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Reduced Pupil Oscillation During Facial Emotion Judgment in People with Autism Spectrum Disorder

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Abstract

People with autism spectrum disorder (ASD) show abnormal face perception and emotion recognition. However, it remains largely unknown whether these differences are associated with abnormal physiological responses when viewing faces. In this study, we employed a sensitive emotion judgment task and conducted a detailed investigation of pupil dilation/constriction and oscillation in high-functioning adult participants with ASD and matched controls. We found that participants with ASD showed normal pupil constriction to faces; however, they demonstrated reduced pupil oscillation, which was independent of stimulus properties and participants’ perception of the emotion. Together, our results have revealed an abnormal physiological response to faces in people with ASD, which may in turn be associated with impaired face perception previously found in many studies.

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References

  • Adolphs, R., Sears, L., & Piven, J. (2001). Abnormal processing of social information from faces in Autism. Journal of Cognitive Neuroscience, 13, 232–240.

    Article  PubMed  Google Scholar 

  • Aldaqre, I., Schuwerk, T., Daum, M. M., Sodian, B., & Paulus, M. (2016). Sensitivity to communicative and non-communicative gestures in adolescents and adults with autism spectrum disorder: Saccadic and pupillary responses. Experimental Brain Research, 234, 2515–2527.

    Article  PubMed  Google Scholar 

  • Alexander, W. H., & Brown, J. W. (2010). Computational models of performance monitoring and cognitive control. Topics in Cognitive Science, 2, 658–677.

    Article  PubMed  PubMed Central  Google Scholar 

  • Anderson, C. J., & Colombo, J. (2009). Larger tonic pupil size in young children with autism spectrum disorder. Developmental Psychobiology, 51, 207–211.

    Article  PubMed  PubMed Central  Google Scholar 

  • Anderson, C. J., Colombo, J., & Jill, S. D. (2006). Visual scanning and pupillary responses in young children with autism spectrum disorder. Journal of Clinical and Experimental Neuropsychology, 28, 1238–1256.

    Article  PubMed  Google Scholar 

  • Anderson, C. J., Colombo, J., & Unruh, K. E. (2013). Pupil and salivary indicators of autonomic dysfunction in autism spectrum disorder. Developmental Psychobiology, 55, 465–482.

    Article  PubMed  Google Scholar 

  • Arora, I., Bellato, A., Ropar, D., Hollis, C., & Groom, M. J. (2021). Is autonomic function during resting-state atypical in Autism: A systematic review of evidence. Neuroscience & Biobehavioral Reviews, 125, 417–441.

    Article  Google Scholar 

  • Aston-Jones, G., & Cohen, J. D. (2005). An integrative theory of locus coeruleus-norepinephrine function: Adaptive Gain and Optimal Performance. Annual Review of Neuroscience, 28, 403–450.

    Article  PubMed  Google Scholar 

  • Baron-Cohen, S., Jolliffe, T., Mortimore, C., & Robertson, M. (1997). Another advanced test of theory of mind: evidence from very high functioning adults with autism or asperger syndrome. Journal of Child Psychology and Psychiatry, 38, 813–822.

    Article  PubMed  Google Scholar 

  • Bast, N., Banaschewski, T., Dziobek, I., Brandeis, D., Poustka, L., & Freitag, C. M. (2019). Pupil dilation progression modulates aberrant social cognition in autism spectrum disorder. Autism Research, 12, 1680–1692.

    Article  PubMed  Google Scholar 

  • Beatty, J. (1982). Task-evoked pupillary responses, processing load, and the structure of processing resources. Psychological Bulletin, 91, 276–292.

    Article  PubMed  Google Scholar 

  • Blaser, E., Eglington, L., Carter, A. S., & Kaldy, Z. (2014). Pupillometry reveals a mechanism for the autism spectrum disorder (ASD) advantage in visual tasks. Scientific Reports, 4, 4301.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bradley, M. M., Miccoli, L., Escrig, M. A., & Lang, P. J. (2008). The pupil as a measure of emotional arousal and autonomic activation. Psychophysiology, 45, 602–607.

    Article  PubMed  PubMed Central  Google Scholar 

  • Brainard, D. H. (1997). The psychophysics toolbox. Spatial Vision, 10, 433–436.

