . Optimal integration of shape information from vision and touch. Exp Brain Res. 2007; 179(4):595-606. DOI: 10.1007/s00221-006-0814-y. View

19.

Rognini G, Petrini F, Raspopovic S, Valle G, Granata G, Strauss I . Multisensory bionic limb to achieve prosthesis embodiment and reduce distorted phantom limb perceptions. J Neurol Neurosurg Psychiatry. 2018; 90(7):833-836. PMC: 6791810. DOI: 10.1136/jnnp-2018-318570. View

20.

Borghini G, Astolfi L, Vecchiato G, Mattia D, Babiloni F . Measuring neurophysiological signals in aircraft pilots and car drivers for the assessment of mental workload, fatigue and drowsiness. Neurosci Biobehav Rev. 2012; 44:58-75. DOI: 10.1016/j.neubiorev.2012.10.003. View