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, 7 (1), 15442

Tactile Frequency-Specific High-Gamma Activities in Human Primary and Secondary Somatosensory Cortices

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Tactile Frequency-Specific High-Gamma Activities in Human Primary and Secondary Somatosensory Cortices

Seokyun Ryun et al. Sci Rep.

Abstract

Humans can easily detect vibrotactile stimuli up to several hundred hertz, but underlying large-scale neuronal processing mechanisms in the cortex are largely unknown. Here, we investigated the macroscopic neural correlates of various vibrotactile stimuli including artificial and naturalistic ones in human primary and secondary somatosensory cortices (S1 and S2, respectively) using electrocorticography (ECoG). We found that tactile frequency-specific high-gamma (HG, 50-140 Hz) activities are seen in both S1 and S2 with different temporal dynamics during vibration (>100 Hz). Stimulus-evoked S1 HG power, which exhibited short-delayed peaks (50-100 ms), was attenuated more quickly in vibration than in flutter (<50 Hz), and their attenuation patterns were frequency-specific within vibration range. In contrast, S2 HG power, which was activated much later than that of S1 (150-250 ms), strikingly increased with increasing stimulus frequencies in vibration range, and their changes were much greater than those in S1. Furthermore, these S1-S2 HG patterns were preserved in naturalistic stimuli such as coarse/fine textures. Our results provide persuasive evidence that S2 is critically involved in neural processing for high-frequency vibrotaction. Therefore, we propose that S1-S2 neuronal co-operation is crucial for full-range, complex vibrotactile perception in human.

Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Figure 1
Figure 1
Representative time-frequency plots for various stimulus conditions (5, 20 and 35 Hz for flutter; 100, 250 and 400 Hz for vibration) in S1 (a), from Subject #4) and S2 (b), from Subject #2). Time t = 0 and t = 1 s indicate stimulus onset and offset, respectively. Dashed boxes indicate the time (0.2 to 0.9 s after stimulus onset) and the frequency range (50 to 140 Hz) which shows prominent HG power decreases in S1 (a), and increases in S2 (b) with an increase the stimulus frequencies above 100 Hz (c and d). Line plots for HG power levels from Subjects #1 (blue), #4 (pink), #5 (cyan) and #6 (gray) in S1 (c) and from Subjects #1 (blue) and #2 (pink) in S2 (d). Error bars in both C and D denote the s.e.m. Significance testing results among the various stimulus conditions are shown in Table S1.
Figure 2
Figure 2
S1 HG power time series during the flutter and vibration stimuli. Data were binned for statistical testing and smoothed for visualization. Time t = 0 s indicates stimulus onset. (a) Average power time series plots across all three subjects (Subjects #4, #5 and #6). Each line indicates the 5 (blue), 20 (dark blue), 35 (dark cyan), 100 (orange), 250 (pink) and 400 Hz (red) conditions. Dashed dark gray and gray lines denote the average flutter and vibration conditions, respectively. The green bars indicate the time bins which show significant power differences between the flutter and vibration conditions (P < 0.001, Bonferroni corrected). (bd) HG power time series of individual subjects. The blue and red lines show the flutter and vibration conditions, respectively.
Figure 3
Figure 3
(a) The accuracy of the stimulus frequency classification by simple SVM (S2 only). The x axis indicates three possible stimulation pairs. The chance level is 50% (dashed line). (b) The accuracy of the stimulus frequency classification by multiclass SVM using the single-trial HG power in S2 (left, green bars) and S1 (right, orange bars). The dashed line indicates the chance level (33%). Error bars in both (a) and (b) indicate the s.e.m.
Figure 4
Figure 4
(a) Representative time-frequency plots for coarse (top) and fine (bottom) textures in S1 (left column, from Subject #5) and S2 (right column, from Subject #3). Time t = 0 and t = 1.5 s indicate stimulus onset and offset, respectively. Dashed boxes indicate the time (0.2 to 1.3 s after stimulus onset) and frequency range (50 to 140 Hz). Bar plots denote the HG power levels in S1 (b) and S2 (c, from subject 3) during coarse and fine texture stimulations. Error bars indicate the s.e.m. The power differences between the two conditions were significant across all subjects (P < 0.001).

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References

    1. Harvey, M. A., Saal, H. P., Dammann, J. F. & Bensmaia, S. J. Multiplexing Stimulus Information through Rate and Temporal Codes in Primate Somatosensory Cortex. Plos Biol11 (2013). - PMC - PubMed
    1. Hollins M, Risner SR. Evidence for the duplex theory of tactile texture perception. Percept Psychophys. 2000;62:695–705. doi: 10.3758/BF03206916. - DOI - PubMed
    1. Romo R, Salinas E. Flutter discrimination: neural codes, perception, memory and decision making. Nat Rev Neurosci. 2003;4:203–218. doi: 10.1038/nrn1058. - DOI - PubMed
    1. Luna R, Hernández A, Brody CD, Romo R. Neural codes for perceptual discrimination in primary somatosensory cortex. Nat Neurosci. 2005;8:1210–1219. doi: 10.1038/nn1513. - DOI - PubMed
    1. Musall S, et al. Tactile frequency discrimination is enhanced by circumventing neocortical adaptation. Nat Neurosci. 2014;17:1567–1573. doi: 10.1038/nn.3821. - DOI - PubMed

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