    Article  PubMed  Google Scholar 

  • Brisson, J., Mainville, M., Mailloux, D., Beaulieu, C., Serres, J., & Sirois, S. (2013). Pupil diameter measurement errors as a function of gaze direction in corneal reflection eyetrackers. Behavior Research Methods, 45, 1322–1331.

    Article  PubMed  Google Scholar 

  • Cole, M. W., Yeung, N., Freiwald, W. A., & Botvinick, M. (2009). Cingulate cortex: Diverging data from humans and monkeys. Trends in Neurosciences, 32, 566–574.

    Article  PubMed  PubMed Central  Google Scholar 

  • Daluwatte, C., Miles, J. H., Christ, S. E., Beversdorf, D. Q., Takahashi, T. N., & Yao, G. (2013). Atypical pupillary light reflex and heart rate variability in children with autism spectrum disorder. Journal of Autism and Developmental Disorders, 43, 1910–1925.

    Article  PubMed  PubMed Central  Google Scholar 

  • Dawson, G., Webb, S. J., & McPartland, J. (2005). Understanding the nature of face processing impairment in autism: insights from behavioral and electrophysiological studies. Developmental Neuropsychology, 27, 403–424.

    Article  PubMed  Google Scholar 

  • de Berker, A. O., Rutledge, R. B., Mathys, C., Marshall, L., Cross, G. F., et al. (2016). Computations of uncertainty mediate acute stress responses in humans. Nature Communications, 7, 10996.

    Article  PubMed  PubMed Central  Google Scholar 

  • Duchaine, B., & Yovel, G. (2015). A revised neural framework for face processing. Annual Review of Vision Science, 1, 393–416.

    Article  PubMed  Google Scholar 

  • Einhauser, W., Koch, C., & Carter, O. (2010). Pupil dilation betrays the timing of decisions. Frontiers in Human Neuroscience. https://doi.org/10.3389/fnhum.2010.00018

    Article  PubMed  PubMed Central  Google Scholar 

  • Falck-Ytter, T. (2008). Face inversion effects in autism: A combined looking time and pupillometric study. Autism Research, 1, 297–306.

    Article  PubMed  Google Scholar 

  • Fuentemilla, L., Marco-Pallarés, J., & Grau, C. (2006). Modulation of spectral power and of phase resetting of EEG contributes differentially to the generation of auditory event-related potentials. NeuroImage, 30, 909–916.

    Article  PubMed  Google Scholar 

  • Gotham, K. O., Siegle, G. J., Han, G. T., Tomarken, A. J., Crist, R. N., et al. (2018). Pupil response to social-emotional material is associated with rumination and depressive symptoms in adults with autism spectrum disorder. PLoS ONE, 13, e0200340.

    Article  PubMed  PubMed Central  Google Scholar 

  • Happe, F., Ronald, A., & Plomin, R. (2006). Time to give up on a single explanation for autism. Nature Neuroscience, 9, 1218–1220.

    Article  PubMed  Google Scholar 

  • Happé, F., & Frith, U. (2006). The weak coherence account: detail-focused cognitive style in autism spectrum disorders. Journal of Autism and Developmental Disorders, 36, 5–25.

    Article  PubMed  Google Scholar 

  • Harms, M., Martin, A., & Wallace, G. (2010). Facial emotion recognition in autism spectrum disorders: A review of behavioral and neuroimaging studies. Neuropsychology Review, 20, 290–322.

    Article  PubMed  Google Scholar 

  • Hartmann, M., & Fischer, M. H. (2014). Pupillometry: the eyes shed fresh light on the mind. Current Biology, 24, R281–R282.

    Article  PubMed  Google Scholar 

  • Joseph, R. M., & Tanaka, J. (2003). Holistic and part-based face recognition in children with autism. Journal of Child Psychology and Psychiatry, 44, 529–542.

    Article  PubMed  Google Scholar 

  • Joshi, S., Li, Y., Kalwani Rishi, M., & Gold, J. I. (2016). Relationships between pupil diameter and neuronal activity in the locus coeruleus, colliculi, and cingulate cortex. Neuron, 89, 221–234.

    Article  PubMed  Google Scholar 

  • Kana, R. K., Patriquin, M. A., Black, B. S., Channell, M. M., & Wicker, B. (2016). Altered medial frontal and superior temporal response to implicit processing of emotions in Autism. Autism Research, 9, 55–66.

