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. Author manuscript; available in PMC: 2021 May 1.
Published in final edited form as: Biol Psychol. 2020 Apr 9;153:107885. doi: 10.1016/j.biopsycho.2020.107885

Motivated action: Pupil diameter during active coping

Christopher T Sege a, Margaret M Bradley a, Peter J Lang a
PMCID: PMC7269865  NIHMSID: NIHMS1583419  PMID: 32278595

Abstract

Pupil diameter is dynamically modulated by a number of factors, including emotion, motor activity, and attention. Here, pupil modulation was examined as it varies with locus of control during aversive processing. Participants could control aversive exposure either by escape (terminating the event) or avoidance (blocking the event entirely), or they had no control. Highly anxious (n=19), moderately anxious (n=23), and less anxious (n=23) participants saw cues that signaled whether a fast button press would terminate, prevent, or not affect subsequent presentation of an aversive picture. Pupil diameter was measured throughout the cuing interval. Pupil diameter was larger when preparing to escape or avoid compared to anticipating uncontrollable exposure. All participants, regardless of reported anxiety, showed increased pupil diameter in coping, relative to uncontrollable, contexts. Results support hypotheses that pupil diameter reflects action preparation and that differences in trait anxiety do not modulate this aspect of coping behavior in healthy subjects.

Keywords: Emotion, Motor Activity, Pupil, Anxiety

Active avoidance and escape each involve action to cope with aversive exposure, but differ in that avoidance eliminates exposure whereas escape does not. Pupil size indexes sympathetic activation in motive contexts; current research tests if pupil diameter differs when aversive stimuli are avoidable, escapable, or uncontrollable. Additionally, because people with exaggerated anxiety or anxiety-related disorders show increased avoidance/escape from aversive stimulation (Foa, Huppert, & Cahill, 2006), this study tests if trait anxiety affects pupil diameter in contexts where aversive exposure can be avoided, escaped, or not controlled.

Pupil size increases during aversive exposure (Bradley, Miccoli, Escrig, & Lang, 2008; Bitsios, Szbadi, & Bradshaw, 1996), imagination (Henderson, Bradley, & Lang, 2018), and anticipation. When anticipating uncontrollable aversive stimulation (e.g., approaching needles or electric shocks), initial constriction is followed by dilation as the aversive event nears (Bitsios, Szabadi, & Bradshaw, 2004; Hofle, Hauck, Engel, & Senkowski, 2013). Pupil also dilates when preparing for rapid action after a cue, with increasing diameter as the time to act nears (van der Molen, Boomsma, Jennings & Nieuwboer, 1989; Moresi, Adam, Rijcken, van Gerven, Kuipers, & Jolles, 2008; Moresi, Adam, Rijcken, Kuipers, Severens, & van Gerven, 2011; Fletcher, Neal, & Yeo, 2017). Given effects of aversion and action on pupil, this study tests if dilation differs when preparing to actively avoid (entirely block) or escape (shorten, not prevent) aversion, and compares each to anticipating uncontrollable exposure.

Anxiety also impacts pupil modulation in certain contexts. In an early study, pupil size during a stressful task was larger for individuals high in “audience sensitivity” than for less sensitive individuals (Simpson & Molloy, 1971). Subsequent research found individuals with heightened anxiety show greater dilation during pain (Bertrand, Garcia, Viera, Santos, & Bertrand, 2013) and emotional face perception (Hepsomali, Hadwin, Liversedge, & Garner, 2017). Additionally, pupil response to threat images is enhanced in individuals with posttraumatic stress disorder (PTSD) relative to trauma-exposed individuals without PTSD (Felmingham, Rennie, Manor, & Bryant, 2011; Cascardi, Armstrong, Chung, & Pare, 2015). While these studies show anxiety effects on pupil during aversive exposure, present research examines pupil change when anticipating controllable or uncontrollable aversive events.

In this experiment, ~5s cues indicate if upcoming disgusting/mutilation-related pictures: a) can be avoided by a rapid button press before picture onset; b) can be escaped by a rapid button press after picture onset, or; c) cannot be controlled. Pupil diameter is measured during each cue and also compared across low-, moderate-, and high-anxiety groups.

Method

Participants

Seventy-five undergraduates participated for course credit. Three participants were excluded for gaze avoidance and 7 for technical problems/poor tracking conditions (e.g., glasses interfered). The analyzed sample was 65 participants (42 women, M age=19 years). The study was approved by the local IRB; participants provided written consent.

