Visual fixation as equilibrium: evidence from superior colliculus inactivation

Abstract

During visual fixation, the image of an object is maintained within the fovea. Previous studies have shown that such maintenance involves the deep superior colliculus (dSC). However, the mechanisms by which the dSC supports visual fixation remain controversial. According to one view, activity in the rostral dSC maintains gaze direction by preventing neurons in the caudal dSC from issuing saccade commands. An alternative hypothesis proposes that gaze direction is achieved through equilibrium of target position signals originating from the two dSCs. Here, we show in monkeys that artificially reducing activity in the rostral half of one dSC results in a biased estimate of target position during fixation, consistent with the second hypothesis, rather than an inability to maintain gaze fixation as predicted by the first hypothesis. After injection of muscimol at rostral sites in the dSC, fixation became more stable since microsaccade rate was reduced rather than increased. Moreover, the scatter of eye positions was offset relative to preinactivation baselines. The magnitude and the direction of the offsets depended on both the target size and the injected site in the collicular map. Other oculomotor parameters, such as the accuracy of saccades to peripheral targets and the amplitude and velocity of fixational saccades, were largely unaffected. These results suggest that the rostral half of the dSC supports visual fixation through a distributed representation of behaviorally relevant target position signals. The inactivation-induced fixation offset establishes the foveal visual stimulation that is required to restore the balance of activity between the two dSCs.

Figure 1.

Distribution of muscimol injection sites within the dSC. Circle and square symbols correspond to the injections made in monkey A and W, respectively. The center of each site was estimated by the target location in retinotopic space that was associated with the largest saccade latency during a visually guided saccade task. This estimate does not reflect the entire extent of the inactivation. A spread of muscimol toward the rostral end of dSC must be considered even during those injections that were made at sites encoding target locations at 6° in the periphery (∼1.5 mm caudal to the rostral border of the dSC). The filled black circle indicates the site for the postinjection data shown in Figures 2, 3, 6, and 8. For each site, a volume of 0.5 μl of muscimol was injected. The open gray symbols indicate the injections that led to nystagmus.

Figure 2.

Sample experiment illustrating the fixation offset after muscimol injection in the right rostral dSC. The horizontal (top) and vertical (middle) eye positions recorded while the monkey looked at a large target are plotted during the last 1500 ms of the fixation interval for 15 randomly selected trials recorded before (Pre) and after muscimol injection (Post). Cartesian plots (bottom) illustrate the average eye position during fixation from all trials in the same session. These data show that the offset is rightward, i.e., toward the injected side.

Figure 3.

Effect of target size on the magnitude of the fixation offset after muscimol injection in the right rostral dSC (same sample experiment as in Fig. 2). A, Average eye position measured over the entire fixation interval for each target size (left, small; middle, medium; right, large) and each trial recorded before (○) and after (●) injection of muscimol. After injection, eye position was offset to the lower right relative to baseline. B, Effects of injecting saline solution in the same site in a separate, control experiment. No clear eye position offset was observed, suggesting that the offset in A was due to muscimol inactivation of dSC neurons.

Figure 4.

Summary of the effects of target size on the magnitude of the fixation offset measured for each experiment. The mean radial amplitude of offsets is plotted for each target size and for each experiment in two monkeys (error bars denote SEM). In both monkeys, an increase in the magnitude of the eye position offset was often observed with larger target sizes, but not always.

Figure 5.

A, B, Summary of the effects of injecting muscimol (A) or saline solution (B) on the fixation of different target sizes. The plot in A shows the average magnitude of the inactivation-induced offset in eye position as a function of the eccentricity encoded at the injected dSC site for each target size (black, small target; blue, medium; red, large). The error bars denote SEM. The offset magnitude depended on the population of neurons that were inactivated, and the pattern of offsets was very similar to that seen in the same monkeys during smooth pursuit (Hafed et al., 2008).

Figure 6.

Effect of inactivating the rostral dSC on the distributions of fixational saccade amplitudes. A, Distribution of horizontal amplitudes recorded before (gray) and after (black) injection of muscimol in the same site as in Figures 2 and 3. B, Distribution of vertical amplitudes. There was no apparent asymmetry in the distribution of fixational saccade amplitudes as might be expected if the eye position offset was caused by dysmetric fixational saccades.

Figure 7.

Summary of the effects of dSC inactivation on the rate of microsaccades generated during fixation of each target size (left, small target; middle, medium; right, large). A, Postinjection rate against preinjection rate. If anything, inactivation caused a reduction of saccade frequency rather than an increase, as might have been expected from the view of the rostral dSC as a region suppressing saccade generation. Filled symbols denote statistically significant differences between preinjection and postinjection rates (p < 0.05). B, Percent change in microsaccade frequency against eccentricity encoded at the injected site.

Figure 8.

Effect of inactivating the rostral dSC on the velocity of fixational saccades. The relationship between the radial amplitude and peak velocity is shown for all saccades generated while the monkey fixated on the central target (left, small target; middle, medium; right, large) before (blue) and after (red) muscimol injection. The same sample experiment as in Figures 2, 3, and 6 was used. No apparent change was caused by muscimol inactivation.

Figure 9.

Summary of the effects of dSC inactivation on the accuracy of saccades toward the peripheral targets. A–D, Each plot describes for each peripheral target location (target in the contralateral visual field, A; target in the ipsilateral field, B; target in the lower visual field, C; and target in the upper visual field, D) the horizontal and vertical dysmetria of saccades. Filled symbols indicate the differences between the preinjection and postinjection amplitude values that were statistically significant (Mann–Whitney test, p < 0.05).

Figure 10.

Accuracy of saccades to the peripheral targets for the experiment that led to the largest horizontal offset (Fig. 4, monkey A). A, Scatter of initial and final eye positions before (open symbols) and after (filled symbols) muscimol injection. Different colors are used to label the saccades toward the different targets (black, 12° up; blue, right; red, down; green, left). B, Relationship between the initial and final horizontal eye positions for each target. R values correspond to the Bravais–Pearson correlation coefficients. Despite a large offset during fixation, the targeting saccades to the periphery were relatively accurate.

Figure 11.

Summary of the effects of dSC inactivation on the latency of saccades toward the peripheral targets. A–D, Median values of latencies before and after injection for each cardinal direction. Filled symbols indicate the differences between the preinjection and postinjection latency values that were statistically significant (Mann–Whitney test, p < 0.05). Depending on the direction of the saccade, there were either increases or decreases in saccade latency.

Figure 12.

Effects of dSC inactivation on the peak velocity of saccades toward the peripheral targets (12° eccentricity) and their relationship to the changes in latency. A–D, Percent changes in latency (abscissa) and in horizontal (A, B) and vertical (C, D) peak velocity (ordinate) are shown for each cardinal direction. For contralesional saccades (A), the sites whose inactivation led to the larger increases in saccade latency were associated with larger reductions in peak velocity.