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Research ArticleResearch Article: New Research, Sensory and Motor Systems

Neural Signatures of Actively Controlled Self-Motion and the Subjective Encoding of Distance

Constanze Schmitt, Milosz Krala and Frank Bremmer
eNeuro 5 December 2022, 9 (6) ENEURO.0137-21.2022; DOI: https://doi.org/10.1523/ENEURO.0137-21.2022
Constanze Schmitt
1Department Neurophysics, Philipps-Universität Marburg, 35043 Marburg, Germany
2Center for Mind, Brain and Behavior (CMBB), Philipps-Universität Marburg and Justus-Liebig-Universität Giessen, Hans-Meerwein-Straße 6, 35032 Marburg, Germany
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Milosz Krala
1Department Neurophysics, Philipps-Universität Marburg, 35043 Marburg, Germany
2Center for Mind, Brain and Behavior (CMBB), Philipps-Universität Marburg and Justus-Liebig-Universität Giessen, Hans-Meerwein-Straße 6, 35032 Marburg, Germany
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Frank Bremmer
1Department Neurophysics, Philipps-Universität Marburg, 35043 Marburg, Germany
2Center for Mind, Brain and Behavior (CMBB), Philipps-Universität Marburg and Justus-Liebig-Universität Giessen, Hans-Meerwein-Straße 6, 35032 Marburg, Germany
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  • Figure 1.
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    Figure 1.

    Stimulus and serial order of the trials from the different conditions. A, Each trial presented a forward displacement across a ground plane simulated by an optic flow stimulus. First, a passive trial was presented. In the passive condition the fixation target was red. The ground plane stimulus, consisting of random white dots, was presented stationary for 700 ms. Then the dots moved for 600–1525 ms depending on the speed (slow or fast) and distance (short, medium or long) simulating forward self-motion (represented by the blue arrow). After movement offset, the ground plane was displayed stationary for another 700 ms before the screen turned black. This triggered an intertrial-interval (ITI) lasting between 750 and 1250 ms. Next, an active trial was started, indicated by a green fixation target. Participants were asked to reproduce double the previously observed passive distance using a gamepad. Self-motion was controlled by deflecting a joystick. After movement offset the ground plane was again presented stationary for 700 ms. The movement (speed profile) was recorded and played back in the replay condition. Here, the fixation target was white, and participants were just asked to observe the self-motion stimulus. B, Three pairs of a passive (red fixation target) and an active trial (green fixation target) each were shown before the corresponding three replay movements were presented in pseudo-randomized order.

  • Figure 2.
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    Figure 2.

    Single participant’s (participant 4) velocity profiles in active trials and the mean of those velocity profiles as well as the mean of the gradient of each velocity profile for all participants. Panels A and B show data from a single participant (participant 4). In contrast, panels C and D show the mean data of all 15 participants. The green lines in A and B represent the velocity profiles. In A, aligned to the onset of the trial (presentation of the ground plane) at t = 0 s, in B, aligned to t_sub, the time passing the subjective single distance (t = 0 s). The data shown in A were recorded in active trials after the presentation of passive trials with low speed and the shortest distance. The velocity profile of the passive condition is depicted in red. In the passive condition, simulated self-motion always started 0.7 s after trial onset. Participants were free to start the movement as soon as they preferred in the active trials. This leads to an earlier increase in speed in some of the active trials as compared with the passive trials. Panel B presents the velocity profiles of all active trials recorded for this participant in green, as well as the mean of those profiles in black and the mean with the added and subtracted SDs in gray. Panels C and D show mean values for each of the 15 participants. In C, the means over all velocity profiles are presented; in D, the means over the respective temporal derivative (acceleration).

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    Figure 3.

    Distance reproduction performance. Bars show the reproduced distances in the active condition for all 15 participants. The mean distance (two times d_sub) over all trials is presented for each participant (error bar: SD). Data are shown for the three passive distances (short, medium and long). The horizontal black solid line in each plot represents double the passive distance, i.e., the required response 2*d_obj. The panel in the lower right depicts the average performance across all participants. The required response is shown in a checkerboard pattern whereas the average response, resulting in an overshoot, is shown in white.

