Convergence of vestibular and visual self-motion signals in an area of the posterior sylvian fissure

Abstract

Convergence of visual motion information (optic flow) and vestibular signals is important for self-motion perception, and such convergence has been observed in the dorsal medial superior temporal (MSTd) and ventral intraparietal areas. In contrast, the parieto-insular vestibular cortex (PIVC), a cortical vestibular area in the sylvian fissure, is not responsive to optic flow. Here, we explore optic flow and vestibular convergence in the visual posterior sylvian area (VPS) of macaque monkeys. This area is located at the posterior end of the sylvian fissure, is strongly interconnected with PIVC, and receives projections from MSTd. We found robust optic flow and vestibular tuning in more than one-third of VPS cells, with all motion directions being represented uniformly. However, visual and vestibular direction preferences for translation were mostly opposite, unlike in area MSTd where roughly equal proportions of neurons have visual/vestibular heading preferences that are congruent or opposite. Overall, optic flow responses in VPS were weaker than those in MSTd, whereas vestibular responses were stronger in VPS than in MSTd. When visual and vestibular stimuli were presented together, VPS responses were dominated by vestibular signals, in contrast to MSTd, where optic flow tuning typically dominates. These findings suggest that VPS is proximal to MSTd in terms of vestibular processing, but distal to MSTd in terms of optic flow processing. Given the preponderance of neurons with opposite visual/vestibular heading preferences in VPS, this area may not play a major role in multisensory heading perception.

Figure 1.

Reconstruction of recording sites. A, Inflated cortical surface illustrating approximate anterior/posterior locations of the coronal sections drawn in B–G. B, D, F, Coronal sections from the left hemisphere of monkey E. C, E, G, Coronal sections from the right hemisphere of monkey A. Cells located within 2 mm of each section have been projected onto that section. The pink symbols represent single units with significant tuning to both vestibular and visual translation stimuli. The black symbols represent cells tuned to vestibular translation only. The yellow symbols represent cells tuned to visual translation only.

Figure 2.

Example of 3D translation tuning for a single-peaked VPS neuron. A, C, E, Response PSTHs during vestibular, visual, and combined stimulation, respectively. The red lines indicate the peak time (t_vestibular = 0.85 s; t_visual = 0.83 s; t_combined = 0.84 s), when the maximum response across stimulus directions occurred. B, D, F, Corresponding 3D tuning curves at peak time are illustrated as color contour maps (Lambert cylindrical projections): vestibular DDI, 0.85; visual DDI, 0.83; combined DDI, 0.82. Tuning curves along the margins of each color map illustrate mean firing rates plotted versus elevation or azimuth (averaged across azimuth or elevation, respectively). From top to bottom, preferred directions for this cell (computed from the vector sum) are as follows: (azimuth, elevation) = (104, 55°), (−94, −50°), and (121, 61°).

Figure 3.

Example of 3D translation tuning for a double-peaked VPS neuron. A, C, E, Response PSTHs during vestibular, visual, and combined stimulation, respectively. The red and green lines indicate the early and late peak times (t_vestibular = 0.88 and 1.58 s; t_visual = 0.94 s; t_combined = 0.81 and 1.48 s). B, D, F, Corresponding 3D tuning curves at each peak time, illustrated as color contour maps. Preferred directions, defined in spherical coordinates as (azimuth, elevation), are as follows: vestibular, (48, −61°) (DDI, 0.79) and (−100, 45°) (DDI, 0.71); visual, (−151, 56°) (DDI, 0.71); and combined, (42, −55°) (DDI, 0.79) and (−126, 39°) (DDI, 0.68).

Figure 4.

Example of 3D translation tuning for an inhibitory VPS neuron. A, C, Response PSTHs during vestibular and visual stimulation. The red lines indicate the peak time (t_vestibular = 0.66 s; t_visual = 0.96 s), when the minimum response across directions occurred. B, D, Three-dimensional tuning profiles are as follows: vestibular DDI, 0.66; visual DDI, 0.69. This cell was not significantly tuned for heading at any time during the 2 s stimulus period.

Figure 5.

Summary of direction selectivity of VPS neurons during translation. A, Scatter plot of the visual DDI as a function of the vestibular DDI. Black-filled symbols, Cells with significant tuning during both vestibular and visual stimulation (n = 61); red symbols, cells with significant tuning during vestibular stimulation only (n = 59); green symbols, cells with significant tuning during visual stimulation only (n = 5); black open symbols, cells without significant tuning for either stimulus condition (n = 41). Dashed line, Unity–slope diagonal. B, C, Comparison of the strength of directional tuning to vestibular and visual stimulation, respectively, in the form of cumulative distributions of DDI. Data are shown for VPS (black, n = 166) and MSTd (gray, n = 336). For double- and triple-peaked cells, the DDI of the spatial tuning at the first peak time has been plotted. For cells without significant tuning, the DDI was computed at the time of maximum firing rate.

Figure 6.

Comparison of the first peak times of VPS and MSTd neurons during translation. Note that only cells with significant directional tuning are included here. A, Cumulative distribution of peak times for vestibular translation responses in VPS (black, n = 120) and MSTd (gray, n = 277). B, Cumulative distribution of peak times for visual translation responses in VPS (black, n = 66) and MSTd (gray, n = 331). The profiles of stimulus velocity and acceleration are also shown (bottom traces). The vertical solid line indicates the time of peak velocity. The dashed lines indicate the times of peak acceleration/deceleration.

