Multi-level processing of emotions in life motion signals revealed through pupil responses

  1. Tian Yuan
  2. Li Wang  Is a corresponding author
  3. Yi Jiang
  1. State Key Laboratory of Brain and Cognitive Science, Institute of Psychology, Chinese Academy of Sciences, China
  2. Department of Psychology, University of Chinese Academy of Sciences, China
12 figures, 1 video, 1 table and 1 additional file

Figures

Schematic representation of the experimental procedure and the stimuli in Experiment 1a.

A happy/sad/neutral biological motion (BM) walker turning 45° leftwards or rightwards was presented at the center of the screen for 4000 ms. Participants were instructed to maintain their fixation on the BM stimuli during stimulus presentation and to continue the procedure through key pressing.

Time course of pupil responses to happy, sad, and neutral biological motion (BM) in Experiments 1–4.

Solid lines represent pupil diameter under each emotional condition as a function of time (happy: red; sad: blue; neutral: gray); shaded areas represent the standard error of the mean (SEM) between participants (N = 24); colored horizontal lines indicate periods during which there are statistically significant differences among conditions at p < 0.05; and black horizontal lines indicate significant differences after cluster-based permutation correction. All the pupil data are in arbitrary units (a.u.) (A) In Experiment 1a, the happy BM evoked larger pupil response as compared to the sad and neutral BM, and the sad BM evoked smaller pupil size than the neutral BM. (B) In Experiment 2, the inverted BM failed to produce such emotional modulation effects. (C) In Experiment 3, the emotional BM that is deprived of the local motion feature exerted no emotional modulation on pupil responses. (D) In Experiment 4, both the happy and sad local BM induced a larger pupil response than the neutral local BM, and such dilation effect started from a relatively early time point.

Normalized mean pupil responses using the neutral condition as baseline, plotted against happy and sad conditions.

(A) In Experiment 1a, the group average pupil response to happy intact biological motion (BM) is significantly larger than that to sad and neutral BM, while the pupil size induced by sad BM is significantly smaller than that evoked by neutral BM. (B, C) Moreover, such an emotional modulation on pupil sizes was again identified in the test and retest of the replication experiment (Experiment 1b). (D) In Experiment 2, no significant differences in pupil responses were observed for inverted BM. (E) In Experiment 3, when the biological characteristic was deprived from the emotional BM, it failed to induce any modulations on pupil sizes. (F) In Experiment 4, both the happy and sad local BM induced a significantly larger pupil size than neutral local BM, with no significant difference between the happy and sad condition. All the pupil data are in arbitrary units (a.u.). Each point represents one individual data. Error bars showed standard errors of the mean (N = 24). *p < 0.05, **p < 0.01, ***p < 0.001.

Correlation results for pupil modulations and autistic quotient (AQ) scores in Experiment 1a and its replication experiment (Experiment 1b).

(A) In Experiment 1a, a significant negative correlation was found between the happy over sad pupil dilation effect and individual AQ. (B, C) No other significant correlations were found. (D–F) The first test of Experiment 1b replicated the negative correlation between happy over sad pupil dilation effect and AQ. Similarly, no other significant correlations were found. (G) In the second test, the negative correlation between happy over sad pupil dilation effect and AQ was similarly observed and even stronger. (H, I) Moreover, we have additionally observed a significant positive correlation between AQ and the happy minus neutral pupil dilation effect, and a significant negative correlation between AQ and the sad minus neutral pupil constriction effect. Dots in the scatter plot indicate the individual data and the shaded region indicates the 95% confidence interval (N = 24).

Correlation results for autistic quotient (AQ) scores and pupil responses toward happy, sad, and neutral biological motion (BM) across four experiments.

No significant correlations were observed. Dots in the scatter plot indicate the individual data and the shaded region indicates the 95% confidence interval (N = 24).

Time course of pupil responses to happy, sad, and neutral biological motion (BM) in Experiment 1b.

Solid lines represent pupil diameter under each emotional condition as a function of time (happy: red; sad: blue; neutral: gray); shaded areas represent the standard error of the mean (SEM) between participants (N = 24); colored horizontal lines indicate periods during which there are statistically significant differences among conditions at p < 0.05; and black horizontal lines indicate significant differences after cluster-based permutation correction. All the pupil data are in arbitrary units (a.u.). (A) In the first test of Experiment 1b, we successfully replicated the results of Experiment 1a: the happy BM evoked larger pupil response as compared to the sad and neutral BM, and the sad BM evoked smaller pupil size than the neutral BM. (B) Such results were similarly observed in the retest.

Author response image 1
Normalized mean pupil responses in the replication experiment (Experiment 1b) of Experiment 1a and its retest, using the neutral condition as baseline, plotted against happy and sad conditions.

(A) In the first test, the group average pupil response to happy intact BM is significantly larger than that to sad and neutral BM, while the pupil response induced by sad BM is significantly smaller than that evoked by neutral BM, replicating the results of Experiment 1a. (B) Moreover, such results were similarly found in the second test.

Author response image 2
Correlation results for pupil modulation effects and AQ scores in the replication experiment (Experiment 1b) of Experiment 1a and its retest.

(A) We replicated the negative correlation between the happy over sad pupil dilation effect and AQ in the first test. (B-C) No other significant correlations were found. (D) In the second test, the negative correlation between the happy over sad pupil dilation effect and AQ was similarly observed and even stronger. (E-F) Moreover, the happy vs. neutral pupil dilation effect and the sad vs. neutral pupil constriction effect respectively correlate with AQ in the second test.

Author response image 3
Time-series change in the microsaccade rates to happy, sad, and neutral BM in Experiments 1-4.

Solid lines represent microsaccade rates under each emotional condition as a function of time (happy: red; sad: blue; neutral: gray); shaded areas represent the SEM between participants. No significant differences were found after cluster-based permutation correction for the four experiments.

Author response image 4
Correlations between the happy over sad pupil dilation effect and AQ scores.

(A) The happy over sad pupil dilation effect correlated negatively with individual autistic scores. (B-C) Such correlation was similarly observed in the test and retest of the replication experiment. (D-F) No such correlations were found for the inverted, nonbiological, and local BM stimuli.

Author response image 5
No significant correlations between AQ and pupil response towards happy and sad intact BM were found in Experiment 1a and the test-retest replication experiment (Experiment 1b).
Author response image 6
Correlation results for pupil modulations and AQ scores.

(A-B) In Experiment 1a, no significant correlation was observed between AQ and the happy pupil modulation effect, as well as between AQ and the sad pupil modulation effect. (C-D) Similarly, no significant correlations were found in the first test of the replication experiment (Experiment 1b). (E-F) Importantly, in the second test of Experiment 1b, the happy vs. neutral pupil dilation effect was positively correlated with AQ, and the sad vs. neutral pupil constriction effect was positively correlated with AQ.

Videos

Video 1
Demonstration of motion stimuli used in Experiments 1–4.

Tables

Author response table 1
Reliability of pupil size and AQ indices.
MeasurementsFirst TestSecond TestTest-retest
M(SD)alphar
happy-sad pupil size0.19(0.22)0.30(0.34)0.600.61^(****)
AQ score19.4(5.6)19.9(6.2)0.820.90^(cdots)

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  1. Tian Yuan
  2. Li Wang
  3. Yi Jiang
(2024)
Multi-level processing of emotions in life motion signals revealed through pupil responses
eLife 12:RP89873.
https://doi.org/10.7554/eLife.89873.3