Background luminance effects on pupil size associated with emotion and saccade preparation

Abstract

Pupil dilation is consistently evoked by affective and cognitive processing, and this dilation can result from sympathetic activation or parasympathetic inhibition. The relative contributions of the sympathetic and parasympathetic systems on the pupillary response induced by emotion and cognition may be different. Sympathetic and parasympathetic activity is regulated by global luminance level. Higher luminance levels lead to greater activation of the parasympathetic system while lower luminance levels lead to greater activation of the sympathetic system. To understand the contributions of the sympathetic and parasympathetic nervous systems to pupillary responses associated with emotion and saccade preparation, emotional auditory stimuli were presented following the fixation cue whose color indicated instruction to perform a pro- or anti-saccade while varying the background luminance level. Pupil dilation was evoked by emotional auditory stimuli and modulated by arousal level. More importantly, greater pupil dilation was observed with a dark background, compared to a bright background. In contrast, pupil dilation responses associated with saccade preparation were larger with the bright background than the dark background. Together, these results suggest that arousal-induced pupil dilation was mainly mediated by sympathetic activation, but pupil dilation related to saccade preparation was primarily mediated by parasympathetic inhibition.

Figure 1

Experimental paradigm. Each trial began with a central fixation point on a background (Dark: 2 cd/m² or Bright: 16 cd/m²). After a delay, an emotional auditory stimulus was presented for 6 s, following with the instructed colored fixation cue (1200 ms) for pro- or anti-saccade condition. A blank screen was presented for 200 ms (gap) before target stimulus presentation, and participants were required to move their eyes to the target in the pro-saccade condition, or look away to the opposite location in the anti-saccade condition, after disappearance of the central fixation point. After that, participants were required to answer two questions about the sound presented.

Figure 2

Background luminance effects on raw pupil diameter (A) (n = 23). Relationships between arousal and valence rating (B). In B, the large-circle and error-bars represent the mean values ± standard error across participants and the small circles represent mean value for each participant.

Figure 3

Effect of background luminance on pupillary responses associated with emotional arousal. Pupil dynamics following emotional sounds in different arousal conditions on dark (A) and, bright (B) backgrounds (n = 23). Mean pupil size (2000 to 6000 ms) (C) and time to peak dilation (D) of pupillary responses can be seen in different arousal conditions with dark and bright backgrounds. In A and B the shaded colored regions surrounding the pupillary response curves represent the ± standard error range (across participants) for different conditions. In C and D, the large-circle and error-bars represent the mean values ± standard error across participants. The small circles represent mean value for each participant. *Indicates differences are statistically significant.

Figure 4

Effect of background luminance on pupillary responses related to saccade preparation. Pupil dynamics following instructed fixation cue in different saccade preparation conditions on dark (A) and, bright (B) backgrounds (n = 23). Mean pupil size (2000 to 6000 ms) (C) and time to peak dilation (D) of pupillary responses can be seen in different saccade preparation conditions with dark and bright backgrounds. In (A) and (B) the shaded colored regions surrounding the pupillary response curves represent the ± standard error range (across participants) for different conditions. In C and D the large-circle and error-bars represent the mean values ± standard error across participants. The small circles represent mean value for each participant.

Figure 5

Effect of background luminance on pupil velocity responses related to saccade preparation. (A) Pupil velocity dynamics following the instructed fixation cue in different saccade preparation conditions between the dark and bright background. (B) Peak pupil constriction velocity in different saccade preparation conditions with dark and bright backgrounds. In (A), the shaded colored regions surrounding the pupillary response curves represent the ± standard error range (across participants) for different conditions. In (B), the large-circle and error-bars represent the mean values ± standard error across participants. The small circles represent mean value for each participant. *Indicates differences are statistically significant.

Figure 6

Effect of background luminance on pupillary responses induced by emotion and saccade preparation. (A) Difference between pupillary responses evoked by negative valence stimuli with dark and bright backgrounds (dark minus bright pupil size) (n = 21). (B) Difference between pupillary responses related to anti-saccade preparation with dark and bright backgrounds (dark minus bright pupil size) (n = 21). (C) Mean participant differences in pupil size between dark and bright backgrounds (dark minus bright pupil size) related to emotion and saccade preparation (emotion: 2000—6000 ms; saccade preparation: 1300–1400 ms). In (A,B), the shaded regions surrounding the pupillary response curves represent the ± standard error range (across participants). The black bar on the x-axis indicates the time line at which differences between the dark and bright conditions were statistically deviated from zero (P < 0.05).

Figure 7

Effects of emotional arousal on saccade behavior. Saccade direction error (A) and saccade reaction times (B) during pro- and anti-saccade tasks with different arousal conditions (n = 23). The large-circle and error-bars represent the mean values ± standard error across participants. The small circles represent mean value for each participant. *Indicates differences are statistically significant.