    Article  PubMed  Google Scholar 

  • Kardon R. 2005. Anatomy and physiology of the autonomic nervous system. Walsh and Hoyt's Clinical Neuro-Ophthalmology: 649–714

  • Kennedy, D. P., & Adolphs, R. (2012). Perception of emotions from facial expressions in high-functioning adults with autism. Neuropsychologia, 50, 3313–3319.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kliemann, D., Dziobek, I., Hatri, A., Steimke, R., & Heekeren, H. R. (2010). Atypical reflexive gaze patterns on emotional faces in autism spectrum disorders. The Journal of Neuroscience, 30, 12281–12287.

    Article  PubMed  PubMed Central  Google Scholar 

  • Klin, A., Jones, W., Schultz, R., Volkmar, F., & Cohen, D. (2002). Visual fixation patterns during viewing of naturalistic social situations as predictors of social competence in individuals with autism. Archives of General Psychiatry, 59, 809–816.

    Article  PubMed  Google Scholar 

  • Kuchinke, L., Schneider, D., Kotz, S. A., & Jacobs, A. M. (2011). Spontaneous but not explicit processing of positive sentences impaired in Asperger’s syndrome: Pupillometric evidence. Neuropsychologia, 49, 331–338.

    Article  PubMed  Google Scholar 

  • Lamirel, C., Ajasse, S., Moulignier, A., Salomon, L., Deschamps, R., et al. (2018). A novel method of inducing endogenous pupil oscillations to detect patients with unilateral optic neuritis. PLoS ONE, 13, e0203170.

    Article  Google Scholar 

  • Lane RD. 2000. Neural correlates of conscious emotional experience. Cognitive neuroscience of emotion: 345–70

  • Latinus, M., & Taylor, M. J. (2006). Face processing stages: Impact of difficulty and the separation of effects. Brain Research, 1123, 179–187.

    Article  PubMed  Google Scholar 

  • Law Smith, M. J., Montagne, B., Perrett, D. I., Gill, M., & Gallagher, L. (2010). Detecting subtle facial emotion recognition deficits in high-functioning Autism using dynamic stimuli of varying intensities. Neuropsychologia, 48, 2777–2781.

    Article  PubMed  Google Scholar 

  • Loewenfeld, I. (1999). The pupil: Anatomy, physiology, and clinical applications. Butterworth-Heinemann.

    Google Scholar 

  • Longtin, A., & Milton, J. G. (1989). Modelling autonomous oscillations in the human pupil light reflex using non-linear delay-differential equations. Bulletin of Mathematical Biology, 51, 605–624.

    Article  PubMed  Google Scholar 

  • Loth, E., Garrido, L., Ahmad, J., Watson, E., Duff, A., & Duchaine, B. (2018). Facial expression recognition as a candidate marker for autism spectrum disorder: How frequent and severe are deficits? Molecular Autism, 9, 7.

    Article  PubMed  PubMed Central  Google Scholar 

  • Lowenstein O, Feinberg R, Loewenfeld IE. 1963. Pupillary movements during acute and chronic fatigue: A new test for the objective evaluation of tiredness. Federal Aviation Agency, Office of Aviation Medicine.

  • Lozier, L. M., Vanmeter, J. W., & Marsh, A. A. (2014). Impairments in facial affect recognition associated with autism spectrum disorders: A meta-analysis. Development and Psychopathology, 26, 933–945.

    Article  PubMed  Google Scholar 

  • Luckhardt, C., Kröger, A., Cholemkery, H., Bender, S., & Freitag, C. M. (2017). Neural Correlates of Explicit Versus Implicit Facial Emotion Processing in ASD. Journal of Autism and Developmental Disorders, 47, 1944–1955.

    Article  PubMed  Google Scholar 

  • Lydon, S., Healy, O., Reed, P., Mulhern, T., Hughes, B. M., & Goodwin, M. S. (2016). A systematic review of physiological reactivity to stimuli in autism. Developmental Neurorehabilitation, 19, 335–355.

    Article  PubMed  Google Scholar 

  • Moriuchi, J. M., Klin, A., & Jones, W. (2017). Mechanisms of diminished attention to eyes in autism. American Journal of Psychiatry, 174, 26–35.

