Contextual saccade adaptation induced by sequential saccades

Abstract

Saccade adaptation is the gradual adjustment of saccade end point to maintain spatial accuracy. Contextual adaptation refers to a situation in which the adaptation-related change in saccade end point is contingent on the behavioral context in which the saccade is made. For example, in some situations, the same saccade to the same retinotopic location can be simultaneously adapted in opposite directions depending on the context in which it is made. Saccade adaptation has traditionally been studied in isolated movements, but in everyday life, saccades are often planned and executed in sequences. The oculomotor system may therefore have adaptive mechanisms specific to sequential saccades. Here, in five experiments, we investigated contextual saccade adaptation in sequences of saccades. In the first experiment, we demonstrate that saccades to a given retinotopic location can be simultaneously adapted in opposite directions depending on whether they occur in isolation or in a sequence. In the other experiments, we measured the extent to which properties of the previous and following saccades in a sequence can induce contextual saccade adaptation. Overall, we find that the existence, direction, and amplitude of previous and subsequent saccades, as well as the order of the current saccade within a movement sequence, can all induce contextual adaptation. These novel findings demonstrate the surprising flexibility of the system in maintaining end point accuracy, and support the idea that saccades made in a movement sequence are planned concurrently rather than independently.NEW & NOTEWORTHY This study reveals a new type of contextual saccade adaptation: sequential saccades are able to induce contextual saccade adaptation when direction, amplitude, or the existence of preceding and following saccades are used as contexts. These novel findings are also consistent with the idea that saccades made in a sequence are planned concurrently rather than independently.

Keywords: eye movement; saccade; saccade adaptation; saccade sequence.

Graphical abstract

Figure 1.

Schematic diagram showing the trial sequence in experiment 1 during the adapting phase, for the backward and forward adaptation contexts. Backward adaptation: i) A fixation point appears and subjects start fixation. ii) After 1,000 ± 250 ms, the fixation point disappears and simultaneously a target appears 10° below the fixation point. Subjects are instructed to perform a single saccade to the target as soon as possible. iii) In the adapting phase, during the saccade, a backward intrasaccadic step (ISS) is applied to the target to induce saccade adaptation. iv) A corrective saccade may be performed by subjects to fixate the target, and subjects are required to maintain fixation on the target for 400 ms. Forward adaptation: i) The fixation point is presented on the upper-right side of the screen and subjects start fixation. ii) After 1,000 ± 250 ms, the fixation point disappears and simultaneously two targets appear on the midline. iii) Subjects are instructed to perform the first saccade horizontally to the upper target and iv) a second saccade to the lower target. Upon initiation of the second saccade, the upper target disappears. Simultaneously, during the adapting phase, a forward ISS is applied to the second target. v) Subjects are required to maintain fixation on the final target for 400 ms, after any corrective saccade has been made.

Figure 2.

Results for adaption of a single saccade vs. a saccade in a sequence (experiment 1). A: saccade amplitude as a function of trial number. Data from a typical subject; black dashed lines separate baseline, adapting, and postadapting phases. Each circle indicates saccade amplitude. Solid lines indicate the moving average over trials. Blue and red colors, respectively, represent forward and backward adaptation. The saccade amplitudes gradually differ for the two contexts during the adapting phase, and this difference begins to decay during the postadapting phase. B: similarly, saccade amplitude is plotted as a function of trial number, averaged across all subjects in experiment 1. Thick lines indicate the moving average and the shaded regions indicate 95% CIs. C: this panel shows the difference in saccade amplitude in the two contexts during the adapting and postadapting phases. Each circle indicates the difference for each individual subject. The black horizontal lines indicate the average of these differences across all the subjects, and the green and yellow shaded bars the 95% CIs, respectively for the adapting (green) and postadapting (yellow) phases. CI, confidence interval.

Figure 3.

Effect of the direction of the preceding saccade on adaptation (experiment 2). Conventions are as in Fig. 2. except where noted. A: schematic diagram showing the trial sequence during the adapting phase. i) The fixation point is presented either on the upper-left side or upper-right side of the screen, respectively, in backward and forward adaptation contexts; then subjects start fixation. ii) After 1,000 ± 250 ms, the fixation point disappears and simultaneously two targets appear on the midline. iii) Subjects are instructed to perform the first saccade horizontally to the upper target; iv) and a second saccade to the lower target. Upon initiation of the second saccade, the upper target disappears. Simultaneously, during the adapting phase, an intrasaccadic step (ISS) is applied to the second target. v) Subjects are required to maintain fixation on the final target for 400 ms, after any corrective saccade has been made. B: saccade amplitude as a function of trial number, across all subjects. Thick and thin lines indicate moving averages with 95% CIs for forward (blue) and backward (red) adaptation. C: the difference in saccade amplitudes for the two contexts during the adapting and postadapting phases with 95% CIs. CI, confidence interval.

