Antero-Posterior vs. Lateral Vestibular Input Processing in Human Visual Cortex

Abstract

Visuo-vestibular integration is crucial for locomotion, yet the cortical mechanisms involved remain poorly understood. We combined binaural monopolar galvanic vestibular stimulation (GVS) and functional magnetic resonance imaging (fMRI) to characterize the cortical networks activated during antero-posterior and lateral stimulations in humans. We focused on functional areas that selectively respond to egomotion-consistent optic flow patterns: the human middle temporal complex (hMT+), V6, the ventral intraparietal (VIP) area, the cingulate sulcus visual (CSv) area and the posterior insular cortex (PIC). Areas hMT+, CSv, and PIC were equivalently responsive during lateral and antero-posterior GVS while areas VIP and V6 were highly activated during antero-posterior GVS, but remained silent during lateral GVS. Using psychophysiological interaction (PPI) analyses, we confirmed that a cortical network including areas V6 and VIP is engaged during antero-posterior GVS. Our results suggest that V6 and VIP play a specific role in processing multisensory signals specific to locomotion during navigation.

Keywords: V6; VIP; fMRI; galvanic vestibular stimulation (GVS); visual cortex; visuo-vestibular integration.

Figure 1

Galvanic vestibular stimulation (GVS) procedure. (A) The two antero-posterior configurations. (B) The two lateral configurations. (C) Sham configuration. (D) Representation of behavioral results. Inverted triangles give the p- and t-values of the permutation tests for each subject.

Figure 2

Images from the brain of one participant showing the key results. (Top-center patches) Egomotion-consistent (EC) and egomotion-inconsistent (EI) optic flow patterns used as localizers stimuli. (A) Contrast between the cortical responses recorded during the egomotion consistent (EC) vs. inconsistent (EI) optic flow conditions. Data are shown on inflated cortical surfaces and flat maps for the left and right hemispheres (p < 0.001, uncorrected). The positions of the parieto-occipital sulcus (POS) and cingulate sulcus (CS) are provided as anatomical landmarks. Colored circles outline the five Regions of Interest (ROIs) in this subject. (B) Responses during the galvanic stimulation (GVS) experiment for the same participant. Voxels whose activations were stronger during GVS conditions than during baseline were colored in blue (antero-posterior, AP), red (lateral, lat) and cyan (both) before being superimposed transparently on the inflated brain and flat maps.

Figure 3

Average beta values obtained in our different ROIs during the antero-posterior (blue) and lateral (red) GVS conditions. Values corresponding to the sham condition are provided in white. The error bars give the standard errors. The # symbols are here to remind that in some subjects, the ventral intraparietal (VIP) and posterior insular cortex (PIC) ROIs were only defined in one hemisphere (see details in the text). We report here the significant differences between AP and Lat conditions (post hoc t-test, ***p < 0.001, *p < 0.05). The results of the other statistical comparisons are reported in the main document.

Figure 4

Control to characterize the influence of the ROI spatial extents on the results. These analyses were performed for V6, cingulate sulcus visual (CSv), hMT+, VIP, and PIC (from top to bottom). (A) Histograms showing the number of voxels within an ROI as a function of the Euclidean distance to the ROI centroid. The green colors give the repartition of 60%, 80%, and 100% closest voxels. (B) Bar graphs of the beta values for the two GVS conditions (AP, in blue and Lat, in red) and the sham stimulation. The analysis only included the 80% closest voxels to the centroid. (C) Idem for the 60% closest voxels.

Figure 5

Psychophysiological interaction (PPI) functional connectivity analysis. Multiregional PPI was run across the five ROIs identified in the localizer protocol. Results are shown for the Lat (A) and AP (B) GVS conditions. A solid line between two ROIs corresponds to a connection that is significantly stronger during this condition (P < 0.001) than during baseline.

Figure 6

Perceptual reports during the control experiment for vergence (n = 5). The proportion of “left,” “aligned” and “right” answers are provided for both the antero-posterior (AP) and lateral (Lat) conditions. The “left” and “right” reports respectively correspond to convergence and divergence eye movements (see details in the text). The error bars give the standard errors.