Figure 7.

Summary of 3D heading preferences of VPS neurons during vestibular (A) and visual (B) stimulation. Each data point in the scatter plot corresponds to the preferred azimuth (abscissa) and elevation (ordinate) of a single neuron with significant unimodal heading tuning (A, n = 103; B, n = 50). The black symbols represent cells with significant tuning during both the vestibular and visual conditions. The red symbols represent cells with significant vestibular tuning only. The green symbols represent cells with significant visual tuning only. The data are plotted on Cartesian axes that represent the Lambert cylindrical equal-area projection of the spherical stimulus space. Histograms along the top and right sides of each scatter plot show the marginal distributions. Note that, for double- and triple-peaked cells, data are shown for the first peak time only. C, Distribution of the difference in 3D preferred direction (|Δ preferred direction|) between visual and vestibular responses (n = 39). Note that bins were computed according to the cosine of the angle (in accordance with the spherical nature of the data). Only neurons with significant unimodal spatial tuning for the first peak time during both vestibular and visual conditions have been included.

Figure 8.

Summary of response properties during combined visual/vestibular stimulation. A, B, Scatter plots of the combined DDI plotted versus the vestibular and visual DDI, respectively. Filled symbols, Cells for which both the combined and vestibular (A) or visual (B) tuning was significant (ANOVA, p < 0.01). Open symbols, Cells for which either the combined and/or the vestibular/visual tuning was not significant (ANOVA, p > 0.01) (n = 7). Black symbols, Cells with significant tuning during both the vestibular and visual conditions (n = 34); red symbols, cells with significant tuning during the vestibular condition only (n = 15); green symbols, cells with significant tuning during the visual condition only (n = 2). C, Cumulative distributions of peak time for responses to vestibular (gray upward triangles, n = 49), visual (gray downward triangles, n = 37), and combined (black circles, n = 51) translation in area VPS. The vertical line (solid) indicates the time of peak velocity. The dashed lines indicate the times of peak acceleration/deceleration. D, Histogram of the absolute difference in 3D preferred direction (|Δ preferred direction|) between combined and vestibular translation responses. Note that data are only plotted for opposite cells with significant, unimodal tuning under both stimulus conditions (n = 17). For double- and triple-peaked cells, only tuning at the first peak time has been included in this analysis.

Figure 9.

Comparison of vestibular versus visual dominance in the combined responses of VPS and MSTd neurons. A, Distributions of R² of the linear model fit (see Materials and Methods) for neurons from VPS (top) and MSTd (bottom). B, Distributions of the gain ratio, describing the relative weighting of visual and vestibular contributions to the combined response. Only cells with significant spatial tuning for both vestibular and visual stimuli and with good fits of the linear model (R² > 0.5) are included in this analysis (VPS, n = 28; MSTd, n = 134).

Figure 10.

Comparison between VPS responses to vestibular translation during fixation and during free viewing in darkness. A, Scatter plot of DDI values for cells tested under both fixation and darkness conditions (n = 74). Filled symbols, Cells with significant spatial tuning during both fixation and darkness (n = 59). Open symbols, Cells without significant spatial tuning during either fixation or darkness (n = 15). B, Distribution of the absolute difference in preferred direction (|Δ preferred direction|) between fixation and darkness for neurons that had significant unimodal tuning under both conditions (n = 42).

Figure 11.

Summary of 3D tuning of responses to rotation in darkness. A, Scatter plot compares DDI values for vestibular rotation and translation. The filled symbols indicate cells with significant tuning under both translation and rotation conditions (ANOVA, p < 0.01; n = 41). The open symbols denote cells without significant tuning for either one or both of the rotation and translation conditions (ANOVA, p > 0.01; n = 17). B, Distribution of 3D rotation preferences of VPS neurons. Each data point in the scatter plot corresponds to the preferred azimuth (abscissa) and elevation (ordinate) of a single neuron with significant rotation tuning (n = 31). The format is as in Figure 7, A and B. Note that, for double- and triple-peaked cells, data are shown for the first peak time only. C, Histogram of the absolute difference in 3D preferred direction (|Δ preferred direction|) between rotation and translation tuning, calculated only for neurons with significant unimodal tuning in both conditions (n = 26). The arrow marks the population mean (80° ± 4.4 SE).

Figure 12.

Anatomical localization of recording sites within and around the lateral sulcus. Each panel shows a lateral view of a 3D surface reconstruction of one hemisphere, with various functional areas denoted by colored regions. The yellow, black, and magenta symbols denote the locations of visual only, vestibular only, and multisensory neurons, respectively. A, The left hemisphere of monkey E from the present study. The region that we functionally define as VPS is located near the boundary of areas Ri (dark red) and 7op (blue). B, The right hemisphere of monkey A from the present study. C, The left hemisphere of monkey U from the study by Chen et al. (2010). D, The right hemisphere of monkey J from the study by Chen et al. (2010). Note that most neurons recorded in PIVC (C, D) are located more anteriorly, near the boundary between Ri (dark red) and S2 (green).