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Pupil Dilation Reflects Perceptual Selection and Predicts Subsequent Stability in Perceptual Rivalry

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Pupil Dilation Reflects Perceptual Selection and Predicts Subsequent Stability in Perceptual Rivalry Pupil dilation reflects perceptual selection and predicts subsequent stability in perceptual rivalry Wolfgang Einha¨ user*†, James Stout*, Christof Koch*, and Olivia Carter‡§¶ *Division of Biology, California Institute of Technology, Pasadena, CA 91125; †Institute of Computational Science, ETH Zentrum, CAB G 81 Universita¨tstrasse, CH-8092 Zurich, Switzerland; ‡Vision Sciences Laboratory, Harvard University, 33 Kirkland Street, Cambridge, MA 02138; and §Brain Research Institute, Waterdale Road Heidelberg West, Victoria 3081, Australia Edited by Dale Purves, Duke University Medical Center, Durham, NC, and approved December 18, 2007 (received for review August 16, 2007) During sustained viewing of an ambiguous stimulus, an individu- In each individual, pupil diameter varies considerably during al’s perceptual experience will generally switch between the dif- constant presentation of an ambiguous visual stimulus (Fig. 1A). ferent possible alternatives rather than stay fixed on one inter- However, after aligning pupil diameter traces to the time of pretation (perceptual rivalry). Here, we measured pupil diameter reported perceptual switches and pooling the data, one observes while subjects viewed different ambiguous visual and auditory a sharp increase around the time of perceptual switching. This stimuli. For all stimuli tested, pupil diameter increased just before time course was qualitatively similar for all rivalry stimuli tested the reported perceptual switch and the relative amount of dilation (Fig. 1 B–E), and for all individuals [supporting information (SI) before this switch was a significant predictor of the subsequent Fig. 4]. A t test was used to compare pupil diameter to the 5-min duration of perceptual stability. These results could not be ex- mean (0 z score) at each of the 6,001 time points spanning Ϯ 3s plained by blink or eye-movement effects, the motor response or from the reported switch. To correct for multiple comparisons, stimulus driven changes in retinal input. Because pupil dilation significance is asserted only for time points with a P value below reflects levels of norepinephrine (NE) released from the locus that corresponding to an expected false discovery rate (FDR) of coeruleus (LC), we interpret these results as suggestive that the 0.05. Under this criterion, pupil diameter is significantly in- LC–NE complex may play the same role in perceptual selection as creased around the time of the perceptual switch in three of four in behavioral decision making. stimuli (black indicators in Fig. 1 B–E) and for five of six subjects (SI Fig. 4 and SI Table 1). When pooling over all subjects and attention ͉ norepinephrine ͉ vision ͉ decision making stimuli (Fig. 1F), the period of significance for the dilation response extends from 244 ms before to 1,552 ms after the reported switch (peaking at ϩ 602 ms: P ϭ 1.5 ϫ 10Ϫ18). ne pervading mystery in neuroscience is how the brain can Surrogate analysis rules out statistical artifacts (uncorrected P Ͼ Ogenerate an ‘‘internal’’ perceptual experience from the 0.12 for all time points). These findings provide evidence of a available ‘‘external’’ sensory information. Ambiguous stimuli, relationship between pupil dilation and perceptual switch events. like the Necker cube, offer a unique means to investigate this Because the pupil response spans nearly 2 s, pupil dilation at process because observers generally experience changes between any time point may be affected by either the preceding or the multiple perceptual states without corresponding changes in the following switch. Indeed, if we minimize the influence of in- stimulus (1). This phenomenon (‘‘perceptual rivalry’’) has been creased dilation stemming from the previous switch by excluding suggested to reflect a general strategy that balances a need for all short (Ͻ3 s) preswitch durations, the calculated preswitch a decisive stable percept for action planning (2), against the need diameter is systematically reduced, although the overall pattern for rapid reinterpretation of sensory information that is often of pupil dilation is conserved (Fig. 1F, green). Because the ambiguous or impoverished (3, 4). Neuroimaging and electro- dominance durations exhibit large variability within and across physiological studies are beginning to tease apart the different subjects (means ranging from 2–155 s, SI Table 2), we reanalyzed aspects of neural activity that correlate with the perception or pupil dilation with respect to a normalized time frame (9). This suppression of