pubmed.ncbi.nlm.nih.gov

Illusory light drives pupil responses in primates - PubMed

  • ️Mon Jan 01 2024

Illusory light drives pupil responses in primates

Jean-Baptiste Durand et al. J Vis. 2024.

Abstract

In humans, the eye pupils respond to both physical light sensed by the retina and mental representations of light produced by the brain. Notably, our pupils constrict when a visual stimulus is illusorily perceived brighter, even if retinal illumination is constant. However, it remains unclear whether such perceptual penetrability of pupil responses is an epiphenomenon unique to humans or whether it represents an adaptive mechanism shared with other animals to anticipate variations in retinal illumination between successive eye fixations. To address this issue, we measured the pupil responses of both humans and macaque monkeys exposed to three chromatic versions (cyan, magenta, and yellow) of the Asahi brightness illusion. We found that the stimuli illusorily perceived brighter or darker trigger differential pupil responses that are very similar in macaques and human participants. Additionally, we show that this phenomenon exhibits an analogous cyan bias in both primate species. Beyond evincing the macaque monkey as a relevant model to study the perceptual penetrability of pupil responses, our results suggest that this phenomenon is tuned to ecological conditions because the exposure to a "bright cyan-bluish sky" may be associated with increased risks of dazzle and retinal damages.

PubMed Disclaimer

Figures

Figure 1.
Figure 1.

Experimental task and design. (A) Stimuli. The bright and dark versions of the Asahi brightness illusion with their overall mean luminance and color baseline (columns) for the three tested colors (cyan, magenta, and yellow; rows). (B) Protocol. Participants maintained their gaze on the central fixation cross while the baseline, bright, and dark Asahi stimuli were shown according to one of the two sequences shown (Asahi 1 or Asahi 2). The sequence was repeated three times in each run for a total duration of about one minute and 20 seconds. The Asahi 1 and Asahi 2 runs were interleaved and each participant performed 10 runs of each. (C) Expected pupil responses (illustrated in a monkey eye). Relative to the baseline condition, the illusory brighter center of the bright Asahi illusion should lead to pupil constriction (i.e., a decrease of its horizontal diameter, DH), whereas the illusory darker center of the dark Asahi illusion should evoke pupil dilation (i.e., an increase of DH).

Figure 2.
Figure 2.

Illustration of individual results. (A) Mean time courses of the baseline-corrected pupil responses (DH) to the bright (solid lines) and dark (dashed lines) Asahi stimuli for three exemplar subjects of the human informed and naïve groups (upper and middle rows) and monkey group (lower row). The left, middle, and right columns display the responses to the cyan, magenta, and yellow stimuli, respectively. (B) Mean baseline-corrected pupil diameter integrated over the early (0.5 to 2.0 sec) and late (2.5 to 4.0 sec) periods of the responses shown in (A) for the six Asahi stimuli. Error bars represent standard errors to the mean over trial repetitions for each subject. Statistical differences between pupil diameters evoked by pairs of illusory bright and dark stimuli were evaluated by unpaired two-sample t-tests (ns = nonsignificant; *p < 0.05; **p < 0.01; ***p < 0.001). Human and monkey silhouette images are from PhyloPic.org, available for reuse under Creative Commons licenses. H = human; I = informed; M = monkey; N = naïve].

Figure 3.
Figure 3.

Group results. (A) Mean time courses of the pupil responses (DH). (B) Mean pupil diameter integrated over the early and late periods of the responses shown in (A). Same conventions as Figure 2. GR = group.

Figure 4.
Figure 4.

(A–C) Mean differences in pupil diameter (DH) between the bright and dark Asahi stimuli during the early versus late periods for all the individuals of the informed human group (A), naïve human group (B) and monkey group (C). Each subject is represented three times for the three bright/dark pairs in cyan, magenta, and yellow (circular symbols of the same colors, with error bars representing the 90% confidence interval of the mean). (D) Overall difference in bright-dark pupil diameter for the three groups across early and late components and across colors (statistical comparisons with unpaired two-tailed t-tests). (E) Overall difference in bright-dark pupil diameter for the three color pairs across early and late components and across groups (statistical comparisons with unpaired two-tailed t-tests). (F) Overall difference in bright-dark pupil diameter for the cyan versus magenta/yellow stimuli in both humans (informed and naïve subjects together; white symbols) and monkeys (black symbols) subjects (statistical comparisons with unpaired one-tailed t-tests, with the hypotheses: cyan > magenta/yellow and monkeys > humans). In D–F, error bars represent the standard error of the mean. ns = non-significant. *p < 0.05; **p < 0.01; ***p < 0.001.

Similar articles

References

    1. Aminihajibashi, S., Hagen, T., Foldal, M. D., Laeng, B., & Espeseth, T. (2019). Individual differences in resting-state pupil size: Evidence for association between working memory capacity and pupil size variability. International Journal of Psychophysiology, 140, 1–7, 10.1016/j.ijpsycho.2019.03.007. - DOI - PubMed
    1. Banks, M. S., Sprague, W. W., Schmoll, J., Parnell, J. A. Q., & Love, G. D. (2015). Why do animal eyes have pupils of different shapes? Science Advances, 1(7), e1500391, 10.1126/sciadv.1500391. - DOI - PMC - PubMed
    1. Beatty, J. (1982). Task-evoked pupillary responses, processing load, and the structure of processing resources. Psychological Bulletin, 91(2), 276–292. - PubMed
    1. Binda, P., Pereverzeva, M., & Murray, S. O. (2013). Pupil constrictions to photographs of the sun. Journal of Vision, 13(6), 8–8, 10.1167/13.6.8. - DOI - PubMed
    1. Bombeke, K., Duthoo, W., Mueller, S. C., Hopf, J.-M., & Boehler, C. N. (2016). Pupil size directly modulates the feedforward response in human primary visual cortex independently of attention. NeuroImage, 127, 67–73, 10.1016/j.neuroimage.2015.11.072. - DOI - PubMed

MeSH terms