  • Figure 4.
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    Figure 4.

    Visual evoked potentials (VEPs) elicited by self-motion onset and offset. Data from electrode clusters F (electrodes Fz, F3, F4), C (electrodes Cz, C3, C4), P (electrodes Pz, P3, P4), and O (electrodes Oz, O1, O2) are shown for the three conditions: passive (red), active (green), and replay (black). In the left column, time 0 ms represents self-motion onset, while in the right column, it represents self-motion offset. In all panels, negative voltages are plotted upward on the y-axes.

  • Figure 5.
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    Figure 5.

    Amplitude differences and latencies of the components P1, N2, and P2 for self-motion onset VEPs of the F cluster. Panels depict data from the active and replay condition (left column), active and passive condition (middle column), and replay and passive condition (right column). Each dot in each panel depicts data from a single subject. In the top row, we present the differences |P1-N2| (purple) and |P2-N2| (yellow) for the different conditions. In the bottom row the peak times for the three components P1 (cyan), N2 (magenta) and P2 (blue) are shown. In all six panels, the mean values of each group of data with the corresponding SDs are presented as a cross.

  • Figure 6.
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    Figure 6.

    Amplitude differences and latencies of the components P1, N2, and P2 for self-motion onset VEPs of the C cluster. Conventions as in Figure 5.

  • Figure 7.
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    Figure 7.

    Amplitude differences and latencies of the components P1, N2, and P2 for self-motion onset VEPs of the P cluster. Conventions as in Figure 5.

  • Figure 8.
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    Figure 8.

    Amplitude differences and latencies of the components P1, N2, and P2 for self-motion onset VEPs of the O cluster. Conventions as in Figure 5.

  • Figure 9.
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    Figure 9.

    Amplitude differences and latencies of the components P1, N2, and P2 for self-motion offset VEPs of the P cluster. Conventions as in Figure 5.

  • Figure 10.
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    Figure 10.

    Amplitude differences and latencies of the components P1, N2, and P2 for self-motion offset VEPs of the O cluster. Conventions as in Figure 5.

  • Figure 11.
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    Figure 11.

    Permutation tests between data recorded in the active and replay conditions for the alignments to t_sub and t_obj averaged over all 14 participants. The panels depict data from the subjective (t_sub; left column) and the objective (t_obj) alignment (right column). The eight panels depict the results of the permutation tests with data recorded from the F, C, P, and O shown from top to bottom. In bright colors, clusters with p-values smaller than p = 0.01 are presented. In all panels, data recorded in active trials are contrasted with data recorded in replay trials.

Tables

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    Table 1

    Travel times

    Participant #12345678
    t_sub [ms]1226 (±348)1380 (±379)1131 (±368)1312 (±493)867 (±287)1362 (±425)1229 (±379)1188 (±294)
    Difference: t_sub –
    t_obj [ms]
    237 (±289)152 (±245)161 (±216)261 (±299)34 (±164)25 (±318)111 (±205)48 (±169)
    Difference: t_sub –
    t_1/2_fulltime [ms]
    34 (±75)93 (±85)88 (±98)36 (±58)12 (±31)61 (±80)43 (±66)64 (±53)
    Participant #9101112131415
    t_sub [ms]1061 (±339)1312 (±403)501 (±119)1141 (±361)1271 (±337)646 (±141)1089 (±425)
    Difference: t_sub –
    t_obj [ms]
    6 (±294)307 (±280)−110 (±382)272 (±279)231 (±277)−78 (±254)206 (±307)
    Difference: t_sub –
    t_1/2_fulltime [ms]
    39 (±67)132 (±97)−10 (±23)43 (±61)−4 (±64)17 (±27)97 (±139)
    • Travel times for half the traveled distance (t_Sub), the difference between the times traveled to reach half of the subjective and the objective distance (t_sub – t_obj), and the difference between the times traveled to reach half of the subjective distance and half of the time traveled (t_Sub – t_1/2_fulltime). Values show the averages over all trials and the respective SDs.