Participants were assigned to anxiety groups based on Spielberger State-Trait Anxiety Inventory – trait form (STAI-T; Spielberger, Gorsuch, Luschene, Vagg, & Jacobs, 1983) scores. Cut-offs were derived and applied a priori based on STAI-T data from previously collected large samples of students and psychology treatment-seeking patients. Because 49 was the median for patients and the 75th %ile score for the previous students, it was the cut-off for the high-anxious group (n=19). Because a score of 39 was the median for the previous students and corresponds to published suggestions that a score of 40 or above indicates elevated anxiety (Knight, Waal-Manning, & Spears, 1983), it was the cut-off for low anxiety (n=23). Scores between 39–49 were considered moderate (n=23).

Design and Materials

Each trial began with a 5–5.5s cue, followed by a “go” signal (avoidance trials) or aversive picture (escape, uncontrollable trials) for 500ms (Figure 1). On avoidance trials, a button press during the go signal led to subsequent 2.5s neutral picture presentation; failure to press the button led to 2.5s aversive picture presentation. On escape trials, a button press during initial exposure switched the picture to a neutral scene for 2.5s; failure to press the button led to continued aversive exposure for 2.5s more. On uncontrollable trials, initial aversive exposure was followed by 2.5s continued presentation regardless of any button press. 11 or 14s intertrial intervals followed each trial.

Figure 1.

Figure 1.

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Experiment design.

Task stimuli included 3 grayscale cues matched in luminance, contrast and complexity and consisting of different shapes (triangle, circle, diamond) that cued whether exposure was avoidable, escapable, or uncontrollable (counterbalanced across participants). The go signal was a central upward-pointing arrow.

Aversive stimuli were pictures depicting disgust/mutilation selected from the International Affective Picture System (IAPS; Lang, Bradley, & Cuthbert, 2008) or located by internet search. Neutral stimuli were selected from the IAPS or Emotional Picture Set (EmoPicS; Wessa, Kanske, Neumeister, Bode, Heissler, & Schonfelder, 2010) and depicted people at work.

Procedure

Each cue’s meaning was described before the task; participants were told to press a button held in the dominant hand as quickly as possible when a go signal (avoidance trials) or picture (escape trials) appeared. Participants were told that pressing the button before cue offset would eliminate control; they were told not to press the button on uncontrollable trials.

Data Collection, Reduction & Analysis

Pupil diameter1 was measured with an ASL D6 desk-mounted eye tracker (Applied Science Laboratories, Bedford, MA). Diameter was sampled at 60Hz from 2s pre to 8s post cue onset. Missing data due to blinks were interpolated. Diameter during a 1-s pre-trial baseline was subtracted from each sample point. Based on resulting waveforms, early constriction was quantified as average change 0.5–1s after cue onset, and late dilation was average change in the final s of cuing. Unsuccessful coping trials (i.e., reaction time>500ms; 13.3% escape trials, 12.5% avoidance trials), trials where the button was pressed before cue offset (<1% of all trials), and uncontrollable trials with a button press (<1% of trials) were excluded.

In a MANOVA framework, context (escape, avoid, uncontrollable) was included as a repeated measure and anxiety (low, moderate, high) as a between-subject factor. Using GPower 3.1.9.4, analyses were determined to be sensitive to a medium-sized interaction (η2=.087) with Power=.80. To complement traditional analysis of the interaction, Bayesian statistics are also presented.

Results

Figure 2 depicts pupil change during the cue, with initial constriction after cue onset followed by subsequent dilation. Early constriction did not differ by context, F(2,62)=1.1, p=.35, ηp2=.03, or anxiety, F(2,62)=0.3, p=.76, ηp2=.01. Late dilation did differ by context, F(2,62)=38.0, p<.001, ηp2=.38, with enhanced dilation when preparing to avoid, t(64)=7.0, p<.001, d=.87, or escape, t(64)=6.8, p<.001, d=.85, compared to anticipating uncontrollable aversion. Dilation did not differ across escape or avoidance contexts, t(64)=0.4, p=.7, d=.06.

Figure 2.

Figure 2.

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Pupillary response in avoidance, escape, and uncontrollable aversive contexts. Left panel depicts pupil diameter change across the cue interval (solid vertical line demarcates cue onset). Right panel depicts mean change during the final second of cuing.

Note: ***p < .001; marks indicate statistical differences from the uncontrollable condition.

Anxiety did not affect overall dilation, F(2,62)=0.3, p=.72, ηp2=.02, or its modulation by context, Context X Anxiety F(4,124)=1.8, p=.15, ηp2 = .05. Bayesian ANOVA also indicated that a model with Context as the only factor (Log[BF10]=24.1) explained pupil variance better than Context+Anxiety (Log[BF10]=23.0) or Context+Anxiety+Context*Anxiety Interaction (Log[BF10]=22.1) models. Specific group (BF10=.32) and interaction (BF10=.42) effects were negligible. Finally, correlating STAI score with pupil change also indicated that anxiety did not relate to dilation in escape, r(64)=−.05, p=.67, avoid, r(64)=−.02, p=.86, or uncontrollable, r(64)=−.19, p=.13, contexts.

