Kinesthetic and vestibular information modulate alpha activity during spatial navigation: a mobile EEG study

Abstract

In everyday life, spatial navigation involving locomotion provides congruent visual, vestibular, and kinesthetic information that need to be integrated. Yet, previous studies on human brain activity during navigation focus on stationary setups, neglecting vestibular and kinesthetic feedback. The aim of our work is to uncover the influence of those sensory modalities on cortical processing. We developed a fully immersive virtual reality setup combined with high-density mobile electroencephalography (EEG). Participants traversed one leg of a triangle, turned on the spot, continued along the second leg, and finally indicated the location of their starting position. Vestibular and kinesthetic information was provided either in combination, as isolated sources of information, or not at all within a 2 × 2 full factorial intra-subjects design. EEG data were processed by clustering independent components, and time-frequency spectrograms were calculated. In parietal, occipital, and temporal clusters, we detected alpha suppression during the turning movement, which is associated with a heightened demand of visuo-attentional processing and closely resembles results reported in previous stationary studies. This decrease is present in all conditions and therefore seems to generalize to more natural settings. Yet, in incongruent conditions, when different sensory modalities did not match, the decrease is significantly stronger. Additionally, in more anterior areas we found that providing only vestibular but no kinesthetic information results in alpha increase. These observations demonstrate that stationary experiments omit important aspects of sensory feedback. Therefore, it is important to develop more natural experimental settings in order to capture a more complete picture of neural correlates of spatial navigation.

Keywords: alpha band; alpha suppression; event related desynchronization; independent component analysis; mobile EEG; spatial navigation; time-frequency analysis; virtual reality.

Figure 1

Walkway. We devised a flexible walkway consisting of two straight segments that are connected by a turnable platform. Subjects were wearing an EEG cap (not shown in the picture) and a Head Mounted Display, and (were) moved along this predefined track while being stabilized by a cart, carrying auxiliary equipment.

Figure 2

Technical setup. The cart ensured that subjects stayed on track and completed the predefined path as required. It furthermore served as convenient repository for auxiliary mobile VR and EEG equipment like laptops or amplifiers.

Figure 3

Task schema and exemplary data. Black arrows: Traversed path. Dashed line: Ideal response. Blue arrows: Underestimated answers (exemplary answers from one single subject in the active condition). Green arrows: Overestimated answers. Red arrows: Mean answer angles. Comparing the difference between the red mean arrow and the dashed line in the 30° and 90° turning angle configurations shows that the amount of underestimation was less pronounced with increasing turning angle.

Figure 4

Interaction of the mean relative errors in the respective four conditions. Within 2 × 2 ANOVA (95% CI). By inspecting the 95% CIs we find underestimation of the correct homing angle (i.e., negative relative error) in all conditions but the kinesthetic one.

Figure 5

Clusters and task-related alpha modulations. The left column displays the locations of all dipoles belonging to the nine separate clusters projected to an MNI standard brain. Log-frequency ERSPs are shown in the central four columns. Blue denotes a decrease and red an increase in EEG power compared with baseline. ERSPs are not shown for PR, MR, and OR—they strongly resemble the pattern of their contralateral equivalents PL, ML, and OL. Boxplots in the right column depict the mean, cluster-wise ERSP activity in the alpha band (8–12 Hz) during the turn for each condition. In cluster OM the vestibular condition differs significantly from that in the passive and kinesthetic condition. More anterior clusters ML and FP show significant alpha band effects between vestibular and passive, vestibular and active, and active and passive conditions. ERSP alpha activity of cluster FP shows a significant difference between the kinesthetic and active condition. The clusters are labeled as follows: OM, Occipital Medial; OL, Occipital Left; OR, Occipital Right; PL, Parietal Left; PM, Parietal Medial; PR, Parietal Right; ML, Motor Left; MR, Motor Right; and FP, Fronto-Parietal.