    • View popup
    Table 2

    EEG data of electrode clusters F and C

    Self-motion onset: F clusterSelf-motion onset: C cluster
    ActiveReplayPassiveActiveReplayPassive
    LatencyLatencyLatencyLatencyLatencyLatency
    P1111 ms114 ms94 ms111 ms114 ms94 ms
    N2153 ms156 ms136 ms153 ms156 ms136 ms
    P2243 ms241 ms236 ms250 ms250 ms236 ms
    AmplitudeAmplitudeAmplitudeAmplitudeAmplitudeAmplitude
    |P1-N2|0.79 μV1.13 μV1.28 μV1.43 μV1.81 μV1.92 μV
    |P2-N2|2.51 μV2.94 μV3.57 μV2.32 μV2.82 μV3.36 μV
    • Latencies and amplitude differences for the P1, N2, and P2 components for the three conditions (active, replay, and passive) for self-motion onset.

    • View popup
    Table 3

    EEG data of electrode cluster P

    Self-motion onset: P clusterSelf-motion offset: P cluster
    ActiveReplayPassiveActiveReplayPassive
    LatencyLatencyLatencyLatencyLatencyLatency
    P1111 ms113 ms96 ms65 ms66 ms110 ms
    N2180 ms190 ms169 ms123 ms134 ms169 ms
    P2260 ms259 ms252 ms259 ms246 ms290 ms
    AmplitudeAmplitudeAmplitudeAmplitudeAmplitudeAmplitude
    |P1-N2|3.2 μV3.23 μV4.68 μV1.3 μV1.08 μV1.3 μV
    |P2-N2|2.89 μV2.82 μV5.08 μV2.33 μV2.8 μV2.79 μV
    • Values are shown for self-motion onset and offset. Conventions as in Table 2.

    • View popup
    Table 4

    EEG data of electrode cluster O

    Self-motion onset: O clusterSelf-motion offset: O cluster
    ActiveReplayPassiveActiveReplayPassive
    LatencyLatencyLatencyLatencyLatencyLatency
    P1111 ms114 ms96 ms54 ms66 ms104 ms
    N2188 ms191 ms171 ms122 ms135 ms169 ms
    P2240 ms248 ms262 ms246 ms232 ms253 ms
    AmplitudeAmplitudeAmplitudeAmplitudeAmplitudeAmplitude
    |P1-N2|3.58 μV3.13 μV5.39 μV1.8 μV1.62 μV1.96 μV
    |P2-N2|2.34 μV1.85 μV4.76 μV3.03 μV2.76 μV2.67 μV
    • Values are shown for self-motion onset and offset. Conventions as in Table 2.

    • View popup
    Table 5

    Results of paired two-tailed t tests for the comparisons between amplitude differences (|P1-N2|, |P2-N2|) and between latencies (P2) for data recorded on the F cluster electrodes

    Self-motion onset: F cluster
    Amplitude differencesLatencies
    |P1-N2||P2-N2|P2
    ActiveReplayActiveReplayReplay
    Passivet(14) = −3.74 p = 0.002Not significantt(14) = −3.94 p = 0.001t(14) = 3.21 p = 0.006t(14) = −4.4 p < 0.001
    Active-Not significant-Not significantt(14) = −3.5 p = 0.004
    • Amplitude differences |P1-N2| and |P2-N2| were significantly larger in the passive as compared with the active condition and for |P2-N2| also larger compared with the replay condition. In addition, the P2 component had shorter latencies in the active and passive condition compared with the replay condition.