Figure 4.

Effect of the direction of the following saccade on adaptation (experiment 3). Conventions are as in Fig. 2. A: schematic of the trial sequence during the adapting phase. The fixation point appears and subjects start fixation; the orientation of a small gap in the fixation circle cues the direction of the second saccade. ii) The fixation point disappears after 1,000 ± 250 ms, and simultaneously three peripheral visual stimuli appear. iii) Subjects first make a saccade to the middle target as quickly as possible; in the adapting phase, upon saccade onset, a forward or backward intrasaccadic step (ISS) (depending on the context) is applied to the target. iv) Subjects may perform a corrective saccade. v) A second saccade toward the final target is made, and subjects are required to hold fixation for 400 ms. B: saccade amplitude as a function of trial number, across all subjects with 95% CIs. C: the difference between the saccade amplitudes in the two contexts during the adapting and postadapting phases with 95% CIs. CI, confidence interval.

Figure 5.

Effect of the amplitude of the following saccade on adaptation (experiment 4). Conventions are as in Fig. 2. A: schematic of the trial sequence during the adapting phase. i) The fixation point appears and subjects start fixation; a small gap in the fixation circle cues the eccentricity of the target for the second saccade. ii) The fixation point disappears after 1,000 ± 250 ms, and simultaneously three peripheral visual stimuli appear. iii) Subjects first make a saccade to the middle target as quickly as possible; in the adapting phase, upon saccade onset, a forward or backward intrasaccadic step (ISS) (depending on the context) is applied to the target. iv) Subjects may perform a corrective saccade. v) A second saccade toward the final target is made, and subjects are required to hold fixation for 400 ms. B: saccade amplitudes as a function of trial number, across all subjects with 95% CIs. C: the difference between the saccade amplitudes in adapting and postadapting phases with 95% CIs. CI, confidence interval.

Figure 6.

Effect of the order of the saccade within a sequence on adaptation (experiment 5). Conventions are as in Fig. 2 except where noted. A: schematic diagram showing the trial sequence during the adapting phase. Backward adaptation: i) The fixation point appears and subjects start fixation. ii) After 1,000 ± 250 ms, fixation point disappears and simultaneously two targets appear 10° below the fixation point. Subjects are instructed to first perform a saccade to the middle target as quickly as possible. iii) In the adapting phase, during the saccade, a backward intrasaccadic step (ISS) is applied to the target to induce saccade adaptation. iv) A corrective saccade may be performed by subjects to fixate the target, and subjects are required to maintain fixation on the target for 400 ms. Forward adaptation: i) The fixation point is presented on the upper-right side of the screen and subjects start fixation. ii) After 1,000 ± 250 ms, the fixation point disappears and simultaneously two targets appear on the midline. iii) Subjects are instructed to perform the first saccade horizontally to the upper target and iv) a second saccade to the lower target. Upon initiation of the second saccade, the upper target disappears. Simultaneously, during the adapting phase, a forward intrasaccadic step applied to the second target. v) Subjects are required to maintain fixation on the final target for 400 ms, after any corrective saccade has been made. B: saccade amplitudes as a function of trial number, across all subjects with 95% CIs. C: the difference between the saccade amplitudes in adapting and postadapting phases with 95% CIs. CI, confidence interval.

Figure 7.

Summary across all five experiments. Summary bar graph representing the amount of contextual saccade adaptation in each experiment. The bars indicate the amplitude difference between the two contexts in each experiment, during the adapting (green) and postadapting (yellow) phases. The error bars represent 95% CIs. Schematic diagrams of saccade sequences and intrasaccadic steps (ISSs) in each experiment are also presented in this figure. The blue arrows indicate the saccade direction and amplitudes, and red arrows indicate the direction of ISSs. Note that the backward and forward intersaccadic steps were switched between the contexts for half of the subjects. CI, confidence interval.