Role of Alpha-Band Oscillations in Spatial Updating across Whole Body Motion

Abstract

When moving around in the world, we have to keep track of important locations in our surroundings. In this process, called spatial updating, we must estimate our body motion and correct representations of memorized spatial locations in accordance with this motion. While the behavioral characteristics of spatial updating across whole body motion have been studied in detail, its neural implementation lacks detailed study. Here we use electroencephalography (EEG) to distinguish various spectral components of this process. Subjects gazed at a central body-fixed point in otherwise complete darkness, while a target was briefly flashed, either left or right from this point. Subjects had to remember the location of this target as either moving along with the body or remaining fixed in the world while being translated sideways on a passive motion platform. After the motion, subjects had to indicate the remembered target location in the instructed reference frame using a mouse response. While the body motion, as detected by the vestibular system, should not affect the representation of body-fixed targets, it should interact with the representation of a world-centered target to update its location relative to the body. We show that the initial presentation of the visual target induced a reduction of alpha band power in contralateral parieto-occipital areas, which evolved to a sustained increase during the subsequent memory period. Motion of the body led to a reduction of alpha band power in central parietal areas extending to lateral parieto-temporal areas, irrespective of whether the targets had to be memorized relative to world or body. When updating a world-fixed target, its internal representation shifts hemispheres, only when subjects' behavioral responses suggested an update across the body midline. Our results suggest that parietal cortex is involved in both self-motion estimation and the selective application of this motion information to maintaining target locations as fixed in the world or fixed to the body.

Keywords: electroencephalography; oscillations; parietal cortex; self-motion; vestibular; visual stability.

FIGURE 1

Paradigm. (A) Schematic drawing of the vestibular sled. (B) Top view of the experimental setup. Subjects performed a spatial updating task with world-fixed (top) and body-fixed (bottom) targets. Using a sled-mounted fixation, a target was flashed, resulting the percept shown in the top left inset. After displacement, either 180, 90, or 45 mm subjects indicated where the remembered target was (dotted circle). This was generally underestimated in the world-fixed condition (compare with filled dots, the actual location). (C) Motion profiles of the large (180 mm), medium (90) and small (45) displacements. (D) Example of condition block order. W, world-fixed; B, body-fixed. Conditions alternated every two or three blocks and started with either world or body-fixed targets.

FIGURE 2

Behavioral results. (A) Signed error, calculated as the mean difference between actual and indicated target position, in the body-fixed condition for all displacement sizes and directions, pooled across participants. Negative error indicates error to the right, error bars denote standard error. (B) Same as A in the world-fixed condition. (C) World- and body-fixed behavior as expressed by gain factors per condition, where the darker bars indicate world-fixed gain and lighter the body-fixed gain. World-fixed gain factors increase with smaller motion. Error bars denote standard error. (D) Remembered target positions for the world-fixed condition, collapsed over left and right motion, relative to fixation (0, dashed line) for each participant (filled circles). Initial targets are indicated by black open circles, actual target locations after motion are indicated in gray open circles. Mean remembered locations do not cross fixation in the small motion condition, but do cross in the medium and large displacement conditions, as indicated by the vertical black lines (mean perceived locations after motion, horizontal lines denote standard deviation).

FIGURE 3

Self-motion estimation activity. Electroencephalography (EEG) scalp topoplots (Left) of alpha-band activity for time windows before, during and after motion for the self-motion contrast. This contrast was created by using body-fixed data, averaged over all target locations, and subtracting small motion from large motion. Rightward motion was flipped across the midline and averaged with the leftward motion. This isolates activity that increases with larger motion, while subtracting out effects of target coding and constant activity. (Right) Time-frequency plot for a parieto-occipital ROI (Pz, PO3/4, POz, and PPO1/2h). Motion occurs between t = 1 and 2 s.

FIGURE 4

Target coding activity. EEG alpha-band scalp topoplots of the body-fixed condition, separately averaged for targets on the left (Top) and right (Middle), before, during and after motion. Activity is averaged over left and right motion directions. (Bottom) Subtraction of left and right target conditions (above). This contrast isolates effects of left vs. right target.

FIGURE 5

Spatial updating within hemifields. EEG topoplots from the world-fixed condition, averaged over trials where subjects indicate that the target remains on the same side as the initial target on the left (Top) and right (Middle). Visually presented targets are initially reflected by contralateralized alpha reductions, and evolve into alpha increases contralateral to the remembered target after motion. (Bottom) Subtraction of left and right target conditions, isolating activity related the target representation.

FIGURE 6

Spatial updating across hemifields. Same as Figure 5, but averaged over trials where the target is updated across hemifields, and is thus perceived to cross fixation. Consequently, the remembered target representation can be seen to remap to the other hemisphere after motion.

FIGURE 7

Behavioral Correlation. (A) Scalp topography plot of the regression t-value distribution for the gain-alpha pre–post analysis. A left parieto-temporal cluster (C3, CP6, CP3, P1, CCP5h, and CPP3h) shows a significant negative correlation (B) with gain values (r = -0.41). Data points mark subject averages of gain and pre–post alpha modulation over the three displacements. This indicates that higher performance (gain) goes along with a larger modulation of alpha band activity, specifically more alpha reduction after motion.