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Research Article: New Research, Sensory and Motor Systems

Brain encoding of naturalistic, continuous, and unpredictable tactile events

Nicolò Castellani, Alessandra Federici, Marta Fantoni, Emiliano Ricciardi, Francesca Garbarini and Davide Bottari
eNeuro 12 September 2024, ENEURO.0238-24.2024; https://doi.org/10.1523/ENEURO.0238-24.2024
Nicolò Castellani
1MoMiLab, IMT School for Advanced Studies, Lucca, Italy
2Manibus Lab, University of Turin, Turin, Italy
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Alessandra Federici
1MoMiLab, IMT School for Advanced Studies, Lucca, Italy
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Marta Fantoni
1MoMiLab, IMT School for Advanced Studies, Lucca, Italy
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Emiliano Ricciardi
1MoMiLab, IMT School for Advanced Studies, Lucca, Italy
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Francesca Garbarini
2Manibus Lab, University of Turin, Turin, Italy
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Davide Bottari
1MoMiLab, IMT School for Advanced Studies, Lucca, Italy
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Abstract

Studies employing EEG to measure somatosensory responses have been typically optimized to compute event-related potentials in response to discrete events (ERPs). However, tactile interactions involve continuous processing of non-stationary inputs that change in location, duration, and intensity. To fill this gap, this study aims to demonstrate the possibility of measuring the neural tracking of continuous and unpredictable tactile information. Twenty-seven young adults (females = 15) were continuously and passively stimulated with a random series of gentle brushes on single fingers of each hand, which were covered from view. Thus, tactile stimulations were unique for each participant, and stimulated fingers. An encoding model measured the degree of synchronization between brain activity and continuous tactile input, generating a temporal response function (TRF). Brain topographies associated with the encoding of each finger stimulation showed a contralateral response at central sensors starting at 50 ms and peaking at about 140 ms of lag, followed by a bilateral response at about 240 ms. A series of analyses highlighted that reliable tactile TRF emerged after just 3 minutes of stimulation. Strikingly, topographical patterns of the TRF allowed discriminating digit lateralization across hands and digit representation within each hand. Our results demonstrated for the first time the possibility of using EEG to measure the neural tracking of a naturalistic, continuous, and unpredictable stimulation in the somatosensory domain. Crucially, this approach allows the study of brain activity following individualized, idiosyncratic tactile events to the fingers.

Significant Statement This study expands the current research conducted on neural tracking, opening the exploration of idiosyncratic tactile events and overcoming constraints of laboratory tasks that typically rely on discrete events. We validated a protocol for the ecological investigations of continuous, slow, tactile processing of the hands. The employed approach enriches the possible use of the EEG to characterize somatosensory neural representations of tactile events. Findings unravel coherent neural responses to continuous and naturalistic touch, with sensitivity for digit lateralization and representation.

Footnotes

  • Authors report no conflict of interest

  • D.B. was supported by a PRIN 2017 grant from the Italian Ministry for University and Research (Prot. 20177894ZH)

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

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Brain encoding of naturalistic, continuous, and unpredictable tactile events
Nicolò Castellani, Alessandra Federici, Marta Fantoni, Emiliano Ricciardi, Francesca Garbarini, Davide Bottari
eNeuro 12 September 2024, ENEURO.0238-24.2024; DOI: 10.1523/ENEURO.0238-24.2024

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Brain encoding of naturalistic, continuous, and unpredictable tactile events
Nicolò Castellani, Alessandra Federici, Marta Fantoni, Emiliano Ricciardi, Francesca Garbarini, Davide Bottari
eNeuro 12 September 2024, ENEURO.0238-24.2024; DOI: 10.1523/ENEURO.0238-24.2024
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