    Article  PubMed  Google Scholar 

  • Naber, M., Alvarez, G., & Nakayama, K. (2013). Tracking the allocation of attention using human pupillary oscillations. Frontiers in Psychology. https://doi.org/10.3389/fpsyg.2013.00919

    Article  PubMed  PubMed Central  Google Scholar 

  • Neumann, D., Spezio, M. L., Piven, J., & Adolphs, R. (2006). Looking you in the mouth: Abnormal gaze in autism resulting from impaired top-down modulation of visual attention. Social Cognitive and Affective Neuroscience, 1, 194–202.

    Article  PubMed  PubMed Central  Google Scholar 

  • Nuske, H. J., Vivanti, G., & Dissanayake, C. (2013). Are emotion impairments unique to, universal, or specific in autism spectrum disorder? A comprehensive review. Cognition and Emotion, 27, 1042–1061.

    Article  PubMed  Google Scholar 

  • Nuske, H. J., Vivanti, G., Hudry, K., & Dissanayake, C. (2014). Pupillometry reveals reduced unconscious emotional reactivity in autism. Biological Psychology, 101, 24–35.

    Article  PubMed  Google Scholar 

  • Nuske, H. J., Vivanti, G., & Dissanayake, C. (2015). No evidence of emotional dysregulation or aversion to mutual gaze in preschoolers with autism spectrum disorder: An eye-tracking pupillometry study. Journal of Autism and Developmental Disorders, 45, 3433–3445.

    Article  PubMed  Google Scholar 

  • Oliva, M., & Anikin, A. (2018). Pupil dilation reflects the time course of emotion recognition in human vocalizations. Scientific Reports, 8, 4871.

    Article  PubMed  PubMed Central  Google Scholar 

  • Pelphrey, K., Sasson, N., Reznick, J. S., Paul, G., Goldman, B., & Piven, J. (2002). Visual scanning of faces in autism. Journal of Autism and Developmental Disorders, 32, 249–261.

    Article  PubMed  Google Scholar 

  • Philip, R. C. M., Whalley, H. C., Stanfield, A. C., Sprengelmeyer, R., Santos, I. M., et al. (2010). Deficits in facial, body movement and vocal emotional processing in autism spectrum disorders. Psychological Medicine, 40, 1919–1929.

    Article  PubMed  Google Scholar 

  • Proulx, T., Sleegers, W., & Tritt, S. M. (2017). The expectancy bias: Expectancy-violating faces evoke earlier pupillary dilation than neutral or negative faces. Journal of Experimental Social Psychology, 70, 69–79.

    Article  Google Scholar 

  • Roy, S., Roy, C., Fortin, I., Ethier-Majcher, C., Belin, P., & Gosselin, F. (2007). A dynamic facial expression database. Journal of Vision, 7, 944–1044.

    Article  Google Scholar 

  • Senju, A. (2013). Atypical development of spontaneous social cognition in autism spectrum disorders. Brain and Development, 35, 96–101.

    Article  PubMed  Google Scholar 

  • Shackman, A. J., Salomons, T. V., Slagter, H. A., Fox, A. S., Winter, J. J., & Davidson, R. J. (2011). The integration of negative affect, pain and cognitive control in the cingulate cortex. Nature Reviews Neuroscience, 12, 154–167.

    Article  PubMed  PubMed Central  Google Scholar 

  • Shenhav, A., Botvinick Matthew, M., & Cohen, J. D. (2013). The expected value of control: An integrative theory of anterior cingulate cortex function. Neuron, 79, 217–240.

    Article  PubMed  PubMed Central  Google Scholar 

  • Sheth, S. A., Mian, M. K., Patel, S. R., Asaad, W. F., Williams, Z. M., et al. (2012). Human dorsal anterior cingulate cortex neurons mediate ongoing behavioural adaptation. Nature, 488, 218–221.

    Article  PubMed  PubMed Central  Google Scholar 

  • Siciliano, L., & Clausi, S. (2020). Implicit vs. Explicit emotion processing in autism spectrum disorders: An opinion on the role of the cerebellum. Frontiers in Psychology. https://doi.org/10.3389/fpsyg.2020.00096

    Article  PubMed  PubMed Central  Google Scholar 

  • Spezio, M. L., Adolphs, R., Hurley, R. S. E., & Piven, J. (2007a). Abnormal use of facial information in high-functioning Autism. Journal of Autism and Developmental Disorders, 37, 929–939.

    Article  PubMed  Google Scholar 

  • Spezio, M. L., Adolphs, R., Hurley, R. S. E., & Piven, J. (2007b). Analysis of face gaze in autism using “Bubbles.” Neuropsychologia, 45, 144–151.