Discussion

Pupil dilation is enhanced when preparing to cope with aversive exposure, regardless of whether coping avoids or escapes stimulation. Trait anxiety did not affect dilation in any context, as high-, moderate-, and low-anxiety groups each showed enhanced dilation during coping preparation. Together, the data suggest that pupil dilation reflects action preparation in anticipatory contexts, and trait anxiety does not affect such processing at least in non-treatment seeking individuals anticipating generally aversive images.

Pupil dilation correlates with sympathetic responses (e.g., galvanic skin response) in emotional exposure (e.g., picture-viewing) contexts (Bradley et al., 2008; Bradley, Sapigao, & Lang, 2017). Current data suggest that, in anticipation, sympathetic dilation is particularly apparent when preparing active coping; in this way, dilation is like other autonomic (e.g., skin conductance) responses that are also enhanced during action preparation relative to passive anticipation, and it differs from startle reflex potentiation which increases with context aversiveness, not action demand (Sege et al., 2018). Inasmuch as action removes exposure in avoidance and escape contexts, similar dilation reflects motivation to act quickly regardless of exposure certainty.

Current data further suggest that, in non-treatment-seeking individuals, sympathetic activation during coping preparation is also similar regardless of trait anxiety. This fits with the fact that each group rated study stimuli as highly aversive (Sege et al., 2018) and thus likely were similarly motivated to remove those stimuli. While current data suggest anxiety does not impact pupil during preparation to cope with aversive scenes, other studies show that anxiety affects dilation during exposure to stress (Simpson & Molloy, 1971), pain, or trauma-relevant stimuli (Felmingham et al. 2011; Bertrand et al., 2013; Cascardi et al., 2015; Hepsomali et al., 2017). Findings suggest potential context-specific anxiety-related disruptions of physiology (Lissek, Pine, & Grillon, 2006; McTeague, 2016), with further research needed to identify specific conditions that reveal anxiety effects.

In sum, pupil dilation when preparing to cope with aversive visual stimuli reflects action readiness that is not affected by high, non-clinical anxiety. Future research could examine generalization to other stimuli and to individuals seeking anxiety-related treatment.

HIGHLIGHTS.

  • The study measures pupil change when preparing to escape or avoid aversive stimuli

  • Pupil size increased in active coping, relative to uncontrollable aversive, contexts

  • Trait anxiety did not affect dilation during escape or avoidance preparation

  • Pupil reflects action preparation that is consistently enhanced in coping contexts

Acknowledgements

The authors thank Lisa McTeague for her helpful input during manuscript preparation. Power analyses were conducted in consultation with the National Center for Advancing Translational Sciences of the National Institutes of Health under Grant Number UL1 TR001450.

Funding Sources

This work was supported by the National Institute of Mental Health [grant numbers MH094386, MH098078].

Footnotes

Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

1

Reaction time, aversiveness ratings, startle blink, heart rate, and skin conductance were also collected and reported in Sege, Bradley & Lang, 2018.

