Does the middle temporal area carry vestibular signals related to self-motion?

Abstract

Recent studies have described vestibular responses in the dorsal medial superior temporal area (MSTd), a region of extrastriate visual cortex thought to be involved in self-motion perception. The pathways by which vestibular signals are conveyed to area MSTd are currently unclear, and one possibility is that vestibular signals are already present in areas that are known to provide visual inputs to MSTd. Thus, we examined whether selective vestibular responses are exhibited by single neurons in the middle temporal area (MT), a visual motion-sensitive region that projects heavily to area MSTd. We compared responses in MT and MSTd to three-dimensional rotational and translational stimuli that were either presented using a motion platform (vestibular condition) or simulated using optic flow (visual condition). When monkeys fixated a visual target generated by a projector, half of MT cells (and most MSTd neurons) showed significant tuning during the vestibular rotation condition. However, when the fixation target was generated by a laser in a dark room, most MT neurons lost their vestibular tuning whereas most MSTd neurons retained their selectivity. Similar results were obtained for free viewing in darkness. Our findings indicate that MT neurons do not show genuine vestibular responses to self-motion; rather, their tuning in the vestibular rotation condition can be explained by retinal slip due to a residual vestibulo-ocular reflex. Thus, the robust vestibular signals observed in area MSTd do not arise through inputs from area MT.

Figure 1.

A–D, 3D rotation tuning for an MT neuron tested during the vestibular condition (A, C), and the visual condition (B, D). The fixation point and visual stimuli were generated by a video projector in this case. Color contour maps in A and B show mean firing rate plotted as a function of 26 distinct azimuth and elevation angles (see inset). Each contour map shows the Lambert cylindrical equal-area projection of the original spherical data (Gu et al., 2006). Tuning curves along the margins of each color map illustrate mean ±SEM firing rates plotted as a function of either elevation or azimuth (averaged across azimuth or elevation, respectively). The PSTHs in C and D illustrate the corresponding temporal response profiles (each PSTH is 2 s in duration). The red Gaussian curves (bottom) illustrate the stimulus velocity profile.

Figure 2.

A–D, Summary of the selectivity of MT neurons in response to (A, B) visual and vestibular rotation and (C, D) visual and vestibular translation. Scatter plots in A and C compare the DDI in the visual versus vestibular conditions. Histograms in B and D show the absolute difference in 3D direction preferences between visual and vestibular conditions (|Δ preferred direction|) for the rotation and translation protocols, respectively. Data in B, D are included only for neurons with significant tuning in both stimulus conditions. All data are from the projector condition.

Figure 3.

Eye movement analysis showing incomplete suppression of reflexive eye movements. A, Average horizontal eye velocity is shown during leftward (black) and rightward (red) yaw rotation (vestibular condition). Traces show average eye velocity across all of the recording sessions for which data are shown in Figure 2. B, Average vertical eye velocity during upward (black) and downward (red) pitch rotation. C, Vector plot summary of the residual eye velocities in response to vestibular rotation for one monkey in the projector condition. Each vector represents the average eye velocity for one direction of rotation in one experimental session (green, leftward yaw; red, pitch down; purple, rightward yaw; black, pitch up). D, Average horizontal eye velocity during left/right translation. E, Average vertical eye velocity during up/down translation. F, Vector plot summary for the vestibular translation condition for the same animal as in C (green, left; red, down; purple, right; black, up). G, Distribution of eye speed (vector magnitude) for the same data depicted in C. H, Distribution of eye direction relative to stimulus direction for the data depicted in C. I, Average eye speed across animals for vestibular rotation (projector, laser, and darkness conditions) and vestibular translation (projector condition only). J, Average eye direction relative to stimulus direction for vestibular rotation and translation (format as in I).

Figure 4.

Receptive field maps and vestibular rotation responses for 4 MT neurons tested in the projector condition. A, D, G, J, Receptive field maps as obtained using a multi-patch reverse correlation method (see Materials and Methods). Each color map represents a region of visual space with a length and width one-half as large as the display screen. The fixation point was presented at the intersection of the dashed white lines. The cell depicted in A had a receptive field that overlapped the fixation point, whereas the other cells did not. B, E, H, K, Vestibular rotation tuning profiles, format as in Figure 1A,B. C, F, I, L, PSTHs corresponding to the 26 distinct directions of rotation tested in the projector condition. Format as in Figure 1C,D.

Figure 5.

A, Relationship between the strength of directional tuning in the vestibular rotation condition (using the projector) and the eccentricity of MT receptive fields. Each receptive field map, as in Figure 4, was fit with a two-dimensional Gaussian function. The eccentricity of the center of the receptive field is plotted on the abscissa, and the DDI is plotted on the ordinate. Filled symbols denote neurons with statistically significant rotation tuning (p < 0.05). Horizontal error bars represent receptive field size as ±2 SD of the Gaussian fit. Thus, the horizontal error bars contain 95% of the area of the receptive field. Symbols filled with stars indicate the 4 example neurons shown in Figure 4. B, Comparison of measured visual direction preferences with predicted preferences from vestibular rotation tuning in the projector condition. See Results for details. The strong correlation suggests that vestibular rotation tuning in the projector condition reflects visual responses to retinal slip.

Figure 6.

A–D, 3D direction tuning profiles for an MT neuron tested in the vestibular rotation condition when the fixation point is generated by (A, C) the video projector or (B, D) a head-fixed laser. Color contour maps in A and B show the mean firing rate as a function of azimuth and elevation angles (format as in Fig. 1). PSTHs in C and D show the corresponding temporal response profiles. E, Receptive field map for this neuron, format as in Figure 4.

Figure 7.

A–D, Comparison of vestibular rotation tuning in MT between projector and laser (A, B) or darkness (C, D) conditions. A, C, Histograms show the distribution of correlation coefficients between 3D tuning profiles measured in the projector versus laser (A) or projector versus darkness (C) conditions. Red bars indicate cells with significant (p < 0.05) correlations. B, D, Scatter plots compare the DDI between stimulus conditions. Filled circles, Cells with significant tuning (ANOVA, p < 0.05) under both conditions. Open circles, Cells with nonsignificant tuning under both conditions. Filled upright triangles, Cells with significant tuning only in the projector condition. Open inverted triangles, Cells with significant tuning only in the laser condition. Red symbols denote cells with significant (p < 0.05) correlation coefficients between the projector/laser or projector/darkness conditions.

Figure 8.

A–D, 3D rotation tuning profiles for an MSTd neuron tested under the projector (A, C) and laser (B, D) conditions. Color contour maps in A and B show mean firing rate as a function of azimuth and elevation angles. PSTHs in C and D illustrate the corresponding temporal response profiles (format as in Fig. 1).

Figure 9.

A–E, Comparison of vestibular rotation tuning in area MSTd between the projector and laser (A–C) or darkness (C–E) conditions. A, D, Histograms show the distribution of correlation coefficients between 3D tuning profiles measured in the projector versus laser (A) or projector versus darkness (D) conditions. B, E, Scatter plots compare the DDI between stimulus conditions (format as in Figure 7). C, F, Histograms show the absolute difference in 3D direction preferences (|Δ preferred direction|) between projector and laser conditions (C) or projector and darkness conditions (F). Only cells with significant tuning in both conditions were included in these histograms.