    Article  PubMed  Google Scholar 

  • Sun, S., Yu, R., & Wang, S. (2017). A neural signature encoding decisions under perceptual ambiguity. Eneuro, 4, 1–14.

    Article  Google Scholar 

  • Sun, S., Zhen, S., Fu, Z., Wu, D.-A., Shimojo, S., et al. (2017). Decision ambiguity is mediated by a late positive potential originating from cingulate cortex. NeuroImage, 157, 400–414.

    Article  PubMed  Google Scholar 

  • Turi, M., Burr, D. C., & Binda, P. (2018). Pupillometry reveals perceptual differences that are tightly linked to autistic traits in typical adults. Life, 7, e32399.

    Google Scholar 

  • Urai, A. E., Braun, A., & Donner, T. H. (2017). Pupil-linked arousal is driven by decision uncertainty and alters serial choice bias. Nature Communications, 8, 14637.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wagner, J. B., Hirsch, S. B., Vogel-Farley, V. K., Redcay, E., & Nelson, C. A. (2013). Eye-tracking, autonomic, and electrophysiological correlates of emotional face processing in adolescents with autism spectrum disorder. Journal of Autism and Developmental Disorders, 43, 188–199.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wallace, G. L., Case, L. K., Harms, M. B., Silvers, J. A., Kenworthy, L., & Martin, A. (2011). Diminished sensitivity to sad facial expressions in high functioning autism spectrum disorders is associated with symptomatology and adaptive functioning. Journal of Autism and Developmental Disorders, 41, 1475–1486.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang, S. (2018). Face size biases emotion judgment through eye movement. Scientific Reports, 8, 317.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang, S., & Adolphs, R. (2017a). Reduced specificity in emotion judgment in people with autism spectrum disorder. Neuropsychologia, 99, 286–295.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang, S., Jiang, M., Duchesne Xavier, M., Laugeson Elizabeth, A., Kennedy Daniel, P., et al. (2015). Atypical visual saliency in autism spectrum disorder quantified through model-based eye tracking. Neuron, 88, 604–616.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang, S., Yu, R., Tyszka, J. M., Zhen, S., Kovach, C., et al. (2017). The human amygdala parametrically encodes the intensity of specific facial emotions and their categorical ambiguity. Nature Communications, 8, 14821.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang S, Adolphs R. 2017b. Social Saliency In Computational and Cognitive Neuroscience of Vision, ed. Q Zhao, pp. 171–93. Singapore: Springer Singapore

  • Wang C-A, Baird T, Huang J, Coutinho JD, Brien DC, Munoz DP. 2018. Arousal Effects on Pupil Size, Heart Rate, and Skin Conductance in an Emotional Face Task. Frontiers in Neurology

  • Warga, M., Lüdtke, H., Wilhelm, H., & Wilhelm, B. (2009). How do spontaneous pupillary oscillations in light relate to light intensity? Vision Research, 49, 295–300.

    Article  PubMed  Google Scholar 

  • Wicker, B., Fonlupt, P., Hubert, B., Tardif, C., Gepner, B., & Deruelle, C. (2008). Abnormal cerebral effective connectivity during explicit emotional processing in adults with autism spectrum disorder. Soc Cogn Affect Neurosci, 3, 135–143.

    Article  PubMed  PubMed Central  Google Scholar 

  • Willenbockel, V., Sadr, J., Fiset, D., Horne, G., Gosselin, F., & Tanaka, J. (2010). Controlling low-level image properties: The SHINE toolbox. Behavior Research Methods, 42, 671–684.

    Article  PubMed  Google Scholar 

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Funding

Funding was provided by AFOSR (Grant No. FA9550-21-1-0088) and National Science Foundation (Grant Nos. BCS-1945230 and IIS-2114644).

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SS and SW designed experiments. SW performed research. SS, HY and SW analyzed data. SS, PJW, YW, RY, and SW wrote the paper.

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Correspondence to Sai Sun or Shuo Wang.

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Sun, S., Webster, P.J., Wang, Y. et al. Reduced Pupil Oscillation During Facial Emotion Judgment in People with Autism Spectrum Disorder. J Autism Dev Disord 53, 1963–1973 (2023). https://doi.org/10.1007/s10803-022-05478-2

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