    • View popup
    Table 6

    Results of paired two-tailed t tests for the comparisons between amplitude differences (|P1-N2|, |P2-N2|) and between latencies (P1) for data recorded at the C cluster electrodes

    Self-motion onset: C cluster
    AmplitudesLatencies
    |P1-N2||P2-N2|P1
    ActiveReplayActiveReplayActiveReplay
    Passivet(14) = −3.25
    p = 0.006
    Not significantt(14) = −4.4
    p < 0.001
    t(14) = 4.32
    p < 0.001
    t(14) = −3.79
    p = 0.002
    t(14) = −4.03
    p = 0.001
    • Amplitude differences |P1-N2| and |P2-N2| were significantly larger in the passive as compared with the active condition and for |P2-N2| also larger compared with the replay conditions. In addition, the P1 component had shorter latencies in the passive condition compared with the active and replay conditions.

    • View popup
    Table 7

    Results of paired two-tailed t tests for the comparisons between amplitude differences (|P1-N2|, |P2-N2|) and between latencies (P1)

    Self-motion onset: P cluster
    AmplitudesLatencies
    |P1-N2||P2-N2|P1
    ActiveReplayActiveReplayActive
    Passivet(14) = −4.94 p < 0.001t(14) = 5.84 p < 0.001t(14) = −7.71 p < 0.001t(14) = 7.58 p < 0.001t(14) = 3.46 p = 0.004
    • Amplitude differences |P1-N2| and |P2-N2| were significantly larger in the passive as compared with the active and replay conditions. In addition, the P1 components had longer latencies in the active condition compared with the passive condition; p-values were not different for the active versus replay comparison.

    • View popup
    Table 8

    Results of paired two-tailed t tests for the comparisons between amplitude differences (|P1-N2|, |P2-N2|) and between latencies (N2)

    Self-motion onset: O cluster
    AmplitudesLatencies
    |P1-N2||P2-N2|N2
    ActiveReplayActiveReplayActive
    Passivet(14) = −5.27 p < 0.001t(14) = 5.92 p < 0.001t(14) = −4.53 p < 0.001t(14) = 4.33 p < 0.001t(14) = 6.28 p < 0.001
    • Amplitude differences |P1-N2| and |P2-N2| were significantly larger in the passive as compared with the active and replay condition. In addition, the N2 component had longer latencies in the active condition compared with the passive condition; p-values were not different for the active versus replay comparison.

    • View popup
    Table 9

    Results of paired two-tailed t tests for the comparisons between latencies (P1, N2, P2)

    Self-motion offset: P cluster
    Latencies
    P1N2P2
    ActiveReplayActiveReplayActiveReplay
    Passivet(14) = −18.05
    p < 0.001
    t(14) = 8.05
    p < 0.001
    t(14) = −5.29
    p < 0.001
    t(14) = 6.14
    p < 0.001
    t(14) = −4.36
    p < 0.001
    t(14) = 3.72
    p = 0.002
    • The VEP components had longer latencies in the passive condition compared with the active and replay conditions; p-values were not different for the active versus replay comparison.

    • View popup
    Table 10

    Results of paired two-tailed t tests for the comparisons between latencies (P1, N2, P2)

    Self-motion offset: O cluster
    Latencies
    P1N2P2
    ActiveReplayActiveReplayReplay
    Passivet(14) = −11.88 p < 0.001t(14) = 8.64 p < 0.001t(14) = −10.37 p < 0.001t(14) = 4.11 p < 0.001t(14) = 3.67 p = 0.003
    • The VEP components had longer latencies in the passive condition compared with the active and replay conditions; p-values were not different for the active versus replay comparison.

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Neural Signatures of Actively Controlled Self-Motion and the Subjective Encoding of Distance
Constanze Schmitt, Milosz Krala, Frank Bremmer
eNeuro 5 December 2022, 9 (6) ENEURO.0137-21.2022; DOI: 10.1523/ENEURO.0137-21.2022

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Neural Signatures of Actively Controlled Self-Motion and the Subjective Encoding of Distance
Constanze Schmitt, Milosz Krala, Frank Bremmer
eNeuro 5 December 2022, 9 (6) ENEURO.0137-21.2022; DOI: 10.1523/ENEURO.0137-21.2022
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Keywords

  • EEG
  • optic flow
  • oscillatory activity
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