Abstract
Tactile perception is a fundamental sensory system, playing a pivotal role in our understanding of the surrounding environment and aiding in motor control. In this study, we investigated the distinct neural underpinnings of discriminative touch, affective touch (specifically the C tactile system), and knismesis. We developed a paradigm of EEG experiment consisted of three types of touch tuned in terms of their force and velocity for different submodalities: discriminative touch (haptics or fast touch), affective touch (C-tactile or slow touch), and knismesis (alerting tickle or ultralight touch). Touch was delivered with a special high-precision robotic rotary touch stimulation device. Thirty nine healthy individuals participated in the study. Utilizing functional brain networks derived from EEG data, we examined the patterns of brain connectivity associated with fast, slow, and ultralight touches. Our findings revealed significant differences in functional connectivity patterns between these touch conditions, with the majority of variations occurring in the theta frequency range. Notably, connections in frontal, frontal-central, frontal-parietal, and occipitotemporal regions exhibited distinct activation strengths. Pairwise statistical comparisons further highlighted the unique characteristics of each touch modality. The theta band, in particular, played a prominent role in distinguishing ultralight from slow touches. These results shed light on the interplay between different touch submodalities and their distinctive processing in the brain, contributing to a comprehensive understanding of tactile perception. This research bridges a critical gap in our knowledge of the neural mechanisms underlying tactile perception and its role in shaping our perception of the world.
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Data Availability
Data are available from Ivan Skorokhodov under request iskor@live.com.
References
V.E. Abraira, D.D. Ginty, The sensory neurons of touch. Neuron 79(4), 618–639 (2013)
F. McGlone, J. Wessberg, H. Olausson, Discriminative and affective touch: sensing and feeling. Neuron 82(4), 737–755 (2014)
M. Björnsdotter, L. Löken, H. Olausson, Å. Vallbo, J. Wessberg, Somatotopic organization of gentle touch processing in the posterior insular cortex. J. Neurosci. 29(29), 9314–9320 (2009)
I. Croy, M.T. Fairhurst, F. McGlone, The role of c-tactile nerve fibers in human social development. Curr. Opin. Behav. Sci. 43, 20–26 (2022)
C.J. Haggarty, P. Malinowski, F.P. McGlone, S.C. Walker, Autistic traits modulate cortical responses to affective but not discriminative touch. Eur. J. Neurosci. 51(8), 1844–1855 (2020)
S.T. Selden, Tickle. J. Am. Acad. Dermatol. 50(1), 93–97 (2004)
C. Harris, Two forms of tickle: Knismesis and gargalesis. The Encyclopedia of Human Behaviour, 611–615 (2012)
A.E. Hramov, N.S. Frolov, V.A. Maksimenko, S.A. Kurkin, V.B. Kazantsev, A.N. Pisarchik, Functional networks of the brain: from connectivity restoration to dynamic integration. Phys. Usp. 64(6), 584 (2021)
J.V. Hull, L.B. Dokovna, Z.J. Jacokes, C.M. Torgerson, A. Irimia, J.D. Van Horn, Resting-state functional connectivity in autism spectrum disorders: a review. Front. Psych. 7, 205 (2017)
N.S. Frolov, V.A. Maksimenko, M.V. Khramova, A.N. Pisarchik, A.E. Hramov, Dynamics of functional connectivity in multilayer cortical brain network during sensory information processing. Eur. Phys. J. Spec. Top. 228, 2381–2389 (2019)
E.N. Pitsik, V.A. Maximenko, S.A. Kurkin, A.P. Sergeev, D. Stoyanov, R. Paunova, S. Kandilarova, D. Simeonova, A.E. Hramov, The topology of fmri-based networks defines the performance of a graph neural network for the classification of patients with major depressive disorder. Chaos Solit. Fractals 167, 113041 (2023)
A.N. Pisarchik, A.V. Andreev, S.A. Kurkin, D. Stoyanov, A.A. Badarin, R. Paunova, A.E. Hramov, Topology switching during window thresholding fmri-based functional networks of patients with major depressive disorder: Consensus network approach. Chaos Interdiscip. J. Nonlinear Sci. (2023). https://doi.org/10.1063/5.0166148
S. Kurkin, N. Smirnov, E. Pitsik, M.S. Kabir, O. Martynova, O. Sysoeva, G. Portnova, A. Hramov, Features of the resting-state functional brain network of children with autism spectrum disorder: Eeg source-level analysis. Eur. Phys. J. Spec. Top. 232(5), 683–693 (2023)
A.V. Andreev, S.A. Kurkin, D. Stoyanov, A.A. Badarin, R. Paunova, A.E. Hramov, Toward interpretability of machine learning methods for the classification of patients with major depressive disorder based on functional network measures. Chaos Interdiscip. J. Nonlinear Sci. (2023). https://doi.org/10.1063/5.0155567
D. Stoyanov, V. Khorev, R. Paunova, S. Kandilarova, D. Simeonova, A. Badarin, A. Hramov, S. Kurkin, Resting-state functional connectivity impairment in patients with major depressive episode. Int. J. Environ. Res. Public Health 19(21), 14045 (2022)
R. Oostenveld, P. Fries, E. Maris, J.-M. Schoffelen, Fieldtrip: open source software for advanced analysis of meg, eeg, and invasive electrophysiological data. Comput. Intell. Neurosci. 2011, 1–9 (2011)
A.M. Bastos, J.-M. Schoffelen, A tutorial review of functional connectivity analysis methods and their interpretational pitfalls. Front. Syst. Neurosci. 9, 175 (2016)
C.R. Genovese, N.A. Lazar, T. Nichols, Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuroimage 15(4), 870–878 (2002)
A. Zalesky, A. Fornito, E.T. Bullmore, Network-based statistic: identifying differences in brain networks. Neuroimage 53(4), 1197–1207 (2010)
A.A. Varlamov, I.V. Skorokhodov, Knismesis: the aversive facet of tickle. Curr. Opin. Behav. Sci. 43, 230–235 (2022)
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This research was funded by a grant of the Russian Ministry of Science and Higher Education project No 075-15-2022-1139 “The role of affective touch in developing brain: fundamental and translational research”.
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Kurkin, S., Khorev, V., Skorokhodov, I. et al. Characteristics of brain functional networks specific for different types of tactile perception. Eur. Phys. J. Spec. Top. (2023). https://doi.org/10.1140/epjs/s11734-023-01051-9
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DOI: https://doi.org/10.1140/epjs/s11734-023-01051-9