References

  1. Bitsios P, Szbadi E, Bradshaw CM. The inhibition of the pupillary light reflex by the threat of an electric shock: A potential laboratory model of human anxiety. J Psychopharmacol. 1996;10(4):279–87. doi: 10.1177/026988119601000404. [DOI] [PubMed] [Google Scholar]
  2. Bertrand AL, Garcia JB, Viera EB, Santos AM, Bertrand RH. Pupillometry: The influence of gender and anxiety on the pain response. Pain Physician. 2013;16(3):E257–66. [PubMed] [Google Scholar]
  3. Bradley MM, Miccoli L, Escrig MA, Lang PJ. The pupil as a measure of emotional arousal and autonomic activation. Psychophysiology. 2008;45(4):602–7. doi: 10.1111/j.1469-8986.2008.00654.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bradley MM, Sapigao RG, Lang PJ. Sympathetic ANS modulation of pupil diameter in emotional scene perception: Effects of hedonic content, brightness, and contrast. Psychophysiology. 2017;54(10):1419–35. doi: 10.1111/psyp.12890. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cascardi M, Armstrong D, Chung L, Paré D Pupil response to threat in trauma-exposed individuals with or without PTSD. J Trauma Stress. 2015;28(4):370–4. doi: 10.1002/jts.22022. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Felmingham KL, Rennie C, Manor B, Bryant RA. Eye tracking and physiological reactivity to threatening stimuli in posttraumatic stress disorder. 2011. J Anxiety Disord. 2011;25(5):668–73. doi: 10.1016/j.janxdis.2011.02.010. [DOI] [PubMed] [Google Scholar]
  7. Fletcher K, Neal A, Yeo G The effect of motor task precision on pupil diameter. Appl Ergon. 2017;65:309–15. doi: 10.1016/j.apergo.2017.07.010. [DOI] [PubMed] [Google Scholar]
  8. Foa EB, Huppert JD, Cahill SP. Emotional processing theory: An update In Rothbaum BO (Ed.), Pathological anxiety: Emotional processing in etiology and treatment (pp. 3–24). 2006;New York, NY: The Guilford Press. [Google Scholar]
  9. Hepsomali P, Hadwin JA, Liversedge SP, Garner M Pupillometric and saccadic measures of affective and executive processing in anxiety. Biol Psychol. 2017;127:173–9. doi: 10.1016/j.biopsycho.2017.05.013. [DOI] [PubMed] [Google Scholar]
  10. Henderson RR, Bradley MM, & Lang PJ (2018). Emotional imagery and pupil diameter. Psychophysiology, 55, e13050. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Höfle M, Hauck M, Engel AK, Senkowski D Viewing a needle pricking a hand that you perceive as yours enhances unpleasantness of pain. Pain. 2012;153(5):1074–81. doi: 10.1016/j.pain.2012.02.010. [DOI] [PubMed] [Google Scholar]
  12. Knight RG, Waal-Manning HJ, Spears GF (1983). Some norms and reliability data for the State-Trait Anxiety Inventory and the Zung Self-Rating Depression Scale. British Journal of Clinical Psychology, 22, 245–249. doi: 10.1111/j.20448260.1983.tb00610.x [DOI] [PubMed] [Google Scholar]
  13. Lang PJ, Bradley MM, Cuthbert BN. International affective picture system (IAPS): Affective ratings of pictures and instruction manual Technical Report A-8. 2008; University of Florida: Gainesville, FL. [Google Scholar]
  14. Lang PJ, Bradley MM, & Cuthbert (1990). Emotion, attention, and the startle reflex. Psychological Review, 97, 377–95. [PubMed] [Google Scholar]
  15. Lissek S, Pine DS, Grillon C The strong situation: A potential impediment to studying the psychobiology and pharmacology of anxiety disorders. Biol Psychol. 2006;72(3):265–70. [DOI] [PubMed] [Google Scholar]
  16. McTeague LM. Reconciling RDoC and DSM approaches in clinical psychophysiology and neuroscience. Psychophysiology. 2016;53(3):336–47. doi: 10.1111/psyp.12462. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Moresi S, Adam JJ, Rijcken J, van Gerven PW, Kuipers H, Jolles J Pupil dilation in response preparation. Int J Psychophysiol. 2008;67(2): 124–30. [DOI] [PubMed] [Google Scholar]
  18. Moresi S, Adam JJ, Rijcken J, Kuipers H, Severens M, van Gerven PW. Response preparation with adjacent versus overlapped hands: A pupillometric study. Int J Psychophysiol. 2011;79(2):280–6. doi: 10.1016/j.ijpsycho.2010.11.005. [DOI] [PubMed] [Google Scholar]
  19. Sege CT, Bradley MM, & Lang PJ (2018). Avoidance and escape: Defensive reactivity and trait anxiety. Behavioural Research & Therapy, 104, 62–8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Simpson HM, Molloy FM. Effects of audience anxiety on pupil size. Psychophysiology. 1971;8(4):491–6. [DOI] [PubMed] [Google Scholar]
  21. Spielberger CD, Gorsuch RL, Luschene PR, Vagg PR, Jacobs GA. Manual for the State-Trait Anxiety Inventory. 1983; Consulting Psychologists Press. [Google Scholar]
  22. Vanderhasselt MA, Remue J, Ng KK, De Raedt R The interplay between the anticipation and subsequent online processing of emotional stimuli as measured by pupillary dilation: The role of cognitive reappraisal. Front Psychol. 2014;5:207. doi: 10.3389/fpsyg.2014.00207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. van der Molen MW, Boomsma DI, Jennings JR, Nieuwboer RT. Does the heart know what the eye sees? A cardiac/pupillometric analysis of motor preparation and response execution. Psychophysiology. 1989;26(1):70–80. doi: 10.1111/j.1469-8986.1989.tb03134.x [DOI] [PubMed] [Google Scholar]
  24. Wessa M, Kanske P, Neumeister P, Bode K, Heissler J, Schonfelder S EmoPics: Subjective and Psychophysiological evaluation of new images for clinical bio-psychological research. J Clin Psychol Psychother. 2010;S1(11):77. [Google Scholar]

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