Binocular disparity tuning and visual-vestibular congruency of multisensory neurons in macaque parietal cortex

Abstract

Many neurons in the dorsal medial superior temporal (MSTd) and ventral intraparietal (VIP) areas of the macaque brain are multisensory, responding to both optic flow and vestibular cues to self-motion. The heading tuning of visual and vestibular responses can be either congruent or opposite, but only congruent cells have been implicated in cue integration for heading perception. Because of the geometric properties of motion parallax, however, both congruent and opposite cells could be involved in coding self-motion when observers fixate a world-fixed target during translation, if congruent cells prefer near disparities and opposite cells prefer far disparities. We characterized the binocular disparity selectivity and heading tuning of MSTd and VIP cells using random-dot stimuli. Most (70%) MSTd neurons were disparity selective with monotonic tuning, and there was no consistent relationship between depth preference and congruency of visual and vestibular heading tuning. One-third of disparity-selective MSTd cells reversed their depth preference for opposite directions of motion [direction-dependent disparity tuning (DDD)], but most of these cells were unisensory with no tuning for vestibular stimuli. Inconsistent with previous reports, the direction preferences of most DDD neurons do not reverse with disparity. By comparison to MSTd, VIP contains fewer disparity-selective neurons (41%) and very few DDD cells. On average, VIP neurons also preferred higher speeds and nearer disparities than MSTd cells. Our findings are inconsistent with the hypothesis that visual/vestibular congruency is linked to depth preference, and also suggest that DDD cells are not involved in multisensory integration for heading perception.

Figure 1.

Viewing geometry and the relationships between depth and retinal velocity. A, When a subject fixates a world-fixed target while translating upward, near objects move downward on the display screen, whereas far objects move upward. B, When the same self-translation occurs while fixating a head-fixed target, both near and far objects move downward in the display.

Figure 2.

3D heading tuning and joint disparity-direction tuning for an “opposite” MSTd neuron. A, B, 3D heading tuning is shown for the vestibular (A) and visual (B) stimulus conditions as color contour maps of mean firing rate as a function of azimuth and elevation angles. Each contour map shows the Lambert cylindrical equal-area projection of the spherical data onto Cartesian coordinates (Gu et al., 2006). In this projection, the ordinate is a sinusoidally transformed version of elevation angle. Tuning curves along the margins of each color map illustrate mean firing rates plotted as a function of either elevation or azimuth (averaged across azimuth or elevation, respectively). C, The joint disparity-direction tuning profile of the same MSTd neuron is shown as a color-contour map, where direction of motion is plotted on the abscissa and binocular disparity on the ordinate. Tuning curves along the margins show direction tuning for each disparity (top) and disparity tuning for each direction (left). Dashed lines denote spontaneous activity levels. This neuron was direction tuned (ANOVA, p < 0.001) but not disparity tuned (ANOVA, p = 0.135).

Figure 3.

Joint direction-disparity tuning profile for a non-DDD, disparity-tuned, congruent MSTd cell. For this neuron, direction and disparity tuning are essentially separable, such that disparity tuning is similar for different directions and direction tuning is similar across disparities. Global DSDI = 0.707 (p < 0.001, permutation test). The format is as in Figure 2C.

Figure 4.

Examples of two DDD neurons from area MSTd. A, For this cell, disparity preference reversed for opposite motion directions (left), and direction preference reversed for near versus far disparities (top). B, For this neuron, disparity preference reversed for opposite motion directions (left), but direction preference did not reverse for near versus far disparities (top). The format is as in Figures 2C and 3. C, The DSDI of the three disparity-selective example neurons (from Fig. 3 and A, B) is plotted as a function of motion direction. For non-DDD cells like the one from Figure 3, the DSDI changes little with direction of motion (red). For DDD cells (cyan, blue), the DSDI shows a strong reversal in sign across different motion directions.

Figure 5.

Population summary of dependence of the DSDI on motion direction. A–D, Data are averaged across all disparity-selective neurons from MSTd (A, C) and VIP (B, D), and are shown separately for DDD (A, B) and non-DDD (C, D) cells. Data are color coded to represent visual-only neurons (red) and multisensory congruent (green) or opposite (blue) cells. Before averages were computed, data for each neuron were horizontally shifted and wrapped such that the peaks of all DSDI curves aligned at a direction of 90°. The necessary shift for each neuron was determined by computing a cross-correlation between the DSDI versus direction curve and a sinusoid (see Materials and Methods). The numbers of neurons contributing to each summary curve are as follows: A, 3 congruent cells, 3 opposite cells, 17 visual-only cells; B, 1 congruent cell, 4 visual-only cells; C, 9 congruent cells, 11 opposite cells, 29 visual-only cells; D, 5 congruent cells, 5 opposite cells, 26 visual-only cells.

Figure 6.

Population summary of response patterns for DDD cells. For each neuron, the scatter plot shows the difference in average response between preferred and null directions at far disparities (ordinate) versus the corresponding difference in response at near disparities (abscissa). Data are shown only for DDD neurons from MSTd (red) and VIP (blue). A–E show disparity tuning curves for preferred and null directions for five different example neurons, corresponding to the labeled data points in the scatter plot.

Figure 7.

Population summary of the DSDI and speed preferences. A, B, Distributions of the global DSDI (computed across all motion directions) for disparity-selective non-DDD neurons from areas MSTd (n = 49) and VIP (n = 36). C, D, Distributions of preferred speed for MSTd (n = 41) and VIP (n = 73) neurons. Data are color coded to represent visual only neurons (red) and multisensory congruent (green) or opposite (blue) cells.

Figure 8.

Dependence of the DSDI on dot density and stimulus speed. Data are shown for non-DDD cells from area MSTd. A, DSDI measured at a higher dot density (0.01 dots · degree⁻²) is plotted against the DSDI measured at the standard density (0.002 dots · degree⁻²; n = 21). B, DSDI is measured as a function of stimulus speed for a subset of MSTd neurons (n = 38).

Figure 9.

Example disparity tuning curves and Gabor fits for MSTd and VIP neurons. For each neuron/row, disparity tuning is shown for the direction of maximum DDI (left) and for the direction 180° opposite to it (right). A–D, Data are shown for two DDD cells from MSTd (A, B), one non-DDD cell from MSTd (C), and one non-DDD neuron from VIP (D). Smooth curves represent Gabor function fits (see Materials and Methods). Gabor fits are shown for both directions of motion for DDD cells, but only for the maximum DDI direction for non-DDD cells.

Figure 10.

Comparison of disparity selectivity in areas MSTd, VIP, and MT. A–C, The top row shows distributions of the DDI (A), preferred disparity (B), and disparity frequency (C) parameters. A, Data for all neurons tested: 103 MSTd neurons (red), 101 VIP cells (blue), and 501 MT neurons (green). B, C, Data for 55 MSTd cells and 29 VIP neurons that had significant disparity tuning (p < 0.01, one-way ANOVA) for the max DDI direction and were well-fit by the Gabor function (R² > 0.8) (see Materials and Methods). The MT data in B and C represent 453 MT neurons with significant disparity tuning (p < 0.01) (DeAngelis and Uka, 2003). Numbers above arrowheads show the median values for each distribution. D, DDI is plotted as a function of receptive field eccentricity for neurons from MT (n = 501), MSTd (n = 65), and VIP (n = 28). E, Preferred disparity as a function of eccentricity (MT, n = 453; MSTd, n = 41; VIP, n = 15). F, Disparity frequency as a function of eccentricity, for the same samples of neurons as in E.