Neural excitability and sensory input determine intensity perception with opposing directions in initial cortical responses

  1. Tilman Stephani  Is a corresponding author
  2. Alice Hodapp
  3. Mina Jamshidi Idaji
  4. Arno Villringer
  5. Vadim V Nikulin  Is a corresponding author
  1. Department of Neurology, Max Planck Institute for Human Cognitive and Brain Sciences, Germany
  2. International Max Planck Research School NeuroCom, Germany
  3. Machine Learning Group, Technical University of Berlin, Germany
  4. Berlin School of Mind and Brain, Humboldt-Universität zu Berlin, Germany
  5. Clinic for Cognitive Neurology, University Hospital Leipzig, Germany
  6. Institute for Cognitive Neuroscience, National Research University Higher School of Economics, Russian Federation
7 figures, 2 tables and 1 additional file

Figures

Experimental paradigm and main electrophysiological measures.

(a) The relationships between pre-stimulus alpha oscillations, stimulus-evoked responses, and perceived intensity of somatosensory stimuli were examined in a continuous sequence of median nerve …

Figure 2 with 3 supplements
Bivariate relationships between pre-stimulus alpha amplitude, N20 peak amplitude, and perceived stimulus intensity.

(a) Time course of the amplitude of pre-stimulus alpha band activity (8–13 Hz) displayed by behavioral response categories. Note that for statistical analyses, pre-stimulus epochs were cut at –5 ms …

Figure 2—source data 1

Trial overlap between extreme bins of N20 and pre-stimulus alpha amplitudes used for the SDT analyses.

Trial overlap between extreme bins of N20 and pre-stimulus alpha amplitudes used for the SDT analyses.

https://cdn.elifesciences.org/articles/67838/elife-67838-fig2-data1-v2.pdf
Figure 2—figure supplement 1
Schematic of the signal detection theory parameters sensitivity d’ and criterion c.

While sensitivity d’ describes the distance between the distributions of the internal responses to two distinct stimuli, criterion c reflects a general threshold above which any internal response is …

Figure 2—figure supplement 2
Representation of the relations between amplitude in the time-frequency domain and N20 amplitudes (panel a), as well as perceived stimulus intensity (panel b).

Both panels show unthresholded statistical values (t values in panel a and z values in panel b) of the effects of predictor t-f amplitude as calculated from random-intercept linear-mixed effects …

Figure 2—figure supplement 3
Simulation of filter effects on the relation between pre-stimulus alpha amplitude and early somatosensory evoked potential (SEP).

In order to exclude the possibility that the observed effects emerged due to data processing-related issues (such as filter artifacts or residual activity leaking in or from the alpha frequency …

Measures to control for peripheral nerve variability.

(a) Single trials of the compound nerve action potential (CNAP) in response to the median nerve stimuli, measured at the inner side of the ipsilateral upper arm (shown for an exemplary subject). (b) …

Multi-level structural equation model of the interplay between pre-stimulus alpha activity, the initial cortical response (N20 component of the somatosensory evoked potential [SEP]), intensity of the presented stimuli, the peripheral control measures of the compound muscle action potential (CMAP) of the M. abductor pollicis brevis and the compound nerve action potential (CNAP) of the median nerve, as well as the perceived intensity as reported by the participants (referred to as SEM 1).

Effect paths were estimated between the manifest variables on level 1 (within participants). Latent variables on level 2 served to estimate the respective random intercepts as well as their …

Figure 5 with 1 supplement
Relations of pre-stimulus alpha amplitude with N20 amplitudes and perceived stimulus intensity as analyzed with linear-mixed-effects models in source space.

(a) Effects of pre-stimulus alpha amplitudes on N20 amplitudes (uncorrected t values). (b) Same as (a) but corrected for multiple comparisons (FDR-corrected; p < 0.01). (c) Effects of pre-stimulus …

Figure 5—figure supplement 1
Effects of pre-stimulus alpha amplitude on signal detection theory parameters criterion c and sensitivity d’ in source space.

(a) Effects on criterion c. (b) Effects on sensitivity d’. Both panels show t values uncorrected for multiple comparisons. The blue outline indicates the hand region of the right somatosensory …

Thalamic activity and later somatosensory evoked potential (SEP) components.

(a) Grand average (N = 13) of the thalamic component derived from canonical correlation analysis (CCA), showing a clear P15 potential which did not differ across behavioral response categories. (b) …

Author response image 1
Phase distributions of pre-stimulus alpha band activity, separately displayed for quintiles of alpha amplitudes (panel a), and N20 amplitudes (panel b).

Alpha phase estimates were based on Fast-Fourier transforms in the pre-stimulus time windows from -200 to -10 ms. For visualization, data were concatenated across all participants (N=32).

Tables

Table 1
Model comparison of structural equation models (SEMs).

The original SEM (1) was compared to the alternative models (2–10) using Akaike information criterion (AIC), Bayesian information criterion (BIC), log-likelihood (LL), and the chi-square difference …

Model fit indices
AIC diff.BIC diff.LL diff.χ2 diff.df diff.p-value
(1) Original SEM (‘SEM 1’)
(2) SEM incl. N20 ~ CNAP1.81310.1660.0930.146–10.702
(3) SEM incl. N20 ~ CMAP0.0888.4410.9560.799–10.371
(4) SEM incl. perceived_int ~ CNAP1.96710.3200.0160.019–10.890
(5) SEM excl. perceived_int ~ prestim8.002–0.351–5.00111.4151<0.001
(6) SEM excl. N20 ~ prestim15.0536.701–8.5278.08710.005
(7) SEM excl. N2047.09922.040–26.55031.0953<0.001
(8) SEM excl. CMAP9586.9069570.200–4795.45387.0302<0.001
(9) SEM incl. CMAP ~ prestim1.4049.7570.2970.220–10.639
(10) SEM incl. CNAP ~ prestim–0.1158.2391.0572.342–10.126
Table 2
Relationships included in the hypothesized structural equation model (‘SEM 1’).

Level 1 equations reflect the within-participant effects between variables of interest. On level 2, only intercepts and variances of each variable were modeled; apart from stimulus intensity which …

Level 1 (within participants):
  N20 amplitude ~ 1 + stimulus intensity + pre-stimulus alpha
  CNAP ~ 1 + stimulus intensity
  CMAP ~ 1 + stimulus intensity
  Perceived intensity ~ 1 + stimulus intensity + N20 amplitude + pre-stimulus alpha + CMAP
Level 2 (between participants):
  N20 amplitude ~~ N20 amplitude
  CNAP ~~ CNAP
  CMAP ~~ CMAP
  Perceived intensity ~~ perceived intensity
  Pre-stimulus alpha ~~ pre-stimulus alpha

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