The superior colliculus and the steering of saccades toward a moving visual target

Abstract

Following the suggestion that a command encoding current target location feeds the oculomotor system during interceptive saccades, we tested the involvement of the deep superior colliculus (dSC). Extracellular activity of 52 saccade-related neurons was recorded in three monkeys while they generated saccades to targets that were static or moving along the preferred axis, away from (outward) or toward (inward) a fixated target with a constant speed (20°/s). Vertical and horizontal motions were tested when possible. Movement field (MF) parameters (boundaries, preferred vector, and firing rate) were estimated after spline fitting of the relation between the average firing rate during the motor burst and saccade amplitude. During radial target motions, the inner MF boundary shifted in the motion direction for some, but not all, neurons. Likewise, for some neurons, the lower boundaries were shifted upward during upward motions and the upper boundaries downward during downward motions. No consistent change was observed during horizontal motions. For some neurons, the preferred vectors were also shifted in the motion direction for outward, upward, and "toward the midline" target motions. The shifts of boundary and preferred vector were not correlated. The burst firing rate was consistently reduced during interceptive saccades. Our study demonstrates an involvement of dSC neurons in steering the interceptive saccade. When observed, the shifts of boundary in the direction of target motion correspond to commands related to past target locations. The absence of shift in the opposite direction implies that dSC activity does not issue predictive commands related to future target location.NEW & NOTEWORTHY The deep superior colliculus is involved in steering the saccade toward the current location of a moving target. During interceptive saccades, the active population consists of a continuum of cells ranging from neurons issuing commands related to past locations of the target to neurons issuing commands related to its current location. The motor burst of collicular neurons does not contain commands related to the future location of a moving target.

Keywords: brain stem; foveation; interception; motion; saccade.

Fig. 1.

Schematic representation of the “dual drive” and “remapping” hypotheses and their predictions for the movement field (MF) of dSC neurons. Let us consider prototypical interceptive saccades directed toward a target moving toward the fixation target (A; inward motion) or along the same axis but in the opposite direction (B; outward motion). According to the dual drive hypothesis, population of activity in the dSC encodes the location where the target appears initially. Thus, the dSC activity is identical regardless of whether the saccade is aimed at a static target (dotted circle in C and D) or at a target moving inward (C) or outward (D). Neuron 2 (preferring amplitude b) situated at the center of the population should fire during both interceptive saccades. However, its MF is expected to be different between the 2 types of saccades (E). Compared with the MF observed with static targets (dashed black curve), the entire profile (preferred amplitude and boundaries) should shift toward smaller values of saccade amplitude during inward target motion and toward larger values during outward motion (gray solid curves). By contrast, neurons 1 (preferring amplitude a) and 3 (preferring amplitude c) are situated outside the active population and thus should not fire during these interceptive saccades. According to the remapping hypothesis, the activity can change after the target appearance; it would recruit neuron 1 during inward target motion (F) and neuron 3 during outward motion (G). The analysis of their MF should reveal more complex changes in MF, with some overlap between saccades toward a static vs. moving target (H).

Fig. 2.

Different target motion paths relative to a canonical movement field. The starting positions of moving targets (T_1ini) were pseudorandomly selected among locations situated along the same imaginary lines used for the targets during static trials. Target motion could be radial (A, inward or outward relative to fixation target T₀), vertical (B, upward or downward relative to T_1ini, motion along an axis parallel to and different from the vertical meridian) or horizontal (C, rightward or leftward motion along an axis parallel to and different from the horizontal meridian).

Fig. 3.

Instantaneous firing rate of a dSC visuomotor neuron after target onset and during single trials. A and B: visual and saccade-related activity following the appearance of a static target at different locations (Cartesian coordinates) of the right visual field. C–E: firing rate of the same neuron after the target appears and moves upward at the same horizontal eccentricity. In A and C, the target appears at a location corresponding to the preferred amplitude of the neuron’s movement field (MF). In D, the saccade is aimed at the same location as in A: the visual response is absent because the moving target appears outside the neuron’s response field. In E, the saccade is aimed at the same location as in B: the neuron does not fire when the target moves. Schema at bottom left shows the boundary of a putative MF (dashed line) and 3 saccade vectors. Crosses labeled A and B schematically represent starting position of saccades illustrated in A and B, respectively. Labels C, D, and E illustrate the saccade vectors shown in C–E.

