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

Abstract

Navigating through an environment requires knowledge about one's direction of self-motion (heading) and traveled distance. Behavioral studies showed that human participants can actively reproduce a previously observed travel distance purely based on visual information. Here, we employed electroencephalography (EEG) to investigate the underlying neural processes. We measured, in human observers, event-related potentials (ERPs) during visually simulated straight-forward self-motion across a ground plane. The participants' task was to reproduce (active condition) double the distance of a previously seen self-displacement (passive condition) using a gamepad. We recorded the trajectories of self-motion during the active condition and played it back to the participants in a third set of trials (replay condition). We analyzed EEG activity separately for four electrode clusters: frontal (F), central (C), parietal (P), and occipital (O). When aligned to self-motion onset or offset, response modulation of the ERPs was stronger, and several ERP components had different latencies in the passive as compared with the active condition. This result is in line with the concept of predictive coding, which implies modified neural activation for self-induced versus externally induced sensory stimulation. We aligned our data also to the times when subjects passed the (objective) single distance d_obj and the (subjective) single distance d_sub. Remarkably, wavelet-based temporal-frequency analyses revealed enhanced theta-band activation for F, P, and O-clusters shortly before passing d_sub. This enhanced activation could be indicative of a navigation related representation of subjective distance. More generally, our study design allows to investigate subjective perception without interfering neural activation because of the required response action.

Keywords: EEG; optic flow; oscillatory activity; path integration; predictive coding; self-motion.

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.

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).

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.

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.

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.

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.

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.

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.

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.

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.

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.