Saccade suppression depends on context

Abstract

Although our eyes are in constant movement, we remain unaware of the high-speed stimulation produced by the retinal displacement. Vision is drastically reduced at the time of saccades. Here, I investigated whether the reduction of the unwanted disturbance could be established through a saccade-contingent habituation to intra-saccadic displacements. In more than 100 context trials, participants were exposed either to an intra-saccadic or to a post-saccadic disturbance or to no disturbance at all. After induction of a specific context, I measured peri-saccadic suppression. Displacement discrimination thresholds of observers were high after participants were exposed to an intra-saccadic disturbance. However, after exposure to a post-saccadic disturbance or a context without any intra-saccadic stimulation, displacement discrimination improved such that observers were able to see shifts as during fixation. Saccade-contingent habituation might explain why we do not perceive trans-saccadic retinal stimulation during saccades.

Keywords: human; motion habituation; neuroscience; saccade suppression; transsaccadic motion.

Figure 1.. Intra-saccadic habituation to sensorimotor contingencies.

(A) Schematic illustration of the proposed model. For saccade generation, a motor command is sent to the motor plant which produces the desired eye movement. Intra-saccadic visual stimulation will activate an extra-retinal storage mechanism. Importantly, this storage mechanism is activated only under the combined condition that an efferent copy signals the occurrence of an eye movement and visual stimulation is sensed. (B) Recurring input of visual stimulation will habituate neurons in the extra-retinal storage, consequently leading to a reduced sensitivity for intra-saccadic stimulation. In a context with low retinal stimulation, habituation remains weak and intra-saccadic neuronal responses to visual stimulation remain comparable to fixation. However, in a context with high retinal stimulation neurons habituate and intra-saccadic neuronal responses become weak.

Figure 2.. Experimental paradigm.

(A) Schematic illustration of a context trial. A full-field grating was presented throughout the entire trial. A trial started with the presentation of a fixation point. After 1000–1500 ms a saccade target was presented together with the fixation point for 60 ms. Then, both, the saccade target and the fixation point disappeared. Subjects were instructed to perform a saccade to the remembered position of the saccade target as soon as the fixation point disappeared. Depending on the session, the grating was displaced upwards after 35, 98, 187 ms or not displaced at all. (B) Time-course of events in the context trials for the fixation point (FP), the saccade target (ST), the seven horizontal eye position (H EP) and the grating displacement (Motion). (C,D) Example eye velocity profiles from one participant representing saccade performance in the context trials (shown in blue). Average eye position is shown by the blue line. Average timing of the actual grating displacement is shown by the red vertical line and the standard deviation of the timing by the shaded area. (E) Summary of conditions. Baseline sessions consisted only of test trials. The remaining four sessions contained context and test trials. In these sessions the grating was displaced 35, 98, 187 ms after saccade execution or not displaced at all. (F) Schematic illustration of a displacement discrimination trial. These trials were identical to the context trials except that the grating was shifted upwards or downwards (indicated by the orange arrows) by various displacement sizes and across trials at various times relative to saccade onset. Participants were instructed to report the displacement direction at the end of the trial by pressing the corresponding arrow key on the computer keyboard. (G,H) Psychometric functions for judgements of the displacement direction in the test trials for all observers. Data in gray represent discrimination performance for grating displacements that occurred outside the saccade execution period and colored data peri-saccadic discrimination. Data in purple derive from sessions in which the grating displacement occurred 35 ms after saccade initiation in the context trials and data in orange from sessions with no grating displacement in the context trials. Discrimination performance was quantified by the JND of the psychometric function.

Figure 3.. The effect of context on intra-saccadic motion discrimination.

(A,B) Thresholds for perceiving grating displacements - measured in the test trials - as a function of time relative to saccade onset for all participants. Data shown in purple derive from sessions in which the grating was displaced 35 ms after saccade onset in the context trials and data shown in orange from sessions with no grating displacement in the context trials. (C) Average saccade peak velocities in the five sessions for saccades performed in context trials (white bars) and saccades performed in test trials (blue bars). The black bar indicates average data from the baseline sessions and the blue bars average data from the context sessions. Error bars represent S.E.M. (D) Average horizontal amplitudes in the five sessions for saccades performed in context trials (white bars) and saccades performed in test trials (blue bars). Same conventions as in 3C. (E) Average vertical amplitudes in the five sessions for saccades performed in context trials (white bars) and saccades performed in test trials (blue bars). Same conventions as in 3C. (F) Saccade gain change calculated by subtracting the last ten vertical saccade amplitude of the context trials by the first ten vertical saccade amplitude of the context trials. (G) Average displacement discrimination thresholds - measured in the test trials - from baseline sessions. Data in gray represent thresholds from discrimination performance measured outside the period of saccade execution and data in red performance measured around saccade execution. Error bars represent S.E.M. (H) Average displacement discrimination thresholds - measured in the test trials - that were preceded by context trials. Same conventions as in 3G. (I) Average motion bias - measured in the test trials - from baseline sessions. Same conventions as in 3G. (J) Average motion bias - measured in the test trials - from test trials that were preceded by context trials. Same conventions as in 3G.

Figure 4.. Direction-specificity of intra-saccadic habituation.

(A) Schematic illustration of a displacement discrimination trial testing direction-specificity of the physical displacement direction. Two gratings were presented, one on the left and one on the right side of the screen. At trial start a fixation point (red color) was shown for 1000–1500 ms, then a saccade target (green color) appeared. After 60 ms both, the fixation point and the saccade target disappeared and participants were required to perform a saccade to the remembered position of the saccade target. One of the two gratings was displaced either during the saccade or after the saccade in either upward or downward direction. At the end of the trials participants had to indicate whether a displacement was seen at the left or the right side of the screen by pressing the corresponding arrow key on the computer keyboard. (B) Average displacement discrimination thresholds measured in the test trials. Bars shown in gray display average thresholds after upward displacements occurred in the test trials and white bars show thresholds after downward displacements occurred in the test trials. The small colored objects indicate performance of individual participants. Error bars represent S.E.M.

Figure 5.. Direction-specificity controlled for retinal speed.

(A) Schematic illustration of a displacement discrimination trial testing direction-specificity of the retinal motion direction. The procedure is identical to that described in Figure 4A except that different gratings were used in the test trials that were displaced in upward and leftward direction. (B) Average displacement discrimination thresholds measured in the test trials in sessions containing an upward motion context. Bars shown in gray display average thresholds after upward displacements occurred in the test trials and white bars show thresholds after downward displacements occurred in the test trials. The small colored objects indicate performance of individual participants. Error bars represent S.E.M. (C) Average displacement discrimination thresholds measured in the test trials in sessions containing a downward displacement context. Same conventions as in B).