Fig. 4.

Movement field (MF) of the same neuron as in Fig. 3 during saccades toward targets located on axis parallel to the vertical meridian (top) or along the radial axis of its MF (bottom). A and D: static target. B: target moving upward. C: target moving downward. E: target moving inward (toward the fixation target). F: target moving outward (away from the fixation target). Arrows in B and E show the shift in the boundary of the MF. Gray traces show the spline fit from static target trials. Insets in B, C, E, and F schematize the moving target (gray arrow) and 1 possible interceptive saccade (black arrow) in a head-centered reference frame.

Fig. 5.

Movement fields of 4 other neurons exhibiting a shift during saccades toward a moving target in comparison to saccades toward a static target. A: target moves to the right. B: target moves outward along the radial axis. C: target moves downward. D: target moves upward. Insets schematize the moving target (gray arrow) and 1 possible interceptive saccade (black arrow) in a head-centered reference frame.

Fig. 6.

Examples of 6 other neurons (A–F) where the shift of either the preferred amplitude or the inner boundary of the movement field was barely visible or almost absent. Gray, firing rate during interceptive saccades; black, firing rate during saccades toward a static target. Insets schematize the moving target (gray arrow) and 1 possible interceptive saccade (black arrow) in a head-centered reference frame.

Fig. 7.

Comparison of the MF boundaries between saccades toward a static target (x-axis) and saccades toward a target (y-axis) moving along the radial axis (A), a horizontal axis (B), and a vertical axis passing through the preferred amplitude (C and D). The moving target moves upward in C and downward in D. Each dot corresponds to the measurement provided by spline fitting the amplitude tuning curves for each neuron when this was possible (see Data set and analysis). In each graph, the mean and SD of differences (D values) and the statistical significance of their comparison with the Wilcoxon test are documented. P values obtained for not statistically significant differences (N.S., P > 0.05) can be found in the text.

Fig. 8.

Comparison of the MF preferred amplitude between saccades toward a static target (x-axis) and saccades toward a target (y-axis) moving along the radial axis (A), the vertical axis (B), and the horizontal axis passing through the preferred amplitude (C). Each dot corresponds to the measurement provided by spline fitting the amplitude tuning curves for each neuron when this was possible (see Data set and analysis). In each graph, the mean and SD of differences (D values) and the statistical significance of their comparison with the Wilcoxon test are documented. P values obtained for not statistically significant differences (N.S., P > 0.05) can be found in the text.

Fig. 9.

Comparison of the shifts of inner boundary and preferred amplitude during saccades toward a target moving inward (A) and outward (B). The shifts of inner boundary (C) and preferred amplitude (D) observed with the inward and outward targets are also shown. Each dot corresponds to the difference between the measurements shown in Figs. 7A and 8A (value during moving target condition − value during static target condition).

Fig. 10.

Comparison of the average firing rate (at MF preferred amplitude) of the motor burst between saccades toward a static target (x-axis) and saccades toward a target (y-axis) moving along the radial axis (A), the vertical axis (B), and the horizontal axis passing through the preferred amplitude (C). Each dot corresponds to the measurement provided by spline fitting the amplitude tuning curves for each neuron when this was possible (see Data set and analysis). In each graph, the mean and SD of differences (D values) and the statistical significance of their comparison with the Wilcoxon test are documented.

Fig. 11.

The firing rate of dSC cells is not related to the velocity of interceptive saccades. Two examples of cells are shown where the largest difference in MF was found between inward and outward target motions. For the neuron shown in A, the firing rate was higher during saccades of amplitude <5° when they were made to a target moving inward than to a target moving outward but lower for amplitudes >5° (left). The relation between the amplitude and the peak velocity of saccades does not show any difference between the 2 groups of saccades (right). For the neuron shown in B, the firing rate was lower for outward moving targets than for inward moving targets (left). Again, the relation between the amplitude and the peak velocity of saccades does not show any difference between the 2 groups of saccades (right).