alternative perceptual states (for review see refs. maps each dominance period to a unit interval, aligning the 1 and 5). However, the mechanisms driving the switch in switches at time t ϭ 0 and the midpoints of each dominance perception are less clear. To date, no physiological marker has duration at Ϯ50%. This makes it possible to measure the been identified that shows any predictive relationship to the phase-shift of pupil-modulation relative to the surrounding duration of stability between successive switch events. switches. In this time frame, pupil dilation has a trough at Ϫ20%, Here we turn to pupil diameter, a physiological measure used i.e., a fifth cycle, before the switch (or four fifth cycles after the frequently half a century ago, but generally disregarded in preceding one), and peaks at ϩ13% after (ϭϪ87% before) each modern eye-tracking and imaging studies. A number of these switch (Fig. 1G). The switch coincides with the strongest slope older studies identified differential pupillary response to flashed of pupil dilation, whereas the mid-point of a dominance period Ϯ lights in the dominant or suppressed eye during binocular rivalry ( 50%) is associated with relatively stable pupil diameters. This (6–8). These findings remain intriguing; however, they are analysis shows that the rate of pupil dilation increase is maximal tangential to our current focus on the relationship between pupil around the time of perceptual switching, and starts just before diameter and the timing of perceptual rivalry switch events. its report. Results Author contributions: W.E. and O.C. designed research; W.E., J.S., and C.K. performed Pupil diameter of the right eye in six naı¨ve observers was research; C.K. contributed new reagents/analytic tools; W.E. analyzed data; and W.E. and recorded at 1 kHz during exposure to four different types of O.C. wrote the paper. rivalry stimuli: a Necker cube, structure from motion, visual The authors declare no conflict of interest. plaid, and auditory streaming. All measurements were recorded This article is a PNAS Direct Submission. in the dark. After familiarization with the stimuli, subjects were ¶To whom correspondence should be addressed. E-mail: [email protected]. presented each stimulus for 5 min and instructed to immediately This article contains supporting information online at www.pnas.org/cgi/content/full/ report any perceptual switch by pressing one of two keys 0707727105/DC1. (‘‘immediate report condition’’). © 2008 by The National Academy of Sciences of the USA 1704–1709 ͉ PNAS ͉ February 5, 2008 ͉ vol. 105 ͉ no. 5 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0707727105 Downloaded by guest on September 27, 2021 A MM - Necker-Cube; immediate response condition A 10-6 C0.4 9000 exp1 rivalry ]z[ exp2 rivalry 10-5 exp1 surrog. exp2 replay .te dia m eter [au] exp2 rivalry o n -4 i 10 exp2 replay c o r r e l a t -3 l d i a m p u p i l 10 0 p=.009 -2 p 10 p=.018 i 0.1 p p<.016 u p p<.016 1 -0.4 6000 -3 0 +3 -3 0 +3 200 210 220 230 240 time to report [s] time to report [s] time since stimulus onset [s] B D +4 ] 0.2 z[ p u pil dia m et. [z] t=-596ms B 0.8 C0.8 p o s p u pil dia m et. [z] p u pil dian=367 m et. [z] n=136 0 y e - pupil e -0.2 0 15% 9% pupil .cc sk nil 0 0 a all (exp1) s b p<.022 plaid 2% p<.009 -4 5% -0.4 -0.4 -1 0 +1 -3 0 +3 -3 0 +3 -3 0 +3 rel. dominance duration time to report [s] time to report [s] time to report [s] Fig. 2. Prediction of dominance durations and control conditions. (A) Sig- nificance of the correlation between relative postswitch dominance duration D0.8 E 0.8 and pupil diameter plotted for each time point Ϯ 3 s around the switch. The ] p u pil dia m et. [z] n=398 n=220 z a m e t . [ logarithmic scale indicates higher significance (lower P values) toward the top. Black, all data from experiment 1; pupil dilation offers the greatest prediction of subsequent perceptual stability 596 ms before the reported switch (r ϭ 0.13, i ϭ ϫ Ϫ5 0 p u p i l d 0 P 8.5 10 ). Blue, all rivalry data from experiment 2. Red, replay data from experiment 2. The lack of significance in the replay condition shows that the p<.014 prediction effect is not an artifact of analysis. For experiment 1, where no -0.4 -0.4 -3 0 +3 -3 0 +3 replay condition exists, this verification is done through surrogate analysis time to report [s] time to report [s] (gray). Horizontal lines indicate the P value thresholds corresponding to an expected FDR of 0.05. (B) Plot of correlation for data of experiment 1 at the time point of peak significance (t ϭϪ596 ms). Pink circles mark data from plaid F 0.4 G0.3 - r m a stimulus, which are significant on their own right. (C) Experiment 2 pooled ]z[ . ]z[ i a m e t . [ z ] n=1121 n=1121 s o e n f n over subjects and stimuli. Red, replay; blue, rivalry.
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